make it look Iike a fish's dorsd fin. In adciition. nre hastet1 to point out that some of the illustrations dep~ct.I tadpole with almost no tall fins, toothlike strtictures on the fisM1ke lower jm; front leg that looks very much like a pectoral fin, and ~ v h a tappear to be scales on tllc tail. Mqo, the sequence of e i ~ h~lluarations t $haws a recently transformed metamorph progressing Into a fislihke tadpole! Our review sugpeas that proqess on understand~ngthe nature of tadpoles n.as belng made but slowlv m d rel~ictantl!: if this paper is any inciication. The fact that the tadpole was d r a ~ ~inn right latcral view, t l ~ u sprecluding the illustration of the spiracle on the left side. also 15 of note. Recause of thi5 common structural asvmmetn: it has become conventional to ill~15tratetadpole5 in-left late'ral vlen: The earliest figure and descript~onof a tadplrv=i mouthparts were those bv Swamn1erd.im (1737-17.78, pl. 40, fig. 1). Nearlv a cennlnf elapsed before Saint-Arise (183 1) described tadpoIe mouthparts and Di1gGi.s (1834) described and pamally ~llustratedl a n d m o u t h p . 1 ~In~h ~ comparative s studv of the o ~ t c o l o pand m v o I o p of ,imphrbl~nc.These cla5s1cd works \trere t'ollo\ved bv the fi rst hlstologlcal s n ~ d v of the de\~clopmcntof 1ahia1 teeth and j.11~. 4ieaths (Vogt 1842). Van Bambeke (1863) pioneered the use of lama1 traits, zncluding rnouthpnns. as rayononilc charac~enand n.as the first to note lnterspecific ditference5 among European specles. There Followed sc\,eral s n ~ d i eon~ tadpoles of Europe,m frogs. Amon9 the more noteworth\. are papen hv Lrvdig (1876) on structural 1ari.ition in morrthparts and Lamste ( 1879) on structural differences in inchvidual labid teeth of L)ircqflfo.c~~ts pictrrs; L a ~ s t ca l ~ ogenerated farnil id names based on chancteri~ticsof the s p ~ ~ i c(e.g., l ~ s Mediogninidae [midventral spiracle] m d L c v o ~ r i n i d a e[s~nirtral spiraclc]). Ke~ffcr(1888) d~scussedthe development and distribunon of labla1 teeth on the oral d ~ s co f A h ~ cobs~rfi-iurrzs, s and Schulze (1888) did the same for Peloltntrrfi~scrrs.Gutzeit (1889) expanded on these comparative \vorh and studied the development of 13wsheaths. Papers by Hiron-Koyer and V J ~Bmbeke (1881, 1889) described and compared the formation and structure of the mouthparts of tadpoles of 22
Ftg 1.2. An early rendition of rhc tadpole of Px~snrdispnmdn.vnfrom Hutchinson 1797, ntr ,\Tnhtm[ Hist? of rlrr Fmq Fir/) ofStrrirmrrr, PI. 3.
kinds of f r o p (15 currently recognized European and 2 African species) and built on the earlier work of Van Bmhekc by recognizing that terrain morphologicd traits were uscful in distinguishing among tadpoles of different species. They d s o pointed o~rtthose 1nn.d characteristics usefill at the generic and E~miliallevels. Roulcnger (1892) recognixci the value of being able to identi& tadpoles and presented a synopsis of u s c f ~ ~l al n d characters for distinguishing amon% species. He darifiecl and expanded the results of previous work, affimied the value of the position of the spiracle and vent tube in distinguishing among groups, argued for including patterns of pigmentation in species descriptions, was the first to p r o p s c a labial tooth r m r formula, discussed the relative value of the distribution of neuromasts in species characterizations, and wrote a key to the tadpoles of 1 Y species of Europcan anurans. This paper had a significant influence a n future workers. Tllc cxccllent illustrarions of the tadpoles m d mouthparts, some of the best elverpublished, nrerc reissued in his nionograph on thc tailless batrachians of Europe (Roulenger 1897-1898). Roulenger described only what he cnllcd "matlire' tadpoles, and only recently have we started looking at all stages of dc\rclopment in our delibcrations o n tadpole morphc~lop. Interest in thc tadpoles of North h e r i c a n frogs also was de\reloping in the later pare of the nineteenth ccntury. At almut die same time that Hkron-Royer and Van Ranibcke (1881) published their iniprt.int paper on European tadpoles, M a n Hlnckle!. independentiy had beLgun to study the lanae of anurans in AIassachusetts (Hitickley 1880). Her subsequent paper describing the mouthparts oitadpoles of seven species was the first compantive work on North American muran l a n w (H~nckley1881) and marked the advent of comparative devclopmentd studies of tadpoles in the Nelv \170rld. She quickly foIlo~vxiwith dc\~elop~iiental studies of nvo other species (Hlnckle!r 1882, 1884). Mre have observed that older literature, even though niformarive, often is slighted m d that cunous obsenrations reported therein too oi'ten are missed. For example, ~ i n c k l e y (1 882:95) reported that Rnnn gdraricn occasionaUy has dual spiracles, a condition not known in rmid tadpoles. In his cInssic stirdies o n North American .kura, A. H. Wright (lC?14, 1932) published detailed descriptions and photop p h s of taciplcs and clrawings of mouthparts of species occurring near Ithaca, New York, and from the Okefenokec region of southern Gcorgia. In a separate svnopsis, A. H. \\'right (1529) described, illusmted, and presented a key to tadpoles of 38 species mostly from the eastern and southern Cnlted States. Some information on tadpoles appeared In the first (1933) and second (1942) edinons ofdie Hn~rdltaoX. of Frqgs nnd Ends by A. A. Wright and Wright, but it wasn't unnI the third edition (1949; rcpr~ntedIn 1995) by A. H. IVright and tjTrisht that a kev and photographs -of tadpoles 2nd their mouthparts appeared. Unfortunatel!; A. H. \lrnsht continued to use only "niature" larvae because "halfgro\ipnlarvae . . . are ofien quite aknormaI in the usual characters used In I,zn.al descriptions." U'hilc the early w o r k by A. H. Ct'r~ghtwcre uulv tlseful, his preoccupation with variof expressing relation ~d measurements m d c o m p l e ~\ln\!~
RONALD ALTIG AND ROY W. McDIARMID
28
sophyne and Stephopaedes, smaü African bufonids that commoniy breed in phytotelmata, have a circular, fleshy "crown" that encircles the eyes and nares (Channing 1978, 1993; Grandison 1980). We suggest that the hnction of this structure remains conjectural because none of the suggestions (e.~., - attachment, floatation, and respiration) seem feasible. Even t h o u"~ hthe dorsai and laterd ~rofilesof the tad~ole snout vary considerably and their shapes appear to be phylogeneticdy and ecological correlated, no descriptive terms have been proposed. Viewed from above, the snout varies from rathe;ac;te to broadly rounded. In lateral profiie (eyes to base of upper labium) the snout varies from uniformiy rounded to sloping, the trajectory of which turns abruptiy near the oral disc.
usages may be inappropriate. If tadpole tails were classified by the same terminology as fish tails, aü tadpoles wouid be diphycercai, aithough presumably not homologous (in diphycercal fishes, aü mediai fins fused into one unit). Terms suggested by Van Dijk (1966) apply oniy to curvature of the tad axis. Fins of lotic tadpoles are lower, thicker, and stiffer than the taüer. thinner more flexible ones of lentic forms. The amount and distribution of connective tissue in the taiis of lotic versus lentic forms have not been studied. Kinematics comparing swimming between the extremes of taii morphology surely wouid be worth investigating, but oniy pond forms have been studied (chap. 9). Van Dijk (1966) and Lambiris (1988a, b) noted that the basai ~ortionof the tail muscle and adiacent fins of Hemisus tadpoles has a sheath of thick connective tissue visible in live Tail Morphology and preserved specimens (see figures in chap. 12). This tail Some aspects of tad size and shape have been discussed pre- sheath is more common than previously suspected but when viouslv. Here we ex~lorethe taii structure in more detail. present, is visible oniy under specific, but undetermined, cirThe tad muscle is composed of bilateral myotomic muscle cumstances of preservation. We know of no explanation of masses divided by V-shaped myosepta, the points of which what the structure is, even if it is conneaive tissue, or of face anteriorly; the epaxiai portion is smaüer than the hypax- how it funaions, but it does occur in other taxa (e.g., O. L. iai portion. The unsupported fins are composed of loose Peixoto, personal communication, Hyh mamuwata group; connective tissue covered by epidermis (Lebedinskaya et ai. I. Grfiths and De Carvalho 1965, StereocycI.ps; personal ob1989; Rhodin and Lametschwandtner 1993; Yoshizato servation, Gartropbvyne carolinensis and Rana sphenocephah). Anvone who works with tadooles from different habitats 1986). Fins extend from various points on the body and taii posterioraüy to slightiy beyond the tip of the notochord and soon questions the influente of environmentai factors on tad muscle. Dorsai fins originate at or near the tad-body morphology. Unfortunately, few definitive data are available. junction (most common), at various points anterior to the Tadpole color and coloration obviously vary in different dorsai tail-body junction as far fonvard as the plane of the environments, and Van Dijk (1966) questioned if tadpoles eyes (e.g., &sina senegalensis and Scinm mbra group), or raised in shaüow water have lower fins than normal. Tadat various points aiong the taii muscle (see fig. 12.1 and poles of Rana chiricahuensis captured in flowing water difsketches of examples of tadpoles in various genera within the fered in the degree of development of abdominal musculataxonomic accounts). The margins of low taii fins usuaüy are ture, pigmentation, and shape compared with conspecifics nearly parde1 with the margins of the taii muscle. Extremes from still water (R. D. Jennings and Scott 1993). Martinez in this case are represented by suctorial species, Poyntoniapa- et ai. (1994) reported skeletai deformities in reared tadpoles ludicoh, and various semiterrestriai forms (e.g., Arthrolep- that were likely nutritionai. tides, Cycloramphus, Nannupbvys, and Thoropa). The anterior part of the dorsai fin of the tadpoles of Occidozy~a(sensu Limbs stricto) rises abruptiy (M. A. Smith 1916b) and then slopes The hind limbs of tadpoles are exposed during much of tadeveniy to the tip. The same descriptors apply to the ventrai pole development, and their pattern of development (see fin, which most commoniy originate at the ventrai terminus Alberch and Gaie 1983; B. I. Baiinsb 1972) is of primary of the body but may originate anywhere on the tail or ante- importance in comparing growth rate among tadpoles of rior to the vent tube at various points on the abdomen (e.g., different sizes and taxa under differing conditions (e.g., phyliomedusine hylids, pipids, some Rhaqhoms, and Znu- Gosner 1960; see fig. 2.1). Even though the front limbs are covered by the opercuium, they foliow a similar developpus in which a distinct lobe may be present). The taii tip takes many shapes: broadly or narrowly mental pattern. Based on our unpublished data, developrounded to various degrees or extended into a flagelium. A ment of the front limbs lags b e h d that of the h d limbs flagelium comprises the terminal part of the taii muscle and by about one stage (i.e., length-diameter changes in limb reduced fins; it is more or less distincdy separated from the buds in Gosner stages 26-30 and toe differentiation in anterior portion of the taii by a prominent reduaion in fin stages 33-37) in spite of the fact that oniy four digits occur height. ~ h flagelium e ofien iBpigmented less and may undu- on the front limb. The apparent differentiai in limb developlate independentiy of the remainder of the tail. A flagelium ment increases greatiy in semiterrestriai tadpoles, but the admay be present in tadpoles of severai ecological types with justments in timing and pattern of the growth trajectories low (e.g., Hyh leucophylhta group, phyliomedusine hylids, required to reach proper metamorphic conditions are not and Znoptts) or high (e.g., some Hyh, Ihsina, and S c i ~ ) known. Drewes et ai. (1989) found a difference of about five fins. D u e h a n (1978) used xiphicercal to describe a taii that stages between comparable development of hind and front narrows abruptiy to a distinct flagelium. Comphentary ter- limbs ofArthroleptides, and Lawson (1993) saw tadpoles of minology for other forms of fins is not available, and such Petropedetes with oniy fuliy developed hind legs hopping i
BODY PLAN
29
of elv~ia. ' aü of whch are assumed to shade the eve from intense light. The umbraculum (e.g., Rana vertebralis) is a projeaion of the dorsal pupiilary margin. Elygia may occur as a hemispherical area of melanophores extending lateraüy from the kddorsal margin of the ;ris (ocular) or i i the dorsal cornea (epidermal).She corneas of an uddentified hyiid tadpole (personal observation) are mostly pigmented; if not a case of teratology, this rnay be an extreme form of epidermal elygium. Wassersug et ai. (1981a) noted similar pigmented corneas in Thelodemza carinensk. Recently we have observed an ocular elygium in a number of other taxa (e.g., some Buf, Hyh, Mantidactylus, Pseudamis, and Rana), although often it is visible only with bright dumination and at rnagnification of iive specimens. The eyes of Stauroisnatator are covered with "thick skin . . . but in stages 36 onward Eyes and NasolucrimalDuct there is a small, clear window over the eyeball" (Inger and Eye position and eye orientation are different concepts (fig. Tan 1990:4). 3.2A). Position indicates where the structures are located on The tadpole iris cornmonly has bright, metdic pigments the head and orientation describes their manner of place- arranped " in comviicated Datterns that seem to be influenced ment or aiignment (e.g., facing direction). Eye position is by the topography of underlying blood vessels. Interspecific generaüy described as dorsal or lateral, although a contin- pattems in the arrangement and distribution of color probuum exists. Dorsal eyes may face dorsaüy (upward), dorso- ably exist, but these features (e.g., D u e h a n 1978; Gaüardo laterally, or lateraüy, while lateral eyes always face laterally. 1961; Scott and Jennings 1985) have seldom been examThe eyebaü of tadpoles is covered by a two-layered cornea ined. Aithough the entire eye can be rnoved, the round pupil that is continuous with the body epidermis. Dorsal eyes have has no abiiity to adjust its size relative to iight intensity. no part of the eye or cornea in the dorsal siihouette, and During &id- to late metamorphosis, either dark pigmenlateral eyes have some part of the eye or cornea included in tation appears or the surroundmg pigmentation decreases in the dorsal siihouette (fig. 3.2). Dorsal eyes e x e m p e benthic intensity to accent a shallow groove that extends in an arc tadpoles in both lentic and lotic systems, whde lateral eyes from the anterior corner of the eve toward the naris. This are rnost common in lentic forms that spend considerable nasolacrimal duct develops in association with the Harderian time in the water column (e.g., many hyiids and microhy- gland (Schmalhausen 1968; see Baccari et al. 1990) that lulids). Relative positions of dorsal or lateral eyes can be quaii- bricates the eye. fied verbaüy or by measurements. Lateral eyes are typicaüy larger and have more cornea curvature and lenticular protru- Integument and Chromatuphores sion than dorsal eyes. Eye size ranges from minute (e.g., Numerou uniceiiular glands throughout the epidermis of centrolenids) to quite large (e.g., some nektonic hylids). The tadpoles produce mucus; chapter 5 has more details of integexceptionaüy smaü eyes of centrolenids are located quite umentary histology. Small serous glands often are scattered close to the midline, and because of their orientation and an generally over the body surface (e.g., Asca.phus and Poyntonia apparent late closure of the choroid fissure, they often ap- paludzcoh) or concentrated along the dorsal fin, w i t h the pear C-shaped in dorsal view. The extent that the eye pro- ventral fin, along the dorsum of tad muscle, and dorsolatertrudes frorn the surface of the head, the curvature of the cor- ally and ventrolateraüy on the body (e.g., Inger 1966; Liem nea, and the lenticular protrusion also vary. We detect some 1961; S. J. Richards 1992; some Amolops, Huza, and Meriscorrelations with ecology, but definitive data to support togenys, Hyla, Hyhrana, Litoria, Rana, Phyllomedusa, and these observations are lacking. Physahmus). Tadpoles of someAmolops have keratinized spiVan Dijk (1966) discussed an umbraculum and two types nules on the dorsum that may abate turbulence as water flows over the body; they also have various patterns of small, densely arranged papiilae and iight keratinization in the roof of the beiiy sucker. Short papiilae occur on the snout of the tadpoles of Hoplophryne rogemz (Noble 1929). Close exarnination of certain tadvoles reveals a circular area of siightly contrasting color anterolateral to the base of the vent tube. This slightly raised area appears glandular, but it mavJ be associated with the lateral line svstem. It is most obvious in darkly pigmented, neotropical, lotic hylids. Bright coloration and distinaive patterns are important sexual and species recognition features for many adult vertebrates but apparently are of little importance to larval or imFig. 3.2. Dorsal views of styiized tadpole bodes showing eye positions. (A) Lateral. (B) Dorsal. mature ones. Dorsal coloration in tadpoles is mostly of about on the forest floor. Definitive data are lachg, but it appears that finger and toe webbing of metamorphs is equal to or less than that of adults. Inhibitory versu stimulatory modulation of iimb growth by hormones of the pituitary and adrenal hormones is stage dependent (M. L. Wright et al. 1994; also Elinson 1994). L. Muntz (1975) recognized four behavioral stages in leg mobiiity and muscle and nerve development during leg myogenesis (also Dunlap 1967; Hughes and Prestige 1967; L. Muntz et ai. 1989). Comparisons of her data on Xenopus to those from species of Merent metamorphic patterns and ecology would be informative. &o, the ontogeny of pigment patterns during limb development, although largely unstudied, may be mefui in species identifications.
i"
i
30
RONALD ALTIG AND ROY W. McDIARMID
muted tones of black, brown, gray, and green arranged in various patterns; ventraily most tadpoles are coppery, silver, or white. Altig and Channing (1993) described the major components of tadpole color pattern; compared to adults the coloration of tadpoles is somber and presumably functions in some aspect of crypsis (i.e., camouflage). Altig and Channing (1993) also identified common patterns that they associated with background matching, disruption, and countershadmg. Other colors (e.g., gold, orange, and red), when present, usudy are comparatively bright or contrasty. After considering the coloration and the behavior of the tadpole ofXenohyla, Izecksohn (1997) considered it to be a leaf mirnic, and the coloration is also surprisingly convergent with young tadpoles of Pseudisparadoxa. Specific pigments sequestered in chromatophores provide color and pattern (Bagnara et al. 1978). Melanophores contain black or brown melanins derived from tyrosine; xanthophores and erythrophores contain synthesized yellow and red pteridines plus dietary carotenoids; and iridophores contain refleaive purine platelets. Chromatophore type can be identified in TEM sections by the structure of the pigment-containing organelles (S. K. Frost and Robinson 1984). Filiform, foliose, punctate, rodular, and stellate are terms that are useful for describing the shapes of chromatophores, especidy of melanophores, that remain in formalinpreserved material. The presence and apparent shape and sue of chromatophores differ when viewed with incident, transmitted, dark-field, or polarized iliurnination. The type of pigment and its distribution within the ceil and the density, location, orientation, shape, and size of the chromatophores m o w the perceived color and pattern. Much of the color and pattern of tadpoles commonly is derived from chromatophores positioned in subintegumentary areas (e.g., w d s of the giii chambers, peritoneum, blood vessels, nerves, and gut). Pubiished figures often show these drfferences without mention in the text. Other components of coloration probably serve to delay (e.g., yeiiow oceh at the base of the tail in Rana alticola) or misdirect (e.g., black tail tips of someAcris tadpoles) a predator attack. Caldwell (1982) published one of the few quantitative studies on the distribution and occurrence of color pattern in tadpoles. She argued that a polymorphic pattern involving black tail-tips in A& is maintained by disruptive seleaion and functions as a defleaion mechanism to misdirect predatory attacks by certain dragonfly naiads from the head of the tadpole to the tail. Integumentary glands that presumably secrete noxious substances occur in some tadpoles (e.g., Liem 1961, Rana chalconota; persond observation, Physahmuspetersi) and their location on the body or tail often is highiighted by bright contrasting coloration (see photographs of Rana altimla and an Indian ranid in figs. 1 H and I in Altig and Channing 1993). Such patterns of aposematic coloration are well known among other organisms and their scattered occurrence among tadpoles is not surprising. Brodie and Formanowicz (1987) argued that the intense black coloration and cutaneous toxicity of many bufonid tadpoles and their tendency to aggregate in slow moving schools are traits indicative of aposematic coloration (see Wassersug 1971, 1973; see chap. 9). The bright red color-
ation of many centrolenid tadpoles is attributable to blood capdiaries and not pigment in the skm (Vilia and Vailerio 1982; personal observation). There also is some evidence that the bright golden band on s m d tadpoles of Rana heckrcheri may serve as a visual cue to promote spatial orientation of schoohg individuals. Altig and Channing (1993) reviewed generalizations about the associations of color and pattern with habitat, behavior, and ontogeny. Metachrosis (i.e., change in color via changes in the distribution of pigments within chromatophores) is iirnited, although considerable blanching and darkening relative to diel light cycles occur. The body of many tadpoles becomes paler at night, whde the tail, particularly the distal third, often gets darker. The tail of the tadpoles of Hylagratwsa has punctate melanophores near the base and steilate ones distally; it is the stellate population of melanophores that dilates at night that produces the intensely black tail of this species. Detailed studies of the distribution and morphology of melanophores are needed to serve as an aid to identification and to help explain certain aspects of behavioral ecology. For example, a chainlike pattern of melanophores visible only at magnification occurs in discoglossid tadpoles (Bytinski-Salzand Eiias 1938). Also, the tadpoles of some species of Leptodactylus have melanophores arranged in rodular bundles that are oriented at various angles to each other. As tadpoles approach metamorphosis, adult pigments begin to appear. Tadpole coloration is known to vary ecologicdy and geographically but detailed studies are lacking. Conspecifics inhabiting turbid water often appear unpigmented whereas those in clear or tannin-stained water even a few meters away often are quite diflerentiy and frequentiy prorninentiy colored. The reddish or yellowish colors that occur in the h s of tadpoles of certain species (e.g., Hyla chlysoscelis, H. cinevea, H. femoralis, H. versicoh, and a s s i n a senegalensis) develop most intensely in individuals that develop in tanninstained waters and seldom in those from turbid water. Experiments by McCollum (1993) and McCollum and Van Buskirk (1996) seemed to indicate that the reddish or yellowish pigments developed only in the presence of predatory odonate naiads. Understandmg details of how color pattern develops during hind limb ontogeny would be usem in distinguishmg arnong species and probably provide interesting data on pattern development in earlier stages as well. For example, hatchhgs of a number of North American hylids have dorsaily banded tail muscles. This pattern subsequently is lost in most species but usually retained by tadpoles of species of A&, Hyla at?ivocu, and Pseua'mi-is crucifer. A similar case occurs in young salamanders of various species ofAmbyrtoma with only A. talpoideum retaining the bands throughout larval ontogeny. Unfortunately, such studies are uncommon (e.g., Altig 1972). Ontogenetic changes in tadpole coloration usudy are not profound after about stage 25. Tadpoles of Hylagratwsa between stages 25-28 have a single black saddle on the tail muscle that disappears later in ontogeny when tail metachrosis appears (see above). Smail tadpoles of Rana vaillianti have bands across the body and tail, and smail tadpoles of Pseudis are prominently banded in contrast to the unicolored, larger ones. The black rim on the tail fins of
BODY PLAN
Rana heckscheri tadpoles begins to develop at about the same stage (28) that the prominent golden band of smaller tadpoles begins to become less prominent; whether there is an ontogenetic change in the orientation of individuals in schools is unknown. The oifactory sacs and both external and internal nares usuaiiy are present during ontogeny, but the external nares of most microhylid tadpoles do not open until metamorphosis; Metaphrynellu (Beny 1972), Ramanella (Kirtisinghe 1958), and Uperodon (Mohanty-Hejmadi et ai. 1979) are reported to have open nares during tadpole ontogeny. Berry (1972) also stated that the nares of Ranaglunduhsa do not open until just before metamorphosis. Embryos of Gastroplnyne mlznensis and Micvobylu heymonsi have external narial openings (personal observation), but the canal is blocked; t h s external opening subsequently closes at the surface for most of larval ontogeny, and, for a while, one can detect where the opening was on SEM photomicrographs. The narial openings presumably form via induction from the oifactory ectoderm (Zwilling 1940), but the mechanism for closure of the external opening and subsequent reopening late in ontogeny is not known. The external nares of the nidicolous cophyhe microhyiids are open throughout ontogeny, although it is not known if they are blocked within the tube during at least early stages. External nares are situated at various points on the snout. Tadpoles with cylindrical bodies and long snouts (e.g., Hylu leucophylluta group) have the nares much closer to the tip of the snout and more lateral than seen in most tadpoles; the nares of Xenupus are distinctly parasagittal and near the mouth (see iüustrations in chap. 12). Most often the narial aperture is rounded, but it may be oval, roughly trianguiar (e.g., Bufo), or transversely ehptical (e.g.,Xenupus). Interspechc differences in snout shape and surface topography cause the aperture to face anterolateraiiy, dorsaiiy, dorsolateraiiy, or lateraiiy. The nares of Bufo are quite large for the size of the tadpole, and comparisons of relative size among species often can be used for identification (e.g., Ranapipiens vs. R. catesbeiana groups). Other detads of narial structure have not been exarnined in detaii (e.g., Channing et al. 1988; G. F. Johnston and Altig 1986). For example, the narial opening may be flush with the surrounding surface, countersunk, or marked with a marginal rim that varies interspecificaiiy in prominence and shape (fig. 3.3F). Other types of narial ornamentation range from a single, medial papilla to various arrangements of several papiüae. Some descriptions suggest that the authors have looked through the transparent skin and mistaken pigmentation around the nasal canal for a tubular external naris. The narial rims ofRrcaphus and certain other suctorial forrns extend as distinct tubes (e.g., fig. 3.3F). Operculum and Spiracle "Operculumyyis the giii covering of tadpoles and a term that has different meanings in other groups; it is not homologous with the giií covering of fishes or the ear element in frogs (chap. 4). "Spiracle," the exit for respiratory water in tadpoles, forms as a result of the growth and fusion pattern of
31
the operculum with the body waii; it is another borrowed term and not homologous with the hyoid pouch derivative in elasmobranchs. We retain both terms because thev have been used for a long time for tadpoles and chang& the names Iikely would produce more confusion than that caused by the multiple meanings that exist in dderent groups today. The number, location, and morphological configuration of the spiracle(s) depend on where and how the o p e r d a r fold íüses with the bodv waii (Starrett 1973). Starrett observed a frequent association of spiracular position with feeding mode and ún shape, especiaiiy of midwater and surface feeding tadpoles. She commented that an excurrent spiracular flow from a single sinistral spiracle would tend to rotate and thereby decrease the efficiency of a tadpole feeding. in the water column and observed that most midwater L7 íiiter-feeding tadpoles have either dual lateral or a single midventral spiracle. The position and number of the spiracle(s) generaiiy are consistent enough among related species and within certain hizher taxa to be useN for svecies identifica" tion and as phylogenetic traits. Exceptions include a midventral spiracle in FhctonutusfEssilis, rather than the sinistral condition typical of hylid tadpoles and a spiracle that opens on the left side of the taii muscle into the same tube as the vent in Stereocyclops, rather than midventraiiy as in most microhyiid tadpoles (I. Grifliths and De Carvaiho 1965). . By f i t h e most common spiracle morphology is a single midiateral opening on the left side (= sinistral or laevogyrinid) but at various positions along the body. At least phyllomedusine hylids, pelobatids, and some myobatrachid and leptodactylid tadpoles have a single spiracle situated far below the midiateral area in a parasagittal position. G. F. Johnston and Altig (1986) coined the term paragyrinid for this condition. A single spiracle situated anywhere from the chest (e.g., Rrcaphus) to near the vent (most microhylids) is termed midventral, medioventral, or mediogyrinid. Dual, lateral spiracles (= amphigyrinid) occur in &e tadpoles of rhinophrynids, pipids, and species of Leprdobatrachus (Leptodactyiidae),although the mode of formation and therefore homology in the latter case (Ruibal and Thomas 1988) is different from the first two. Laviila and Langone (1991) described the ontogenetic changes in the spiracle of Elachistochis ovalis, and Inger and Frogner (1979) cautioned workers about using spiradar characteristics of smaii microhyiid larvae because of ontogenetic changes. For example, the edge of the ventral waii of the spiracular tube of Paraduxophyla palmata is entire, but older individuals have four streamers extending posteriorly (personal observation). The unique spiracle of Otoplnynepybumi (l'yburn 1980) includes a free tube that is the longest spiradar tube known (i.e., extends weií past the body) and a seemingly sinistral position unique withn microhylids. Wassersug and l'yburn (1987) showed that the spiracle in Otophryne starts out in the expected medioventral position and ontogeneticaüy moves to the left side. These authors suggested that the tadpole feeds passively whde embedded in the bottom of sandy streams. ~ a t e flowing r over the orifice of the long spiracle traiiing upwardiy in the water acts as an aspirator to p d water into the mouth. Other tadpoles with rather long spiracular tubes
RONALD ALTIG AND ROY W. McDIARMID
Fig. 3.3. Representative anatomical and morphological features of select tadpoles. Typical arrangement of the recrus abdominis musde (origin uppermost in all frames, viewed with polarized light) in (A) Gastivphye caroliincnris (Microhylidae), (B)Agalycbnk callidym (Hylidae), and (C) L c p i k b d u ( hmk (Leptodactylidae).(D) Adhesive gland of Scupbbpu holhkii (Pelobatidae). (E)Abdominal flap (dorsal
view, transmitted light) of T h m o p a ~ l i t a n (Leptodactylidae). a (F) Narial aperture of HercOphyepumIli (Helwphrynidae). (G) Head flap of -bcS c a m (Bufonidae). (H) Belly ''finger" (right side, ventral view, head at top) of Hopluphye r o (Microhylidae). ~ ~ (I) Belly sucker (anterior to right, longitudinal section) ofAtelopw &Mum (Bufonidae).
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genetic link exists between the variations in spiracular tube length and middorsal stripe.
Fig. 3.4. Basic patterns of spiracular tube arrangement in anuran lar(Dendrobatidae). (B) vae. (A) Single, sinistral, Dendvobates tiwononus Single, sinistral with long spiracular tube, Otophynepybumi (Microhylidae). ( C )Dual, lateral, Lepidabatruchw LlanennS (Jiptodactylidae). (D) Dual, lateroventral, Rbinophynus dorsalis (Rhinophrynidae).(E) Single, posterior ventral, KahlapuLhva (Microhylidae). (F) Single, midventral (on chest),Acaphw tmei (Ascaphidae).
includeAcrrs and Heleophvyne. Scaphzophvyne (Scaphiophryninae) has many odd features (e.g., jaw sheaths) for a microhylid tadpole, including a spiracle that is between midventral and sinistral. Representative spiracle arrangements are shown in figure 3.4. Because of differences in the pattern of fusion between the opercular fold and body wall, the spiracular aperture may face various drections and have different shapes and tube codgurations. The different developmental patterns that produce dual, lateral spiracles, a single medial spiracle at various sites, or a sinistral spiracle are understood in general, but details of which tissues are involved and the Datterns of formation among taxa are unclear (Inger 1967; Nieuwkoop and Faber 1967; 0.M. Sokol1975; Starrett 1973). The inner or centripetal wall of a sinistral, paragyrinid, or midventral spiracle may be absent (e.g., Rrcaphm; phyllomedusine hylids), present only as a partial or complete ridge, or present as the wall of a tube of various lengths that posteriorly or terminally is free from the body wall with the posterior tip free from the body wall (fig. 3.5A-D). The lateral wall may end anterior to, at the same plane as, or posterior to the insertion of the medal wall. The spatial limits of the spiracular walls determine the shape and orientation of the aperture. In certain cases the aperture faces laterally and is commonly smaller than the bore of the s~iraculartube. Functional explanations to account for the Merent spir a d a r arrangements are few. Starrett (1973) suggested that midventral (e.g., microhylid) or dual lateral (e.g., pipid) spiracles in suspension-feeding, nektonic species may allow the tadpole to avoid disturbance of planktonic or particulate food items. At least some of these forms can maneuver solely by the force of the spiracular jet (Starrett 1973; personal obm a t i o n , several taxa). Wassersug and Viertel (1993) sugp t e d that folds in the inner walls of the long spiracle of OtopiCnyne may provide elasticity t o modulate water flow. Based on tadpoles raised from a single clutch of Stereoyclups eggs,I. Griffiths and De Carvalho (1965) suggested that a
Vent Tube An anus is the posterior opening of the mammalian digestive tract. Amphbians have a common collecting chamber -a cloaca-into whch the dgestive, urinary, and reproductive tracts empty. The aperture through which feces exit to the outside is not the anus in the adult and probably not in the tadpole either. Without knowing more details of the development and origin, the use of proctodeum in association with the vent is also debatable. For tadpoles, we suggest the terms vent and vent tube in deference ;o the samelotation (i.e., snout-vent length) used for frogs. See previous dscussions of why body and tail length measurements should not involve the vent or vent tube as a landmark. The digestive tract of a typical tadpole exits the abdominal cavity through a tube, the aperture of whch usually is located in the sagittal plane and commonly associated with the ventral fin (fig. 3.5). The location of the aperture usually is consistent enough within taxa to be usefid for identhcation. The primary character states, recognized more than
Fig. 3.5. Schematic drawings of major configurations of spiracle and vent tubes. (Uppw)kft-lateral views of spiracular tubes that essentially face posteriorly: (A) inner (= cenmpetal) wall absent; (B) inner wall present as slight ridge; ( C )inner wall free from body; and (D) inner wall free and formed such that aperture opens laterally instead of posteriorly. (Mtddk)Lateral views of the right side of supine tadpoles showing vent tubes (arrowsindicate points of attachment of right wall): (E) right wall displaced dorsally; (F) right wall displaced anteriorly; (G) right wall displaced dorsally and anteriorly; (H) medial vent tube. ( h e r ) Schematic cross-sectionsthrough the base of the d fin of supine tadpoles showing various placements of the vent tube: (I)right wall displaced dorsally, as in (E) above; (J) medial vent tube with lateral displacement; (K) medial vent tube with web between tube and fin; and (L) meha1 vent tube with both walls attached directly to ventral fin.
34
RONALD ALTIG AND ROY W. McDIARMID
100 years ago (see Camerano 1890, 1892; Willey 1893), involve the position and orientation of the opening; apertures open medially (in line with the plane of the ventral fin) or dextrally (to the right of the plane of the ventral fin). Some authors (e.g., Cei 1980; Duellman and H-illis 1987; Kehr and Basso 1990) reported sinistral vent tubes in Pleuro&ma, Gastrotheca, and Lysapsus, respectively, and we have seen aperture variation within a single lot of Ceratuphlys cornuta. Numerous other variations w i b each basic type are known (G. F. Johnston and Altig 1986), but no significance has been attached to the different configurations. We recommend that the character state (medial, dextral, sinistral) of the vent be determined relative to the position of the aperture, not the position of the tube. A vent tube that parallels the ventral margin of the fin may still have a dextral or sinistral aperture. We know of no data supporting the notion that the vent tube is abdominal in origin but we assume that llkely it is. All vents are medal duri& early development, and the ontogeny of vent tube formation has not been studed well. Those phyllomedusine hylids in which the entire vent tube and ape&re is displaced to the right and not associated with the tail fin in any way have not been examined as embryos. The dextral condition in Phyllobates lugubris (Domelly et d . 1990b) is not attained until later than normally expected (i.e., by stage 25; also see Lavilla and Langone 1991). Davies and Richards (1990) noted that until stage 32 the limb buds of Nyctimystes h y i are enclosed in a membranous sac associated with the vent flap (also see Van Dijk 1966; Hemisw). Variations on these themes are found among a number of rheophilous forms (see below). A medial vent may or may not be associated with the ventral fin in several different ways (fig. 3.5). The tube may be long or short, free or attached directly to the fin,or attached via an intervening, fleshy web. The ventral wall may be shorter than, equal to, or longer than the dorsal wall. Differences in wall lengths produce distinctly shaped apertures that usually face in different drections. The right wall of dextral vent often is displaced anteriorly, dorsally, or more commonlv anteriorlv and dorsallv. A ventral wall.that is longer than the other w d s causes the aperture to face in a number of drections, includmg dorsally. In some cases, dextral vents are com~letelv se~arated from the tail fin and musl i l d e (e.g., Phasrnahylaguttata). In a number of suctorial forms (e.g., Ascapbus, Heleuphly, H y h bogotensis group, Telmatobufo) a flap of tissue lies below the vent; these vent flaps take on several dfferent sha~es.In Asca~hw.the vent tube is attached to the dorsal surface of this kapYJandthe vent aperture is even with the dstal margin of the flap. The margin of the aperture normally is smooth, but B. T. Clarke (1983) noted that in tadpoles of Nannuphlys ceylonensis it was fluted and appeared similar to marginal papillae on the oral disc. We know of no data that indicate a correlation between vent tube morphology and position and tadpole ecology. Transitory Embryonic Structures Adhesive glands (fig. 3.3D), external gills, integumentary ciliated cells (visible in fig. 3. lo), and hatching glands occur
for various periods during embryology. The adhesive gland usually is visible between stages 18-25; it can be detected much earlier with proper techniques and may persist at least as a pigmented spot for several stages later in ontogeny. The term "sucker" should not be used in reference to the adhesive gland. The mode of attachment is via sticky secretions; there is no suction comparable to that found in the belly or abdominal sucker o f gastromyzophorous tadpoles and the oral d s c of suctorial forms. Hatchlings use the sticky secretions (Eakin 1963, Pseudacris regilla) of these transient glands to provide stabhzation prior to the further development of the oral d s c and tail whch afford more coordinated adhesion and locomotion for active tadpoles. Znopzw and perhaps other hatchlings may hang from a mucous strand from this gland immediately after hatchmg (Bles 1905; also see Sive and Bradley 1996). Adhesive glands inxinupus l& first appear at about Gosner 18 (Nieuwkoop/Faber 15, early neurula), reach full development at stages 22-23 (35-36; see Drysdale and E h s o n 1993), functionally degenerate by Gosner 25 (49), but persist as pigmented remnants posterolateral to the oral d s c as late as Gosner 27-28. Lieberkund (1937) and Thiele (1888) surveyed the gross and histological structure of these glands in Burope& tadpoles. External gills (see chap. 5) are present in most tadpoles for a short ~ e r i o d(Gosner 19-24'1 in earlv, develo~ment.External gills appear as short nodules or long, branched fimbriae and their morphology may reflect the developmental environment. Lsvtrup and Pig6n (1968) discussed the influence of 0, and CO, concentrations on their develo~ment. and there is some evidence of similar gill morphology among related species. Gdls usually are on two visceral arches. Tadpoles of Boophis, Manti+lus (BlommersSchlosser 1979a) and a number of microhylids lack external f l s . Ciliated cells scattered throughout the epidermis of anuran embryos (Steinman 1968; see fig. 3.10) may have the following functions: removing micro6rganisms i d impurities from the epidermis, transporting newly hatched embryos, providing- respiratory ventilation of the body surface wide & the egg as well as .after hatching, and redicing the drag coefficient (Nachtigall 1982). Embryos move frequently within the egg jellies, and hatchlings move at surprising speeds via these cilia while lying on their side. Ciliated epidermal cells produce a cephalocaudal current along the embryo in the egg and after hatchmg (Kessel et al. 1974). The hatching gland is a Y-shaped array of unicellular glands on the 6 p o f the head; the open end of the series faces anteriorly (Drysdale and Elinson 1993; Ohzu et al. 1987). Presumptive cells of the gland are present by the end of gastrulation, and differentiated cells start to form after n e d a t i o n is completed. These glands produce an enzyme that dissolves or weakens the egg jehes and facilitates hatching (Carroll and Hedrick 1974; K. W. Cooper 1936). Yoshzaki (1973, 1974, 1975, 1991), Yoshzaki and Katagiri ( 1975), ,, and Yoshizaki and Yamamoto ( 1979) discussed the ontogeny of these glands and their enzymes (also see Gollman and Gollman 1993a; Noble 1926a). I
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describing: relative locations of structures on the face of the oral dlsc, we prefer "anterior/posteriorn relative to the longiTemzimlogy t u h a l axis of the body and "proximal/dlstal" relative to a Terminology used to describe certain features of the oral ap- landmark (usually the mouth or jaw sheaths) and reserve abparatus (fig. 3.6) is confusing and sometimes inappropriate. oral (= opposite) and adoral (= same) for denoting the back The terms "mouth" and "oral" have multiple usages, and and face of the oral disc, respectively. Orientation of the oral clarification is required to avoid confusion and apparent disc relative to the longitudinal axis of the tadpole varies contradictions. Anatomically, "mouth" refers specifically to among tadpoles and is-correlated with habitat- and feedthe opening that forms by the invagination of the stomo- ing mechanics; unfortunately, this variability complicates dedeum, anterior growth of the archenteron, and eventual rup- tailed descriptions. For example, the oral dlsc is positioned ture of the oropharyngeal membrane (Cusimano-Carollo (see fig. 12.1 and other examples in chap. 12) ventrally et al. 1962; Watanabe et al. 1984). The mouth provides ac- (about 180") in suctorial forms, anteroventrally (about 40") cess from the outside to the buccal or buccopharyngeal cav- in many tadpoles, terminally (90") in some carnivores and ity. Use of "mouth" to refer to the oral dlsc is incorrect, and some forms with reduced oral discs. and uvturned or umits use to refer to the buccal cavity is colloquial. We use belliform (more than 90") in certain surface feeders. As a "oral" as a general term to refer to the oral disc and its associ- result, the leading edge of the anterior labium may be anteated keratinized and soft structures that are situated adjacent rior (oral disc ventral), dorsal (oral dlsc terminal), or posteand external to the mouth. Collective terms for these struc- rior (oral disc umbelliform); and the trailing edge of the tures are oral apparatus and mouthparts. Restricting usage lower labium would be posterior, ventral, and anterior, reto these definitions means that papdlae on the oral dlsc exter- spectively. In addition, a tadpole can attain many positions nal to the mouth have incorrectly been called buccal (Cei in the water. Understanding " the orientation of the oral disc 1980) or peribuccal (Lamotte and Lescure 1989) papillae. is an essential component of what we consider to be a satisL~kewise,papillae on the roof and floor of the buccal cavity factory tadpole description and essential to interpreting data confusingly have been called oral papdlae (Wassersug 1980). from other studies (e.g., feeding studies). To facilitate comIn the latter case we recommend that "buccal" or "buccopha- parisons and refer to the location of structures of the oral ryngeal" are more appropriate terms to refer to those pa- dlsc without appearing contradictory, and certainly confuspillae and other structures on the roof and floor of the ing, we have adopted an unspoken convention of &dung buccopharynx. of the oral disc as if it were a published figure in face view The infrequently used terms "aboral" (opposite, away, or with anterior (= dorsal, upper) at the top and posterior (= distal from the mouth) and "adoral" (same, toward, or prox- ventral, lower) at the bottom, regardless of the actual locaimal to the mouth) can be interpreted in several ways. For tion of the dlsc on the tadpole or of the position of the tadpole in the water. We strongly recommend that the term "denticle" be forever struck from the tadpole lexicon because of confusion "2 A-2 GAP resulting from its multiple usages for different structures of tadpoles and other organisms as well: labial teeth (e.g., Inger 1983), cusps on labial teeth (e.g., Faier 1972), serrations on jaw sheaths (e.g., Ruibal and Thomas 1988; M. H. Wake 1993a), and other small pointed structures. The preferred term is labial teeth and their structure and form'ation are much more complicated than the simple structure implied by "denticle" (e.g., Altig 1970; Boulenger 1892). By extension. the serrations on the head of an individual labial tooth are termed "cusps." Because a consistent terminology decreases the likelihood of confusion, and when coupled with long-term usage provides stabhty and understanding, a unique terminology (e.g., Van Dijk 1966) seems unwar'P-3 ranted or is premature pending better understandmg of the OD EMARGINATE NOT EMARGINATE distribution of morphological traits and their homology. The jaws cartilages of tadpoles (chap. 4) are without basal Fig.3.6. Oral apparatus of a tadpole showing emarginate (&side) articulation and significant adult derivatives and thereby and not emarginate (lightside) conditions of an oral disc. Abbreviadiffer from those of all other vertebrates. The sheaths that nons for descriptive terminology: AL = anterior (upper) labium; A-l overlie the cartilaginous jaws of tadpoles are transitory and and A-2 = first and second anterior (upper) tooth rows; A-2 GAP = have a columnar histological structure dtfferent from that of medial gap in second anterior tooth row; LJ = lower jaw sheath; similarly keratinized structures in birds, turtles, and some LP = lateral process of upper jaw sheath; M = mouth; M P = marsalamander larvae. In contrast. the beaks of other vertebrates ginal papilla; OD = oral disc; PL = posterior (lower) labium; P-l, (e.g., turtles and birds) are a&t structures that overlie basP-2, and P-3= first, second, and third posterior (lower) tooth rows; SJI = submarginal papilla; and UJ = upper jaw sheath. ally articulating jaws comprised of dermal bone. Because the
Morphology and Ontogeny: Oral Apparatus
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RONALD ALTIG AND ROY W. McDIARMID
sheaths that cover the jaws of tadpoles and the keratinized shape, as seen in tadpoles ofMegophvys. In tadpoles of the coverings (= rhamphotheca) of the jaws of other animals hylid Scarthyla ( D u e h a n and De Sa 1988) and members of surely are not homologs, we believe they warrant a distinct the Scinm ccowata group (e.g., McDiarmid and Altig 1990), term and recommend "jaw sheath." The so called jaw sheaths the exceptionally short P-3 lies at the end of an armlike modfound in certain salamander larvae (e.g., Ambystoma and Si- ification of the medal part of the posterior labium that rests ren) have not been examined hstologically, but they appear in a gap in the ventral papillae. The lower labium commonly to differ structurally from either of the previous two cases; is larger than the upper labium and more of its area is free although they overlie dermal bones, the specific bones in- from the body wall. Tadpoles of species with many tooth volved are not entirely the same in larval salamanders as in rows have larger oral discs than those with fewer rows. The other taxa. Also, the jaw sheaths of anuran larvae typically lower labium particularly may extend a considerabledstance are not pointed and do not project, as is implied by the usual posterior to the last tooth row in some tadpoles (e.g., some connotation of beak. Finally, the term "beak" has been used Ansonia, some Litoria, and Stauois). The labia consist of to denote the prominent medal convex projection of the loose connective tissue covered with an epidermis of varied margin of the upper jaw sheath of certain carnivorous tad- thtckness. Although the disc is more rigid in lotic than in poles; this usage adds addtional confusion, and we recom- lentic forms, the structural modifications that contribute to mend incised as more appropriate descriptive terms for this these differences in rigidity have not been determined. Aljaw sheath morphology. though the cores of papdlae and bases of tooth ridges someThe conventional use of length to refer to the longer and times are pigmented, the face of the d s c usually lacks pig-, usually longitudinal dimensions of a structure poses a con- ment, and mucous glands are absent. An inverted U-shaped flict when describing jaw sheaths because their greatest di- depression or transverse slit commonly, perhaps always, ocmension is transverse. For convenience we retain length for curs within the medial gap of the anterior tooth row adjacent the transverse measurement. This dunension is usually mea- to the upper jaw sheath. Neither the function nor developsured or described without considering curvature because it ment of this structure has been studied, and its occurrence is the only measure that can be obtained without dissection. in those species with a complete proximal, upper row is Jaw length as appropriate for a mammal (= gape, the basal not known. Most commonly the oral disc has all but its anterior marterminus of the jaw sheath in a straight line to the peak of the front curvature) has never been suggested as a measure- gin free from the body wall. In tadpoles with a dorsal gap in ment for a tadpole, again perhaps because it could not be the marginal papillae, the upper labium essentially is a conmeasured on an intact specimen and because the jaw carti- tinuation of the snout; in species with complete marginal lages do not articulate basally. By retaining length for the papdlae (e.g., suctorial forms) the entire margin is free. In longest but transverse dunension and width for the shorter, some rheophilous Litoria from the Australopapuan region, longitudinal dimension, jaw sheaths may be described and the snout and anterior margin of the oral disc are separated measured as follows: long/short (transverse measurement), by a crevice that appears to be covered by a thin membrane widelnarrow (basal boundary of keratinization to serrated (personal observation). The function of this morphology is edge), and thicwthin (front, oral or adoral to back, buccal unknown but surely it signals a novel structure in streamor aboral surface). Thickness has not been examined in dwelling pelodryadine tadpoles as compared to streamdwelling tadpoles of neotropical hylids. The back of the free many tadpoles. The jaw sheath is only the keratinized part of the jaw portion of the oral disc, which is primarily in the lower lacovering and is usually pigmented. Descriptions should be bium, is typically smooth. In tadpoles of Ceratupblys, this based only on the sheath and should not include jaw and surface is often fluted. associated soft tissues. In those rare cases where the sheath An umbelliform or upturned oral disc appears as a conis not pigmented (e.g., Scaphiophlyne), determining the lim- vergent trait in tadpoles of some arthroleptids, dendrobatits of the sheath is diicult. If the excised jaws of tadpoles ids, hylids, mantelline rhacophorids, megophryids, and miare placed in water, the jaw sheaths will detach (soon if speci- crohyline microhylids (fig. 9.5). Most umbelliform tadpoles men not preserved, several days for preserved specimens) occur in the backwaters of lotic systems. Tooth rows and jaw from their underlying cartilages, thereby facilitating de- sheaths are reduced to absent in these forms, and large tailed observations. ridgelike papillae that project radially from the mouth are common. When present, marginal papillae are complete but Oral Disc and P a p i l h greatly reduced in size. Morphological comparisons among The oral disc of a typical tadpole is round to transversely umbelliform tadpoles have not been made, but cursory elliptical. The poorly delimited upper (anterior) and lower examinations show that both labia or primarily the lower (posterior) labia of a M y formed d s c in nonsuctorial tad- labium form most of the disc. The bi-triangular disc o f M g poles are delineated by a fold that during closure (as usually ophvys is the most bizarre; when the tadpole submerges, the occurs in preserved specimens) develops along a line that lateral, pointed flaps of the oral disc by their own elasticity approximates the angles of the jaw cartilages. The degree to fold medally; when the tadpole rises to the surface to feed, whch parts of the upper and lower labia contribute to the the flaps unfold to form a bi-triangular oral d s c with the entire disc determines the disc shape. For example, enlarge- longer dimension oriented transversely. Even though funcment of lateral portions of the disc produce a bi-triangular tions other than feeding have been suggested for an umbelli-
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form disc (e.g., stabilization among vegetation, float, etc.), observations on certain forms suggest to us that feedmg on materials caught in the surface meniscus seems to be the most likely functional explanation for all umbelliform discs. The umbelliform disc tadpole of Mimhyla heymonsi has a large, infolded semicircular structure at each corner of the mouth that appears derived from the lower labium. The oral disc of some suctorial tad~olesdoes not fold shut, even in preserved specimens, and the discs of rheophllous forms commonly have lateral pleats (see emarginate below). These pleats presumably permit the seal between the disc and substrate to be maintained whde the disc margin " is expanding during the extension-retraction cycles of oral locomotion (C. L. Taylor and Altig 1995). Other folds and specimens, primarily flexures commonly seen in along the disc margin, are caused by differential contractions of muscles and different types of connective tissues and may not occur in living tadpoles. Emarginations, which are marginal indentations and not simply folds of a uniform margin, occur at various sites on the oral d s c (fig. 3.6). Lateral emarginations are the most common (e.g., most Bufi and Rana) but emarginations may occur dorsally, ventrally, and or ventrolaterally. The dsc often must be opened to distinguish an emargination from a pleat or fold. Margins of the labia usually are defined by papillae that vary in density (number/dstance), basal diameter, length, orientation, pigmentation, and shape (pointed vs. rounded tip). These marginal papillae occur in four basic patterns on the disc: complete (no gap), dorsal gap only (taxonomically and ecologically common), ventral gap only (rare), and dorsal and ventral gaps (most bufonids and a few hylids, mantellines, ranids, and rhacophorids). The condition of complete marginal papillae is most common in tadpoles that attach to rocky surfaces in fast-moving streams; it occurs uncommonly in a few nonrheophllous forms (e.g., Anotheca). The closely spaced, short, and numerous papillae presumably aid in forming a tight seal between the oral disc and the irregularities of the substrate. Van Dijk (1981) suggested that the ventral gap in the marginal papillae of bufonid tadpoles serves as a weirlike c o n t r o h g device during feeding. Other explanations to account for gaps in marginal papillae have not been offered, but a large phylogenetic component seems obvious. In some species, the size of the ventral gap is associated with the length of the adjacent tooth row, but notions that these patterns may be developmentally linked have not been pursued. We have noted obvious aualitative differences in the size (e.g., smaller in hylids than ;anids) and density of marginal papillae among tadpoles but have found few published notices (e.g., I. Griffiths and De Carvalho 1965) of this variation. ~Cnerallythe marginal papillae are relatively similar in size around the oral disc, but some ventral papillae may be greatly elongated (e.g., in Hemisus, some Phlynobatrmhus, and some Rana). Elongate ventral papillae are rarely bifid (Charming 1978), and Van Dijk (1966) noted that the length of the long ventral papillae in Phlynobatrmhus may decr ase ontogenetically.Marginal papillae typically occur in
'%
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one (uniserial) row but dscs bordered by two (biserial) or several (multiserial) rows are not uncommon. Sometimes the bases of ventral paplllae are slightly offset toward the back of the labium. The paplllae forming a single (uniserial) row are properly aligned, but those that occur in two or more rows have their bases slightly offset and appear double, or the bases are in one series but alternate papillae project in different directions (also emulating a doubl; row): ~ h e s e alternative patterns seemingly represent different solutions to the same problem and for clarity and understanding, they should be ex~lainedin descri~tions. Submarginal papillae, which occur on the face of the disc and sometimes grade centripetally from the marginal papillae, vary in density, distribution, shape, and size. The bases of submarginal ~ a ~ i l l usuallv ae are Sircular but sometimes " (e.g., Njctimystes ahyi, Phasmahylaguttata, and several umbelliform types) are elongate in a longitudinal or radial direction; S. J. Richards (1992) suggested that these types of papillae may be secretory. A patch of submarginal papillae commonly occurs near the lateral ends of the lower tooth rows, particularly in lotic tadpoles, and single rows of widely spaced, large papillae may occur dstal to the first upper and last lower tooth rows in other forms. Some species of Cardi&ma and Hyalinobatrmhium euqv~nathahave a row of paiillae that crosses the ~roxirnalface of the lower labium &d is continuous with the lateral marginal papillae. In these situations, papillae lie in front of the recessed jaw sheaths. It is tempting to speculate that these papillae may be a vestige of a tooth ridge(s). The oral disc and its presumed derivatives are reduced in various ways in tadpoles in several different lineages (e.g., some species groups of neotropical hylids, microhylids in general, pipids, and a few ranids) and feeding modes (see fig. 12.2). Some tadpoles have few (e.g., Hyla mamzorata group) to no (e.g., leucuphylluta, miwocephala, and parpiceps groups of Hylu spp., Occiduzy~asp.) labial teeth but have normal or unusual (e.g., Otophrynepyburni) jaw sheaths. In these forms, the oral dsc is reduced to differing degrees, typically to a U-shaped yoke around the mouth, and the marginal papillae appear as slightly differentiated mounds or are absent. The iaw sheaths. which sometimes are massive for the size of the tadpole, often are deeply recessed. During feeding, the snout is deformed and the jaws protruded to bring the sheaths in contact with the substrate. This configuration presumably is what prompted Lavilla (1990; Hylu nana) to describe what he called an "oral tube" that was visible only during feeding. The report (I. Grifiths 1963) of minute keratinized "denticles" in the oral amaratus ofPseudhymenochirus needs verification. A few tadpoles other than microhylids, pipids, and rhinophry~lldslack both labial teeth and at least keratinized jaw sheaths. Tadpoles of Litoria subglandulosa (Tyler and Anstis 1975) have complete marginal papillae, abundant papillae over the face of the disc, and small, unpigmented jaw sheaths. Six large papillae occur in a transverse row above, and a flat, white structure lies between the papillae adjacent to the midline. The tip of this structure is divided into 4-7 toothhke structures, each bearing 1 4 black, hairlike filaI
I
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ments, some of which are branched. Below k s structure there are 2-6 papillae with lightly keratinized tips. Our unpublished data show some surprising similarities between the mouthparts of the tadpole of Mantida~tylussguttulatus ( m a n t e h e rhacophorid; jaw sheaths absent) and those of L. subglandulosa. kn unidentified Boophis has an immense oral d s c that lacks keratinized structures and consumes exclusively clean-looking pieces of sand. spehes without keratinized mouthparts often have different or unusual soft structures. The paired, semicircular labial flaps of many microhylids presumably are homologs of the upper labium of a typical oral dsc. These labial flaps, with or without papillate edges, are suspended in front of the mouth and separated by an inverted U-shaped medal notch (see Donnelly et al. 1990a for review). The flaps may be strongly semicircular, short and essentially without the medal notch (i.e., upper lip is transversely straight), excessively long and almost rectangular, or reduced to small protuberances around an extremely wide medial notch. A few microhylid tadpoles (e.g., NelsolMphlyne from the New World and some Mzcrohyla and Scaphtophlyne from the Old World) have other structures that may be derived from the upper, lower, or both labia (Donnelly et al. 1990a). The unconventional microhylid tadpoles of Nelsonophyne (microhyline) and ~cupbzophlyne(icaphiophrynine with nonpigmented jaw sheaths) have oral discs with papillae. Except for vestigial structures that presumably are derived from typical jaw sheaths, the macrophagous carnivorous tadpole of Lepidoba~rmhwhas an immense, slit-shaped mouth and no other mouthparts. The su~erficialsirnilaritv of the soft mouth~artsof rhinophrynids and pipids diminishes upon closer examination. Both Rhil~phlynusand &nopus have slight folds at the corners of the mouth that may represent vestiges of an oral disc (Orton 1943; Thibaudeau and Altig 1988), but the barbels of the two tadpoles are not homologous (Cannatella and Trueb 1988a). The single long barbel at each corner of the mouth of Xihoiws has muscle-fibers attached to an internal cartilaginous support and is mobile. The shorter and more numerous barbels in tadpoles of RhilMphlynus lack these characteristics; they also seemingly vary in number and length ontogenetically and certainly between cohorts at one site and between sites. Tadpoles ofRhinophynw also have a at the symphisis of the lower single papilla-like jaw cartilages that probably is not a barbel. L
Tooth Ridges and Labial Teeth Transversely arranged tooth ridges form on the face of the oral d s c during early ontogeny (Thibaudeau and Altig 1988: see Cherdantseva and Cherdantsev 1995). The number, length, position, shape (curved vs. straight), and spacing of these ridges on the disc vary interspecifically and ontogenetically. Darkly keratinized labial teeth that develop from mitotic sites in-the tooth ridge are arranged linearliin one or more rows along the ridge. The tooth ridges of pond tadpoles are tall and have narrow bases and wide interridge valleys that are situated about equidstant between ridges; the ridges are quite flexible, and teeth generally can be removed
Fig. 3.7. Representative photomicrographs of labial teeth and jaw sheath of various tadpoles. (A) Multiserial tooth row (A-1) and biserial tooth rows (A-2 and A-3) inhcaphw w e t (Ascaphidae). (B) Tooth series in an intact tooth row of H y h chysoscelis (Hylidae). (C) Cross section (viewed with polarized light) of two posterior tooth rows (mouth a t bottom) of Hyhgratiasa (Hylidae) showing two tooth series (black structures), each surrounded by patches of connective tissue @ale areas) within the tooth ridge (P-2 and P-1) and with mitotic (toothforming) cells (dark areas) near their bases; slips of the mandibulolabialis muscle (pale structures) also visible (her&). (D) Labial teeth in nonnormal hillocks of tissue and on marginal papillae on oral disc of Scaphiopusholbrookii (Pelobatidae). (E) Lateral view of tooth series of about 15 teeth (series dissected from posterior tooth ridge, erupted tooth to h e r right) ofRrcaphtrs tmzi showing lengthy extensions of anterior base of each tooth sheath with associated connective tissue (white in polarized light). (F) Part of a posterior tooth row ofkcpphus twei (distalperspective, mouth to @ht) showing extensive connective tissue (white in polarized light) in tooth ridge. (G) P-2 and P-3 tooth rows of Hylagratwsa (Hylidae) showing (proximdperspective) fibers of the mandibulolabialis inferior muscle (white in polarized light) inserting on tooth ridges and marginal papillae lateral to tooth rows. (H) Serrations on jaw sheath (buccalsuYfke to left) of Ram catesbeianu (Ramdae). (I) Lateral view of five labial teeth (distal suYfke or bad to r2ht) from last posterior (multiserial) row ofhcaphw tmzi.
easily. Rheophilous and particularly suctorial forms have shorter, flat-topped ridges with narrow interridge valleys that lie immediately behind the next proximal ridge. I n all cases, the ridges become shorter and more closely spaced in the distal rows, and this is particularly pronounced 111species with many tooth rows. Judged by the dstribution of polarizing birefringence, the tooth ridge contains considerable connective tissue proximal and distal to a mitotic zone in the base of the tooth ridge that produces the labial teeth (figs. 3.7C, F). Although known for some time (e.g., Schulze 1892; Weber 1898), the extrinsic musculature of the oral d s c has not been well documented (e.g., Carr and Altig 1991; Gradwell 1968, 1972b, c; Noble 1929; Starrett 1973). Undoubtedly many unknown variations remain to be described, and several errors or omissions need to be clarified. Fibers of the m. mandbulolabialis (fig. 3.7G; see chap. 4) originate on the basal, ventrolateral surface of Meckel's cartilage. The m. mandibulolabiahs superior serves the upper labium, and the m.m. inferior serves the lower labium (Carr and Altig 1991; McDiarmid and Altig 1990). When present, fibers of the muscle insert at the bases of the lateral quarters of the valleys between tooth ridges and at the bases of marginal papillae lateral to the tooth rows. Fibers of the m. mandibulolabialis usually do not extend distal to the most distal tooth row in either labium, although they do so in some suctorial Litoria. Examination of 24 species (Carr and Altig 1991) demonstrated little ontogenetic but considerable interspecific variation in these muscles. Typically, slips of both muscles are present, but in some species only the m. m. inferior has been detected. Contractions of these muscles apparently change the shape particularly of the lateral portions of the oral d s c and of the tooth ridges. Distortion of the tooth ridges ~resumablvrotates the labial teeth dstallv and effects a better contact with the substrate. Although the sequence
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RONALD ALTIG A N D ROY W. M c D I A R M I D
and timing of these muscle contractions during a feedmg cycle are not clear, it seems that the muscles relax soon after maximum oral dsc excursion and as closure begins (C. L. Taylor et al. 1996). The m. intermandibularis posterior (Gradwell 1972b) also may aid in tooth reorientation. Gradwell (1968) noted that the m. mandibulolabiahs is innervated by the trigeminal nerve. We suspect that lymphatic spaces in and near the oral disc (chap. 5) also may function in the operation of some of the mouthparts. The number and arrangement of tooth rows on the oral disc of tadpoles is species specific. The labial tooth row formula (LTRF) is a synoptic representation of this arrangement. A number of systems have been devised for numbering labial tooth rows and designating the rows with medal gaps. Any system is clear to an experienced user, but many systems are not obvious to a neophyte. To us, less cumbersome schemes seem to be more useful. Dubois (1995) and Dubois and Ohler (1994) present the most recent variations. Accordingly, we continue-to use the fractional designation (e.g., Altig 1970) to spec@ the number and gross morphology of tooth row. Thls system accommodates all row configurations easily, does not use Roman numerals, has been used for quite a long time and is familiar to many workers, and takes less space than formulas that are written in spatial order. Rows on the anterior labium are numbered distal (labial margin) to proximal (mouth). The notation "A-1" denotes the first anterior (most dstal from mouth) row, and designations extended sequentially through A-n to the row adiacent to the mouth. Rows on the vosterior labium are numbered proximal to distal. The first row adjacent to the mouth is P-1, and more distal rows are numbered sequentially through P-n. Notations such as "PR-1" and "AR-1," denoting the tooth ridge for tooth row P-1 and A-1, can be extended for any anterior or posterior row if in developmental studies one wishes to refer to tooth ridges dstinct from tooth rows. Rows with medial gaps are-designated with parentheses, and rows that vary between individuals (gap present or absent) are placed w i t h brackets. A gap in a tooth row is a physical break in the tooth ridge and therefore expressed in the tooth row; teeth occur only on tooth ridges. Even apparent atavistic teeth are positioned on hillocks of tooth ridge tissue (see below and fig. 3.7D). If the gap is quite narrow, as it often is in row P-1, staining (see chap. 2) may be necessary to discern if the ridge in fact is broken. The absence of teeth on part (or all) of a tooth ridge should be noted, but these breaks do not constitute gaps as defined here. Also, sharp bends in tooth rows caused by flexures of the d s c in preservation are sometimes interpreted as gaps; one should open the oral disc manually to ver@ that a gap probably is not present in most of these cases. The functional and developmental considerations of gaps in tooth rows have not been examined. These gaps may allow larger excursions of the jaw sheaths during feeding; adjacent tooth rows that have only narrow or no gaps perhaps signal smaller jaw excursions during feeding. We assume that most gaps are neither gained nor lost ontogenetically w i t h rows and that in most cases gaps - - can be used to evaluate row homology.
In summary, a labial tooth row formula (LTRF) of 5(2-5)/3[1] indcates a tadpole with 5 upper tooth rows with medal gaps in rows A-2 through A-5 and 3 lower rows with or without a gap in P-1. An advantage is that this system apparently numbers homologous rows the same in different species and does so more often than other systems. In fact, no system will always number supposed homologs the same because of different patterns of ontogenetic and phylogenetic row alterations (Altig and Johnston 1989). Some tadpoles, particularly of species of ranids and pelobatids, have accessory tooth rows situated in the lateral areas of the oral dsc. The functional importance, developmental association, and homologous nature of these short rows compared to the more typical rows are not known. Two types of these accessory rows are distinguishable. In ranids, accessory rows essentially parallel the lateral ends of the posterior tooth rows; in pelobatids the rows tend to lie off the ends of and are oriented at nearly right angles to the posterior tooth rows. The formulation ofAltig (1970) was modified by R. G. Webb and Korky (1977) by placing the number of accessory rows between solid - 5 (2-5)/4/3 [l]. Other than notations concerning ontogenetic change, few data (e.g., Bragg and Bragg 1958) illustrate the natural variations in tooth formulas. Echeverria and Filipello (1994) found that 77.4% of the tadpoles Odontopbvnus occzdentalis had one formula and the remaining 22.6% had several other formulas. The most deformities (26.7%) were in A-1, while P-1 showed the least (6.7%). Grdhtsch and Grillitsch (1989) and C. L. Rowe et al. (l996,1998a, b) reported similar data on ranid tadpoles. Tadpoles of Phq~nohym,Tvachycephalus, and some species of the Hylageogvaphicu group share the uncommon feature of having A- 1 with a wide medan gap but with A-2 entire. In such cases, this row is probably not homologous with A- 1 (but A-2 is) of other tadpoles. Certain structures on the oral disc of tadpoles with reduced mouthparts may be nascent tooth ridges without teeth. Bresler (1954) showed that the incidence of abnormal tooth rows (and jaw sheaths) increased with temperature, but all tooth rows were not affected equally. Jaw sheaths seemed to be less affected than tooth rows. Bresler and Bragg (1954) reported variations in tooth rows of five species in five genera, including Spea bombzj?ons. It is interesting that variation in tooth rows appears to be greater among individuals and populations of species of Spea than for almost any other tadpoles. Perhaps this is a reflection of the relatively warm aquatic environment and shorter developmental period characteristic of these species, but a phylogenetic d u e n c e cannot be ruled out. A review of tooth row variability in other pelobatids and an experimental test of the effect of different rearing temperature on tooth row variability would provide some insight. It also is tempting to speculate that this variation somehow is tied to the drastic ontogenetic changes that occur in cannibal morphotypes of this group. Altig and Johnston (1989) proposed a balance value (i.e., the difference between the number of upper and lower tooth rows) to aid in understanding and comparing suspected functional Merences in tooth row formulas among species.
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They assumed that differences in balance values reflected Merences in feeding mode. A tadpole with more tooth rows on the upper labium than on the lower labium has a positive imbalance (e.g., LTRF of 513, BV = +2); one with more rows on the lower labium than the upper has a negative imbalance (213, BV = - 1); and one with equal number of rows on both labia is balanced (515, BV = 0). A balance value of - 1 in the formula 213 is by far the most common. The extremes are + 7 (1013, Bouphis sp.) and - 11 (4115,Heleuplnyne sp.), and not all intermedate values occur. The distribution of values shows that 88% of 627 species surveyed (51% had a LTRF of 213) had balance values between + 2 and -2. A tadpole with a strong negative imbalance (e.g., LTRF 4/15; BV = - 11) surely must use their labial teeth Merently than one with a strong positive value (LTRF 101 3; BV = +7). A comparison of foraging behavior and feeding efficiency among tadpoles with the same total number of tooth rows (e.g., 12) but Merent balance values (LTRFs of 418 vs. 616 vs. 814) would provide needed data. It is interesting that the tadpole with the largest number of tooth rows (LTRF 17/21; Hyla sp.) has a nearly balanced formula. Except for the pronounced ontogenetic changes characteristic of tadpoles of species with many tooth rows, the number and arrangement of labial tooth rows (LTRs) after about Gosner stages 25-26 are stable enough to be definitive of the species. A LTRF does not provide information about the position on or spacing between tooth rows on the face of the oral dsc. Row spacing has not been examined, perhaps because the flexible oral disc makes it dfficult to standardize the measurements, but dfferences apparently exist. An unidentified suctorial hylid tadpole from Papua New Guinea with a LTRF of 213 has an unusual arrangement of tooth rows on the lower labium; the space between P- 1and P-2 is over twice the distance between the other two rows. Large areas of the d s c in certain tadpoles (e.g., Duellmunubyla, some Tauductylus; species with large oral discs and short tooth rows situated close to the jaw sheaths) are without teeth. Tadpoles of some centrolenids (personal observation) and suctorial forms of Litoria and Staurois (Inger and Wassersug 1990) have a large expanse of oral d s c beyond the dstal posterior row. Although we have a poor appreciation of the nature of and limits to intraspecific variation, tadpole morphology at the generic level often is remarkably consistent. Interspecific variation in some taxa (e.g., most bufonids) is much less than in others (e.g., hylids, leptodactylids). Other than the cannibalistic morphotypes of Spea, true polymorphism, not just pronounced variation, is rare or poorly documented in tadpoles. Annandale (1917, 1918), Berry (1972), E. R. Dunn (1924), Khan and Mufti (1994), and M. A. Smith (1917) talked about notable dfferences within species, but the causes of the differences are unclear. I. Grfiths and De Carvalho (1965) used some of these cases as examples of dimorphisms that must be considered with caution when using larval features in systematic studes. Although the premise is valid, the underlying assumptions that the tadpoles were correctly identified and that the correct number of species was involved in all cases went unquestioned. Likewise,
41
M. Kaplan (1994) suggested that variations of labial tooth rows in Hyla mznuta prohibited the use of these features in phylogenetic studies; the problem here most certainly centers on the variation representing multiple species. A smattering of reports (e.g., Annandale 1917; Korky and Webb 1991; Lavilla 1984a, b; J. M. Savage 1960; M. A. Smith 1917) described apparent geographic variation in mouthparts, and a few others (Annandale 1917,1918; Berry 1972; Caldwell 1982; E. R Dunn 1924; Khan and Mufti 1994; M. A. Smith 1917) have documented notable examples of other types of morphological variation (e.g., coloration and pattern) within species. The paucity of data on both the nature of and limits to intraspecific variation raises questions about the reliabilitv , of some t a d ~ o l eidentdications. We hequently ask ourselves if observed differences are an indcation of geographic variation w i h a species or a reflection of dfferences between species. Tadpoles of s~eciesoi's~eaare notorious for having variable mLuthpartsLbeyondLose induced by cannibalis; ( q . , Bragg 1956; Bragg and Bragg; 1958; Bragg and Hayes 1963; Bresler and Bragg 1954; Hampton and Volpe 1963; Orton 1954; Potthoff and Lynch 1986). Yet, the relationship between a reported missing tooth row or patch of teeth and the presence of the underlying tooth ridge (see Bresler 1954') seldom has been explored. A missing " Goth row mav be the consequence of a missing tooth ridge (i.e., developmentally induced) or merely reflect the loss of teeth on the ridge (i.e., attributable to some postembryonic response). Too often, the condition is masked by an imprecise or incomplete description. If we are to make progress in understanding the nature of presumed geographic variation, this needs to be corrected! Although intraspecific variation is poorly documented, the morphology of closely related species often is remarkably consistent. We have suggested (e.g., chap. 12) that this consistency occasionally signals the need for taxonomic reevaluation. Exceptions to this generic uniformity are known; the dramatically Merent tadpoles of Litoria citrupa and L. sub&ndulosa (Tyler and Anstis 1975) and Hyla chlysoscelis and H. avivoca are examples. In some tadpoles with an exceptionally short P-3 row, such as Pseudacvis trisertertata and P s e u h s crucifer (Gosner and Black 1957a), the third row is frequently absent, and a gap of equal size in the marginal papillae below the expected position of P-3 may be present. A LTRF of 213 is typical in most members of the Ranapipiens group, but a LTRF of 3/ 3 is not uncommon; the occurrence of the unconventional formulas of 214 and 314 in Ram bevlandieri (Bresler and Bragg 1954) needs further study. Cannibal morphotypes of Spea have larger, differently shaped jaw sheaths and few to no teeth compared to the conspecific omnivorous morphs. Aberrant and dsplaced tooth rows are not uncommon; parts of rows may be absent, rows may merge at any point or connect laterallv. and teeth mav form small circles within a row. Gosner (1959) attributed these alterations to wear, but thls seems unlikely. Documentation of wear is not as common (e.g., Tubbs et al. 1993) as one might expect from structures that are being replaced continually. ~ e m ~ e r a t u r e , i'
RONALD ALTIG AND ROY W. McDIARMID
nutrition, disease, and the substrates on which the teeth act may contribute to aberrant patterns. Cultured tadpoles often have higher incidences of abnormal tooth rows (and in specific patterns; Grdlitsch and Grillitsch 1989), including a complete lack of keratinized structures, than field-collected specimens. Some taxa (e.g., Bu.) seem more likely to show such alterations than others (e.g., Rana). In 8 of 10 simultaneously field-collected specimens of Heleophryne purcelli aberrant teeth appear in the two proximal upper and three proximal lower rows. Apparently teeth were not shed as replacement teeth were produced, and the result was a remarkable array of long flexible strands of up to 40 teeth extendng above the surface of the tooth ridge at the site where a single tooth would normally be. This condition surely prevented the teeth from working properly, but the tadpoles appeared healthy. Interpretation of some kinds of anomalies may provide hypotheses about the formation, evolution, and functions of mouthparts. Each keratinized labial tooth (fig. 3.8) is derived from cells in the base of the tooth ridge and consists of three indistinct regions: a distal head, an intermediate body, and a basal, hollow sheath (Gosner 1959). A fracture plane in the body often is evident. At this point, the tooth head can break free of its body and expose the head of the next replacement tooth interdgitated in the sheath. The head of a tooth may be straight or variously curved and spoon-shaped (i.e., bluntly rounded and flattened; fig. 3.71), thin with a sharp point (noncusped), or of various shapes with 2-18 terminal cusps. Even though the head often is flattened front to back, the body is the reverse -wide in lateral view and narrow in anterior view. Strands of connective tissue anchor the hollow sheath of the tooth within the tooth ridge; attachment is most prominent at the front (proximal to the mouth) base of each tooth. In most teeth, the front and back bases of the sheath in cross section are of comparable shape, but in suctorial forms, the front base of the sheath often extends considerably toward the mouth. This extension protrudes (fig. 3.7E) into the tissue of the tooth ridge proximal to the row and presumably acts as a brace to keep the tooth series and row from folding backward. The imprint of the nucleus of the original cell can be seen in the wall of the sheath of a tooth cleared in potassium hydroxide. Tips of the labial teeth on both labia face the mouththat is, in opposite directions. Usually two to three f d y formed replacement teeth are successively interdigitated in the sheathof the p r e c e h g tooth below ;he erupted tooth. The amount and style of interdigitation appear to vary, but data are laclung. An erupted tooth and all its replacements are termed a tooth serieL(figs. 3.7B, E), and the population of tooth-forming cells is renewed continuously in a mitotic zone near the base of a tooth ridge (fig. 3.7C; Beaumont and DeunfT 1958; DeunfT and Beaumont 1959; Luckenbdl 1964,1965; Tachibana 1978). As the presumptive tooth cell moves toward the top of the tooth ridge, a replacement tooth slowly forms from the head toward the sheath. A tooth row comprises numerous tooth series aligned side by side within a tooth ridge. If the tissue of the tooth ridge is sufficiently transparent, the tooth series can be seen through
Fig. 3.8. Photomicrographs showing variations in labial teeth and their marks. (A) Short-cusped, moderately curved teeth ofMgaelosia Joeldii (Leptodactylidae). ( B ) Long-cusped, strongly curved teeth in single row/tooth ridge of Hyla bwbeba (Hylidae). (C) Cusped, relatively straight tooth (emw~entin upper left) and replacement series of Lepto+lus chagmnsis (Leptodactylidae). ( D )Noncusped (pointed), short-sheathedtooth of Spea bombcfions (Pelobatidae). ( E ) Negative cast of mark (uppwjawsheath entered on left) made on agar-based food by feeding tadpole of Rana sphenouphala (Ranidae). (F) Cusped, biserial teeth of Bombina van'gata (Bombinatoridae).From Altig and Johnston (1989);reprinted by permission ofHetpetologzcalMonogvaphs.
the tissue. What appears as a single long tooth with sequential light and dark areas are actually the replacement teeth stacked in a series. Sometimes an older tooth sticks to a newly erupted one and makes it appear longer than others in the row, and other times a tooth looks longer because of the dfficulty of interpreting the extent of the soft tissue of the tooth ridge on the shaft. However, closely adjacent teeth are comparable in size and shape. Tooth size may vary in different parts of a row or in dfferent rows (e.g., fig. 3.7A, I; Gosner 19-59), but the usual pattern is a gradual shlft to smaller size laterally within a row and dstally among rows. Smaller specimens have smaller teeth than larger specimens. Meager data suggest that rows increase in length without changing tooth density; where and in what pattern teeth are added remains a mystery. Most tadpoles have a single tooth row per ridge (= uniserial), but tadpoles with bi- (e.g., dscoglossids) and even tri- or multiserial (fig. 3.7A) rows are known. Tooth densities of 30-100/mm, with higher counts in lotic tadpoles, are typical, and the number of cusps range from 0 (simple spike) to at least 18. Biserial sections in typically uniserial rows are not uncommon. The teeth of Bombina orientalis are uniserial at first appearance but become biserial during development. Noble (1929) noted biserial tooth rows in Hopfobatrachw rttgufosus, but the text and adjoining figure leave doubt if these rows actually are biserial. Tadpoles ofXenopus lamis develop true calcified teeth precociously (J. E Shaw 1979). True teeth usually appear late in metamorphosis as the maxlllae and premaxillae ossify, but in X. laevts, tooth buds are present at about stage 33 and start to calcify at stage 37. True teeth begin to form at about stage 36 in tadpoles of Lepidobatrachw (Starrett 1973). Jaw Sheaths Jaw sheaths are formed by the fusion of palisades of keratinized cells along their lateral margins (Kaung 1975; Kaung and Kollros 1976). Sometimes iaw sheaths have a striated appearance to at least their basal parts. As the serrated edges of the jaw sheaths wear away or break off, mitotic cells in the base of the sheaths continually produce new cells that keratinue in transit to the dstal edge. Typically, jaw sheaths have a serrated edge, and the serrations vary in density, orientation (straight medially and angled laterally), presence (rarely absent, e.g., Osteopilusbrunneus group; Noble 1929), shape (broad-based and short vs. narrow-based and long), and sue. In a few cases, 1-3 enlarged serrations occur withtn
RONALD ALTIG AND ROY W. McDIARMID
44
a normal graded series on the upper (e.g., Plectrohyla ixil and
l? matudai) or both (e.g., Leptodactylodon ventrimamratus) sheaths. Individual serrations lackmg a common sheath occur as transitory structures (e.g., Visser 1985, some young Heleophyne) or for the duration of larval life (e.g., Cei 1980, Ruibal and Thomas 1988, Lepzdobatrachus; personal observation, Mantiaktylus lzgubris; Pyburn 1980, Wassersug and Pyburn 1987, Otophlyne). Jaw sheaths with 30-80 serrations/mm are typical, and higher counts are known in lotic forms. In a few cases (e.g., some Amlops and Boophis), serrations on the edges are only 5-8/mm. Among suctorial forms of some Boophis, the sheaths appear to be composed of a series of fused columns; the irregular surfaces of these sheaths are in stark contrast to the smooth surfaces of typical forms. Some Amlops (Ranidae), Ansonia (Bufonidae), and Litoria (Hylidae) have one or both jaw sheaths divided medally; the functional significance of such arrangements is unknown. A comment bv Menzies and Zweifel(1974) that older specimens of a species of Litoria with broken sheaths have a single sheath suggests ontogenetic changes, but this needs to be examined more closelv. The umer and lower sheaths are usually similar in si7~,but the U-shaped lower sheath ofRrcaphus is minute relative to the large, flattened, upper sheath. Tadpoles of Heleophryne lack one (upper) or both sheaths, and the upper one is absent in an unidentified tadpole of Boophis (personal observation). As with tooth rows and ridges discussed above, the apparent absence of jaw sheaths must be evaluated carefully. Absence of pigmentation does not corroborate the lack of keratinization (e.g., Scaphiophlyne), so a judgment of absence should be based on an actual lack of a sheath on the labial cartilages. " Taw sheaths usually co-occur with labial teeth but may occur alone (e.g., hylid: Hyla leucophyllata group; ranid: Occidozyja; microhylid: Scaphiophlyne). Rarely do tadpoles have labial teeth and no jaw sheaths (e.g., some ~deophlyne).The upper sheath of some suctorial forms may be M-shaped, and some species (e.g., Hylapiccipes) appear to have a scouring surface iust ~roximalto the on the front face of the umer sheath , serrated edge. Based on the various accounts, the structures of the upper sheath of Hoplobatrachzts tigerinus (surely confusion exists in dstinguishing between the tadpoles of Hoplobatrmhus tigerinus and Hoplobatrachus rttgulosus) apparently are unique, although it cannot be determined whether one or two features are involved. Khan and Mufti (1994:28) stated that there is "A pair of long cylindrical thick papillae, tipped with keratinized plates . . . at the angles of the mouth opening. . . ." These structures, perhaps keratinized buccal papilla< do not appear associatedwiththe upper jaw sheath. Kirtisinghe (1957) illustrated the lateral margins of the upper sheath with convexities but made no mention of them in the text. Khan and Mufti (1994) also noted that a ". . . median-buccal keratinized shikld is'observable through the mouth." This structure must be similar to the keratinized boss on the roof of the buccal cavity of Spea and some Hyla. Various iaw sheaths are included in fig. 3.9. shapds of jaw sheaths are difficultyo describe because of their complex curved shapes. The curved jaw sheaths and trajectory of the cutting edge vary tremendously among taxa, L L
L L
L
but neither have been described well. Wide infra- or suprarostral cartilages accompanied by narrow keratinized sheaths occur, and the difference between this situation and one where narrow sheaths cover most or all of the cartilages needs to be qualified. To visuahze jaw sheath shapes better, imagine a rectangular piece of paper with the opposite short ends placed on a table so that the paper forms an arch that represents the typical smooth arc of the upper jaw sheath. The same concepts pertain to the lower sheath, although it is more difficult to simulate because the sheath is most often V-shaped. With proper pressures on and repositioning of the ends, the paper can be fashioned into various uniform (e.g., tall and narrow vs. short and wide) or nonudorm (e.g., less curvature in medial section) arches that effectively illustrate the known variations in the shapes of jaw sheaths. The facing edge, which equals the serrated edge of the sheath, can be cut to form various uniform or nonuniform (e.g., incised sheath with a medial convexity) borders. Also, various (uniform and nonuniform) serrations that usually grade from the largest medally to the smallest laterally can be cut into the facing edge. The ends of the arch can be modified in shape and lateral flexure to form the indstinctly differentiated lateral processes. Last, the roof (= front, oral, or adoral surface of sheath) and ceiling (= rear, back, aboral, or buccal surface of sheath) of the arch could be nearly flat and parallel, similar to the paper, or could curve to various degrees. The line of keratinization on the front face of the upper sheath typically describes a smooth, either abrupt or graded, arc, but the line of dark keratinization on the buccal face of the upper sheath often takes various shapes (Altig and Johnston 1989) with graded or abrupt margins. The lower sheath passes inside the upper sheath during a feeding stroke, and through scissorlike interactions serrations on the two sheaths cut or gouge surfaces for food removal. The degree of keratinization varies from weak (yellow to light brown) to strong (dense black); other than color differences, there is no system for even subjective evaluation of these differences. The cause or functional significance of light keratinization in sheaths that normally are heavily keratinized is unknown. Structures with melanic pigment are stronger than those that lack h s pigment, but the strength and resistance to wear of sheaths that differ in degrees of keratinization have not been evaluated. Because of the way jaw cartilages articulate with their supportive structures, jaw sheaths are oriented and operate at several angles. A wide variety of sheath shapes can be seen in buccal view in Wassersug and Heyer (1988). Other keratinized structures are associated with the oral d s c and buccal cavity. A rounded, heavlly keratinized boss occurs on the ceiling of the buccal cavity just posterior to the buccal base of the upper jaw sheath in tadpoles of Spea. Tadpoles of Kassina sengalensis, T~chobatrachusrobustus, and several members of the Ranapipiens group, mostly with robust lower jaw sheaths, commonly have areas of thin keratinization lateral to the oral face of the lower jaw sheath. Although unclear, a comment by Annandale and Rao (1918) suggested a unique feature of the tadpole of Euphlyctis hexadactylus: "There is a deep groove, with its sides and base
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BODY PLAN
Fig. 3.11. Photomicrographsshowing development of the oral apparaars in three tadpol~es.Top: Hyh s a y d (Hylidae), a tadpole with jrw sheaths, reduced oral disc, and no labial teeth. (A) Jaw sheath visiblc, mvginapapillae starthg to appear, Gosna 24. (B) Distinct seratioason jaw sheaths and marginal papillae arc obvious, Gosna 25. W: G&qhtync & d (Mimhylidae),a tadpole with oral Saps and no keratinized mouthparts. (C) Oral disc relatively un&a&ad, conical adhesive gland visible in lowa lefi coma, Gosna 24. @) Labial flaps beghmng to difkentiate, lower jaw (= idkhbial pornincnce) visible as rounded projection in notch between labial
flaps, Gosna 25. Bottom: R b i ~ d o ~ a J(Rhinophrynidae), j s a tadwle without keratinized mouthparts. (E)Oral disc u n e n t i a&, without jaw sheaths or &, line& tranmrse adhesive gland visible below mouth, nares visible dorsal to mouth and still plugged with cdls,Gosna 22. (F) Barbels bcghnq to differentiate around slitlike mouth, floor of the buccal cavity d i d y inside mouth visible becaw of slight downward flexure of lower jaw, medial papilla on lowa jaw visible, Gosner 25. From Thibaudeau and Altig (1988), copyright 0 1988, Wdey-Liss, Inc., a subsidiary of John Wiley & Sons,Inc.; qrinted by permission.
48
RONALD ALTIG AND ROY W. McDIARMID
somewhat later in ontogeny compared with more typical tadpoles. Heyer (1985, Hyalinobatrachium uranoscopa) and Inger (1966, Leptolalux gracilis) noted cases where tooth rows are lost and the tooth ridges seemingly are transformed into a series of papillae. Some data (Altig and Johnston 1989) suggest several patterns of tooth row appearance once a formula of 213 (see above) has developed. Some tadpoles add rows proximally to the rows of the 213 formula on the anterior labium and-distallvon the lower labium. Others add rows distally on both labia: Teeth first appear near the medal parts of tooth ridges and then laterally. The sequence of tooth row appearance among ridges is the same as that for ridge formation. Hemispherical bulges in the epithelium can be seen where teeth are forming underneath, and the first teeth that appear may have a dfferent form than subsequent ones (Thibaudeau and Altig 1988; Tubbs et al. 1993). From their first appearance and throughout tadpole ontogeny, as labial teeth are lost after wear or breakage, replacement teeth are continually formed from mitotic zones in the bases of the tooth ridges (e.g., Luckenbill 1964, 1965; Kaung and Kollros 1976). In most tadpoles, several replacement teeth are interdigitated in a series (figs. 3.6B, E); in a few cases replacement teeth apparently are absent (e.g., dstalrnost rows in Ascupbus). Atrophy of the oral apparatus has not been well studied, but apparently it occurs in the approximate reverse order of ontogeny and more haphazardly. Presumably, mitoses that produce teeth cease and the last teeth are lost in patches. It is not known if a Dattern to tooth loss within rows exists. The initiation, duration, and perhaps pattern of metamorphic atrophy varies among taxa and ecological types. For example, row P-3 (LTRF of 213) is the first to dsappear, and A - i usuallv is the last. Taw sheaths are lost after or most tooth row;. ventrolatek marginal papillae are the last structures on the oral disc to atrophy.
Functional and Evolutionary Aspects of Tadpole Morphology Too often we have indicated the paucity of information regarding the functional or evolutionary aspects of various larval structures; although bothersome, this reflects the inadequacies of our knowledge. Morphological features and their dstributions among taxa are stdl being described, and often we have relatively little information on the development of such features and less on their functions. Until more of these holes in our knowledge are Ned, probing discussions on the evolution of morphological structures in tadpoles will remain speculative. Body Motpbology Exemplified by the hypotheses on ecomorphological guilds proposed by Altig and Johnston (1989), further observations suggest strong correlations among the following traits: behavior, body and fin configurations, ecology, metamorphic pattern (e.g., Nodzenski et al. 1989), and taxonomic position. Seven generalizations abstracted from Altig and Johnston's (1989) guild hypotheses involve associations
among features of the body, eyes, fins, tail muscle, and mouthparts. (1) Lentic forms have less massive tail muscles than lo& forms, and the smallest muscles are associated with the largest fins. (2) Benthic forms have depressed bodes, dorsal eyes, and low fins whether in lentic or lotic environments. (3) Lentic (pond), nektonic (rarely lotic) forms have compressed (e.g., many hylids), depressed (e.g., microhylids and pipids, sometimes with a tail flagellum), or equidimensional (e.g., macrophagous feeders with jaw sheaths but lacking labial teeth, some Hyla, often with a tail flagellum) bodies and live in different parts of the water column. (4) Burrowers (e.g., centrolenids) and those tadpoles that live in confined spaces (e.g., bromeliad cisterns; Hyla bromeliacia, H. dendrosma) are vermiform with depressed bodies, dorsal eyes, and low fins. (5) Semiterrestrial tadpoles have elongate bodies, narrow tail muscles with abbreviated fins, large eyes that bulge above the surrounding body surface, and hmd legs that develop precociously (Drewes et al. 1989). (6) TadDoles that live in slower reaches of streams resemble lenticbenthic forms except for a typical increase in the number of tooth rows; ranids make up a large component of this assemblage, and the number of upper tooth rows is often larger than the lower. (7) Lotic forms that use the oral dsc to maintain position and feed in fast-moving water have complete marginal papillae and frequently have more tooth rows and higher tooth density; larger numbers of tooth rows presumably signal faster water habitats. The largest LTRF .of 17/21 is from an unidentified Hyla from a high-energy stream in Venezuela. In these tad~olesthe fins are low and the eves are dorsal. There probably are two poorly understood patterns of streamlining. Almost no data (see Gradwell 1971a, 1973,1975b) exist on the actual functional proficiency of the basic morphological categories described above. The functions of other features (e.g., vent flaps, dextral vs. medial vent tubes and their many variations, tubular nares, naris size, and long, free spir a d a r tubes) have not been suggested or are seldom supportable by data. Based on obse~ationsof where tadpoles occur in the water column (e.g., Alford 1986b; S. L. Mitchell 1983: see Abelson et al. 1993 and Lancaster and Hildrew 1993) and their swimming abilities, associations between tail fin shapes and tail muscle configurations surely signal different ca~abilities.Unfortunatelv. ,' the data on the swimming kinematics of tadpoles pertain only to a few species of lentic tadpoles (e.g., Hoff and Wassersug 1985, 1986; Wassersug 1989a; Wassersug and Hoff 1985). \
,
Oral Morphology The functional roles that have been proposed for oral papillae fall into two basic categories: chemosensory and tactile receptors and structures that control water flow (Van Dijk 1981), enhance attachment to substrates (Altig and Brodie 1972; Gradwell 1971a, 1975b), mod@ the shape of the oral disc during feeding, and manipulate food and substrate particles. As is usually the case, few data are available. The size and density of oral papillae in many cases seem to reflect lineages and habitats. For example, ranid tadpoles have larger papillae arranged more sparsely than hylids, and stream hy-
BODY PLAN
lids have smaller, more densely arranged papillae than pond h!lids. The number and prominence of marginal papillae \=aria concordantly with observed reductions in the size of d x oral disc among tadpoles w i h n the same lineage. A comprehensive survey of labial tooth structure has not been made, and the few descriptions that have been published vary in many details (e.g., Altig 1973; Altig and Pace 1974; Faier 1972; Gosner 1959; Heron-Royer and Van Bambeke 1889; Hosoi et al. 1995; Inger 1983; Korky and Webb 1994; R. J. Nichols 1937). Little can be said about functional diierences in tooth morphologies (e.g., Altig and Johnston 1989; Faier 1972; Gosner 1959; Inger 1983). Some suggested functions include acting as a broom, serving zs a current generator, breaking up mucilaginous layers, sieving pamcles, combing strands into alignment for easier cutting (Altig and Johnston 1989), piercing plant cells, rasping hd particles from a substrate (R. M. Savage 1952), holding food (Luckenbill 1965), attachmg to a substrate (Altig md Brodie 1972; Gradwell 1975a, b), and trapping food iT:-Ier 1963). Few data exist to support any of these suggesdons, and the immense variations remain enigmatic. Mertrns (1960) and Nachtigall(1974) compared the morpholoejes of tadpole teeth to those of structures in other groups ;bar presumably serve similar functions. Publications that m u a s t tadpole teeth to the snail radulae (e.g., Steneck and mahg 1982) provide other pertinent examples. Likewise, only a few workers (e.g., Altig and Johnston 1%9) have attempted to place the sizes, shapes, and serration patterns (e.g., fig. 3.6H) ofjaw sheaths into a functional mm.Even though the upper and lower jaw sheaths in a tl~picaltadpole are similar in size and probably serve as gougiug'bitingjscraping structures, their striking differences in dupe and the extensive array of morphologies across taxa qgat an innumerable variety of performance abilities. The immense, flattened upper sheath ofAscaphus is unique and must shave periphyton from various substrates during the mraaion phase of the oral dsc: the small lower sheath is @ably inconsequential. The robust, narrowly arched jaw s&arfis (i.e., short surface for actual biting) of semiterrestrial n l p o l a presumably provide strength and may be essential Q feedmg on tough materials or unusual substrates characd c of these thin (water film) habitats. E-xcept in the most general sense, the functional morpholog-of the oral apparatus of tadpoles is largely unknown. Enensive work has focused on the structural components d functional design of the food-trapping mechanisms in rbc buccopharyngeal area (e.g., Kenny 1969b, c; R. M. Savq c 1955; Viertel 1984a, c, 1987; Wassersug 1972, 1980; V k s m u g and Heyer 1988), but insufficient attention has haen p d to the mechanics of the external feedmg strucmaa. Their small size and the rapid operation of these nmudpm pose several challenges to be overcome in desiping a detailed study of the functional components of kcdug by tadpoles. These problems are compounded by the pucedural difficulty of producing standard food substrates &xcomparative testing. When these complications are conridaedin light of the enormous amount of interspecific varixim eluciaating the functional and evolutionary aspects of
49
the workings of the oral apparatus during feedmg has proved to be especially difficult. Even so, a brief review is possible and worthwhile. The upper supra- and lower infi-arostral cartllages (chap. 4) that are the jaws of a tadpole have almost no adult derivatives, are not articulated at their bases, and are operated in a unique mechanical fashion. The suprarostral cartilage articulates and is movable against the chondrocranium. The lnfrarostral cartilage articulates and is movable against Meckel's cartilage, which articulates and is movable against the chondrocranium. Therefore, two joints occur in the lower system and one in the upper. In addition, the suprarostral cartilage is not closed through muscular contraction; rather, this cartilage with its attached upper jaw sheath is closed through a tendon-and-pulley system via movements of the lower, infrarostral cartilage (Gradwell 1968, 1972b). This arrangement leads one to conclude that the jaws must operate together and that both sheaths are involved in food removal. Two sets of unpublished data (G. F. Johnston 1982, 1990) and other observations confirm that we do not understand the exquisite mechanics of h s system. Carr and Altig (1992) also found interspecific differences of the rectus abdominis muscle that apparently correlate with feeding mode (figs. 3.3A-C). Among others factors, species, stage, position of the food in the water column, and density of agar-based food alter the following generalities. It also is important to remember that only a small group of ecologically similar tadpoles has been compared. Feeding trials in the laboratory indicate that the lower sheath alone or the two sheaths acting together can remove agar-based food. In the latter case, the mark of the lower sheath on the agar is usually longer than the mark made by the upper sheath. Even though the two sheaths must move simultaneously, both do not have to contact the substrate. Substrate contact may be avoided by changing the angle that the tadpole takes relative to the substrate or perhaps by adjusting the longitudmal relationship of the two sheaths. The angle between the two infrarostral cartilages probably can change during a bite, and the depth of penetration of either jaw sheath can change during a bite. The lower jaw sheath may strrke several times while the upper sheath takes but a single gouge from agar-based food. On agar that is too dense to penetrate, both jaws may strike repeatedly without closure. The labial teeth may leave no mark, leave a mark but show no movement, or show rasping movements with marks left on top of those made late in a feedmg stroke by the jaw sheaths. Insufficient information has contributed substantially to an inadequate understanding of how tadpole mouthparts work. A better appreciation of the following issues would add considerably to understandmg their evolution: those factors important to the evolution and maintenance of the tadpole stage in the life history of a frog; a consensus on primitive or derived state of various larval traits; an appreciation of the full compliment of morphological variations and their functions; baseline data on geographic variation; and further facts on ontogenetic variation, developmental information, and the ecological significance of various larval morphologies. For these and other reasons, oral structures have
RONALD ALTIG AND ROY W. McDIARMID
50
been used infrequently in systematics analyses (e.g., Duellman and Trueb 1983, 1986; Grandison 1981; I. Griffiths 1963; I. Griffiths and De Carvalho 1965; Inger 1967; Kluge and Farris 1969; 0. M. Sokol1975) and debated less often. The lack of a clear phylogenetic hypothesis of some groups surelv has exacerbated the situation. but cursorv examinations suggest to us that tadpole morphology commonly is concordant with perceived taxonomic boundaries and perchance signals the need for closer examination of relationships (e.g., B u . debilis group vs. other B u f , Hyla leucophyllata group vs. other groups of hylids, Scinm yostrata vs. S. rubva groups, Otophrynepyburnivs. other microhylids). Boulenger (1897:110) made a knowing statement in this regard: "The structural differences which separate the genera and species in their tadpole condition reflect, on the whole, pretty accurately the system based on the perfect animals. . . ." Yet, even heuristic attempts to gain ideas on evolutionary patterns by overlaying larval traits on cladograms derived from analyses of adult traits have not been done (see chap. 4). Degree dfcommonness, at least as presently known (e.g., a 213 LTRF in many g d d s and taxa), coupled with a bewildering array of morphological diversity, makes the situation aooear chaotic. Even so. inclusion of larval traits in I I phylogenetic analyses of anuran groups is essential. We are not sure whether external or internal characteristics will prove to be more informative, so we recommend investigators consider both. A few examples adequately illustrate the need for much more work. J. D. Lynch (1971) considered a LTRF of 313 or greater as primitive within leptodactylid frogs, and Drewes (1984) noted that larger LTRFs belong to the more primitive tava in hyperoliids. Noncusped teeth have been considered primitive by Noble (1931) and derived bv Gosner ( 1959). Al&ough devklopkental and functional data may help define characters and their states, their inclusion in phyloeenetic analvses should be with caution. We are convinced V that understandmg the developmental morphology of a character often provides insight into character homology. For example, determining the developmental history of a trait across lineages may enable one to distinguish between instances of what appears to be the independent occurrences of the same trait (homoplasy) and those that actually represent the occurrence of G o traits (apparent homoplasy).~ Altig and Johnston (1989) pointed out that patterns of early development and metamorphic atrophy were informative'and suggestive of tooth row homoldgi. Based on data from several sources (e.g., Dutta and Mohanty-Hejmadi 1984; Echeverria et al. 1987; Fiorito de Lopez and Echeverria 1984; Limbaugh and Volpe 1957; R. J. Nichols 1937; Thibaudeau and Altig 1988; Tubbs et al. 1993),tooth rows in species with a LTRF of 213 commonly appear in the developmental sequence of A-1, P-2, P-1, A-2, and P-3 (sequential formulas 110, 111, 112,212,213). Rows A-1 and P-2 are closely linked during development and may appear slightly reversed in time. Likewise, the first five rows to develop in species with LTRFs larger than 213 commonly appear in this sequence. In species with more than five tooth rows, subsequent rows apparently are added alternately on i
the upper and lower labia, but in at least four different patterns two of these are apparently common. In ranids, tooth rows are added proximally on at least the upper labium, whereas in ascaphids, heleophrymds, and hylids, additional rows are located distally on both labia. Species with many tooth rows (e.g., suctorial forms) attain the full compliment much later in ontogeny and retain tooth rows further into metamorphosis than species with fewer tooth rows (Menzies and Zweifel1974; Nodzenski and Inger 1990). A thorough evaluation of row homology is hindered by the paucity of developmental series and the lack of understanding of how medial gaps in tooth rows develop and evolve. The rows in a 213 formula are designated the prime formula. In species with a formula greater than 213, the pattern differences that were proposed to account for additional tooth rows reauire that the orirne rows be renumbered once the entire compliment of tooth rows is present. Based on this observation, certain LTRFs should not exist. Of 124 species with fewer than 213 rows, 88 fit within the expected categories of 212 (loss of P-3), 112 (loss of A-2), 111 (loss of P-1), and 110 (loss of P-2) or 011 (loss of A-1). If homology is assumed, LTRFs such as 012, 211, and 113 (common in hyperoliids and African ranids) indicate the presence of other patterns. The genetics of tooth row formation, and for that matter of most other morphological characteristics of tadpoles, essentially is unknown. Fortman and Altig ( 1973) showed that F, crosses among species of Hyla from the southeastern United States resulted in hybrids that more closely resembled one parent than the other; seemingly many traits acted as simple dominants. Crosses of Rana sp. with LTRFs of 213 and 314 produced hybrids with a formula of 214 (Haertel and Storm 1970; also see Kawamura and Kobayashi 1960, Michalowski 1966). Although the relative sizes of various mouthparts remain nearly constant throughout large parts of larval ontogeny (Gates 1983), the patterns of growth of oral structures as they relate to feeding ecology are poorly known.
Summary The biphasic life cycle of anuran amphibians comprises two quite different body plans on which selection can operate: tadpoles and adults. The products of this selection especially among the larval forms are amazing! As discoveries are made and papers are published, one is coerced into believing that the total morphological diversity of anuran tadpoles is nearly endless. Except for the pelagic areas in a continually flowing river or stream, there seems to be no freshwater habitat of any duration that does not harbor tadpoles. Even though we do not understand them well, numerous adaptations allow tadpoles to live and feed in these various habitats. The distinctions between ecological forces and phylogenetic restrictions remain muddled in part because of the shortage of phylogenetic hypotheses within major clades of advanced frogs. Throughout much of tadpole diversity, a tadpole is a tadpole is a tadpole: a simple, depressed body shape, dorsal eyes, sinistral spiracle, marginal papillae with a dorsal gap, and 213 tooth rows describes many anuran larvae. W i t h
ARCHITECTURE Cranial and Axial Musculoskeleton David Cannatella
Semina limus habet virides generantia ranas
Et generat truncas pedibus, mox apta natando Crura dat, utque eadem sint longis saltibus apta, Posterior superat partes mensura priores. Ovid, Metamorphoses, book XV (Pattist 1956) Ev'n slime begets the frog's loquacious race: Short of their feet at first, in little space With arms, and legs endu'd, long leaps they take Rais'd o n their hinder part, and swim the lake, And waves repel: for Nature gives their kind,
To that intent, a length of legs behind. Translation by John Dryden in Garth (1961)
Introduction Ovid's epic poem Metamorphoses chronicles miraculous changes of all sorts-a boy is transformed into an eft for offendmg Ceres, a statue carved by Pygmalion becomes a woman, the eyes of the dead musician Argus are made to adorn a peacock's train, and tadpoles metamorphose into frogs. The Roman poet's view of tadpoles as ephemeral stages is not unexpected, for even amphibian biologists do not M y appreciate the significance of tadpoles as free-living organisms. Tadpoles use the transient source of energy available in aquatic primary production, which is not available to adults (Wassersug 1975); the larval stage provides the advantage of rapid growth in unstable environments. Being a tadpole means that cranial morphology is canalized into unique feedng structures at the expense of all else. The body cavity contains mostly gut. The tail is emphasized over the h b s as the instrument of locomotion. The reproductive tissue lies outside of the body cavity, so reproduction (and thus neoteny) is not possible until metamorphosis, when the tad is resorbed, the lunbs develop, and the body cavity enlarges. Thus, except for sex, tadpoles engage in most of the same activities as adult frogs- feeding, respiration, and locomotion- but in very dfferent ways. This chapter emphasizes the structure and function of the musculoskeleton as it relates to these activities.
Anuran Phylqeny and the First Tadpole What did the first tadpole look like? Given a phylogeny, some inferences are possible. L. S. Ford and Cannatella (1993) reviewed the status of anuran phylogeny and presented trees based on mostly adult and a few larval morphological characters (fig. 4.1; alternative phylogenies are d s cussed at the end of the chapter). The four most basal lineages of living Anura are Ascaphus trztei, Leiopelma, Bombinatoridae, and Discoglossidae. These taxa have the Type 3 tadpole of Orton (1957). Pipanura (fig. 4.1) is composed of Mesobatrachia and Neobatrachia. Mesobatrachia includes Pipoidea, with Type 1tadpoles, and Pelobatoidea,with Type 4 tadpoles. The tadpoles of Neobatrachia are Type 4 except for those of Microhylidae, which are Type 2. If Orton's (1953, 1957) four tadpole types are mapped as unordered character-states onto the phylogeny, it can be inferred that the ancestor of Anura had a Type 3 tadpole (jaw sheaths, labial teeth, medial spiracle), the ancestor of Pipanura had a Type 4 tadpole (jaw sheaths, labial teeth, sinistral spiracle), and the Type 1 tadpoles (no jaw sheaths or labial teeth, paired spiracles) and Type 2 tadpoles (no jaw sheaths or labial teeth, medial spiracle) were independently derived from Type 4 (fig. 4.2). This is similar to a proposal by 0.M. Sokol
53
ARCHITECTURE Caudata Ascaphus truei Leiopelma Bombinatoridae Discoglossidae Megophryidae Pelobatidae Pelodytes Rhinophrynusdorsalis
I
Discoglossanura
LA Neobatrachia
Micrhylidae
I
Allophryne Brachycephalidae Bufonidae Heleophryne "Leptodactylidae" Limnodynastinae Myobatrachinae Sooglossidae ~hiniderma Hylidae Pseudidae Centrolenidae Scaphiophryninae' Scoptanura Dendrobatidae Hemisus Arlhroleptidae' 'Ranidae"
Fig. 4.1. Phylogenetic relationships among the major taxa of Anura. The dots represknt node-based names. Symbols: asterisk = metataxon, names in quotation marks = nonmonophyletic m a , and dots = nodebased names (L. S. Ford and Cannatella 1993).
(1975) and in stark contrast to that of Starrett (1973), which is discussed in the section Evolution of Orton's Tadpole Types. Although the ancestor of Anura can be inferred to have a Type 3 tadpole, in itself this is not very informative. Orton's tadpole types are defined primarily by the presence/absence of jaw sheaths and labial teeth, and the number and position of the spiracles. The taxa possessing the plesiomorphic Type 3 larva (fig. 4.2) are &verse.Ascaphus truei has a stream tadpole, and Lewpelma has larvae with "direct" development (chaps. 2 and 7). More typical pond tadpoles are present in Bumbina and Disw~lossusand in many other groups, but their nidespread phylogenetic dstribution does not guarantee that the pond tadpole morphology is plesiomorphic for Anura. It is generally assumed that the speciahzed morphologies of the Ascaphus tadpoles andhwpelma larvae are derived from some pond tadpole ancestor (I. Griffiths 1963), but phylogenetic analysis of larval characters does not demand this interpretation. Certain features of the Ascapbus tadpole (e.g., reduced muscular process of the palatoquadrate) might be either plesiomorphic for Anura or apomorphic for Asmphus. What can be said with confidence is that the ancestor of Bombinanura (figs. 4.14.2) had a pond tadpole, but h s ancestral larva is quite removed phylogenetically from the typical pond larvae of Rana catesbeiana and R. temporarta on which much of this chapter is based. It is doubtful that the first anuran tadpole wasstructurally or functionally similar to the pond tadpoles ofRana, and the reader is cautioned not to extrapolate structure or function from Rana to other
species. Instead, it is hoped that h s chapter will stimulate descriptive and functional studies of other taxa, so that a more complete phylogenetic synthesis of tadpole structure and function may emerge. GeneralAnatomy This chapter provides an overview of the skeleton and muscles of the chondrocranium, jaws, hyobranchium, and trunk. The general anatomy of each region is described, and intertaxic variation is discussed in a ~hvlogenetic context when u possible. Following the general comparative anatomy are sections treating changes during metamorphosis, the functional anatomyand evolution OFgill irrigation mechanisms, and phylogenetic aspects of tadpole morphology. Only recently (e.g., Haas 1993, 1996b, 1997a) have phylogenetic analyses using primarily larval musculoskeletal characters apA
,
An ideal general description of tadpole anatomy would be based on a plesiomorphic pond tadpole such as Bombina or Discog-lossus.Unfortunately, the literature on these species is not rich enough to permit this, although that situation is changing with papers such as those by Haas (1997) and Schlosser and Roth (1995). The descriptive cranial anatomy herein is based primarily on Rana temporaria (De ~ o n ~ h 1968; Edgeworth 1935; Pusey 1938), and the functional aspects are based on Rana catesbeiana (Gradwell 1968, 1969a, b, 1970, 1972b, c; Gradwell and Pasztor 1968). Most of the terminology for the cranium derives from Gaupp (1893, 1894, 1896), and that for muscles comes from Edgewotth (1920,1935), with modifications by Haas (1997). Although Edgeworth's terminology has been almost standard for many years, recent work has altered the proposed homologies of muscles, especially in the branchial region. The description of metamorphosis is generally based on De Jongh (1968) and Ridewood (1897b, 1898a). The information for the vertebral column and associated muscles is derived from Xineus laevis because the literature on that s~ecies is much more com~letethan for Rana. The most I comprehensive summary of development of all organ systems is that of Nieuwkoop and Faber (1967) for Ximpw h s . Unfortunately, there are no anatomical illustrations, but there is an extensive literature section. Staging systems used in the text include Gosner (1960), Kopsch (1952), and Nieuwkoop and Faber (1967). In general, English anatomical terms are used if both English and Latin are available. If no English term is available, or if the English term is ambiguous in meaning, the Latin is used; synonyms are listed in parentheses. Edgeworth (1935) provided a table of muscle synonyms for the early literature.
The Chondrocranium The first study of the frog chondrocranium apparently was by Dug& (1834), who described and figured the larval chondrocranium of Pelobatesfiscus; other literature on tadpole crania is summarized in table 4.1. Intertaxic variation in the larval chondrocranium is &scussed below and in Haas
54
DAVID CANNATELLA
(1993, 1995, 1996b, 1997a) and O. M. Sokol (1975, 1981b) The reader is referred to Cannatella (1985), Dueiirnan and Tmeb (1986), and Tmeb (1973, 1993) for variation of bones among taxa. The chondrocranium of tadpoles is a cartilaginous case that protects the brain and supports the sense organs and jaw apparatus. The chondrocranium initidy appears as two pairs of cartilaginous elernents, the parachordals and trabeculae (fig. 4.3). The parachordals appear as longinidinal rods flanking the anterior end of the notochord. The trabeculae form in the same plane but anterior to the parachordais; the notochord does not intemene between the trabeculae. The trabeculae íüse anteromedialiy to forrn a trabecdar
plate (ethmoid plate, planum trabecdae anterior). The space where the trabeciilae have not yet hsed is the basicranial (hypophyseai) fenestra, which disappears as the trabeculae coalesce to forrn the cranial floor (basii cranii). Fusion of the parachordais forrns the basal plate (planum basale; fig. 4.3) as the floor of the neurocranium; the planum rnay be perforated by the notochord. Before the basicranial fenestra disappears, the trabeculae and basai plate fuse. The junction between the basai plate and craniai floor is indicated by the prirnary carotid foramina (foramina carotica primaria) through which the internai carotid arteries pass. The parachordals project posteriorly to the otic capsules and support the occipital arch, whch is seridy hornologous with the ver-
Fig. 4.2. Evolution of Orton's (1953) tadpole types under the assumption of unordered states, based on the phylogenies of L. S. Ford and Cannateiia (1993), Haas (1997a), and Hay et al. (1995).
ARCHITECTURE
55
Table 4.1 Summary of iitenture concerning tadpole chondrocrania, muscles, and giü apparatus. Since t h s table was first compiled, similar compendia have appeared (Haas 1993, 1995, 1996b) that were of great help in updating the present table. Aii taxa treated in Haas (1996b) are also iisted in Haas (1993). Some species names may be incorrect according to current taxonomy. A&caphustmei LEIOPELMA Leiupelma archeyi Lewpelma hochstetteri BOMINATORIDAE Bombina bombina Bombina urientalis Bombina variegata DISCOGLOSSIDAE A&es obstetncans
Discoglossus sardas MEGOPHRYIDAE Leptobrachium hasseltii Megophtys montana Megophtys nasuta Megophtyspania Megophtys robusta Megophtys stejnegmi PELOBATIDAE PelobatesfiLscus Pelobates syn6cus Scaphiopus holbrookii Spea bombtfions PELODYTIDAE Pelodytespunctatus PIPIDAE Hpnochims boettgeri P i p canialhoi P9apart.a P@apipa
RHINOPHRYNIDAE Rhinuphtynus donalis ATOBATRACHIA Heleophtyne natalensis Heleophyepurcelli .\IYOBATRACHINAE Pseudophtyne australis Pseudophtyne bibronii Uperoleia lithomodu LU'NODYNASITNAE Limvwdynmtesperonii Limvwdynbes tasmaniensis Mixophyesfasciolatus -LEMODACIYLIDAEn Alsodes bawioi Caudiverberamudiverbera Ceratophtys comuta Cwatophtys cranwelli Cychamphusstejnegmi Eiatherodactylus coqui Eieutherodac~lusnubicoiu Lepidobatrachus h k Lepidobatrachw liunensis I~ptodmtyluschaqwnsis LLptodmtylus ocellatus Leptodmtyluspentadadylus
Gradwell1971a, 1973; Haas 1995,1996b, 1997a, b; Pusey 1943; Reiss 1997; Van Eeden 1951; Wassersug and Hoff 1982 N. G. Stephenson 1951b N. G. Stephenson 1955 Goette 1875; Ridewood 1898b (as B. &teus); Severtsov 1969b Haas 1997a; 0 . M. Sokol 1975; Wassersug and Hoff 1982 Haas 1995,1996b, 1997a De Beer 1985; Haas 1995,1996b, 1997a; Kmjitzer 1931; Magnin 1959; Pusey 1938; Ridewood 1898a, b; O. M. Sokol 1981b; Van Seters 1922; Wassersug and Hoff 1979, 1982 Kraemer 1974; Haas 1995, 1996b, 1997a; Pusey 1943; Ridewood 1898b; Schiosser and Roth 1995, 1997a, 199% PÚgener and Maglia 1997; 0 . M. Sokol1981b Ridewood 1898b Haas 1996b; h j i t z e r 1931; Ramaswami 1943 Haas 1995 Ramaswami 1943 Ramaswami 1943 Haas 1995 Dugès 1834; Haas 1997a; Luther 1914; Plasota 1974; Ridewood 1898b; Rotek 1981; Schultze 1888, 1892; Severtsov 1969a O. M. Sokol 1975,1981b Haas 1995 O. M. Sokol 1981b; Wassersug and Hoff 1979, 1982 (as Scaphwpus);J. J. Wiens 1989 Ridewood 189%, 1898b; 0 . M. Sokol1981a, b O. M. Sokol 1959,1962,1977a O. M. Sokol 1977a Haas 1995; 0 . M. Sokol 1997a W. K. Parker 1876 (as l? monstrosa);Ridewood 1897a, 1898b (as l? americana);Rozek 1989, 1990; Rozek and Veself 1989 O. M. Sokol1977a, b (asXenupw) Dreyer 1915; Edgeworth 1930; Gradwell 1971b; Haas 1995, 1997a; Kotthaus 1933; W. K. Parker 1876 (as Dadyiethra cnpensis);Paterson 1939a; Ramaswami 1941; Ridewood 1897a, 1898b; Sedra and Michael1956a, 1957; Tmeb and Hanken 1993; Wassersug and Hoff 1979,1982; Weisz 1945a, 1945b Haas 1995,1996b; Orton 1943; 0.M. Sokol1975,1977a, 1981b; Swatt and De Sá 1998; Wassersug and Hoff 1982 Wassersug and Hoff 1979, 1982 Ramaswami 1944; Van Der Westhuizen 1961 C. M. Jacobson 1968 C. M. Jacobson 1968 Davies 1989 Haas 1996b, 1997a W. K. Parker 1881 Kesteven 1944 W. K. Parker 1881; Reinbach 1939; Ridewood 1898b (as Calyptocephalmgayi);O. M. Sokol 1981b Wild 1997 Fabrezi and García 1994; Lavilla and Fabrezi 1992 Lavilla 1991 Hanken et ai. 1992; Schiosser and Roth 199% Lynn 1942 Haas 1995,1996b; Ruibal and Thomas 1988 Lavdla and Fabrezi 1992 O. M. Sokol l 9 8 l b W. K. Parker 1881 Haas 1995,1996b
DAVID CANNATELLA Table 4.1 umtinued Odontophvynusachalemis Physaiaemwpumlosus Pleurodema bibronii Pleurodema borellii Telmatobius bolavianus Telmatobiw ceimum Telmatobiw mleus Telmatobiusjelskii Telmatobius latkps Telmatobius cf. m a m a t u s Telmatobiuspisanoi PSEUDIDAE Pseudisparadoxa RHINODERMA Rhinoderma ahtwt'nii BUFONIDAE Bufo cf. americanus BufD amwr'canus BufD angusti'ceps Bufò bufo Bufò %ntiginosusn Bufo melanostictus Bufo regulanS Bufo cf. spinulosw BufD p i d h HYLTDAE Agabchnh callidym Anotheca spinosa Cycloranaplapphala F~ctonotusgoeidii Gastrotheca espeletia Gastrothecagracilh Gastrotheca cf. manupiata Gastrotheca manupiata Gastrotheca orophylax Gastmthecaperuana Gnrtmtbecapse21stes Gastrotheca riobambae Hyla arbma Hyla cinerea Hyla laruzfomtis Hyla microcephala Hyla nana Hyla pukcheh Hyla rosenbergi Hyla sguirella Phnrmabyhguttata Phyllomedusa boliviana Phylhedusa sauvagii Phylhedusa trinitatir Pseudacris cru& PseuMs regila Scinat:acuminata S c i m mbra ''WAE" Amolops af8hana Euphlyctis hexadaqlw Hoploba&chus tigerinus Occidazyga iuevis Rana catesbeiana Rana clamitans Rana mrtipes Rana ahlmatina Rana esculenta Rana cf.pipiens Rana pipiem Rana temporaria Rana "whitehendi"
Haas 1997a Schlosser and Roth 199% O. M. Sokol 1981b Fabrezi and García 1994; Wassersug and Hoff 1982 Laviiia and De Ia Riva 1993 Fabrezi and Lavilla 1993 W. K. Parker 1881 W. K. Parker 1881 (as Cyclmhamphw culeus, fide Ridewood 1898b) Fabrezi and Lavilla 1993 Ridewood 1898b Fabrezi and Lavilla 1993 W. K. Parker 1881; Ridewood 1898b
W. K. Parker 1881 Wassersug and Hoff 1982 Barry 1956 Haas 1995, 1996b; W. K. Parker 1876; Ridewood 1898b (as B. rmbaris) Sedra 1951 Ramaswami 1940 Sedra 1950; Sedra and Michael1956b, 1958,1959 W. K. Parker 1881 O. M. Sokol1975 Haas 1995,1996b Haas 1996b; Wassersug and Hoff 1982 Ridewood 1898b (as Chimleptes) Haas 1996a Haas 1996b Fabrezi 1985; Fabrezi and Lavilla 1992 W. K. Parker 1881 Haas 1996b Haas 1996b Haas 1996b Haas 1996b Haas 1995,1996b, 1997a Haas 1996b; Ridewood 1898b; Severtsov 1969a Haas 1996b De Sá 1988 Haas 1996b Fabrezi and L a d a 1992 Fabrezi and Lavdia 1992; Lavilla and Fabrezi 1987 Haas 1996b O. M. Sokol1981b Fabrezi and Lavilla 1992 Fabrezi and Lavilla 1992 Fabrezi and Lavilla 1992 Haas 1996b; Kemy 1969a W. K. Parker 1881 (asAcvispicken'ngi) O. M. Sokol1981b (as Hyla) Fabrezi and L a d a 1992 Haas 1996b Ramaswami 1940,1943 (as Rana) Ramaswami 1940 (as Ram) Chacko 1965,1976; Ramaswami 1940 (as Rana) Ridewood 1898b (as Oyglossw) Gradwell 1968, 1970, 1972a, b; Starrett 1968 W. K. Parker 1881 Ramaswami 1940 Kratochwiil 1933 (as R agilh) Ridewood 1898b W. K. Parker 1881 Starrett 1968; Wassersug and Hoff 1979 De Beer 1985; De Jongh 1968; Gaupp 1893; Haas 1995, 1996b, 1997a; W. K. Parker 1871; Plasota 1974; Pusey 1938; Ridewood 1898b; 0 . M. Sokol1975; Spemann 1898; Stohr 1882 Ridewood 1898b
ARCHITECTURE
57
Table 4.1 wntinued RHACOPHORIDAE Buw~eriabuegeri Philautus variabilk Rhaeaphms ieucomystm: ,WCROJ5YLDAE Brevrkps aakpevsus Dennatonotus muelieri Grrrtmphyne mrolinensis Grrrtmphyne wta Hamptophlyne boliviana Hp~pdw bavberi Hpqachus vario[osw M k h y l a omata M k h y l a pukhva Otophynepybumi Phrynonauntk annectens Upmdon ystoma DENDROBATIDAE Caiostethusnubicola Caiostethw subpunctatus Caiostethrrshinztatis Dendrobates auratus Dendrobates tinctoriw Epipdobates anthonyi Epipdobates buuh~eri Eppedobates Phyhbates bicoior
Trabecular horn
Okutomi 1937 Ramaswami 1938 Ridewood 1898b Swanepoel1970 Laviiia 1992b Wassersug and Hoff 1982 Haas 1995,1996b De Sá and Tmeb 1991 O. M. Sokol1975,1981b Starrett 1968 (as H. albooenter) Ramaswami 1940; Ridewood 1898b Haas 1995,1996b Wassersug and Pyburn 1987 (as 0. vobwta) Gradwell 1974 (as Phynomerrts) Ramaswami 1940 Haas 1995,1996b Haas 1995,1996b Rtdewood 1898b (as Phyhbates) De Sá and Hdl1998 Haas 1995,1996b Haas 1995,1996b Haas 1995,1996b Haas 1995,1996b Haas 1993,1996b, 1997a
\
,Trabecular
plate
Quadratocranial
\
,Trabecula
Notochord Parachordal cart.
F g . 4.3. Developing chondrocranium of Rana temporaria (7.5-mm lama) in dorsal view. Redrawn from Stohr (1882).
tebral neural arches. The occipital arch fuses to the rear end of the skull.
Etbmoid Region The anterior end of the primordial chondrocranium is elaborated to support the nasal capsuies and the larval jaws. Two C
trabecuiar horns (cornua trabecuiarum) extend forward vent r d v and anterolateraiiv from the ethmoid í= trabecuiar plati, fig. 4.3). The trabedar horns articulati with, or are fused to, a pair of suprarostral cartiiages (cartilago labialis superior, superior rostral carulage), the skeletal elements of thê tadpole kpper jaw. In other gnathostomes, the functional upper jaws are formed either by the palatoquadrate cartilage or by a series of dermal bones (e.g., maxillae and premaxiiiae). In this region two ligaments, the quadratoethmoid ligament (ligamentum quadratoethmoidale, I. cornuquadratum mediale; Van Der Westhuizen 1961) and the lateral circumoral ligament (I. cornu-quadratum laterale, I. cornu-auadratum. I. circumoralis: 0.M. Sokol1981b) ioin the ethmoid regi& to the palatocguadrate cartilage; sie'details below under Circumoral Ligaments. The nasal septum (septum nasi; fig. 4.4) arises from the trabecuiar dati and s e ~ k a t e sthe naial ca~suies.The nasal capsuies ofllarvae u s d y are partidy forked spheres. The roof of the nasal capsuie (tectum nasi) is confluent posteriorlv with the lamina orbitonasalis and is united to the seDtum nasi. The confluente of the trabecuiar horns joins the ventral part of the nasal capsuie and forms the floor of the nasal capsuie (solum nasi, trabecuiar plate, ethmoid plate; O. M. Sokol1981b). The anterior w d of the nasal ca~suie is the anterior cupola (cupola anterior). The nasal capsuie is separated from the orbit by a w d , the lamina orbitonasalis (planum antorbitale). The lamina orbitonasalis is confluent &th the tectum nasi anteriorlv and the anterior end of the orbital cartiiage (via the sphenethmoid commissure; see below) medidy. The muscular process of the palatoquadrate is bound to the processus antorbitalis (Haas 1995) of the larnina orbitonasalis by the ligamentum
58
DAVID CANNATELLA
teai, which has two parts, the I. teai superius and 1. tecti inferius. These iigaments may be chondrified in some taxa to form the cartilago tecti ("cartilago tectum" of Sokol 1975) or comrnissura quadrato-orbitalis (Haas 1995). As metamorphosis begins, the cartiiages and olfaaory epithelium of the nasal region become elaborated into a highly folded saclike structure; detaiis of these structures can be found in R. S. Cooper (1943), Denis (1959), Higgins (1920), Jurgens (1971), Rowedder (1937), and Swanepoel(1970). Ossifications associated with the nasal region include several well-known dermal bones and some neomorphic elements. The nasais form part of the roof of the nasal capsules. The vomers are palatal bones that form the floor of the nasal capsule; these are absent prirnitively in frogs (Cannatella 1985) and secondarily lost in several taxa. The septomaxillae are generally small elements that are intimately associated with the nasolacrimal duct but develop independently of the nasal cartilages (De Jongh 1968; Jurgens 1971). Neomorphic elements, such as the internasals and prenasals in various taxa of casque-headed frogs (Tmeb 1973), appear relatively late in ontogeny (Trueb 1985). Hanken and Hall (1984, 1988), N,E. Kemp and Hoyt (1969), Stokely and List (1954), and citations in Trueb (1985) provided ossiíication sequences in variou5 species. Diversity. The ligamentum tecti was figured for Pelodytes (O. M. Sokol1981b) andXenopush 5 (Sedra and Michael
1956a). Gradwell (1972b) dustrated it in Rana catesbeiana as the composite of the 1. supraorbitale cranii and 1. supraorbitalis ethmoidale. It is not mentioned in some taxa for which the chondrocranium is well described: Aseaphus, Heleophlyne, or Rana temporaria (De Jongh 1968; Van Der Westhuizen 1961: Van Eeden 1951). Variation in the lateral circumoral ligament is discussed below under Circumoral Ligaments. The ethmoid region of pipoids is difficult to compare with that of other frogs. For example, there is a single medial cartiiaginous bar that supports the nasal septum. 0 . M. Sokol (1975) argued reasonably that this bar represents the fused trabecular horns, but RoCek and Vesely (1989) considered this planum internasale to be nonhomologous with the trabecular horns. Thev also described several other features in which the ethmoidJregion of pipids differs from those of other frogs. The homology of ethrnoidal structures was also discussed by Haas (1993, 1995).
Orbital Region The lateral wall of the cranial cavity (cavum cranii) consists of an orbital cartilage (cartdago orbitalis; fig. 4.4) that arises from the posterior parts of the trabecular cartilages and the anterior ends of the parachordal cartilages. The orbital cartilage is joined to the floor of the braincase by several cartilaginous pillars; in some vertebrates the orbital cartilage arises as a discrete elernent, but it is not clear if this is so in frogs.
\
Pila antotica T r o c . f Oz!!om!?!orf.8,
Taenia tecti rnarginalis Orbital cart., \\
\
ParEtal fen. Taenia tecti rnedialis Anterior semicircular canal
---.--
1 r O
sem. canal Posterior serni. canal
'~ugu1ar.f. Operculurn Stapes Fenestra ovalis Otic proc.
Quadratoethrnoid Trabecular horn Arcus subocularis
Lateral circurnoral
basitrabecular proc.
/ 1 I
1
Muscular proc.
Articular Droc. I Meckel's ca,laie
Ceratohyal
Infrarostralcartilage
Fig. 4.4. Lateral view of the chondrocranium of a Rana temporaria tadpole (13 mm body length). Abbreviations: cart. men, fen. = fenestra, lig. = ligament, and proc. = process. Redrawn from Pusey (1938).
=
carrilage, f.
= fora.
ARCHITECTURE
The anteriormost of these piiiars is the preoptic root forming the anterior margin of the optic foramen and attaching to the trabecula. In frogs and salamanders the preoptic root forms an extensive cartilaginous waii between the optic foramen and the sphenethmoid commissure; in caecilians (M. H. Wake and Hanken 1982) it is more of a stmt. The pila metoptica grows upward from the trabecula and separates the optic foramen from the oculomotor (metoptic) foramen, the latter for the oculomotor nerve (111), ophthalmic artery, and pituitary vein. The pila antotica (pila prootica) arises bom the parachordais and separates the oculomotor and prootic foramina. A fourth, more transitory stmt, the pila ethmoidaiis, forms the mediai waüs of the nasai capsules and olfaaory canals (canales olfactorii, forarnina olfaaoria evehentia) and merges into the nasai septum (De Beer 1985). Posteriorly, the orbitai cartiiage joins the otic capsules via the raenia teai marginalis. Anteriorly, the sphenethmoid commissure conneas the orbitai cartiiage to the lamina orbitonas a h and the nasai capsule. The orbitonasai foramen (foramen orbitonasaiis; fig. 4.4) demarcates the lamina orbitonasalis from the orbitai cartilage; the p r o h d u s nerve (ophthalmic branch of V) passes out of the orbit into the nasai cavity through this foramen. The optic foramen (for craniai nerve 11)is the largest of the foramina of the orbitai cartiiage and is located posteriorly in the orbitai cartiiage. The oculomotor foramen (for cranial rime 111)is smaüer and lies just posterior to the optic foramen. The tiny trochlear foramen (for craniai nerve IV) is k t e d dorsai to the two aforementioned foramina near the raenia tecti marginaiis. The prootic foramen (foramen prooticum) more or less separates the orbitai cartiiage from the otic capsule. The trigeminai (V) and faciai nerves (VII; from the combined prootic gangiion), the abducens nerve (VI), and the laterai cephalic vein (vena capitis lateralis) pass rhrough the prootic foramen. ~s&catiÔns in this retzion include the valatines and sphenethmoid (orbitospheioid). The palatinis form along the larnina orbitonasaiis and usuaüy extend from the maxilla mediallv to near the midline. The svhenethmoid. usuaüv an unpaired bone in adults, ossifies as paired elements along the anterolaterai waü of the braincase anterior to the optic foramen.
Braincase and Otic Capsules The braincase of frog larvae and adults is open dorsaüy via the frontoparietai fenestra (fenestra frontoparietalis; fig. 4.5). The laterai rim of the fenestra is formed by strips of cartilage caüed taeniae tecti marginaies, which are confluent with the orbital cartiiages ventraüy and with the tecturn anterius anteriorly. Posteriorly, the taeniae roof the gap between the otic capsules and form the tectum synoticum. The frontoparietai fenestra may be subdivided by additional stmts of cartiiage, as in Rama. The taenia teai transversalis is a transverse stmt that partitions the parietai fenestra posteriorly from the frontoparietai fenestra anteriorly. The taenia tecti medialis, if present, extends from the taenia tecti transversalis to the tectum synoticum and subdivides the parietai fenestra into left and right parietai fenestrae. These tectai cartilages persist in adults. The occipitai arch forms the posterior end of the cranium; it is seriaiiy homologous with the neurai arches of the vertebrae. Frogs have only one occipitai arch; most other vertebrates have more than one (De Beer 1985). There are no pre-occipitai arches in frogs (De Beer 1985), but see Kraemer (1974). The occipitai arch is supported ventraiiy by the parachordais; early in ontogeny it fuses to the basai plate and otic capsules. The tectum posterius joins the halves of the occipitai arch dorsaiiy and fuses anteriorly to the tectum synoticum. The ventral part of the occipitai arch bears the occipitai condyles, which articulate with the cotyles of the atlas. The otic capsules (capsulae auditivae; figs. 4 . 4 4 . 5 ) are subsphericai stmctures that adjoin the posterior end of the braincase. Ontogeneticaüy, they begin as hemispheres that are open mediaüy. The hemispheres fuse to the parachordais and attach to the basai plate ventraiiy, the tectum synoticum dorsaüy, and the taeniae tecti marginaies anterodorsally. Within these capsules the anterior and lateral semicircular canals (canalis semicircularis) appear and slightly later the posterior semicircular canals form. Each otic capsule develops a flattened crest, the crista parotica, that extends lateraüy from the outer waü of the lateral semicircular canal. The posterior part of the ear capsule forms the processus muscularis capsulae auditivae for muscle attachment. The otic ligament joins the anterior part of the crista parotica to the otic process (processus oticus) of the palatoquadrate (see below unDiversity. The pila antotica is absent in rnicrohyiid larvae der Jaws). O . M. Sokol 1975) and Rhirwphrynus (Tmeb and CannaThe dorsai features and general size of the larvai otic capd a 1982). In the basai clades of frogs (Ascaphus, Leiupelma, sules are determined by the three semicircular canals of Diw~lussus,and Bombina) the prootic foramen is subdivided the inner ear. Chondrification and later ossification around by a strip of cartiiage caüed the prefaciai commissure into these, especiaiiy the anterior and posterior canals, are evident the prootic foramen (for craniai nerve V) and palatine fora- as the epiotic eminentes. Metamorphic changes in the inner men (for cranial nerve VII; O. M. Sokol 1975). In taxa with ear are minimal; those of the middle ear are pronounced. the prefacial commissure, the trigeminal and facial gangiia The middle ear of adult frogs includes an opercularis system are unfused, whereas in those lacking the commissure the and usuaüy a tympanic-columeiiarsystem; the Merences in _pnglia are fused to form a prootic gangiion. As suggested developmental timing of these two systems suggest that they by Sokol(1975),the lack of the commissure is a synapomor- are h a i o n a ü y independent (Hetherington 1988). Both of phy of Pipanura. Other aspects of variation were discussed these communicate with the inner ear via the fenestra ovalis, by Haas (1993). a prominent opening in the ventrolateral waü of the otic capsule that is covered by a membrane in the tadpole. In the adult, the fenestra ovalis is largely occluded by two stmc-
DAVID CANNATELLA
62
tive tissue that is associated with the processus posterior dorsalis of the pars alaris. Haas (1995) described the details of its connection to the mandibulosuprarostral iigament and the lateral circumoral ligament (iigamentum cornuq u a d r a m ) in dendrobatids. ~e noted its presence (apomorphic) only in T j ~ 4e tadpoles. I interpret its absence in microhylid larvae ( T p e 2) as a loss. Its absence in pipoids (Type 1) may aiso be a loss or may indicate that pelobatoids are more closely related to Neobatrachia than to pipoids, resulting in paraphyly - . . of Mesobatrachia. Noble (1929) claimed-that &e absence of the suprarostral cartilage was characteristic of microhylid (his "brevicipitid") larvae. Starrett (1973) reported that the suprarostrai was lacking i11pipoid ( T p e 1) and microhylid (Type 2) larvae; t h s was linked to her view that the absence of jaw sheaths was pleiomorphic for anurans. 0.M. Sokol (1975) pointed out that all frog larvae have suprarostral cartilages; in Types 1 and 2 larvae they are firmly ankylosed to the trabecular horns. The presence of keratinized jaw sheaths may be correlated with mobility of the suprarostral. The posteroventral process of the suprarostral (0.M. Sokol 1981b) is absent in Pipanura. Alytes and DWcoglossus have long, distinctive, U-shaped corpora ( 0 . M. Sokol1981b). The lateral tip of the suprarostral Diate LI Z n o ~ u íuevis s fuses with the ~uadratoethmoidcartilage to form the tentacular cartilage, which supports the tentacle (Tmeb and Hanken 1993). L
Palatoquadrate and Suspeitsorium The larvai palatoquadrate (pterygoquadrate; figs. 4.3 and 4.6) is a long flat strip of cartiiage anchored to the neurocranium by four cartilaginous processes: ascending process (processus ascendens), basal process (processus basalis, processus pseudobasalis, hyobasai process), otic process (processus oticus), and the quadratocranial commissure (commissura quadratocranialis anterior). The term suspensorium was used in its present sense by T. H . H d e y (1858) for the common attachnient of the mandibular and hyoid arches to the skuil (Pyles 1987). According to O. M. Sokol (1981b), the suspensorium is the posterior end of the palatoquadrate that iies at the anterior end of the otic capsule. It articulates with the otic capsules via the ascending and otic processes. The ascendmg process is a round bar that curves mediaiiy and fuses with the region of the pila antotica (see Diversity below). The otic process is the lateral part of the suspensorium; it is a thick plate that is curved almost verticaiiv. The otic Drocess is attached to the wall of the lateral seniicircular canal near the crista parotica by the otic ligament; in some taxa this process chondrifies and is then caiied the larvai otic process, which is considered homologous with the adult otic process (Van Der Westhuizen 1961; Van Eeden 1951). The larval otic process is destroyed during metamorphosis, but the ceiis released in the process rechondre to form the adult process. Ln most vertebrates the basal process of the palatoquadrate articulates with the basitrabecular process (fig. 4.4; a lateral projection of the trabecula) anterior to the palatine nerve. However, in most frogs the basitrabecular process is lost during ontogeny, and the basai process articulates or füses with the neurocranium posterior to the paiatine nerve
(De Beer 1926). Because of the position of the process relative to the palatine nerve, Pusey (1938) rejected the homology of the two conditions; the newer process and its postpalatine connection have been termed the pseudobasal process (De Beer 1926) and pseudobasal connection (Pusey 1938). Van Der Westhui7~n(1961) offered compehng evidence that the basal process simply has moved from the basitrabecular articulation to a more lateral position on the otic ledge to produce a postpalatine connection (commissure). Therefore, the basal and pseudobasal processes are homologous (Pyles 1987; Reiss 1997). As one proceeds anteriorly, the paiatoquadrate underlies the orbit and in this region is named the arcus subocularis (fig. 4.4). The wide gai that separates the paiatoquadrate from the neurocranium is the subocular fenestra. The region anterior to the a r a s subocularis is termed the quadrate (O. M. Sokol 1981b). The most prominent part of the quadrate is the muscular process (processus muscularis), a flattened triangular process that curves dorsally and medially and is the site of attachnient for the orbitohyoideus and suspensoriohyoideus muscles. The muscular process is bound to the processus antorbitalis (Haas 1995) of the neurocranium by the ligamentum tecti (cartilago te& or commissura quadrato-orbitalis when chondrified), which may be composed of two ligaments (see Ethmoid Region above), the ligamenti tecti superius et inferius. Anteromedially, the quadratocraniai commissure (figs. 4.3 and 4.5) rises dorsally as a thick cartilaginous strip to join the quadrate to the floor of the braincase near the ethmoid plate. On the anterior margin of the commissure is the s m d triangular quadratoethmoid process (processus quadratoethmoidahs) to which the quadratoethmoid ligament (ligamentum quadratoethmoidale) is attached. A smail processus pseudopterygoideus (Haas 1995) projects from the posterior part of the cornrnissure into the fenestra subocularis. The hyoquadrate process (processus hyoquadrati) is a condyle for the synoviai articulation with the ceratohyal (figs. 4.4 and 4.7) and is located ventrally at the posterior part of the quadrate region. The hyoquadrate ligament attaches to a ridge posterior to the hyoquadrate process and binds the ceratohyai to the quadrate. The most anterior part of the quadrate is the stout articular process (pars articularis quadrati), which forms a synovial articulation, the adult jaw joint, with the posterior end of Meckel's cartiiage. During metamorphosis, the arcus subocularis, ascending process, hyoquadrate process, and muscular process are resorbed as the paiatoquadrate rotates posteriorly (fig. 4.6). The quadratocranial cornniissure is partly destroyed, but its surviving part, with the quadratoethmoid process and processus m d a r i s posterior of the lamina orbitonasalis. forms the pterygoid process (processus pterygoideus) of the adult. Most of the larval paiatoquadrate disappears at metamorphosis, and some of its supportive function is assisted or taken over by severai ossifications: m d a , p r e m d a , quadrate, quadratojugai, pterygoid, and squamosai. The auadrate is an endochondral ossification that forms in the similarly named region of the palatoquadrate at the articular process, the point of articulation with the lower jaw. An arc of the p r e m d a e , m d a e , and quadratojugals takes
ARCHITECTURE
Palatoquadrate
\
Infrarostral caltilage
Meckel's cartilage
Fig. 4.6. Four arbitrary stages in the metamorphosis of the paiatoquadrate of a generalized tadpole; lateral view. Arrow indicates direction of metamorphic shift of the jaw elements. After Sedra (1950).
over the role of the palatoquadrate in forming the upper jaw of the addt frog. The squamosal forms in association with the otic process and quadrate of the palatoquadrate cartilage. The pterygoid invests the addt pterygoid process, which forms in part from the quadratoethmoid process and the basal process. Diversity. Several features of the palatoquadrate are highly m d e d in pipoids ( 0 . M. Sokol 1977a; Swart and De Sá 1998). A nove1 structure, the ventrolateral process, is a synapomorphy of Pipoidea; it is present in Pipa, Rhinq&ynus, Silurana, and Xenopus but not Hymenochirus. The muscular process and arcus subocdaris are absent in H. boetcgeri 1 0 .M. Sokol 1962). The arcus subocdaris is tenuously complete in Xenupus laaXr (Trueb and Hanken 1993). In pipids, the otic process does not reach the anterior end of the otic capsde ( 0 . M. Sokol1975), and the ascending and otic processes are h e d into a broad plate ( 0 . M. Sokol 1977a). The connection of the ascending process to the neuroaanium is more dorsaliy placed (a "high" attachment) in basal taxa such as Ascaphus and Bombina and more ventraliy placed ("low") in neobatrachians ( 0 . M. Sokol 1975). In microhylids, the ascending process has a low attachment directly to the trabecula because the pila antotica is absent i O. M. Sokol1975). The ascending process is absent in larvae of Heleophlyne, Otqhlyne, and Philautus (see Haas 1995). The ascending process is lost during metamorphosis in ali frogs except Ascaphus tmei (Van Eeden 1951); Reiss i 1997) disagreed with this interpretation, claiming that the persistent ascending process in Ascaphw is oniy part of &e neurocranium. Ascaphus -i is also unique among -inura in retaining the "true" basal process in which the connection to the neurocranium is anterior to the palatine nerve i De Beer 1985; Pusey 1938). The condition in Lewpelma is somewhat intermediate (Pusey 1938; E. M. T. Stephenson 1951), and ali other frogs surveyed have the pseudobasal process. Pyles (1987) summarized the issues regarding the homology of the pseudobasal/basal process. Reiss's (1997) intensive study of the larva of Ascaphus reached somewhat
63
different conclusions about the phylogenetic significance of certain suspensorial characters than did L. S. Ford and Cannateiia (1993), but because these characters are germane primariiy to addts, a U e r critique of Reiss (1997) wiii not be undertaken here. In Leupelma archeyi, which has nidicolous development (Altig and Johnston 1989), the larval otic process remains unbroken through metamorphosis (N. G. Stephenson 1951b). Heleophlyne purcelli has an apparently unique quadrato-oticligament that attaches the rear end of the palatoquadrate to the floor of the otic capsde (Ramaswami 1944; Van Der Westhuizen 1961); this is distinct from the connection of the larvai otic process to the otic capsdes. Orton (1943) figured a cartilGe of unknown hokology in a RhinUphlynus donalis tadpole, which was identified as a free hyoquadrate process by O. M. Sokol(1975: fig. 12). Ossification of the quadrate is known in onlv a few taxa of frogs (e.g., Ascaphus truei), and quadratojugais are absent in many taxa. The maxillae, premaxillae, pterygoids, and squamosals are present in ahost ali taxa (Tnieb 1993). Four principal ligaments are associated with the jaws (fig. 4.4; see aiso fig. 4.16): (1) the quadratoethmoid ligament (ligamentum quadratoethmoidaie,I. cornu-quadraturn mediale; Schulze 1892), (2) lateral circumoral ligament ( 0 . M. Sokol 1981b) (I. cornu-quadraturn; I. cornu-quadram laterale; 1. circumorale; trabecular quadrate li&ment; Pusey 1943), (3) mandibdosuprarostral ligament (I. rostraie superius cartilago Meckeli of Gradweii 1968), and (4) the suirarostrai-quadrate ligament (I. rostrale superius quadrati; Gradweii 1968). The quadratoethmoid ligament extends from a process (processus lateralis trabecdae; Haas 1995) on the posterolateral aspect of the trabecdar horn to the quadratoethmoid process of the quadratocranial commissure. This ligament lies ventral and lateral to the internal naris. The lateral circumoral ligament passes from the tip of the trabecular horn to the anterolateral margin of the pars articdaris quadrati. The 1. mandibdosuprarostraiearises from the insertion of the m. levator mandibdae ~osteriorsu~eríicialison the dorsal surface of Meckel's cartilage and passes to the posterior dorsal process of the suprarostral or adrostral. The 1. rostrale superius quadrati connects the posterior dorsal process of the suprarostral to the anterolateral margin of the pars articdaris quadrati near the attachment of the lateral circumoral ligament. Diversity. The quadratoethmoid ligament seems to be universaliy present. The mandibdosuprarostral ligament is absent in Ascaphus, microhylids, and pipoids (Haas 1995); in Type 4 tadpoles it attaches to the adrostral tissue mass rather than to the suprarostral cartilage as in discoglossids (Haas 1995). The lateral circumoral ligament attaches to the suprarostral rather than the trabecdar horn in Alytes, Ascaphw, Bombina, and Discoglossus (0.M. Sokol 1981b). Pipids have lost the lateral circumoral ligament but Rhinophlynus apparently retains it in the discoglossoid condition (0.M. Sokol 1981b).
64
DAVID CANNATELLA
h e rJaws The lower jaws consist of paired Meckel's cartilages and paired infrarostral cartilages (infralabial cartilages, mentomeckelian cartilages) joined at the midline by connective tissue (fig. 4.5). The infrarostrals are placed posterior and slightly lateral to the suprarostrals. The two infrarostrals are connected by a slender cartilage, the commissura intrarnandibularis (fig. 4.5). In Rana, a second, condylar articulation is present ventral to the cornrnissura, but it is not synovid. Although the infrarostrals have been termed mentomeckelian cartilages (0. M. Sokol 1975), the extent of these is much greater than the mentomeckelian bones (J. J. Wiens 1989). Meckel's cartilages are generally stout and shallowly V-shaped; they are not associated with the lower jaw sheath. The medial end of Meckel's cartilage generally bears a cotyle for articulation with the infrarostral cartilages. The articulation with the pars articularis quadrati of the palatoquadrate is saddle-shaped and subterminal; thus, there is a posterolaterally directed retroarticular process on which the suspensorio-, hyo-, and quadratoangularis muscles insert (0. M. Sokol1981b). The articulation with the palatoquadrate has a well-developed synovial capsule. The bones associated with the lower jaw are the paired angulars (angulosplenials), articulars, dentaries, and mentomeckelians. The endochondral mentomeckelian bone ossifies in the medial ends of the larval infrarostral cartilage. The dentary and angular are elongate dermal bones that invest Meckel's cartilage. The angular is posterior and medial and the dentary anterior and lateral to Meckel's cartilage. The ar-
ticular ossifies endochondrally in the posterior end of Meckel's cartilage at the jaw articulation. Diversity. The infrarostrals of R r c a p h are splintlike elements (Van Eeden 1951). In pipoids, the shape of the lower jaw resembles the adult co~guration-slender and gently curved. The angular ossifies earlier than in nonpipoid frogs (0. M. Sokol 1977a; Trueb 1985). The infrarostrals are fused medially in some microhylids (De S i and Trueb 1991; 0.M. Sokol 1981b) and apparently in Huplobatrachus tigerinus (Ramaswarni 1940). Fused infrarostrals (0. M. Sokol 1975) are a synapomorphy for Pipoidea. A syrnphysial joint later develops between the infi-arostrals during metamorphosis, but mentomeckelian bones do not develop in Pipoidea. Separate, so-called sub-meckelian cartilages are known in Heleophryne (Van Der Westhuizen 1961), and Alytes (called pararnandibularia; Van Seters 1922); these cartilages are not in the same position in Alytes o b s t (per~ ~ sonal observation) as in Heleuphryne.
B d Flow Muscles Most of the cranial muscles of premetamorphic larvae are found in the adult frog, albeit with different names at times. However, all muscles are transformed during metamorphosis as the larval fibers die and adult-type fibers develop from myoblasts (Takisawa et al. 1952a, b; Takisawa and Sunaga 1951). Gradwell and Walcott (1971) discussed the dual functional and structural aspects of these fiber types in the interhyoideus muscle. These muscles are summarized in table 4.2. In a premetamorphic tadpole of Raw tempmaria at Kopsch stage 25 (Kopsch 1952), the muscles of the buccal
Ceratobranchial IV
Terminal commissure
Fig. 4.7. Ventral view of the gill arch skeleton of a Rana catesbeiana tadpole. Symbols: dashed lines = lower jaw. Afier Gradwell (1972a).
65
ARCHITECTURE Table 4.2 Origins and insertions of selected cranial muscles in a Gosner stagc 35 tadpc)te of Ranacatefbeiam, modified from Gradwell 1972b. Terminology is based on Ram t m p u r i a (Edgeworth 1935) as modified by Haas (1997a); CB = ceratobranchial. Muscle
Origin
Insertion
Mandibular Group -
Levator mandib~daeposterior superficiaiis L. m. p. profundus L. m. anterior
I-. m. externus L. m. a. articularis L. m. a. subexernus L. m. a. lateralis Intermandibularis anterior Intermandibularis posterior Mandibulolabialis
-
Dorsal part of palatoquadrate
Dorsal, medial part of Meckel's cartdage
Dorsal part of palatoquadrate Dorsal part of ascending process of palatoquadrate; otic capsule Anterior part of muscular process of palatoquadrate Dorsal, lateral part of palatoquadrate Anterior, medial surface of muscular process of palatquacirate (appears at stage 40 in Rana catesbeianu) Anterior, medial surface of muscular process of palatoquadrate (appears at stage 39 in Ram caesbeiana) Interconnectsinfkarostrals; no median raphe Median raphe Anterior part of Meckel's cartilage
Lateral part of suprarostral cardage Dorsal, lared part of Meckel's cartilage Lateral part of suprarostral cartilage Dorsal, lateral part of Meckel's cartilage Lateral part of suprarostral cartilage Dorsal, lateral part of Meckel's cartilage Medial part of Meckel's cartilage Lower lip
Hyoid Group Lateral part of ceratohyd
Orbitohyoideus Suspensoriohyoideus Interhyoideus Interhyoideusposterior
Inferior, lateral part of muscular process of palatoquadate Superior, lateral part of muscular process of palatoquadate Lateral part of muscular process of palatoquadate Posterior, lateral part of muscular process of palatoquadate Median raphe Median raphe -
Retroarticular process of Meckel's cartilage Retroarticular process of ~Meckel's adage RetroarticuIar process of Meckel's cartilage Lateral part of ceratohyal Lateral part of ceratohyal Lateral part of ceratohyal Palatoquadrate + otic process + diaphragm
-
Branchial Group Levator arcus branchiatis I
I.a. b. I1 L. a. b. I11 L. a. b. IV Constrictor branchidis I C. b. I1 C. b. 111 C. b. N Subarcualis rectus I, dorsal head S. r. 11, ventral head S. r. 11-IV Subarcualis obliquus Transversus ventralis IV T>mpanopharyngeus Diaphragmato-branchialisIV LTnnarnedmuscle (Cucullaris?)
Lateral part of palatoquadrate Otic process Auditory capsule Auditory capsule Not present in Ram; see text medial part of CB I1 Medial part of CB I1 medial part of CB 111 Posterior, medial part of ceratohyal Posterior, medial part of ceratohyal Medial part of CB I1 Crista hyoidea Not present in Ram; see text Auditory capsale Medial part of diaphragm Lateral part of CB N
Lateral part of CB I Lateral part of CB I Anterior, lateral part of CB I1 Posterior, lateral part of CB II Tenninal commissure of CB I and I1 Terminal Commissure of CB I1 and 111 Terminal Cornmissure of CB I1 and 111 Medial part of CB I Medial part of CB II Medial part of CB IV Medial part of CB I1 Lateral part of CB IV Terminal commissure of CB I1 and I11 Scapula
Spinal Group Geniohyoideus Rectus c e ~ c i s
Hypobranchid plate Medial part of diaphragm; continuation of rectus abdorninis
Infrarostral cartilage Medal part of CB 11
ARCHITECTURE
coili) lies posterior to the interhyoideus; its haives join at a mediai raphe and extend laterdy to attach to the posterior paiatoquadrate, the otic process, and the lateral part of the diaphragm. The larvai diaphragm is the posterior w d of the sinus cervicaiis, or pericardial space, surrounding the heart. In the adult frog these muscles are expanded to form a more or less continuous muscular floor for the buccai cavity. The geniohyoideus is a paired, thm, elongate muscle (figs. 4.84.9) that originates on the hypobranchal plate and inserts on the infrarostrai cartdage near the symphysis. In Rana temporaria it consists of a pars lateralis and pars medialis innervated by spinal nerves that comprise the hypoglossai nerve. The rectus cervicis muscle (sternohyoideus, diaphragmato-branchalis medialis), whch extends from the branchial process of ceratobranchial I1 to attach to the larval diaphragm, is also suppiied by the hypoglossai nerve. The tongue muscles proper, the genioglossus and hyoglossus, have not yet formed, but in Rana temporaria these diierentiate as the foreiimbs are emerging (De Jongh 1968). Diversity. Differentiated portions of the intermandibularis form supplementary elements (Emerson 1976; Tyler 1971)
67
in various taxa, but these are not apparent until near metamorphosis. Starrett (1973) reported that in microhylid tadpoles the intermandibularis posterior inserts on the basihyai (copula 11) rather than a mediai raphe. She also reported an infraiabial retractor muscle that joins the infrarostrai cartilage to Meckel's cartilage in microhylids. Presumably it retracts the lower jaw and closes the mouth. Starrett (1973) speculated that t h s muscle was homologous with the mandibulolabialis of Types 3 and 4 tadpoles. In several species a mandibulolabialis superior inserts onto the upper iip and a mandibulolabialis inferior inserts onto the lower iip (Carr and Altig 1991). The mandibulolabiaiis is apparently absent in some Type 1 larvae; it is present in Gastrqpblyne carolinensis and Microbyla pulchra and absent in Hoplophlyne rogersi and Pblynomantis (= Pblynomerus) annectens (Gradweii 1974; Noble 1929). Gradweii (1972b, c) pointed out that the interhyoideus posterior muscle (H3b in his terminology) occurs in Pelobates, Pseudis, Rana catesbeiana (contrary to Edgeworth 1935), and R. fiscigztla but not in Ascapbus, Pblynomantis, pipoids, or Scapbzopus. Gradweii (1974) later diustrated and described an extensive interhyoideus posterior in Pblyno-
ideus
(
~iaphragmato-branchiali; ~ympano~hafyn~euS ~ e c t u çcervicis
Fig. 4.9. Ventraiview of the musdes of the jaws and branchiai apparatus of an idealized tadpole, based on Gradwell (1972a), with additions.
I
68
DAVID CANNATELLA
mantis annectens. Noble (1929) mentioned that an extensive subbranchialis (interhyoideus posterior) covering the ventral w d of the branchiai chamber in Gactrophlynecarolinensis and Micvohyh pulchra is absent in two species of HoplUplnyne. O. M. Sokol (1975) reported that the interhyoideus posterior is absent in bufonids and leptodactylids and present in some hylids, microhylids, and some pelobatids. Gradweii (1972b) ais0 claimed that the superíicial and deep layers of the interhyoideus posterior of Rana catesbeiana were identical to the subbranchialis and diaphragmatopraecordialis muscles (respectively) described by Schulze (1892) for Pelobates. Haas (1997a) pointed out that the diaphragmatopraecordialis muscle of Pelobates is a specialized part of the interhyoideus posterior. 0 . M. Sokol (1975; see fig. 4.9) iilustrated the superficial and deep layers of the interhyoideus posterior of Pelobates syriacus. My comparison of the illustrations in Gradwell (1972b), Schulze (1892), and O. M. Sokol (1975) supports Gradwell's contention. Muscles with similar names were described by Noble (1929) in the suctoriai tadpoles ofAmolUpsricketti. Haas's (1997a) phylogenetic anaiysis indicates that the presence of an interhyoideus posterior is a synapomorphy of Pelobates + Neobatracha, a clade that would render Mesobatrachia (fig. 4.1) paraphyletic. However, if the interhyoideus posterior is absent in Scaphzopus as claimed by Gradweii (1972b, c), and assurning that Pelobatidae (Scaphzupus + Pelobates) is monophyletic, then homoplasy in this character makes the putative synapomorphy for Pelobates + Neobatracha ambigÜous. Noble (1929) described a pars locomotorius of the subhyoideus (interhyoideus) that inserts bilaterdy into paired cutaneous flaps flanking the mediai spiracle in HoplUphlyne. Noble speculated that these flaps served as locomotor organs in the damp leaf crevices in which these nonaquatic larvae hve. Edgeworth's (1935) table of muscle synonyms lists the constrictor coiii muscle in frogs as a synonym of the subbranchaiis, but his text does not mention the constrictor colli. Jaw Levator Muscles There are two morphologicai units of levator (adductor) muscles. One group consists of three levator muscles that
originate from the posterior portion of the paiatoquadrate and adjacent otic capsule and extend fonvard through the floor of the orbit mediai to the muscular process of the paiatoquadrate to insert onto the suprarostral and Meckel's cartilage. The second group originates from the anterior mediai region of the muscular process and extends ventromedidy to insert on Meckel's cartiiage and the suprarostral. Aü of these muscles are innervated by the trigeminai nerve (V). The terminology of these muscles is particularly confused (table 4.3), and Starrett's use of the path of the mandibular brandi (V,) of the trigeminai nerve for distinguishmg anterior, posterior, and externus groups of adductor muscles is not used here. The most superíicial muscle (fig. 4.10) in the first group is the levator mandibulae posterior superficialis. It originates on the dorsai surface of the palatoquadrate laterai to the ascending process and extends fonvard to insert on a rounded process on Meckel's c a d a g e lateral to its articulation with the drarostrai cadage. The levator mandibulae posterior profimdus lies just below the I. m. p. superficialis and originates on the dorsai surface of the paiatoquadrate just below and slightly laterai to the origin of the I. m. p. superíicialis. In Rana temporaria the I. m. p. superíicialis and 1. m. p. profundus are fused through the posterior haifof their lengths (De Jongh 1968). The I. m. p. profundus inserts via a compound tendon on the ventrolateral edge of the suprarostral. This compound tendon aiso receives the insertion of the I. m. externus complex in &na temporaria but apparently not in R. catesbeiana (Gradwell 1972b). The deepest and most mediai of the three muscles traversing the orbit is the levator mandibulae anterior (fig. 4.10). It originates from the anteroventrai surface of the auditory capsule and the ventral aspect of the ascending process of the paiatoquadrate; the area of origin is mediai to that of the I. m. posterior superficialis and I. m. posterior profimdus. Its fibers converge into a distinctive long tendon that inserts on the dorsai side of Meckel's cartilage just mediai-to the jaw joint. The I. m. anterior lateralis differentiates from the I. m. anterior during metamorphosis in &na temporavia and at Gosner stage 39 in R. catesbeiana (Gradwell 1972b). The second group of muscles arises from the muscular process of the paiatoquadrate (fig. 4.10): the levator mandi-
Table 4.3 Comparisons of the terminology of jaw muscles in tadpoles (adapted from Starrett 1968) of Edgeworth 1935, Starrett 1968, Luther 1914, Sedra 1950, and the terminology for adults from Edgeworth 1935 Edgeworth
Starrett
Luther
A. m. pterygoideus Levator mandibulae anterior Adductor rnandibulae anterior internus A. m. anterior longus A. m. posterior longus L. m. posterior superficialis A. m. posterior superficialis superficialis A. rn. posterior profundus A. m. posterior longus L. m. posterior profundus profundus A. rn. posterior subexternus L. m. anterior subexternus A. m. posterior subexternus A. m. posterior articularis A. rn. posterior articularis L. m. anterior artidaris A. m. externus superficialis A. rn. externus L. m. externus L. m. anterior lateralis
A. m. externus lateralis
A. rn. posterior lateralis
Sedra L. rn. anterior
Edgavorth (Adult) Levator rnandibulae anterior
L. rn. posterior superficialis L. m. posterior L. rn. posterior profundus
L. m. posterior
L. m. externus pars anterior L. m. externus pars posterior L. m. anterior lateralis
L. m. anterior subexternus L. m. anterior artidaris L. m. externus L. m. anterior lateralis
70
DAVID CANNATELLA
ified drawing in which the pars posterior was no longer pres- to the insertion of the suspensorioanguiaris. The quadratoent, and he remarked that h s pars anterior was homologous anguiaris originates on the ventrolaterai aspect of the paiatowith the 1. m. externus and that the I. m. subexternus (pre- quadrate, is bounded laterdy by the bodies of the hyoangusumably his pars posterior) did not appear u n d stage 40 in laris and suspensorioanguiaris, and inserts on a common Rana uztesbeiana. The distinction between the I. m. externus aponeurosis with the hyoanguiaris. These three muscles and I. m. subexternus is particularly important because Star- form part of the depressor mandibulae of the adult. rett (1968) defined character states for the levator muscles based on the relationship of the mandibular branch of the Diversity. Starrett (1968) reported the occurrence of these muscles in many taxa, but these data are inconsistent with trigeminal nerve (V,) to these muscles. The fates of the larvai mandibular and hvoid muscles of some other reports, including Starrett (1973). For example, Bufi regularis, Rana temporaria, and Xenopus lmis were dis- pipoids have a single mandibular depressor muscle, the cussed by Sedra (1950) and Sedra and Michael (1957). quadratohyoangularis, which is thought to represent fusion Metamorphosis in Xenopus appears to be very different from of the three muscles ( 0 . M. Sokol1962,1977a); ontogenetthat in the other two taxa, but this may be caused by rnis- icdy, it appears as a single muscle in Xenopus laevis (Nieuwidentifications of certain muscles. Sedra and Michael (1957) koop and Faber 1967). However, Starrett (1968) reported claimed to foliow Edgeworth's (1930) muscle terminology both the hyoangularis and quadratoanguiaris present in for Xenqus lami, but their treatment is problematic. For ex- Xenopusgilli and X. l m i . The hyoanguiaris is said to be abi 1943; Starrett 1968) and Disample, they named the largest and most superficial of the sent inhcaphus ~ e (Pusey mandibular muscles the 1. m. anterior and divided it into the coglosuspictus (Starrett 1968), but Starrett (1973) reported I. m. anterior pars intermedius, pars lateraiis, and pars medi- it present in Type 3 tadpoles. aiis. The 1. m. anterior pars medialis, on the basis of its toHaas (1997a) noted that the origin of the suspensorioanpography and its long, slender tendon, corresponds to the guiaris from the paiatoquadrate is behind the orbit in Alytes, I. m. anterior ofRana temporaria. The 1. m. anterior pars in- Ascuphus, Bombina, and Discoglosus (state O of his character termedius corresponds to the I. m. posterior pars super- 23) but in front of the orbit in Pelobates and Neobatrachia ficialis, and the I. m. anterior pars lateraiis corresponds to (state 1). In pipids, he described the origin of the single anthe I. m. posterior pars profunda based on relative positions gularis muscle as from both the quadrate and the ceratohyai and points of insertion; compare Sedra and Michael(1957) and coded the state as missing. Sokol (1977a) provided to De Jongh (1968), Edgeworth (1935), and Gradweli greater detail on the origin of this muscle, but even so, the (1971b, 1972b). Gradweii (1971b) d e d attention to this extreme distortion of the pipid paiatoquadrate precludes a discrepancy, but unfortunately followed the terminology of clear assignment to either state. In Haas's tree (1997a: fig. Sedra and Michael (1956a, 1957). 15) with charaaers optimized using accelerated transformaIn Rana, the 1. m. posterior profundus inserts on the su- tion (Swofford and Olsen 1990), state 1 is a synapomorphy prarosuai cartilage. In pipids the suprarostrai is fused to the of Pipanura. However, the delayed transformation optimizatrabecular horns, and the 1. m. posterior profundus (mis- tion would suggest that state 1is a synapomorphy of Pelobanamed the I. m. anterior pars lateralis by Sedra and Michael toidea + Neobatracha. 1957) inserts on the cartilaginous base of the tentacle of Silurana tropicalis and Xenopus lmis (Gradweii 1971b; O. M. Sokol 1977a); t h s muscle was aiso called the m. tentaculi Hyobranchial Apparatus (Nieuwkoop and Faber 1967). In Hymenochirus boettgri, The ceratohyais and branchiai baskets (fig. 4.7) are the two whch lacks tentacles, this siip inserts on the supralabial pad major components of the hyobranchial skeleton. The cera(O. M. Sokol 1977a), a transversely oval connective tissue tohyais and basibranchiai elements (copulae and hypopad that lies at the anterior edge of the ethmoid plate ( 0 . M. branchiai plates) are the pistons of the buccal pump that conSokol1962). Starrett (1973) tabulated differences in adduc- veys currents of food-laden water to the gdi filters and tor muscles among Orton's four classes of tadpoles but more branchiai food traps and irrigates the respiratory surfaces of the giiis. The branchiai baskets support the giii filters and variation exists ( 0 . M. Sokol1975) than she reported. gills. Water pumped posteriorly passes through the pharynJaw Depressor Muscles geal slits, opercular c a v i ~and findy, the spiracle(s). The hyoanguiaris, quadratoanguiaris, and suspensorioangularis, which are hyoid arch muscles innervated by the faciai Ceratohyals and Branchial Bashets nerve (VII), insert on the retroarticular process of Meckel's The ceratohyals are the main levers of the pump upon which cartiiage. The suspensorioangularis is a fan-shaped muscle muscle contraction aas. The ceratohyals lie anterior to the that extends from the lateral aspea of the base of the muscu- branchiai baskets and are generdy oriented transversely. The lar process and inserts via a short aponeurosis on the retroar- ceratohyais articulate with the paiatoquadrates by means of ticular process of the lower jaw (figs. 4.94.10). The hyoan- the synoviai hyoquadrate articulations, which are reinforced guiaris is cone-shaped and originates from the laterai aspect by a stout hyoquadrate iigament. The ceratohyals articulate of the ceratohyal slightly ventral to the articulation of the with each other medidy via copula I1 (posterior copula, ceratohyal and palatoquadrate cartilage. It inserts via an apo- copula posterior, basibranchial) and the interhyoid iigament neurosis in comrnon with the quadratomgularis just laterai (iigamentum interhyoideum, iigamentum interhyale), of
ARCHITECTURE
which the posterior part is a mass of fibrous cartilage called copula I (anterior copula, copula anterior, basihyale). The copulae represent the medial basihyobranchial structures. The pars reuniens (fig. 4.7) is a medial mass of white fibrous tissue that binds the ceratohyals together medially and also separates copula I and copula 11. The subtriangular space bemeen copula 11,the hypobranchid plate, and the ceratohyal is occupied by the intrahyoid ligament (ligamentum intrahyoideum; Gradwell 1972b). The crista hyoidea (urobranchial process) projects posteriorly Erom copula I1 and is the origin of the transversus ventralis 11 muscle. Within Am~hibia. copula I is unique to tadpoles; the pars reuniens is believed to be homologous with the hypohyals of salamander larvae and copula I1 is believed to be homologous with the basibranchials and urobranchials (0.M. Sokol1975). Together, the ceratohyals, copulae, ligaments, and parts of the hypobranchial plates form the major skeletal support of the buccal floor. The branchial baskets are posterior to the ceratohyals. Each branchial basket (fig. 4.7) is composed of a subtriangular hyobranchiai plate and four ceratobranchials. The hypobranchial plate is traditionally considered to be formed From m-o fused hypobranchial elements. However, Haas (1997a) argued that the plate is composed only of hypobranchial I, homologous with the slrmlarly named urodelan structure. The four curved ceratobranchids are fused at their ~roximal and distal ends to form a bowl with three eloniate slits; ceratobranchial I is most anterolateral. The proximal fusions are the proximal commissures (comn~issuraeproxlmales) and the distal firsions are the terminal cornrnissures (cornmissurae terminales). Near the anterior end of ceratobran&ids I1 and I11 there is a prominence, the branchial process (processusbranchialis), to which a number of bralchial muscia attach (table 4.2; Gradwell 1972b). In Rana catesbeiana mtobrandhial I is ksed to the hypob;ancl~ialplate by hyaline cartilage; the other three ceratobranchials are joined by connective tissue [Gradwell 1972b). The spicules (spicula) are four elongate cartilaginous processes projecting dorsally and posteriorly from the ceratobranchials to support the ventral velum (chap. 5). Together tfie hwobranchials and ceratobranchials form the skeletal supGr?cfor the gills and filter apparatus. Diversity. Haas (1997a) provided detailed comparative accounts of the hyobranchial skeleton and muscles of Alytes, Ascapbus, Bmsbina, and DiscoJhssus. Ridewood (1898b) first pointed out that in Alytes, Bombina, and Discoglosus, copula II separates the two l~ypobranchialplates. This state is also present in Ascapbus, and the derived condition (hypobranchial plates in contact) is a synapomorphy of Pipanura. The fusion of hypobranchial I with ceratobranchial I is also a nnapomorphy of Pipanura (Haas 1997a). Pipaparpa andxinupuslack copula I and Pipa lacks copula II (Haas 1995; 0. M. Sokol1975). Copula I of microhylids is r&e (Haas 1995). Ridewood (1897b) stated that there is no copula I in Pehbates or Pehdpes, but Rotek (1981) reported copula I in Pelobates &stus. Ridewood (1897a) termed copula I1 the basihyal but acknowledged the homol-
71
ogy of copula I1 with the basibranchial and of copula I with the basihyal. In certain taxa the ceratobranchials are fi~sedto the hypobranchial plates, and in other taxa the attachment is perichondrial or collagenous; the branchial baskets are bound to the copula by ligaments or perichondrium or may be fused in sorne taxa, such as suspension-feeding microhylids (Haas 199613; 0.M. Soko11975).Hymenochirines have only two of the four ceratobranchials (Memies 1967; 0. M. Sokol 1962). Certain ceratobranchials are also lost in the bromeliad-dwelling larvae of Hylapicadui and H. zeteki (personal observation). Noble (1929) reported only one ceratobranchial, with a single branchial slit posterior to it, in two species of Hqkrphlyne. In most pipoid larvae and in some microhylid larvae, the filter plates, which are supported by the ceratobranchials, are chondrified. In many species, both ceratobranchials I1 and I11 bear a branchial process for muscle attachment at their proximal ends (Haas 1997a). Dendrobatids are unique in having free proximal ends of ceratobranchids I1 and I11 (Haas 1995). Haas (1993, 1995, 1997a) described several character states for the ceratobranchials it1 a wide variety of taxa. Muscles Associated with the Ceratohyal The orbitohyoideus and suspensoriohyoideus (figs. 4.94.10), which are hyoid muscles innervated by the facial nerve (VII), originate on the muscular process and insert on the ceratohyal. The orbitohyoideus is a very large, tapering muscle that originates along the curved upper margin of the muscular process. Most of the concave lateral surface of the process lacks muscle fiber attachments. The orbitohyoideus extends ventrally and slightly posteriorly to a fleshy insertion on the ventrolateral edge of the ceratohyal and conceals the origins of the hyoangularis, quadratoangularis, and suspensorioangularis. The suspensoriohyoideus muscle originates from a broad surface on the posterior edge of the muscular process and is partially concealed by the orbitohyoideus; it extends ventrally to insert just dorsal and slightly posterior to the orbitohyoideus. In the adult these muscles form part of the depressor mandbulae. Diversity. Haas (1997a) compared the hyobranchial musdes of Alytes, Ascapbus, Bombilza, and Dis~o~hssus. His work indicates significant discrepancies in the literature treating these muscles. For example, the suspensoriohyoideus is reported absent in Ascaphus (Pusey 1943), but Haas (1997a) reported it as present. 0. M. Sokol (1977a) reported the suspensoriohyoideus as absent in Pipa mrpalboi and present in Iiym~nochirwsboettflmem and Silurana mpicaLis. Gradwell (1971b) said it was present in Xenopus laeve?. Starrett (1968) indicated that the suspensoriohyoideus was absent in Rhinophpus and X. hems but later (1973) reported it present in pipoids. The muscles associated with the ceratobranchials are cornplex; difficulties in assessing their homology within Anura and with other vertebrates have resulted in various sets of terminology. Clarification of the homologies would require
72
DAVID CANNATELLA
extensive comparative work (see Fox 1965; Haas 1997a; Joiiie 1982; Wiley 1979), but compared to the jaw muscles and chondrocranium, there are few comparative data on the muscles of the branchial baskets. Because of the general confusion regardiig muscle identities, taxic diversity is included with the description of each muscle. These muscles are supplied by the glossopharyngeai ( E ) and vagus (X) nerves. The functions of these musdes are discussed below under Gdi Irrigation in Rana catesbeiana.
explanation, placed the branchiohyoideus correctiy in his branchiai rather than hyoid group. Schiosser and Roth (1995) did not discuss the significance of their findings for issues of muscle homology. Haas (1997a) interpreted their implicit homologization to mean that the constrictor branchiahs muscles had traditionaiiy been misnumbered, and he argued strongly for adoption of the new labels. Some observations support this new scheme: (1) the seriai innervation of the four putative constrictor muscles by Levator Arcus Branchiaiis. Four h, wide muscles com- craniai nerve M and three rami of craniai nerve X is consisprise the levator arcus branchialis series or levatores arcuum tent with this scheme, (2) the branchiohyoideus of saiamanbranchialium (branchiai levators; fig. 4.9). In Rana tempora- ders is reportedly innervated by craniai nerve VI1 and thus ria these are four discrete muscles that extend from the lat- is unlikely to be homologous with the ccbranchiohyoideus eral and posterolaterai margin of the ceratobranchiai basket externus" of frogs (constrictor branchialis I, sensu novo), dorsaiiy and attach to the posterior part of the paiatoqua- and (3) the dista1 end of the constrictor branchialis I1 and &ate and adjacent otic capsde. This series was confúsingiy I11 (sensu novo) is closely placed to the proximai ends of caiied the constrictor branchialis (for 1-111) and levator arcus levators I1 and 111. The distai end of constrictor branchiahs branchiahs (for IV) by Sedra and Michael (1957) and the I (sensu novo) is aiso closely placed to levator I. This is in constrictor arcus branchialis by O. M. Sokol(1977b). accord with Edgeworth's (1935) contention that the anuran Levators 1-111 are fused in Xenopus l d s ; Sedra and Mi- constrictors and levators form fiom the dorsai portion of the chael (1957) incorrectiy reported fusion of I-IV accordiig four branchai muscle plates. to O. M. Sokol (197%). In Pipa carnalboi muscles 1-11 are Other observations do not support the proposed homolfused, and Hymenochirzrs boetijeri lacks levators I1 and 111, ogy but are not directiy contradictory. (1) The constrictor apparentiy related to the fusion (or lack) of ceratobranchais branchialis I (sensu novo) extends between arches (i.e., 11-IV (O. M. Sokol 1977a). These musdes apparentiy have ceratobranchai I to the ceratohyal) whereas each other condisappeared in addt Rana or possibly form the petrohyoid strictor lies aiong one ceratobranchiai, and (2) the urodelan branchial depressors are believed to be homologous with the series. anuran constrictors. The urodelan depressor branchalis I lies Constrictor Branchiaiis. There are three constrictor only aiong ceratobranchai I and has no attachment to the branchialis muscles (1-111) in Rana catesbeiana; each musde ceratohyal (Haas 1997a: fig. 13), so ifthis muscle is homoloextends from the mediai end of its own ceratobranchiai g o u with the anuran constrictor branchialis I (sensu novo) aiong the anterior margin of the giü slit to the terminal com- then the attachments of the latter have shifted considerably. missure. These muscles are intimately associated with the (3) The general placement of the urodelan depressors I, 11, afTerent and efferent branchial arteries and gdis. The con- and I11 closely matches that of the three traditional anuran strictors apparentiy regulate the flow of water through the constrictors I, 11, and 111. (4) Each of the three classical angiii slits by changing the position of the interbranchiai septa uran constrictors lies in intimate contact with an afTerent (O. M. Sokol 1977a) but do not function during regular branchiai artery aiong the ceratobranchiai; the constrictor phasic pumping (Gradweii 1971b, 1972~).No tadpole has branchiahs I (sensu novo) has no such association. (5) Ala muscle extendiig aiong the length of ceratobranchiai IV though the innervation of constrictor branchaiis I (sensu (O. M. Sokol1975); Pusey (1943) claimed that constrictor novo) by nerve M is consistent with that muscle belonging to the first branchial arch, it does not necessarily foiiow that IV was fused with levator n! The traditional seriation of the constrictors was chal- the musde is a constrictor branchahs per se. These differences do not reject the proposed homology lenged recentiy. Using whole-mount imrnunohistochemistry, Schiosser and Roth (1995) identified the innervation of with constrictor branchiahs I (sensu novo) but simply indifbur branchai arch muscles by the principal ramus of craniai cate that the anatomy of that muscle is somewhat modified. nerve M and three branchiai trunks of craniai nerve X, re- For example, Schiosser and Roth (1995) reported that the spectively. They named these muscles constrictor branchialis first branchiai trunk of craniai nerve X innervates structures I, 11, and 111. What was surprisingwas that their constrictors of the second branchial arch, including levator arcus I1 and I11 corresponded in anatomical position to the tradi- branchialis 11, constrictor branchalis 11, subarcualis rectus tionai constrictors I and I1 as described for Rana by others. 11-n! and transversus ventrahs I1 (= subarcualis obliquus of Their (new) constrictor branchalis I had been caiied the Haas 1997a). However, their constrictor branchialis I1 actubranchiohyoideus externus (= ceratohyoideus externus) be- aiiy lies aiong the first branchiai arch in intimate contact with cause of its presumed homology to the urodelan branchio- the first afTerent branchial artery. The same applies to the sechyoideus, a muscle of the hyoid arch. The branchohyoideus ond branchai trunk of craniai nerve X, which innervates the externus was reported inrlscapbus,Bombina, Dismjlossus (h-third branchial arch. One can infer that the constrictor mussey 1943), and Scaphiopus (O. M. Sokol 1975) but not in cles must have significantiy shfted their points of attachPelobates or any neobatrachian. Gradweii (1971a), without ment, assuming that the new homologies are correct. Accep-
ARCHITECTURE 'Table 4.4 Homologies of muscles of the branchial baskets, as described by various authors for specified taxa .-
Edgeworth 1935 Ram
Pusey 1943 Ascupbus
Sedra and Michael 1957
Sokol 1975,1977a Pipa
Subarcualis rectus I1
Constrictores m u m branchialium (hsed) (fused) (fused) Ceratohyoideus externus Interbranchialis I
Subarcualis re~tus111 Subarcualis recms I V Subarn~alisrectus 1
Interbranchialis I1 S. r. IT-IV S. r. I
Absent
Ceratohyoideus internus Absent
Ws
Levator arcus branchiah I
Levator arcus brachialis I
Constrictores arcuum branchialium
L a. b. Il L a. b. LII L a. b. IV
L. a. b. 11 L. a. b. I11 L. a. b. N
.knt
Branchiohyoideus externus Constrictor branchialis I C. b. I1 C. b. I11 Subarcualis rectu.9 I Absent
(fused) (fused) Levator arcuum IV Absent
Consmctor branchialis I C . b. II C . b. I11 Subardis r mI 5. r. II S. r.
m +N
Tiam-ersus venrralis II Dqhragrnatobranchialis IV Sot described -bsent -Absent
Subarcuales recti IV and ?V Subarcualis obliquu% 11-IV and ?V Diaphrapatobranchiah Absent Transversus ventralis N Absent
Absent
Haas 1996b Gamtheca
Haas 1997a Bombina
Levator arcus branchialium I
Levator arcuum branchialium I
L. a. b. TI Laa. b. 111 L. a. b. N
L. a. b. I1 L, a. b. 111 L, a. b. IV
Absent
Constrictor branchidis I C. b. I1
Constrictor branchidis I C. b. I1 C b. 111 Branchiohyoideus internus Subarcualis rectus
n
C. b. 111 C. b. IV S. r. I (dorsal head) S. r. I (ventral head) S. r. 11-IV
Transversus ventralis I1
Subarcualis obliq uus
Subarcualis rectus IV Transversus ventralis I1
Not described Transversus ventralis IV Absent
Diaphragmatobranchi alis Tympanopharyngeus Absent
Diapluagmatobranchialis Tympanopharyngeus Absent
Diaphragmatobmchialis Absent Absent
Absent
Laryngcobranchialis
Absent
Absent
Subarcualis obliquus
m c e of this shift in attachment of constrictores branchiales but were named subarcualis rectus 11-TV. In reporting tlwee II and IIIleads to the conclusion that the attachment of con- muscles in Xinopus, Gradwell (1971b) followed Sedra and rtrictor branchialis I is part of a common pattern. Given the Michael's terminology but named them B2a, 2b, and 2c, as rrature of their whole-mount preparations, it is not clear he did with the constrictor branchialis muscles of other nonakxher Schlosser and Roth (1995) were able to see the pipid taxa that he studied. banchial arch or the artery, or whether they recognized the Haas (1997a: fig. 13) also illustrated, but did not discuss, significance of their muscle identifications. three branchial constrictors in Oduntibvynus and Pelabates. I have followed the new arrangement of Schlosser and The first of these in Odontophyus is labeled constrictor RMh (1995) as promoted by Haas (1997a). The traditional branchialis 11, but the last avo are both labeled constrictor amsnictors I, 11, and I11 are simply renumbered 11,111, and branchialis 111, an error in labeling (Haas, personal commun-:and the branchiohyoideus externus muscle (found in nication). Assuming the last muscle is in fact constrictor ant)- a few frog species) is renamed constrictor branchialis I branchialis IV, its origin is correctly shown on ceratobranI @. 4.9; table 4.4). chid I11 rather than TV as Haas (199%) illustrated forhcaHaas (1997a: fig. 13b) reported a short constrictor phus; this does not tnean that Haas's illustration ofhmphus banchialis IV (sensu novo) in two specimens of leutphus, is incorrect. The attachments of the three constrictor muscles similar in appearance to that described by Pusey (1943). in Oduntophrynus and Pelabates are almost identical to those Hon-ever, Haas described and illustrated it attaching to the in Rana (fig. 4.9). tnse of ceratobranchial IV rather than ceratobranchial I11 as Haas's (1997a) phylogenetic analysis indicated that the in Pusep (1943). Gradwell (1973) reported and illustrated absence of the constrictor branchialis I (sensu novo) was a the same muscle (as R2c) on ceratobranchialII1 ofAscapbus. synapomorphy (character 19) for the ciade Pipanura. HowBixh Gradwell and Pusey reported that the muscle is ever, Haas did not include data from Smphiqpus or Spea, and amached to the incipient branchial process at the base of Sokol (1975) reported that these larvae have the muscle (I oaarobranchial 111and inserted into soft tissue rather than have verified &is for Speu bombzfions). If one assumes that mto the ceratobranchial. Haas (1997a) reported this muscle Speu is the closest relative of Pelabates (among the taxa Haas &mt in Alytes, Bombina, and Disc~lassus.Pusey (1943) examined), then under parsimony optimization the muscle ared its presence on ceratobranchial I11 in Dis~~lassus.must have reappeared in Spea. Clearly, a greater range of tax0.AI. Sokol(1975) erred in claiming that there was no con- onomic sampling is needed. striaor (he termed these interbranchialis muscles) on cerato'bc;Lochlal n I in Types 1 and 3 tadpoles. Three constrictors Subarcuaiis Rectus, The homology of the four subarcualis me illustrated in Xmpus hem (Sedra and Michael 1957) rectus muscles with those of other amphibians and fish is
74
DAVID CANNATELLA
particularly troublesome (Jollie 1982; Wiley 1979). In anurans these muscles extend more or less longitudinally, connecting each gill arch to the one in iiont. Subarcualis rectus I connects the ceratohyal to the ceratobranchials, and subarcualis rectus 11,111, and IV span the ceratobranchlals. Haas's (1997a) interpretation of subarcualis rectus I is followed here. This muscle has several conformations. InAscapbus it has but one head. In some species (e.g., Bombina) there are two closely placed slips that connect the base of ceratobranchial to the ceratohyal. In other species the two slips are more dstinct, and the deeper (viewed ventrally; fig. 4.9) dorsal head extends from the base of ceratobranchial I to the processus posterior hyalis on the ceratohyal. The ventral head stretches &om the branchial process of ceratobranchid I1 to the ceratohval. These heads are so distinct as to have been given different names (e,g., ceratohyoideus internus; table 4.4). Subarcualis rectus I is innervated by the principal ramus of cranial nerve LX (Schlosser and Roth 1975). The remaining part of the muscle series, the subarcualis rectus 11-IV, is a band of muscle extending across the proximal parts of ceratobranchials I-IN, as in Ascapbus. The compound nature of this muscle is suggested by the observation that in Dism~lassussubarcualis rectus 11-IV is innervated by the first, second, and (probably) the third branchial rami of cranial nerve X (Schlosser and Roth 1995). In other species (e.g., R a m temporaria) the muscle spans ceratobranchials 11-IV (as subarcualis reams 111-IV) or only ceratobranchials III-IV (as subarcualis rectus IV,Haas 1997a). The literature indicates general confusion about these muscles. The subarcualis rectus 11,111, and IV of Sedra and Michael (1957) are actually constrictor branchiatis muscies. 0 . M. Sokol illustrated a muscle in Pipa he termed the fused subarcualis reaus 11-IS( but this appears to be the third branchial constrictor (1977a: fig. 6). Subarcualis rectus 11-XV is absent inH-~emchiws ( 0 . M.Sokol1977a). Thus, it seems that there is no verified subarcualis rectus 11-IV muscle in pipids. In Rana the subarcualis rectus muscles disappear at metamorphosis.
arcualis rectus I might actually represent subarcualis obliquus I, whch is missing in frogs and salamanders. This muscle does not persist past metamorphosis.
Transversus Ventralis IV. Transversus ventralis lV is present in Ascaphus truei and salamanders (Gradwell 1973; Haas 1997a; Pusey 1943) but is not present in Rana catesbeiana (Gradwell 1972b). Haas (1997a) reported that in Ascapbus the origin is the proximal part of ceratobranchial IV and the insertion is a median coimective tissue raphe anterior to the glottis. Edgeworth (1920, 1935) reported that a poorly developed transversus ventralis IV (hyopharyngeus in his terminology) disappeared during ontogeny in young larvae of Ram. tempmaria; he also (1935) reported it absent in P$a pipa and Xenopus lamis. Sedra and Michael (1957) reported the muscle present in Xenopus t m ? , and Gradwell (1971b) fbllowed their usage. 0. M. Sokol (1977a) considered the tranmersus ventralis nTof Silurana tropicalis and Xenclpus Lamis to be synonymous with the tympanopharyngeus of Pipa. Haas (1997a) believed that Sokol was correct in his interpretation, and I follow his opinion here; in his data matrix only Ascapbus has transversus ventralis rV:Noble (1929) reported a "hyopharyngeus" in Hophphyte, but its topography does not correspond to the transversus ventralis IV of other taxa. The transversus ventralis IV does not survive metamorphosis. Tympanopharyngeus. The tympanopharyngeus muscle, as described in Rana catesbeiana (Gradwell 1972b) and Pelabates@scus (Schulze 1892), extends from the lateral aspect of ceratobranchial IV laterally to the tympanic region of the otic capsule. According to Sedra and Michael (1957) and Gradwell (1971b), in Xenupus the muscle extends from the medial aspect of ceratobranchial IV dorsal to the dilator laryngis muscle to meet the fibers of its companion in a medial raphe. In Pipa the tyrnpanopharyngeus originates medial to the dilatator laryngis and inserts on the ventral surface of the posterior pharynx (0. M. Sokol 1977a). Gradwell (1972b: fig. 1) described and figured the tympanopharyngeus of Rana catesbeiana as extendirlg from the otic capsule to ceratobranchial essentiaUy following Schulze (1892). Haas (1996b) gave the origin of the tympanopharyngeus in Gmtrotheca as the pharyngeal wall and the insertion as the pericardium and indicated that it was closely associated with the levator arcus branchialis IV and the dilatator laryngis. The descriptions presented by 0.M. Sokol, Sedra and Michael, Gradwell, and Haas are somewhat different. However, Haas (1997a) examined the muscle in a wide variety of frogs, and I accept his conclusions about the distribution of this muscle; the tympanopharyngeus is absent in Alytes, Ascaphus, Bornbina, Dism~lossus,and Ximpus and present in G ~ o t b e c a , Pelabates, and other neobatrachians but not Rana tmporamk. In his analysis, the presence of the muscle (character 16) is a synapomorphy of Pelabates + neobamchians but is reversed in Rana.
Subarcualis Obliquus. The subarcualis obliquus I1 (transversus ventralis 11) is a stout muscle that extends from the crista hyoidea of copula I1 to the branchial process in Rana (Edgeworth 1935). Pusey (1943) argued, probably correctly, that Edgeworth's (1935) terminoloby was in error and that this muscle should be called subarcualis obliquus 11. However, he pointed out that Edgeworth's transversus ventralis IV was correctly labeled. Edgeworth (1920) had earlier stated that transversus ventralis I1 was not present in any amphibian, so his (1935) listing of transversus ventralis I1 is curious. Pusey (1943) also pointed out that only Ascapbus among frogs has subarcualis obliquus 11-V. Muscles 111-V are a fused series of slips that attach to the crista hyoidea and fan out to insert on the medial portions of the ceratobrar~chials and spicdum IV (Gradwell 1973; k e y 1943). Other frogs, indudng Alytes, Bornbina, and ~ s c ~ l o s s uhave s , only subarcualis obliquus 11, which Haas (1997a) referred to as the Diaphragmato-branchialis. The diaphragmato-branchialis subarcualis obliquus. Haas (1997a) also speculated that sub- (IV) (diaphragmato-branchialis lateralis) extends antero-
ARCHITECTURE
laterally from the larval diaphragm to the process at the distal end of ceratobranch~al111; identification of this muscle in various taxa seems to be unproblematic. It is present in A[ytes, Ascaphus, Bombina, Discogloms, Gas~votheca,Pehbates, and Rana catesbeiana (Gradwell 1972b, 1973; Haas 1996b, 1997a; Pusey 1943; Schulze 1892). It is also present in Hymenochirus and Pipa ( 0 . M. Sokol 1977a) but not reported in ;Yenopus. Although the muscle name is often followed by a 'W," it does not attach to the fourth arch. However, the muscle is innervated by the third branchial ramus of cranial nenre X, which supplies the fourth branchial arch. Pusey (1943) hypothesized this muscle to be homologous to the onloarmalis muscle of salamanders. Schulze (1892) described a diaphragmato-branchialismedialis in Pelobatesfisas, but Edgeworth (1935) and Noble (1929) considered this part of the rectus cervicis/rectus abdominis series. The diaphragmato-branchialis does not persist in adults.
Cucullaris. Gradwell (1971b) and Sedra and Michael (1957) described the cucdaris in Ahupus W . F ;it extends from the lateral part of ceratobranchial IV to the scapula. In Discglossus the muscle appears in a Gosner 33 tadpole (Schlosser and Roth 1997a). The cucullaris is a classical branchial arch derivative in tetrapods, but it is not described from any other frogs. Gradwell (1972b: fig. 1 and table 2) figured an unnamed branchial muscle with its origin on the lateral part of ceratobranchial and insertion on the scapula. This may be the cucullaris.
The Larynx and Its Muschs In adult frogs (except pipids) the larynx consists of paired, crescent-shaped, movable arytenoid cartilages that are nestled within the cricoid ring (annulus cricoideus); in pipids the larynx is highly modified (Ridewood 18976). In Rana tempovaria the laryngeal muscles form before the arytenoid and cricoid ring chondrifjr during metamorphosis (Edgeworth 1920). Ridewood (1897a) noted that the larynx begins to appear in ;Yenupus at stages in which the hind legs are just appearing, and that in Pipapipa the larynx is present in embryos of 12 rnm SVL. Sedra and Michael (1957) noted that the primordia of the arytenoids are feebly developed in a Nieuwkoop/Faber 55 cadpole of %nupus laevis. J. J.Wens (1989) noted that the larynx of Spea bombzj+ons chondrifies rapidly at the end of metamorphosis. Trewavas (1933) discussed the laryngeal development of several raxa. It appears that the larynx develops earlier in P+a and Xenqus than in other frogs. The muscles of the larynx are derived from esophageal constrictor muscles rather than from the muscle of the gill arches (Edgeworth 1920); they are innervated by the la*geal branch (ramus laryngeus) of the vagus nerve (X). Most of the laryngeal muscles develop after metamorphosis and are not discussed here. A few arise just prior to metamorphosis -the dilatator laryngis muscle arises from the edge of levator arms branchialis IV and inserts on the arytenoid cartilage and the cricoid ring. The constrictor laryngis muscle consists of dorsd and ventral uarts that arise from medial raphe and insert on the arytedid cartilages (Sedra and Mi-
75
chael 1957). 1nDbco~lo.r~~~ the ramus Iaryngeus brevis innervates the dilatator laryngis and the r. laryngeus longus supplies the constrictor laryngis (Schlosser and Roth 1995).The dilatator and constrictor survive metamorphosis and bear the same name in the adult. The laryngeobranchialis muscle may be unique to Pipa (0. M. Sokol 1977a); it originates from the medial end of ceratobranchial III and inserts on the developing larynx.
M e t a ~ h o s i osf the Hyot?ranchium The hyobranchial apparatus does not undergo any appreciable change in shape until the beginning of metamorphosis (fig. 4.11). Metamorphosis of the apparatus generally begins at the time when the tadpole loses its jaw sheaths and the forelimbs break out. Metamorphosis will be described generally in three stages-the beginning of metamorphosis (Gosner 41-43), metamorphosis (stages 44-45.), and newly metamorphosed (stage 46). At the beginning of metmorphosis, the transversely oriented ceratohyals assume a more longitudiial orientation. The ceratohyals become larger and are in close medial contact when they reach their maximum size. The ceratobranchials are smaller. The spicules of the ceratobranchials disappear before the ceratobranchials. The cartilage of the ceratobranchids shrinks, and the clefts decrease in size. Copula I disappears and the pars reuniens gradually dlsitltegrates. A thyroid fenestra or foramen initially forms as a depression near the medial margin of the hypobranchial plate and then perforates. The medial margin of this fenestra becomes rodlike and forms the incipient posteromedial process (thyrohyal). The hyoglossal and laryngeal sinuses enlarge. Meckel's cartilages begin to straighten and lose their sharp angulation; they lie in a gentle curve with the infrarostds. As metamorphosis proceeds, the ceratohyals orient yet more posteriorly and become slender (fig. 4.11D). They are united mediauy and lose their articulation with the palatoquadrate. In some taxa, new pieces of cartilage form along the anteromedial margin of the ceratohyal; these will form the anterior process of the ceratohyal. (This process of the metamorphosing ceratohyal is not homologous to the larval "anterior process" on the ceratohyal, which is resorbed; see De Jongh 1968.) The hypobranchial plates reduce, and the thyroid foramina enlarge. The distinction of the hypobranchial plates from copula I1 is less obvious but persists as a clear zone in the cartilage plate demarcating the posterior limits of copula 11. The posteromedial processes form from the hypobranchial plate and do not represent the remnants of the fourth ceratobranchials (Ridewood 1897b). Lateral margins of the hypobranchial plate begin to form the anterolateral and posterolareral processes. The ceratobranchials are much smaller and break up, and the laryngeal and hyoglossal sinuses enlarge. The lower jaw is much larger and more U-shaped. The lnfrarostrals fuse to Meckel's cartilage giving the appearance of one element. The angulospienial and later the dentary ossifies. In the final and third stage of metamorphosis (stage 46) the ceratohyals are very slender and their posterior ends are fused to the otic capsule. They are no longer united medially,
DAVID CANNATELLA
Thyroid f.
Posterornedial proc. (incipient)
osterolateral proc.
Posterornedial proc
Mentorneckelian bone
E
D
1
Ceratobranchials Laryngeal sinus
Parahyoid bone
Posterornedial proc. (bony)
Fig. 4.11. Changes in the hyobranchiai apparatus during metamorphosis in Peiudpespunctatus. (A) Dorsal view, tadpole with intaa mouthparts, h d limbs 1mm long; (B) dorsal view, rnetamorphosing tadpole with rnouthparts absent and empted forelimbs, tail23 mm,
hind lunb 28 mm; (C) dorsai view, rnetamorphosing tadpole, tail2.5 mm; (D) dorsai view, froglet with resorbed tail, 21 mm SVL, (E) ventral view, froglet with resorbed tail, 17 mm SVL, and (F) ventral view, adult frog, 37 mm SVL. Redrawn frorn Ridewood (1897%).
and resorption of cartilage results in copula I1 forming part of the margin of the large hyoglossal sinus. The body (corpus) of the hyoid generaliy is a flat plate (fig. 4.11F). The anterior processes of the ceratohyal, formed from autochthonous cartilage, become indistinguishable from the ceratohyal proper. The ceratobranchials have disappeared completely, and the thyroid foramen is a sinus in the margin of the hyoid plate. The posteromedial processes begin to ossi$, and the anterolateral and posterolateral processes are weli forrned. The lower iaw at&ins the twicd U shave of the adult, and Meckei's caklage is investedlby the anghosplenial and'dentary bones; the mentomeckelian bones appear. Overaii the appearance of the hyoid apparatus in a newly metamorphosed froglet is very similar to that of the adult. The general development of fate of the craniai muscles is summarized from Edgeworth (1935) in figure 4.12.
ment in adult Hymemchims and Pseudhymenochims (Cannatelia and Tmeb 1988a, b). In some pelobatoids (e.g., Pelodytes) fusion of the anterolateral process to the ceratohyal forms a "lateral foramen" (Ridewood 189%) that is traversed by the glossopharyngeainerve and the lingual branch of the carotid arterv. The anterolateral Drocess of Alvtes is formed by adhsion of an autochthonous cartilage rather than from the lateral margins of the hypobranchial plate (Ridewood 1898a). In ali pelobatoids and in Rhinupbrynus, the middle Dart of the ceratohval is resorbed in late metamorphosis (fig. 4.11) to produce a disjunct ceratohyal (Cannatelia 1985; Ridewood 189%). In contrast to Ridewood (1898a), Pusey (1943) claimed that the fourth spiculum becomes the thyrohyal of the adult. In pipoid larvae the anterior processes of the ceratohyals are greatly enlarged and underlie aimost ali of the buccal cavity (0.M. Sokol 1975). The vosteromedial Drocesses of the hvoid are ossified in aii frogs. A parahyoid bone forms late in metamorphosis; it is present prirnitively in Anura but lost independently in different lineages (Cannatelia 1985). According to RideI
i
Diversity. W. K. Parker's (1871) account of development of the hyobranchial apparatus is riddled with inconsistencies (fide Ridewood 189%). Copula I persists as an ossified ele-
78
DAVID CANNATELLA
Fig. 4.13. Transverse sections of body wall muscles ofXenopw laepis. Consecutive stages in a premetamorphic tadpole: (A) presence of the myotome, (B) appearance of the Unvirbelfbrsatz (= primordial vertebral process), (C) detachment of the ventral muscles, and (D) appearance of secondary muscles. (E) Sections from the anterior, middle, and posterior body regions of a metamorphosing tadpole. (F) Sections from the anterior, middle, and posterior body regions of a young postmetamorphic animal. Symbols: pale gray = notochord and spinal cord, medium gray = primary musdes, and black = secondary muscles. Redrawn from Ryke (1953).
cles, but because it forms late in ontogeny, Ryke (1953) did not regard it as a homolog of the horizontal septum. Ti-unk myotome HI spans the atlas and second vertebra. The first parts of the vertebrae to appear are the cartilaginous neural arches, which do so in an anterior-posterior sequence beginning at Nieuwkoop/Faber 48 (Gosner 27-28; Trueb and Hanken 1993). Although there are only 8 presacral vertebrae in Xinopus h s , there are 12 neural arch rudiments. Vertebra IX forms the sacrum, and X-XI1 (postsacral) contribute to formation of the urostyle (coccyx) by fusion with the hypochord. The cartilaginous rudiments of the centrum begin to appear after neural arches X-XI. Neural arches I-VIII and centra I-IV ossitjr at the same time as the first cranial elements, the fiontoparietal and parasphenoid, at Nieuwkoop/Faber 55 (Gosner 35) in Xinopus l u k (Trueb and Hanken 1993). Vertebral ossification begins at Gosner 33 in Hyh hncfmis (De Sa' 1988), stage 36 in Spea bombzjvns (J. J. Wiens 1989), and just prior to stage 36 in Hamptqhyw boliaiana (De Sa' and Trueb 1991). Ossification of the urostyle was investigated by Stokely &d List (1955). In pipids the ribs appear as distinct cartilaginous elements on presacral vertebrae II-IV and later fuse to the transverse processes of the vertebrae. The rib anlagen osslfy at Nieuwkoop/Faber 57-58 (Gosner 40-41) at the same stage that all eight presacral centra and the sacrum ossltjr. By Nieuwkoop/ Faber 64-65 (Gosner 44-45) the ribs fuse to the transverse processes, which themselves osslfy at Nieuwkoop/Faber 64 (Gosner 44). The sacral diapophysis does not assume its expanded form until just after metamorphosis. The hypochord appears in cartilage at Nieuwkoop/Faber 60 (Gosner 41), ossifies at about Nieuwkoop/Faber 63 (Gosner 43), and fuses with the postsacral vertebrae to form the urostyle at Nieuwkoop/Faber 66 (Gosner 46). By this stage, the tadpole tail has largely been resorbed. The myotomal trunk muscles can be grouped based on the time of development. The primary muscles develop directly from the myotomes, and secondary muscles develop from mesenchyme that has proliferated from the primary muscles closer to the time of metamorphosis. The primary somatic muscles of the adult fiog trunk (fig. 4.13) are the coccygeo-iliacus, ileolumbalis pars medialis, longissimus dorsi, and reaus abdominis (also see fig. 3.3A-C). The secondary muscles (fig. 4.13) are the interarcuales, intertransversarii, obliquus abdominis extemus superficialis, sternohyoideus, transversus abdominis, and perhaps the reaus abdominis superficialis.
Spinal cord
eob Rectus abdominis atulomlntis
Obliquus aWor exfernus superfciafis
-
Interarcualis
- , lnterarcualis
Anterior
Anterior
Dorsalls trunci
Middle
Middle
Coccygewacralis
Posterior
Posterior
The mass of primary myotomal muscle, called the dorsalis trunci (fig. 4.13A), is covered dorsally by a sheet of connective tissue, the fascia dorsalis. The first secondary muscles to differentiate from the dorsalis trunci are the interarcuales (fig. 4.13D), located between successive neural arches. Near the time of metamorphosis the intertransversarii (secondary)
DAVID CANNATELLA
80
Rana catesbeiana
Ascaphus truei
Fig. 4.15. Diagrammatic view of water flow relative to the visceral skeleton (dorsal view) of Rnna catwbcianu. Upon entering the mouth, the water current is divided into lefi and right streams that come together just before the flow exits the spiracle. Redrawn from Gradwe11 (1972b).
functions at some time as the reservoir of a pump that moves water into the mouth, over the gills, and out through the spiracle.
Xenopus laevis ~ i 4 .~~ 4. .composite diagramsofsagirtaland parasagidsections through the heah of hna catM&cianu,Amphw ; andX IatPis. Abbreviations and symbols: arrows = passage ofwater into the buccal cavity, BC = buccal cavity, GC = @ cavity, I and PC = pharyngeal cavity. Redrawn from Gradwell (1971a, 1971b, 1972b).
and Wassersug 1988, 1989). However, too few taxa have been studied kinematically to permit broad generalizations about the relationship of neuroanatomy and locomotion in tadpoles (chaps. 6 and 9).
Gill Irrigation in Rana catesbeiana The first important accounts of gill irrigation by Schulze remained the definitive (1888, 1892) for Pehbates works on the subject for many years. In a series of papers, Gradwell (l968,1970,1972b, c) and Gradwell and Pasztor (1968) described the anatomy of the gill irrigation mechanism in R a m catesbeiana as consisting of a buccal cavity (the principal one), pharyngeal cavity, and gill cavity. Each cavity
Buccal, Pharyn~eal,a d Gill Cavities The buccal cavity is demarcated from the pharyngeal cavity (fig. 4.14) by the ventral velum (anterior filter valve), a nonmuscular epithelial fold supported by the cartilaginous spicules of the ceratobranchials (Wassersug 1976a). The v e n d velum extends laterally and dorsally to form the paired dorsal vela, which have no muscular or skeletal support. In most tadpoles the ventral velum produces strings of foodentrapping mucus from secretory columnar cells on its underside. Kenny (1969b, c) pointed out that rows of secretory co~umnarcells on the ventral velum were incorrectly identified as muscle fibers by R M. Savage (1952). Together, the dorsal and ventral vela form a valve preventing backflow of water into the buccal cavity (Gradwell 1970). In Rana catesbeiana the floor of the pharyngeal cavity has three gill clefts or slits. Additionally, endodermal pouch I1 is perforated to form an additional gill cleft, numbered I (figs. 4.7 and 4.15), which lies between ceratobranchial I and the ceratohyal. This gdl cleft opens directly from the buccal cavity into the gill cavity and is not present in any discoglossoids or XenopuJ; it is open in many neobatrachians, but Gradwell (1972b) and Haas (1997a) disagree on its condition in Ranatempmaria. The pharyngeal cavity of R. catesbeiana is separated from the gill cavity by three gdl clefts corresponding to endodermal pouches 111, n!and I?The gill cavity is enclosed by the operculum, a fold of integument that grows back from the hyoid arch and is fused to the skin of the abdomen (Brock 1929), except at a sinistral opening called the spiracle (=
81
ARCHITECTURE
spout of Gradweii). The spiracle has no muscular or membranous valves in Rana. The lefi and right sides of the giü cavity are conneaed across the rnidline by the opercular canal through which water passes fiom the right side, joining the stream from the lefi, to exit the spiracle (fig. 4.15). Within the giü cavity, there are four pairs of giüs, each consisting of a series of about 7-15 highly vascularized tufts attached along a ceratobranchial in close association with branchial arteries and constriaor branchialis muscles 11-TV (sensu novo); no muscle is associated with ceratobranchial N; Additiondy, the opercular cavity has a vascular iining, the membrana vasculosa operculans (Gradweii 1969b). Gradweli (1972b) discussed the association of the first gdi clefi with a weii-vascularized operculum and the absence of the clefi in taxa with a poorly vascularized opercular lining. Haas (1997a) found the first gill clefi to be open (charaaer 30) in Pelobates and d but one of the neobatrachians he examined. Gradweli (1972a, c) reviewed the literature on giü irrigation and pointed out that De Jongh (1968), Kenny (1969c), and R. M. Savage (1952) recognized only a buccal pumping mechanism, whereas Kratochwill (1933) and Schulze (1892) recognized branchial and pharyngeal pumps in addition to the buccal pump. The movements associated with giü irrigation wiü be considered in several sections that overlap temporally: movements of the jaws, the buccal pump, the
pharyngeal pump, and the branchial pump. Gradwell's (1968,1972~)work was done on Rana catesbeiana tadpoles under light anesthesia in a supine (beiiy-up) position; it is unclear whether his results can be appiied to tadpoles under more natural conditions. However, his extensive analysis employed muscle stimulation, denervation, electromyography, and pressure recordings. Gradwell's ( 1 9 7 2 ~ )account differs somewhat fiom his eariier report, and the latter one is used here.
Opening and Closing tbeJaws In general, jaw opening is effeaed by the jaw depressors: hyoanguiaris, suspensorioangularis, and quadratoangularis. However, opening of the upper jaw is accomplished not by muscles but by a coupling of the mandibulo-suprarostral ligament ("iigamentum rostrale superior cartilago Meckeli"; Gradweii 1968, 1972b). Jaw opening during irrigation occurs in three sequential phases: narrow opening, wide opening, and protrusion. During narrow opening of the mouth (fig. 4.16B), contraction of the quadratoanguiaris muscle causes Meckel's cartilage and the infrarostral to swing forward and outward fiom the buccal cavity, p d i n g open the lower jaw. Wider opening of the lower jaw is effected by additional recruitrnent of the hyoangularis musde (fig. 4.16C). However, the suprarostral cartiiage has not yet moved. During protrusion, additional contraction of the suspensorio-
\C&-
-D Hyoangulans
Fig. 4.16. Lateral views of the jaws of Rana ~ b e i a m during various phases of opening: (A) closed, (B) narrow opening, (C) wide opening, and (D) protrusion. Symbols: dashed arrows = direction of muscle action. Redrawn from Gradweii (1972b).
DAVID CANNATELLA
82
angularis causes yet fiuther forward excursion of the lower jaw, and this takes up slack in the mandibulosuprarostral ligament, which relays the force to the suprarostral cartilage (fig. 4.16D). The lateral circumoral ligament (1. cornuquadratwn laterale) and ligamentum rostrale superius quadrati prevent hyperabduction of the jaws. The coupling protrudes upper and lower jaws at the same time, and the angle formed by the jaws becomes more obtuse. Although the geniohyoid muscle appears to be in a position to open the lower jaw, its role during rhythmic jaw opening is doubtll (see Starrett 1973). It may function durGg hyperinspiration. In Rana catesbeiana, closing of the mouth occurs faster than the opening. Adduction of the upper and lower jaws takes place simultaneously Closing during gill irrigation does not produce the close shearing of the upper and lower jaw sheaths as does feeding. In addition to elastic recoil, Gradwell (1968) suggested that closing may be effected by three muscles attached to Meckel's cartilage (i.e.. levator mandibulae anterior, 1. m. anterior articularis, and 1. m. posterior superficialis) and two attached to the suprarostral cartilage (i.e., 1. m. posterior profundus and 1. m. externus, which-is considered-to have a pars anterior and pars posterior by Gradwell 1968). Gradwell (1972~)later retreated from this opinion because he was unable to detect electrical activity in the I. rn. posterior superficialis, 1. m. posterior profundus, 1. m. anterior, and I. m. externus. The first three of these muscles lack pink, phasically contracting fibers, and it may be that these muscles function only during - feeding and not during gill irrigation. According to Gradwell (1972c), movements between the two jaws are tightly coupled by the ligaments. If the upper jaw is held closed, the lower jaw does not open; if the upper iaw is held ooen.- the lower iaw cannot clos;. Similar rest&tion of movement applies to the upper jaw if the lower jaw is stabilized. If all of the levator muscles attached to the suprarostral cartilage are bilaterally cut, the upper jaw is still pulled closed by the ligamentum rostrale superius quadrati during closing of the lower jaw. Likewise, the lower jaw was closed by the ligament after the levators to Meckel's cartilage were cut bilaterally. De Jongh (1968) considered musculoskeletal movements during feeding and irrigation to be essentially the same, but muscular contractions during feeding apparently have not been studied explicitly (Altig and Johnston 1989). Gradwell (1968, 1972a) suggested that the mandibulolabialis and intermandibularis posterior muscles function during feeding, perhaps to move the labial papillae and to bring the upper and lower jaws into a shearing position, respectively. Lesion of both muscles did not affect jaw movements during gill irrigation, and Gradwell (1972a) doubted De Jongh's (1968) contention that the intermandibularis wsterior eleiated ;he floor of the buccal cavity. "
\
'
.
B m l Pump The buccal oumo is the mechanism that draws water into the buccal cavity of the tadpole. Its piston is formed by the paired ceratohyal cartilages that underlie the floor of the bucI
L
orbnohyoldeus end Suspensorbhyddeus
Inspiration
-
, - - ~ - ~
Expiration
Fig. 4.17. The visceral skeleton of a Ram catubciana tadpole. (A) Dor-
sal view. (B) Inspiration occurs by depression of the buccal floor by contractions of the orbitohyoideusand suspensoriohyoideus. (C) Expiration occurs by contraction of the interhyoideus, which elevates the buccal floor. Symbols: dashed arrows = direction of musde contracdon, dashed line = position of the transverse sections in B and C, and gray elements = skeletal elements of the buccal floor. Redrawn fiorn Gradwell (1968).
cal cavity. The ceratohyals are joined medially by the pars reuniens, copulae, interhyoid, and intrahyoid ligaments discussed earlier. These joints, plus the juxtaposition of the hypobranchial plates along the midline, permit bending along the longitudinal axis. The articulations between the anterior part of each hypobranchial plate and the posterior process of the ceratohyal, and between the hypobranchials and copula 11, permit some bending in the transverse plane. Most of the excursion about the elliptical hyoquadrate joint occurs such that the medial part of the ceratohyal moves dorsad and ventrad. Some movement also occurs such that the ceratohyal tilts anteroposteriorly The lateral part of the ceratohyal bears a flat surface for the attachment of the hyoangularis, orbitohyoideus, and suspensoriohyoideus muscles. Contraction of the stout interhyoideus muscle causes the ceratohyals to rotate upward around their amculations with the palatoquadrate and elevates the floor of the buccal cavity (expiration; fig. 4.17C). The water stream is divided into two parts, one to the right and one to the left of the pharynx, as verified by observing the flow of dye particles. The interhyoideus (and its principal antagonist, the orbitohyoideus) has both larval and "adult" fiber types. Larval fibers are his-
ARCHITECTURE
tologicaily distinct in that they are thicker and have peripheral nuclei; these pink fibers, with "slow" contrade propertia, many mitochondria, and phasic activity, are used primarily in the regular contractions of giii irrigation. The "adult" fibers are thinner, with centrally placed nuclei; these white fibers, of the "fast" type with fewer mitochondria and intermittent activity, are used primariiy in hyperexpiration. The two types of fibers have different functions in the tadpole of Rana catesbeiana (Gradweii and Walcott 1971). It is the more anteriorly located pink fibers of the interhyoideus
83
muscle that are active during gdi irrigation; correspondingly, the anterior part of the buccal cavity, supported by the ceratohyals, is raised more than the posterior part. This configuration directs the water stream posteriorly into the pharynx. The white fibers of the interhyoideus do not function during pumping or hyperinspiration. The interhyoideus posterior consists only of white fibers; its contraction is sporadic and constricts the giii cavity, forcing water out through the spiracle. Electromyographs and mechanograms (fig. 4.18; Grad-
Levator arcus branchialis I-IV Quadratoangularis Rectus cervicis (Tyrnpanopharyngeus)
Orbitohyoideus Hyoangularis
=
Suspensoriohyoideus (Suspensorioangularis, Geniohyoideus)
0
0
Geniohyoideus (Constrictor branchialis 11-IV, Subarcualis rectus 11-IV) Hyoangularis Suspensorioangularis Orbitohyoideus
0.5 sec
Interhyoideus Subarcualis obliquus
Interhyoideus Subarcualis obliquus Interhyoideus posterior (Levator mandibulae posterior L. rn. anterior, L. m. externus) Subarcualis rectus I Diaphragrnato-branchialis (L. m. anterior articularis)
0
Fig. 4.18. Sumrnary of muscle activity and hydrostatic pressures during gill irrigation in Rana catesbeiana. Muscle names in parentheses indicate that activity is postuiated, not observed. Symbols: dashed line = typicai cyde of pharyngeai pressure, dotted line = branchiai cav-
0
0
ity pressure, open rectangles = data frorn anatorny and direa observation, solid line = pressure tracing of buccai pressure for severai cycles, and solid rectangles = data from electromyography.Redrawn from Gradweli (1972b).
84
DAVID CANNATELLA
well 1972c) indicate that both elastic recoil and contraction ment joining the crista hyoidea of copula I1 to the branchial of the hyoidean depressors (orbitohyoideus and suspensori- process of ceratobranchiaiI1. Thus, during buccal floor eleohyoideus) depress the buccai floor for inspiration. The neg- vation, the ceratobranchiais are puiied fonvard and mediaiiy. ative pressure draws water into the buccai cavity through the The movements are assisted by subarcualis rectus I, which mouth. Sedra (1950) incorrectly judged that the hyoidean aiso assist in opening gill clefi I. depressors lifi the buccai floor. The suspensoriohyoideus aiso may help to stabilize the jaw joint during hyperinspira- Branchzal Pump tory contraction o€the hyoanguiaris muscle and to assist in Substantiai changes in branchiai cavity volume are only occaclosing gdi clefi I (Gradweii 1968, 1972a). During inspira- sionai and occur during hyperexpiration (figs. 4.184.19). tion in Rana catesbeiana and R. Jùsc@da (Gradweii 1972a) Contraction of the interhyoideus posterior muscle comwater flows in through the nares as weii, and a nariai vaive presses the opercular charnber, and contraction o€the subarprevents egress of water during expiration (Gradweii cualis obiiquus (= transversus ventraiis I1 of Gradweii) and 1969a). Experiments using dye particles suggest that the lefi the normaiiy inaaive fibrdiar parts of the interhyoideus musand right currents do not mix in the pharyngeai and buccai d e elevates the buccai floor. Water is thus forcehlly expeiied through the spiracle. cavities (Gradweii 1972a) of these two species. Gradwell (1968) found that denervation of the interhyoideus, orbitohyoideus, and suspensoriohyoideus muscles Pressure Dynamzc~ greatiy reduced ceratohyai osciiiations, but a siight rhythmtc Inspiration begins with elastic recoil of the buccai floor from pumping was maintained. Bilateral denervation of the hy- an elevated position. The buccai pressure drops (fig. 4.18), oidean depressors did not completely eliminate osciiiatory and as it approaches its minimum, the orbitohyoideus and buccai floor depression caused by the continued activity of hyoangularis contract, actively depressing the buccai floor the r e m s cervicis and elastic recoii of the buccai floor. De- and opening the mouth, respectively. Probably the suspennervation of the interhvoideus showed that buccai floor ele- soriohyoideus and suspensorioanguiaris aiso contract at this vation persisted because of contraction of the subarcuaiis time. Just after buccal pressure reaches its minimum, the inobiiquus (transversus ventralis 11) and subarcuaiis rectus I terhyoideus and subarcuaiis obiiquus contract to begin the . the iigamentum te& (liga- expiration phase. The pharyngeai cavity is enlarged as the (Gradweii 1 9 7 2 ~ ) Severing mentum supraorbitale cranii and I. supraorbitale ethmoi- buccai floor is elevated and the ceratobranchiais are displaced daie) caused the muscular process of the quadrate to bend anteromedidy. Probably the subarcualis rectus I and diaoutward, suggesting that these iigarnents stabilize the ori- phragmato-branchiaiis assist as weii. The mouth closes from gins of the hyoidean depressors (Gradweii 1972~). elastic recoil, and buccai pressure increases greatiy. The osciiiations of the buccai pump are mechanicaiiy At the peak of buccai pressure, the branchiai levators and iinked with opening and closing of the mouth. When the reaus cervicis contract, constricting the pharyngeai cavity, ceratohyai was held against the buccai roof, contraction of closing the velar vaive, and elevating the pharyngeai presthe jaw depressors opened the mouth only siightiy, and the sure. The resultant hydrostatic pressure is added to that just jaws were not protruded as in normal mouth opening. When transrnitted to the pharym from the buccai cavity. Thus, wathe mouth was held open the amplitude of ceratohyai excur- ter is pushed further posteriorly across the giii clefis. Immesion was reduced. diately after the peak of buccal pressure, the inspiration phase begins again as the ceratohyals begin to recoii pasPharyngeal Pump sively, the mouth opens, and buccai pressure drops. The phaMovements of the ceratobranchiais during irrigation cause ryngeai pressure drops as weii but lags behind the buccal changes in the volume of the pharyngeai cavity; t h s consti- pressure curve. At the onset of inspiration the pressure in tutes the pharyngeai pump. Simultaneous with buccai floor the branchiai cavity rises because of d o w generated by elevation (expiration), anteromediai displacement of the compression of the pharyngeai cavity; this is the time of ceratobranchids enlarges the pharyngeai cavity, and the gds greatest efflux from the spiracle. Most other workers have are swept through the water in the gill cavity (fig. 4.19). This suggested incorrectiy that spiracular outflow is greatest durmovement is effected by contraction of the subarcualis obli- ing expiration (Gradweii 1 9 7 2 ~ ) . quus (transversus ventraiis 11), which is synchronized with that of the interhvoideus. When the ceratobranchiais reach their fonvard limit, the buccai floor recoils passively, and the Evolutionary and Comparative Aspects grlls are swept posterolaterally, reducing the pharyngeal cav- of Gil1 Irrigation and Feeding ity. The spicules support the ventral velum against the buccal The mechanics of giii irrigation were studied in hmphus roof and prevent backflow into the buccal cavity. Movement w e i (Gradweii 1971a, 1973), Bufo regularis (Sedra 1950), of the ceratobranchiais occurs both by elastic recoii and ap- Hymenochiws boett~eri(0.M . Sokol 1962), PelobatesJùscus parentiy by contraction of the rectus cervicis and the (Schulze 1888, 1892), Phlynomantis annectens (Gradweii branchiai levators I-R the apparent antagonists of the sub- 1974), Phyllomedusa trinitatzs (Kenny 1969c), various species ofRana (De Jongh 1968; Gradwell1968,1970,1972b, arcualis obliquus. Movements of the ceratobranchiais and ceratohyals are c; Kratochwdi 1933; Severtsov 1969a), and Xenopus laeas synchronized to some degree by the subarcualis obiiquus, (Gradweii 1971b). Gradwell's studies of Rrcaphus, Phlynowhich in addition to contraction apparently acts as a liga- mantzs, Rana, and XencIpus provide consistent anatomicai
ARCHITECTURE
and functional comparisons of a species from each of the tòur tadpole types. The reader is cautioned against generalizing single-speciesaccounts to aii members of a particular tadpole type. Moreover, it is worth investigating whether the differences described herein exist at a more inclusive leve1 for any tadpole type. The tadpole ofhcaphus truei (Type 3) has a large oral disc c see Noble 1929 for comparison with Amolops ricketti, another species with a large oral disc). The buccal purnping mechanism, powered by the orbitohyoideus, sucks water trapped between the substrate and the disc into the buccal cavity and generates negative pressure by which the sucker &era to the substrate (fig. 4.14). A passive oral valve seals
85
the mouth when sucker pressure becomes less than buccal pressure, thus maintaining the suction (fig. 4.20). Experimental lesions to the periphery of the oral disc or to the oral valve greatly decrease the effectiveness of the sucker mechanism. Rrmphus tadpoles can "hitch" forward (but not lateraiiy or backward) while adherent by altemating movements of the upper and lower iip (Altig and Brodie 1972; GradweIi 1971a; M. H. Wake 1993a). Backward movement of the lower jaw and iip by the quadratoangularis muscle opens the mouth and oral valve. Suction is thus reduced, and the friction of the lower labium against the substrate aiiows the snout to be pushed forward. During this phase the trunk and tail are abducted from the substrate, probably by contraction of the dorsalis trunci muscles. Closing of the lower
Levator arcus branchialis I-IV
Inspiration
Tyrnpanopharyngeus
nares
/'i7
Rectus cewicis
Suspensoriohyoideus
Expiration
Levator rnandibulae anterior articularis
i
'-F> Diaphragrnatobranchialis
obliquus
I
Interhyoideus (Interhyoideus posterior)
Fig. 4.19. Gradweii's model of the mechanics of giü inigation in Rana catesbeiana. Symbols: dashed white arrows = direction of muscle action, gray area = pharyngeal cavity, and solid black arrows = water flow. The musdes in this model clearly have conuacted or have elecuical activity during giü irngation (see fig. 4.14). The interhyoideus posterior muscle is enclosed with parentheses to designate its activity only dunng hyperexpiration. After Gradweii (1972b).
DAVID CANNATELLA
Disengaged sucker
Peripheral contact
Fig. 4.20. Cornposite drawings of cross sections of the rnouth and nares during oral disc engagernent in Ascaphur tncei. (A) Narial and oral valves closed during expiration. (B) During inspiration, water enters rnostly through the mouth but some also enters through the nares; the periphery of the oral disc becomes sealed to the substrate
Engaged sucker
and evacuation of water frorn the sucker cavity into the buccal cavity causes the oral disc to becorne engaged to the substrate. (C) During inspiration, reduction in buccal pressure draws in water through the nares, but the oral valve rernains closed and adherence to the substrate is maintained. Redrawn from Gradweii (1971a).
iaw bv adduaor muscle contraction moves it fonvard. de- ryngeai force pumps that operate siightly out of phase. Unpression of the buccal floor increases the suction, and the like Rana, the pharyngeal pump is smaii relative to the bucbody is puiied close to the substrate, possibly by the rectus cai pump, and the outfíow of water from the branchial abdominis muscles. The combination of suction pressure chamber is intermittent rather than continuous. Although a and friction of the lower lip may rasp aigae from &e sub- ventral velum is present, it is reduced and not completely strate. Thus, "hitching" may aiso function sirnultaneously in free, and the dorsai velum assists substantiaiiyin maintaining feeding. However, the labial teeth do not serve in anchoring unidirectional flow, &eAscaphus and Rana. A large interthe tad~oleto the substrate (Gradwell 1971a). hyoideus posterior muscle can simultaneously constria the Tracings of buccai pressure and suction pressure are iden- buccal, pharyngeal, and gili cavities and may function in extical, and the frequency and amplitude of irrigation is similar peiiing detritus from the irrigation system. The flow of water in tadpoles whether or not suction is engaged. The flow of from the midventral spiracle is intermittent, but because this indicator ~articlesdemonstrates that when the sucker is en- tadpole is nektonic, there is no interferente from the subgaged, water enters the buccal cavity only through the nos- strate. trils; when not engaged, water enters through both nostrils and mouth. Nariai valves prevent reflux of water through Xenupus 1amG the nostrils. As in Rana, there are both buccal and pharyn- The tadpole ofXenopuslua% (Type 1)has a simpler jaw sysgeal force pumps, siightly out of phase, with a velar valve tem than those described for Ascaphus, Phynomantis, or that ensures the posterior flow of water over the gilis. Pres- Rana (fig. 4.14). Keratinized jaw sheaths and labial teeth are sure in the gili cavity fluauates but is continuously positive, lacking, and the larva is obligately microphagous. Meckel's indicating a constant flow of water from the branchial cavity. cartilage is elongate, as in the adult frog, and h e d to the Unlike Rana, there is no interhyoideus posterior muscle in infrarostrals. The suprarostrals are fused to the trabecular the opercular waii, so there is nó branchial pump. Gradweíi horns. This results in a wide transverse slit for the mouth. (1971a) speculated that the single, midventral spiracular Many of the jaw muscles appear to be fused. &nupus larvae opening maintains a constant oudow and prevents detritus aiso lack gilis and are obiigate air breathers, so it is inappropriate to refer to buccal pumping as giii irrigation. Gradweíi or parasites from entering the giii cavity. (1971b) stated that the buccai pump is not active until the Phrynomantis annectens larva finds suspended food particles. Phasic pumping then In contrast to Ascaphus and Rana, Phlynomantzs annectens begins, and the larva suspends itself in the water column. (Type 2) is a midwater filter feeder and lacks keratinized jaw InXenopus the mouth opens as inspiration begins, but the sheaths and labial teeth. In the larvai stage, the external nares lower jaw is not protnided because of the nature of the jaw have not yet opened (as in most microhylid taxa), so the only joint. Also, Meckel's cartilage is restricted to movement in inlet is the mouth. As described for Rana, there is a jaw- the dorsoventral plane, like Phyrwmantis but not as in Ascaligament coupling such that both upper and lower jaws are phus or Rana. Correspondingly, the three depressors of the protnided simultaneously. The intermandibularis anterior lower jaw are h e d into a single quadratohyoangularis. Unand mandibulolabialis muscles are absent. Unlike Rana, the like the ligament-dependent linkage of Rana, the quadratolower jaw rotates in only one plane and the suspensorioan- hyoangularis muscle provides the only force to open the gularis muscle is absent (Gradwell1974). lower jaw during buccai depression. The upper jaw does not Like Ascaphus and Rana, there are cyclic buccal and pha- move during mouth opening and closing. I
ARCHITECTURE
There is no ventral velum in Xknrtpus, and the combined mouth and throat cavity is called the buccopharyngealcavity. Simultaneous recordings of pressure in the anterior and posmior parts of the cavity are perfectly in phase as expected considering the absence of a ventral velum; therefore, there is one functional pump. The posterior pressures are less than thase recorded anteriorly, indicating a posterior flow of auer.The interhyoideus muscle is the principal elevator of dx buccal floor, but the subarcualis obliquus and the four bxamhal ievators assist as well. -4s buccopharyngeal compression begins, the mouth and uarial valves are closed as in Rana and water passes posterithrough the branchial clefts (there are no gills) and into rhe operdar cavity. The spiracles are paired and lateral with @like covers; water that enters the opercular chambers does not mix between left and right sides and passes quickly o m of the spiracles. Passive depression of the buccal floor contributes more rn water intake than in other taxa. but contraction of the otbitohyoideus is important as well. The inspiration phase is much shorter than expiration. Because there is no ventral d u n , the entire buccopharyngeal cavity fills with water, md reflux of water through the gill clefts is a possibility. However, depression of the buccopharyngeal floor causes rhe spiracular flaps to close, preventing reflux (Gradwell 1975~).Thus, water egress from the opercular cavities is ind t t e n t , as i11 microhylids, but for a different reason. The constrictor branchialis muscles close the gill clefts, but they do not fire during normal phasic pumping. They do contract simultaneouslv with the interhvoideus muscle as shown &en India ir;k is introduced iito the buccopharynx. The mouth remains open, and the ink is regurgitated from the buccopharynx. There is no interhyoideus posterior to power a branchial Dump. Overall, k e ;urnping apparatus of Xiruytzls is simplified compared to other tadpoles. Because of the fusion of suprarwnal cartilage and shape of Meckel's cartilage, the number of movable skeletal joints and planes of movement is reduced. Several of the muscles are absent or fused to others. The ventral velum and a separate pharyngeal pump are absent. GiUs and active muscular control of the gill cleft closing are absent, as is the interhyoideus posterior muscle and the branchial pump.
+-
GmtparatipeEcowholo~iGaland F~nctianal Aspects @Buccal P m p i n ~ ,ilthough the diverse ecologies of tadpoles have been appreciated, relatively little attention has been given to the relationship of ecology and the mechanics of buccal pumping. Wassersug and Hoff (1979) devised a model by which they estimated buccal volumes in a broad spectrum of tadpole pi&: Ranacatesbeiana, 50 p1; Ranasylvutica, 10.55 p1; and Xmopus kvis, 14.7 p1. Negative allometry of body length mith buccal volume among and within species suggests that f h g structures impose a size limit on how big a tadpole can get before it must metamorphose. The lever arm ratio, the ratio of the projected width of the lateral part of the ceratohyal (that part to which the buccal floor depressors
87
attach) to the total width of the ceratohyal and the amount of rotation of the ceratohyal in the transverse plane about the hyoquadrate joint (assuming a contraction to 90% of resting length of the fibers of the orbitohyoideus) are two other morphological variables that correlate with feeding ecology. Buccal volume is strongly correlated with snoutvent length, but neither lever arm ratio nor ceratohyal rotation show significant correlation with size (Wassersug and Hoff 1979). Wassersug and Hoff (1979) demonstrated that species they considered c'microphagous suspension feeders" had small lever arm ratios (0.14-0.17) and largest angles of rotation (33.5"45.0°); these included three species of microhylids, Pachymdusa ducniwlor, and Xenopus M s . Species they classhed as "macrophagous carnivores" are at the other end of the range of lever arm ratio (0.40-0.50) and rotation angles (14O-23'): Anotheca spinosa (oophagous), Hymemchiws boettoeri, Scaphiopts holbrookii, and Spea bombzfions (see Altig and Johnston 1989 for a different classification). Species termed "benthic, thigmotactic," such as Heleophyne natalensis, Hyalimbahzl~hiumfiisch~nni, and noropa miliaris, were less tightly clumped but distributed in the same half of the range for either lever arm ratio or angle of rotation. The middle part of the range consisted mostly of species with "typical" pond tadpoles. A regression of predicted buccal volume against snout-vent length (although not accounting for phylogenetic structure; Pelsenstein 1985) was highly sigt&cant and indicated that both microphagous suspension feeders and carnivores had predicted buccal volumes that were larger than those expected from the regression model. In contrast, benthic larvae with suctorial discs had smaller buccal volumes than expected from the regression (Wassersug and Hoff 1979). These oatterns were exolained bv a considerationof feeding mechanics and prey characteristics (fig. 4.21). Carnivo-
Buccal Floor Area
---
+
Fig. 4.21. Patterns UI buccal pumping design of tadpoles related to the feeding ecology oftadpoles (see text). The size of the clouds is arbit r r . Redrawn from Wassersug and Hoff (1979).
88
DAVID CANNATELLA
rous tadpoles were predicted t o require a large buccal vol- t o rocks. Slow-water stream forms such as Hyla lgleri and ume to produce the single burst of suaion needed t o capture Rana boylii had a lower mean vaiue (0.30) than did pond moving prey. In contrast, the feeding efficiency of micropha- generalists (0.44), but the three species of obiigate, suctorial gous forms depends on the quantity of water passed through stream forms (Rrcaphus, Heleophryne, and Litoria) had a mean the buccai cavity, and a larger buccal cavity wiü increase food value of 0.44, not different from generalists. The small samintake. In bo& cases, b&cal volume i; increased, but in ple sizes may be inadequate to detect significant Merences. different ways. Macrophagous tadpoles had a short angle of These comparative studies were done before appropriate ceratohyai rotation (stroke of the piston) and long lever arm methods were avadable for anaiyzing correlations among combined with a large buccal floor area (bore of the cylin- continuous characters in an expiicitly phylogenetic context der). Conversely, midwater suspension feeders had a large (Harvey and Pagel 1991). Apparent correlations among degree of rotation and short lever arm, but a s m d buccal traits surveyed in a range of taxa may be artificidy high because a certain component of the covariation is attributable floor area (Wassersug and Hoff 1979). Like the carnivores, the benthic larvae examined had long to phylogeny. It wouid be instruaive to readdress these lever arms and iittle rotation of the ceratohyal, but the buccal questions in an explicitly phylogenetic context with the apfloor, and thus buccal volume, was smaii. The large mechani- propriate methods. Reiiable information on tadpole diet and cal advantage of long lever arms generates lar& negative ecology is also needed. Although macrophagous tadpoles pressures at the suctoriai disc for adhering to the substrate have certain traits in conimon, the actual diet of these may (e.g., hmphus; Gradwell 1971a, 1973). Because benthic vary greatly. Some are oophagous bromeiiad dweiiers (e.g., larvae presumably feed on periphyton on the rocks, large Anothecaspinosa; Lannoo et ai. 1987), while others are openbuccal volumes needed for either elusive prey or to move water predators (Hymenochimsboe~~eri; 0 . M. Sokol1962). large volumes of water with tiny food particles were not ob- Other faaors, such as physiological constraints (Feder et ai. 1984a, b), merit consideration in generalizations concerning served. Tadpoles can effea a constant ingestion rate when food associations of diet, morphology, and function. concentration is experimentaiiy altercci (Seale and Wassersug 1979). For suspension-feeding tadpoles, the rate of water Phylogenetic Aspects of Tadpole Morphology pumping must be adjusted such that the g d íiiters do not become obstruaed; this can be accompiished by either am- Caenogenesis and Pipoid Tadpoh plitude moduiation (AM) or frequency moduiation (FM) Frog tadpoles are caenogenetic (De Beer 1951; Gouid of the buccal pump (Wassersug and Hoff 1979). In frequency 1977); they have deviated from the ancestral ontogeny in moduiation the rate of pumping is adjusted, but each pump having larval specializations (nonterminal additions, such as cycle transports the same volume of water (e.g., Xenupw keratinized jaw sheaths and labial teeth) and less obvious but laevis). In am~litudemodulation the volume of the buccd e q u d y important skeletal modifications (e.g., orientation of cavity is altered so that more or less water is pumped in one the palatoquadrate and presence of suprarostral and infraroscycle (e.g., Rana sylaatica). The type of moduiation appears trai cartilages). These larvai feeding specializations provide a to be related to the feeding morphology. Forms with short way of prolonging the larval Me cycle (Slade and Wassersug lever arms are prediaed t o have more difficuity in moduiat- 1975), and it may be that a reduaion in food is a cue for ing the amplitude of buccal floor displacement than do those metamorphosis (Wassersug 1986).At metamorphosis, these with longer lever arms. Xenopus h s , with a short lever arm, larval specializations are lost as the cranium of most tadpoles is a FM tadpole, and R. sylvatica, with a longer lever arm, is is extensively remodeled (Orton 1957). Metamorphosis in saiamanders, the outgroup, is relatively gradual, but phyloan AM tadpole (Sede and Wassersug 1979). The muscles involved in moduiating either amplitude or genetic analysis indicates that the ancestor of Anura had frequency of the buccal pump are primarily the orbitohy- drastic metamorphosis. oideus (buccal floor depressor) and interhyoideus (elevator). In Pipoidea, nearly ali of the skuii bones appear prior to Satel and Wassersug (1981) prediaed that because macro- the completion of metamorphosis whereas in other frogs phagous carnivores must generate a large suction pressure, several of the skull bones appear after metamorphosis (Trueb they would have orbitohyoideus (OH) muscles that are large 1985; Trueb and Hanken 1993). It seems that the appearrelative to the interhyoideus (IH), or a low IH/OH ratio. ance of craniai ossifications is accelerated because metamorMicrophagous larvae have dense giü íiiters that strain s m d phosis in these pipoids is not as drastic as in other frogs partic&s &d were predicted to rec$re large buccal pressures (Wassersug and Hoff 1982) and less remodeling of the osand a large IH/OH ratio to force water through these filters. teocranium is required. Pipoids have several peramorphic Quantification of muscle cross-sectional areas supported features (i.e., new morphologies or shapes that are added to these predictions (Satel and Wassersug 1981). The cross- the end of the ontogenetic sequence; Aiberch et ai. 1979). sectional areas were isometric to body length. Obiigate mid- Examples of such features are the fusion of the frontopariewater feeders (i.e., five species of microhyiids, Agalychnis tais in Pipoidea, fusion of the vomers in Xenopus, fusion of callidryas, Rhinuphrynus domalir, and Xenupus hms) had the the parasphenoid to the sphenethmoid, expansion of the mehighest IH/OH values of 0.82), and macrophagous tadpoles dial ramus of the pterygoid, and an elongate columeiia in such as Anotheca spinosa, Hymenochims boett~eri,and Spea Pipidae (Canriateiia and Trueb 1988a, b). In contrast, some bombifions had a mean IH/OH value of 0.26. Suaorial forms features are interpretable as paedomorphic (i.e., developwere expected to have strong buccal depressors for clinging ment has been arrested at an earlier stage in the ontogenetic
ARCHITECTURE
trajectory): lateral line organs of the tadpoles retained in adults of Pipidae, the absence of eyelids and quadratojugals in Pipidae, and the absence of mentomeckelians in Pipoidea. Pipids remain aquatic as adults (they arc the most aquatic frogs), and lack of a transition to a terrestrial life may explain, in part, the less dramatic metamorphosis. Ossification begins earlier, and peramorphic features result from prolonged development. Although the extreme degree of filter feeding in most pipid larvae is apomorphic, pipids have reverted to an ontogeny reminiscent of salamanders by abandoning specializations associated with feeding.
Ewlgtion of Orton's Tdpole T9es Starrett (1968,1973), following Orton (1953,1957), conceived of an evolutionary sequence (fig. 4.22) in which Type 1 was the most primitive, Type 2 was more derived, and
T p e s 3 and 4 were the most derived, with T p e 4 more specialized than Type 3. These assumptions of the primitiveness of pipoid larvae led to a historical controversy about hgher level frog relationships because of incongruence of trees derived kom larval data with trees based on adult data. Studies of adult morphology had concluded that "discogiossoid" frogs such as Ascapbus, Bombina, and LeiqeImu, were the most primitive anurans (1. Griffiths 1963; Noblc 1922). This "larva versus adult" controversy was comparable to the recent, but now obsolete, c'molecules versus morphologyn debates. Starrett suggested that the plesiomorphic mode of feeding was similar to that of the Type 1 (pipoid) larvae. Water passing through the "beakless" mouth carries food particles, which are filtered out, and a steady stream of water exits the two spiracles. Feeding and respiration are the same actions.
Type 2 tadpole
Type 3 tadpole
Type 4 tadpole
Feeding and respiration sirnilar actions Some modification of Meckel's cartilage, separate infralabial cartilages MuscJes specialized for protrusible lower jaw *Separate branchial chambers with single ventral external opening Forelimbs develop posterior to branchial chambers
*Separate branchial chambers with median external opening Forelimbs develop close to branchial chambers
*Single branchial chamber with sinistral external opening Forelimbs develop within branchial chambers
Type 1 tadpole
*Feeding actions more separated from respiration *Long coiled gut for algae feeding Extra jaw cartilages, muscles and accessory mouth structures for feeding *Smaller branchial chambers Forelimbs develop close to branchial chambers
\
\\
*Characters same as Primitive tadpole
Prirni1:ivetadpole --
-
-
Feeding and respiration same action Jaw cartilages simple Mandibular and hyoid muscles not specialized for feeding Separate branchial chambers with two external openings Forelimbs develop posterior to branchial chambers
Fig. 4.22. Starren's interpretation of the evoiutionary sequence of Orton's (1953) tadpole types. Characters Redrawn from Starrett (1973).
in boldface are discussed in the text.
89
DAVID CANNATELLA
90
The mouth is opened by the angularis complex and the geniohyoideus and dosed by the adductor muscles. She further argued that in the Type 2 (microhylid) tadpole some separation of feeding from respiration occurs. A strange, spoon-shaped lower lip is extended by the geniohyoideus and intermandibularisposterior. The lower lip and mouth are closed by the infralabial retractor, interhyoideus, and interhyoideus posterior. The evolution of keratinized jaw siieaths in ~~~i 3 and 4 tadpoles contributes to the separation of feedng and respiration. The adductor muscles move the jaws in a rasping motion. The labial teeth and papillae are controlled by opposing actions of the geniohyoideus and adductor muscles. The addition of a joint between the infrarostral and Meckel's cartilage increases the range of motion of the lower jaw. The intermandibularis nosterior muscle has abandoned its ori~inal function of as" &ing the interhyoideus in buccal floor elevation and functions in feeding only. This evolutionarv seauence suffers &om rwo ~roblems. One is the misinterpretation of larval anatomical and functional data, and the second is the lack of a phylogenetic context. Starrett's statenlent that feeding and respiration are the same action in pipoid larvae is incorrect. AU pipoid larvae lack internal gills and are obligate air breathers ( 0 . M. Sokol 1977a; Wassersug 1996); thus the movement of water through the buccal cavity serves no apparent (or a minor) respiratory fiuiction. LXCmpus laePis tadpoles die if they cannot get air, even in highly oxygenated water (Wassersug 1992). Moreover, feeding in pipoid larvae is more diverse . larvae than was represented by ~ k r e k x 1 9 7 3 )Rhinopbrynus are known to be both carnivorous and microphagous (Satel and Wassersug 1981). Silwana anddXbwpus larvae are obligtely microphagous. Hymenuchimcs boett$jni is a predatory zooplanktivore and lacks gdl filter plates completely (0. M. Sokol 1962), free-swimming Pipa larvac are macrophagous filter feeders (0.M. Sokol 1977a), and the direct-developing Pipa species (Tmeb and Cannatella 1986) cannot feed as larvae. I suggest that the diversification of heterogenous feeding modes of pipoid larvae results from the complete decoupling (sensu Lauder 1981) of feeding from respiration. When the buccal Dumn is freed from the constraint of irrigating the giUs, its mechanical parts are then able to evolve with the exploration of other trophic niches. Some of Starrett's other statements ( i s , purported action of the geniohyoideus in opening the mouth and controlling the mouthparts, the muscles that close the mouth in microhylid tadpoles, the action of the intermandibularis in tadpoles with jaw sheaths, and a steady watcr strem exiting the spiracles in pipoid tadpoles) are not supported by the work of Gradwell (1968, 1971a, b, 1972b, c, 1973, 1974, 1975~).Other discrepancies were addressed by 0. M. Sokol(1975). Starrett's (1973) proposal assumed that the simpler musculoskeletal system (lack of jaw sheaths and labial teeth, fewer muscles and joints) of pipoid larvae is primitive for Anura, following an implicit assumption that structural simplicity is plesiomorphic. It is well established that determination of character polarity must be based on outgroup com1
I
1
parison ( W e y 1981) rather than preconceptions about the direction of momhological evolution. The structural sim" plicity argument is flawed because it assumes as fact the very hypothesis of morphological evolution that one is testing. It should be noted that although 0.M. Sokol(1975) opposed many of Starrett's interpretations, his conclusions as well were often based on a priori notions of morphological transformation, including the assumption that fusiolls of cartilaginous elements are evol&ionarily derived. Regardless of whether or not one accepts the struaural simplicity argument, both outgroup comparison and the ontogenetic criterion (G. Nelson 1978) suggest a priori that certain "simple" characters of pipoid and rnicrohylid larvae are plesiomorphic for Anura. Salamandersand caecilians lack labial teeth, and keratinized jaw sheaths are questionable in salamanders (perhaps only in sirenids), so ou&roup analysis suggests their absence is plesiomorpluc for frogs. These jaw sheaths and labial teeth appear later in ontogeny than do infiarostral and suprarostral cartilages, so by the ontogenetic criterion their absence is plesiomorphic. By either criterion, Starrett's assumption was correct. However, such a priori hypotheses are tested by other data in the context of phylogenetic analysis. That is, the bestfitting phylogeny, based on all of the relevant data (Kluge 1989),will corroborate certain evolutionary transformations but reiect others. An~arentcoficts in trees derived from differekt data sets often resolvable if one analyzes the character data on which the trees are based (,Miyamoto 1985). Starrett's hypothesis of the primitiveness of Type 1 larvae was not corroborated by phylogenetic analysis of other data. Analyses of primarily adult characters (Cannatella 1985; L. S. Ford and Cannatella 1993; J. D. Lynch 1973) indicated that the Type 3 larva is plesiomorphic, and that absence of jaw sheaths and labial teeth is derived within frogs " and is an e;olutionary loss. More recently, a phylogeny from larval morphological characters (Haas 1997a; fig. 4.2) also supported the placenlent of the Type 3 tadpole as plesiomorphic for Anura. In contrast, the phylogeny based on mitochondrial 12s and 16s nucleotide sequences (Hay et al. 1995; fig. 4.2) suggested that the Type 4 tadpole is plesiomorphic for Anura. However, a combined analysis by Kjer, Graybeal, and Cannatella (unpublished data) of morphological characters and this sequence data yielded a tree that supwrts that of L. S. Ford and Cannatella (1993). This analvsis also i~ldicatcdmuch of the inconmence is because of the rooting position of the molecular Free. The continued use of Orton's tadpole types diverts attention from issues of morphological'evol~ion to issues of definitions. L. S. Ford and Camatella (1993) discussed the problem of the Tjpe 2 (microhylid) tadpole, whose definition was strained after the discovery that tadpoles of at least one species of scaphophqnine microhylid have jaw sheaths (Wassersug 1984, 1989b). None of the four tadpole types is homogeneous in structure or function, and the acceptance of Orton's groups as monolithic categories will ordy hinder our understanding of the tadpole evolution. Morphology evolves, and one would expea that definitions of the larval types wiU become fuzzy as more data are available.
sways
ANATOMY Viscera and Endocrines Bruno Viertel and Susanne Richter
The s m d , apparently insignificant, arnphibian tadpole is a wondrous mechanism of organic complexity that is of profound significance in the study of basic biological problems . . . Fox 1984:x
Introduction An anuran larva is a nonreproductive, highly specialized stage within the complex, amphtbian life cycle and not simply an extended embryonic phase that concludes with metamorphosis. A tadpole is a mosaic of organs that are either remodeled (e.g., exocrine pancreas and posterior alimentary traa; see Pretty et al. 1995; F. Sasaki and Kinoshita 1994; Yoshizato 1992) or degenerated during metamorphosis (e.g., blood-forming organs, flter apparatus, integumentary ceiis, lymphatic system, and pronephros), remain functionaiiy quiescent (e.g., parts of the excretory and reproduaive systems), or are functional throughout both larval and adult stages of the cycle (e.g., liver, lungs, pancreas, spleen, thymus, and thyroid, and the vascular system). The nonreproductive tadpole feeds and grows to produce a metamorph that has some probability of entering the breeding component of the population. In that context, much of the anatomy of a tadpole involves the gathering and processing of food, and many of the structures used in these aaivities, especiaiiy involving the buccopharyngeal area, are unique among vertebrates. We summarize the anatomical diversity of the circulatory, digestive, respiratory, urogenital, and endocrine systems of tadpoles. Much of the data available on these subjeas is derived from studies of only a few genera (e.g., Bufo, b n a , and Xenopus); when known, information on embryonic development and metamorphic changes is included. Additional information on some subjeas is found in chapters 3, 4, and 6. We used the staging tables of the original authors; translations of selected staging systems to that of Gosner (1960) are shown in table 2.1. The foiiowing staging systems are cited in this chapter and are presented by the author name(s) and the appropriate arabic or roman nunieral(s): Cambar and Gipouloux (1956a, Bufo bufo), Cambar and Marrot (1954, Rana dalmatina), Cambar and Martin (1959, Alytes obstetricam), Gailien and Houhon ( 1951,Disco~lossuspictzls), Gosner (1960, ali generalized anuran larvae), Nieuwkoop and Faber (1956, Xenopus laePir), Rossi (1959, Bufa bufo), Sedra and Michael (1961, Bufo rgularis), Shumway (1940, Ranapipiem), and A. C. Taylor and Kollros (1946, Ranapipiem). The terminology we used in defining periods of development are as foiiows: embryonic = Gosner 1-24 (zygote to closure of operculum); larval or tadpole = Gosner 2 5 4 6 ; premetamorphic = Gosner 25-35 (growth of trunk and tail); prometamorphic = Gosner 3 6 4 1 (growth of iimbs, thyroxine titers increase), and metamorphic climax = Gos-
93
ANATOMY
ner 4 2 4 6 (remodeling and degeneration of rnany larval structures, thyroxine titers reduced).
dium and together with blood flow affects the epithelial folds. Cells migrating between the rnyocardium and endocardiurn stiffen-the fõlds and forrn a &e. The conal valve changes sequentially (fig. 5.1E-G) from dorsal, to left, to Circulatory System ventral positions, and hally comes to lie near the ventricle The organs of the circulatory system are derived frorn rneso- at the proxirnal end of the conus (Shumway 25). At Shumderrn, and the heart and viteiiine vessels are the first fúlly wav 24 an endothelial double-lavered inter&ricular sevtum fünctional embryonic organs. The circulatory system trans- divides the atrium. By ~ h u m w a i 2 5the auriculo-ventricular ports rnaterials between organs with extemal contaas (e.g., valves are connected with the interauricular septum, the sialimentary tract, lungs, giils, and skm) and those with inter- nus venosus is distina. trabeculae have develo~edin the vennal fünctions (e.g., endocrine, excretory, muscular, nervous, tricle, and the wall of the ventricle is spongy. The heart does and reproductive systems). The lyrnphomyeloid systern is an not develop fürther until &er rnetarnorphosis. Bending and immunological buf'ier between the external and cellular envi- twisting of the heart tube is a typical feature in tetrapod heart ronments of the larva, especially for those organs that come develo~rnent.In anurans the twisting. of the ventricdar reu into contact with an aquatic environment rich in micro- gion and the transitional region of ventricle and conus conorganisrns. stitute essential changes, whereas the sinus venosus retains its position. The conus approaches the atrium (fig. 5.1H-I). Heart In the fúllv develoved larva. the heart is dorsal to and The histogenesis of the heart is similar in all vertebrates bounded láterally the pósterior branchial arches. In (Hirakow 1989; Hirakow et al. 1987, Cynopspyrrhogaser; adults, the heart tilts more anteriorly than in the lama (fig. Hirakow and Sugi 1990, Gallus;Volkov 1982, R. &bunda; 5.1H-K; Benninghoff 1921, Bombina parigata, Bu$ bufo, also Burggren and Fritsche 1997; Farrell 1997; Icardo Leptodaqlus pentadactylus, R. catesbeiana, R. escubnta com1997). Heart-forming potency is expressed only in the dor- plex, and R. temporaria; Ekrnan 1924, 1925, R. temporaria; sal lip of the blastopore and in deep mesoderm between 30' Erdmann 1921, Bombina and Rana; Goette 1875, Bombina; and 45" lateral to the dorsal midhne of the gastrula. Trans- Ison 1968: Nieuwkoov and Faber 1956. X. h s ; Prakash plantation experiments show that heart rnesoderrn is estab- 1954 and'Thornas 1672, ~oplobatracbistigerinis; Rugh hhed by a dorsalizing signal frorn the dorsal blastopore lip 1951). (Sater and Jacobson 1990,Xenopushis) well before the end of gastrulation. In contrast to the results of A. G. Jacobson Arteries and Ve'eins and Duncan (1968, Caudata), Sater and Jacobson (1989,X. In Xenupus h s , elongated cells appear in the lateral plate h) showed that the pharyngeal endoderm does not have near the inner laver 31-32. , of skin at Nieuwkoo~Raber I' an induaive effea and does not promote the onset of heart They migrate frorn the lateral plate and engulf and surround fünction. the blood celis, and by Nieuwkoop/Faber 33-34 they are flat In Rana temporaria (Shumway 1940), cells from the dor- and in desrnosornal contact with each other. At Nieuwkoopl sal edge of the visceropleura forrn a single endocardial tube Faber 35-36 these cells are found throughout the ventral that is continuous with the endothelium of the ventral aorta side of the ernbryo, and by stage 37-38 they have extended by Shumway 18 (fig. 5.1A-G). The rnyocardial anlage origi- toward the endoderm to forrn the blood vessels of the vennates from mesoderrn at the ventral edge of the lateral plates tral intestinal tract (Mangia et al. 1970). (somatopleura and visceropleura; C0penhaver 1955 and The forrnation of ao& arches and vulmonarv arteries at DeHaan 1965). The dorsal part of the ventral edge folds the sixth aortic arch and the anatomical displacement and around the endocardial tube frorn anterior to posterior. At reduction of the aomc arches during metamorphosis have Shumway 18 the heart is a longitudinal tube consisting of been studied extensively (figs. 5.2-5.3; see Delsol and Flatin the conus arteriosus, ventricle, and sino-auricular cornplex 1972 and references therein). In contrast to the arterial sys(i.e., füture sinus venosus and atrium). At this time, the peri- tem of the pharynx, little anatornical change occurs in the cardium develops as a folding of the more lateral soma- arterial svstem of the trunk and limbs. The subclavian (foretopleura around the rnyocardium. Dorsally (Shumway 20) limbs), rnesentrial (intestines and kidneys), and iiiac arteries the myocardium attaches at the dorsal pericardium in the (hind limbs) branch sequentiallyfrom the dorsal aorta posteregion between the conus arteriosus and the paired aortic rior to the pharynx. The dorsal aorta extends into the tail as trunks.The ~airedvitelline veins come into contact with the the caudal arterv, (see Rhodin and Lametschwandtner 1993). , undivided auricular region and form the sinus venosus. Tra- and this vessel degenerates at rnetarnorphosis. Rernodeling of the venous systern occurs before and durbeculae forrn shortly &er the heart begins to beat at Shumn-ay 20. Up to Shumway 22, the ernbryonic heart tube is ing rnetamorphosis prirnarily in the postcranial region (figs. situated ventrornedially and posterior to the pharynx. At 5.4-5.5). The rnedial posterior cardinal veins füse to form Shumway 23 the right, left, and posterior distal conal valves an unpaired interrenal vein; the lateral posterior cardinal and the septum coni differentiate frorn the endotheliallining veins forrn and supply the opisthonephros with blood indeof the conus arteriosus at the bfircation of the aortic tninks. pendently of arteries. As such, they represent the rnain drainThe endothelium grows rapidly cornpared to the rnyocar- age systern for the caudal and iiiac veins (i.e., the lateral posI
i
x
,
BRUNO VIERTEL AND SUSANNE R I C H T E R
H C
Q++p v
: ; &c
v
AKm
@: 4 V
RA
v VA
Fig. 5.1. Development of the heart of Rana temporaria. Cross sections of (A) plate of ceiis that wiii form the endocardium of the heart (Taylor/Koiiros stage 17),(B) dorsai mesocardium (Taylor/Koikos 18), (C) endocardium continuous with the endothelial lining of the aortic arches (Taylor/Koiíros 18), and (D) septum coni originating anteriorly as a continuation of the nght distal conai vaive (section through conus septum). Three horizontal sections (E-G) from dorsai to ventral, interauricular septum developing from the anterodorsal w d (Taylor/Koiiros 24). Twisting of heart tube at early (H) and later (I) stages. Right lateral view of the heart at Taylor/Koiiros 25 (J) and in the adult (K). Abbreviations: A = auride, AS = interauricular sepnim, C = conus, DM = dorsai mesocardium, E = endocardium, EP = plate of ceiis that wiii form the endocardium of heart, LA = left auricle, LAT = left aortic arch, LDCV = left distal conai valve, M = myocardium, P = floor of pharynx, RA = nght auricle, RDCV = right dorsai conai vaive, S = sinus venosus, SC = septum coni, SM = splanchnic mesoderm, V = ventnde, and VA = ventral aorta. Orientationai crosses: A = anterior, D = dorsai, L = left, P = posterior, R = nght, and V = ventral. From Ison (1968); reprinted by permission of Taylor & Francis, Ltd.
95
ANATOMY
terior cardinal veins are the afFerent renal veins). One of the flow into the anterior and only persistent ventral commistwo omphalomesenteric veins forms capiiiaries in the liver sural vessel and thereby drain the hind lirnbs and t d . The and, passing caudaily, drains the intestine via the newly head-pharynx region drains via the external (especiaily the formed portal vein; the lefi omphalomesenteric vein drains flter apparatus) and internal jugular veins. the stomach region via the gastric vein. The posterior vena cava arises anteriorly from the hepatic vein and posteriorly Blood from the interrenal vein. A capiliary network connects the Turpen and Knudson (1982, Ranapz$iens) described hemaabdominal and musculo-abdominal veins. Blood flows pos- topoietic precursor ceiis in the late gastrula and early n e d a teriorly via three ventral cornrnissural vessels to the inter- (fig. 5.6). Celi aggregates in these plates of precursor ceiis renal vein, then to the hepatic vein (i.e., the posterior vena differentiate to hematic cords of the blood islands and oval, cava), and from there to the sinus venosus. During meta- primitive blood cells. Precursor celis identical with common morphosis, a blood sinus connects to the larval subintestinal plunpotent hematopoietic stem ceUs (PHSC; Broyles et ai. vein (from the lefi omphalomesenteric vein) and forms the 1981 and Cltne and Golden 1979) migrate from the dorsal adult abdominal vein; blood flows anteriorly, opposite to part of the lateral plates into the larval hematopoietic organs that of the larval abdominal vein. Femoral and iliac veins (Broyles 1981; Turpen et al. 1979; Turpen and Knudson
A
Anterior cardinal vein (jugular) H/
/
..W' .. ,
Internal carotid artery
Bulbus arteriosus icle
Anterior calinal vein (jugular) Dorsal aorta
\.
Ductus Cuvieri
+C 1
Subclavian vein
=-/I"
A
:-:.: . ,
\ \
C
_Ductus arteriosus
Externa1 carotid
'
// / tyC
artery / Pulmonary artery Posterior vena cava
Hepatic vein
-:......:.. ............ . .. . . . ..: .:. -......... .... .:.::....:. L
Ventricle
Right auricle
Sinus venosus
Fig. 5.2. Blood vascular systems of an early (A) and late (B) frog embryo viewed from the nght side. From Rugh (1951); reprinted by perrnission of McGraw-Hiü, Inc.
96
BRUNO VIERTEL AND SUSANNE RICHTER
FA BRANCH III
FA BRANCH IV TO SUBRECT III
SUBRECT 111
1982). Hemoproteins, first detectable in the anterolateral blood islands, diflerentiate in the lateral plates at Nieuwkoop/Faber 33-34. Ln subsequent stages, hematic cor& extend into the posteroventrai trunk region, and by Nieuwkooppaber 39 the anterior cords have disappeared. At Nieuwkoop/Faber 40 the subintestinai veins contain hemo-
proteins (Mangia et al. 1970). The intertubular liver and hepatic ducts, pro- and opisthonephros, and spleen are primary centers of hematopoiesis (Broyles et ai. 1981, R. catesbeiana; G. Frank 1988,1989a, b, R. esculenta complex; Maniatis and Ingram 1971a, b, c, R. catesbeiana (fig. 5.7). In Ranapipiens (Shumway 24-25) and other species, hematopoiesis begins
ANATOMY Fig. 5.3. Ventral views of the development of the aortic arches ofXeno-
p laevis. (A) In a 5-mm embryo, aches 1, 3, and 4 are complete; the other two have primary and secondary vessels. (B) In a 6-mm embryo, aches 3,4, and 5 are complete; arch 1 is degenerating at point x; aches 2 and 6 are stumps.-(c) In an 8-rnm larva, secõnd&y vessels of arches 3 and 4 loop backward into externai giüs; nght side (&in d&ram) is unusual in having two externai giiis on branchial arch 1, the second of which is supplied by an extra loop formed by the anastomosis between arch 3 and its secondary vessel. (D) Arrangement of aortic arches and arterial supply of a t e r apparatus (m$pled) in a fourlegged larva before completion of metamorphosis; note relative siw of aortic arches; arch 5 is starting t o degenerate (dushed line). (E) Reconmuction of aortic arches, branchiai skeleton, and associated musdes in a 10-mm larva. Vessels supplying extemal gills are starting t o atrophy, and arch 3 is wider than others; arteries to filter apparanis were omitted. Abbreviations: ANAST = anastomosis, AORTA = aorta, BAS = basihyal, BRANCH I - N = branchial bars I-TV, CAR EXT = arteria carotis externa, CAR INT = arteria carotis interna, CER = ceratohyal, FA BRANCH I-TV = arteries of filter apparatus of branchiai bars I - R GC 11-TV = giü clefts I-IV, GEN = musculus geniohyoideus, ILC = inferior labial cartilage, MECK = Meckel's cartiiage, CITERHY = musculus interhyoideus, INTERMAND = musculus intemandibularis, ORBHY = musculus orbitohyoideus, QUADHYrLUG = musculus quadrato-hyoangularis, RECTCERV = musculus recnis cervicis, SUBRECT I-IV = musculi subarcuales recti I-ní TRVENT I1 = musculus transversus ventralis 11, numerals 1-6 = aortic arches 1-6, OCCVERT = arteria occipito-vertebraiis, PAL = artena paiatina, PDA = paired dorsai aorta, PR 3 4 = primary vessel of aomc arches 3-4, PULM = arteria pulmonalis, RMUSC = arteria carotis externa, ramus muscularis, SEC 3 4 = secondary vessel of aortic arches 3 4 , SUBCL = arteria subdavia, and T R = t m c u s arteriosus. From Millard (1945); reprinted by permission of the Royal Society of South Africa.
97
about 100 days in premetamorphic R. catesbeiana (Forman and Just 1976). Spleen In X. h s , the spleen anlage forms at the dorsal mesentery near the anterior end of the stomach by Nieuwkoop/Faber 43 and is well-defined by stage 4 5 4 6 . Blood corpuscles are visible at Nieuwkoop/Faber 47, lymphocytic diierentiation is detectable at stage 48, and the organ is highly vascularized by stage 49. Large celis in the white pulp (lymphoid foiiicles) do not mature into medium or large lymphocytes before Nieuwkoop/Faber 50 or into s m d lymphocytes before stage 51 (Manning and Horton 1969; Turner and Manning 1972, 1974). At Nieuwkoop/Faber 50 "degenerating macrolymphocytes" are present in the boundary between the red and white splenic pulp. The spleen aniage of Ranapipiens appears at Shumway 24-25 and contains erythrocytes, mesenchymal celis, and yolk platelets at Taylor/Koiiros I. At Taylor/Koliros I1 the aniage consists of s m d masses of mesenchymal and elongated reticular ceiis interspersed with erythrocytes, large and medium lymphocytes, and a connective tissue capsule. At Taylor/Kollros I11 s m d lymphocytes, neutrophils, and granuiocytes occur in the mesentery near the spleen, and the spleen begins to increase in size. The white pulp is formed during Tay1orF;ollros VIII-IX. The red pulp merges smoothly into the white puip as in the aduit spleen (J. D. Horton 1971a, b). The spleen is an important secondary lymphoid organ with significant reticuloendotheiiai functions. Phagocytic c e h of the reticuioendotheliai system of aduits are situated in the red pulp and grouped around the white pulp (E. L. Cooper and Wright 1976, Ascaphus mei; and Diener and Nossai 1966, B u . marinus). Macrophages prevent large particles and other ceiis from entering the white pulp. Turner (1969) ascertained that free macrophages of the body cavities have the same funaion in X. b i s .
in the pronephros (Broyles and Deutsch 1975 and Broyles and Frieden 1973, R. catesbeiana; K. L. Carpenter 1978, K. L. Carpenter and Turpen 1979, Foxon 1964, Hoiiyfield 1966, and Jordan 1933, R. pipiens; Meseguer et ai. 1985, R. ridibunda; and Turpen et ai. 1979, Ranapipiens), but the majority of larvai erythocytes is produced in the liver (Maniatis and Ingram 1971a, b, c, and Turpen et ai. 1979, R. Lymphatu and Reticuloendothelzal Organs catesbeiana). The increased chance of mfection caused bv bucco~hawnSalvatoreh (1970) distinguished four generations of geai contaa with the water that passes through it is counerythrocytesin Bufi b.u. Ceii diameters decrease in size from tered by the lymphatic and reticuloendothelial systems embryo to larva and increase at the beginning of metamor- (Aschoff 1924).The lvm~hatic.reticuloendothelial. and imphosis. In embryos, the ceiis are 250-750 p,m2 (Cambar/ mune systems are closely related to each other and to the Gipouioux I11 10), 150-500 p,m2in larvae (Cambar/Gipou- immune responses. Especidy in amphibians, lymphoid and loux IV 5), and 150-350 p,m2at the beginning of metamor- myeloid tissue appear together with macrophages and other phosis (Cambar/Gipouioux N 12). Rana catesbeiana (Tay- reticuloendotheliai ceiis (i.e., p h a g o q c ceiis) in the same lor/Kollros X-XII; Broyles et ai. 1981) has Type 1 cells organ. Lymph vessels drain body fluid from interstitial (26.920.03 [S.E.] p,m; dorninates in the kidney; contains spaces back to the veins and to lymph glands, where it is Td-4) that are oblong to oval with an acentric nucleus, and filtered ffirr. 5.8). The reticuioendothelial svstem consists of Type 2 (23.5020.04 p,m; dorninates in the liver; contains phagocytic macrophages in most organs and myeloid tisTd-l,2, and 3) cells are eiiiptical to round with the nucleus sues, which diierentiate into eosinophils, erythrocytes, maccentered (Benbassat 1970; Hoiiyfield 1966; McCutcheon rophages, neutrophils, and thrombocytes. During ontogen1936). In contrast to V. I. Ingram (1972), Broyles et ai. esis, stem ceiis popuiate many stmctures (e.g., Ijmph glands, (1981) concluded that there were different erythrocytes lin- thymus, ventral cavity bodies, branchial and aortic arches, eages (Type I) emanating from the kidneys and (Type 2) the intertubular tissue of the kidneys, intestinal w d , liver, lungs, liver. The distribution of erythrocyte classes in the vessels mesenteries, skin, and the w d i of the bile and hepatic duas; varies individually within a species, and these ceii survive for E. L. Cooper 1966 and Witschi 1956). E. L. Cooper (1967, L
i
\
"
T
I
,
T OMR ANAST SUB
SUB HEP
ABD
OML MPC
MPC DUOD
CAUD GAS
M
L
. MP
ST
PVC
RAC SUBC
ISCH
'OP
3,& J[ "Pr" ...^ ..
......... . . ..'.. .. '..... :.. . :.:... :: ....... .... .. . . .,...: .. :. . ', ;.:.
40
20
...I.____
.-.......
o
-E
+
Gills
$-/
Skin
Skin
õ .>"
40
w.. .. ....,...
o
+/+
Lungs
-.A~ills (IV-V)
(XVI-XIX)
(XXill-XXIV)
ADULT
DEVELOPMENTAL STAGE
Fig. 8.5. The relative contributions of giiis, skin, and lungs to gas exchange in tadpoles and adults of Rana catesbeiana at 20°C. (Ufler) O, uptake (vo,). (Lower) CO, elimination (vco,). Tadpoles and metamorphosing individual staged according to Taylor and Kohos (1946). Dotted lines connect to presumed values. After Burggren and West (1982).
199
PHYSIOLOGY
ana tadpoles related aeriai and aquatic respiration. West and Burggren (1982) studied Taylor/KoUros XVI-Wí (Gosner 4 0 4 1 ) tadpoles in water of 140, 82, 43, and 21 rnm H g (see Crowder et al. 1998). There were progressive increases in the frequency of lung ventilation with increasing hypoxia (l/hr at 140 rnm H g to 51/hr, with much variability, at 21 mm He) with an indication that tidai volume aiso increased. Average giil irrigation fi-equency and heart rate were unafFected by hypoxia (aiso Xenupus laevis larvae, Feder and Wassersug 1984; see Tang and Rovainen 1996), but there was a transient decrease d o t h the frequency and amplitude of giil ventiiations in hypoxic water after an air breath. Marian et ai. (1980) found an increase in surfacing frequency with a decrease in water PO, in Euph(yctis cyanophlycts, but in contrast to the studies just mentioned, they aiso found an increase in the frequency of gill ventilation as hypoxia increased. West and Burggren (1983) concluded that both lung idation (via stretch receptors) and the PO, of lung gas a e c t the giil irrigation ninute-volume. They suggested that the decrease in giil irrigation immediately &er an air breath could be adaptive in preventing diffusive 0, loss to the hypoxic water. Feder and Wassersug (1984) examined aerial and aquatic VO, in Xenopus b i s larvae, which lack giil fiiaments and presumably use the eniarged giil filters, buccopharyngeai epithelia, and skm for aquatic gas exchange. In water with more than 100 mm H g of O,, the aerial component of VO, was a relatively minor 17%, as was the case in buiifrog tadpoles (Burggren and West 1982). At a water PO, of 75-85 mm Hg, the frequency of lung-breathng started to increase fi-om control vaiues of about 2/hr to a high of 45/hr at 25-50 mm Hg. When the water PO, became very low, there was an indication of a reduction in overaü VO,, demonstrating that the lungs were not able to make up the shortfail in thiaciuatic VO,: * laaate did not increase. There was much scatter in the data, so a suggestion that these results indicate a depression of metabolic rate in hypoxic water must remain tentative. In addition. Wakeman and Ultsch (1976). in similar studies with three species of salamanders ranging from completely to partially aquatic, found that total VO, could be maintained in all three s~eciesdown to a water PO, of 20 mrn Hg. Whether a metabolic suppression (or a controiied reduction) occurs among tadpoles in severely hypoxic water probably wiii aiso be dependent upon such factors as degree of lung development and temperature. It is diflicult to draw general conclusions about the extent other variables. For exof partitioning witho~tconsiderin~ arnple, the developmentalstage has significant effects on partitioning related to differences in the relative development of lungi and giils and the large increases in tadpoli body size between hatching and the late premetamorphic stages (Burggren and Doyle 1986). The giii-lung-skin partitioning of VO, in buiifrog tadpoles was relatively independent of temperature from 15"-33°C in spite of increases in metabolic rate (Burggren and Pinder 1983). The relative importance of air breathing wili depend upon species-specific differences in the efficacy of exchange mechanisms, and these vary greatly. For example, Osteopilus bmnneus, a tropical "I
L
1 ,
liyiid, is an obiigate air breather in its natural environment and does not irrigate its buccai cavity (Lannoo et ai. 1987). Although Burggren and West (1982), Burggren and Pinder (1983), and Feder and Wassersug (1984) have shown that air breathing is infrequent and that pulmonary respiration is a minor component of total VO, for tadpoles in normoxic water. it is clear that an increased deoendence on air breathing wdl occur in hypoxic water. In order to minirnize predation risk, one would expect tadpoles to use one or more of a variety of adaptations, includmg selection of highPO, habitats, unpalatability, minimizing exposure time during breathing, acclimatization to hypoxic habitats (see below), and adaptive behavior patterns associated with air breathing. The selection of habitats with high PO, wouid reduce the dependence upon air breathing and wouid be adaptive if all other factors were equai. In habitats where the distribution of dissolved 0, is heterogeneous, PO, is normaüy highest in open (i.e., lacking dense vegetation) water (Ultsch 1973, 1976a; Wakeman and Ultsch 1976). Open water is not a good place for tadpoles to hide or find food, and when they do surface, they are much more likely to be detected by predators (Feder 1 9 8 3 ~ ) . Noland and Ultsch (1981) studied the relationships among temperature tolerance, hypoxia tolerance, and habitat seleaion in lungless tadpoles of Bufo tewestris and lunged tadpoles of Rana sphenocephaiu. Water temperature and dissolved 0, (DO) were measured from March to August at nine sites where one or both species occurred, and an attempt was made to samole all-microhabitats at each site. After these measurements, each microhabitat at each site was sampled to determine if either of the species was present. ~ h e ;found a trend toward a lowering of the criticalthermal maximum with increasing stage of development (aiso Bufo woodhousii, Shermaii 1980). Bufo tadpoles had a CT,, about 2°C above that of Rana at all stages; higher acclunation temperatures resuited in higher values of CT,,. Critical 0, tensions (Pc)of submerged larvae were relatively low at 20152 rnrn H " e i d tended to increase with temperáture but showed no clear relationship with stage or between species. Several conclusions can be drawn from the field data (fig. 8.6). (1) The range of temperature and D O was similar at sites containing Bufo and those with Rana (some sites had both species). (2) Bufo tended to live at higher temperatures (median of 30°C) than Rana (median of 24"C), largely because of their occurrence in shallow water and ternporary ponds. (3) Eighty-two percent of Bufo larvae were found at a D O of more than 50% air saturation, and 92% were found above their Pc. (4) Oniy 37% of the Rana larvae were found in water with a DO more than 50% of air saturation, whde 38% were found below their P,. From these data, Noland and Ultsch concluded that Bufo breed in temporary ponds partly because such ponds tend to have both a high D O and hghtemperature reiative to permanent ponds. ~ h high e DO is obviously adaptive to a tadpole that lacks lungs, while both high D O and high temperature wiil increase the already relativeh, hieh " metabGlic rate of Bufo larvae. speed their development, and increase the probability of metamorphosis before pond drying (see also Dupré and Petranka 1985; Pat-
(a*,)
,
L
GORDON R. U L T S C H , D A V I D F. B R A D F O R D , A N D J O S E P H F R E D A
i
50% SATURATION
C*
. .. Om.
RANA SPHENOCEPHALA
DISSOLVED OXYGEN (ppm) Fig. 8.6. Dissolved oxygen-temperature polygons for some aquatic habitats in Alabama. These areas represent the sum of possible combinations of dissolved oxygen and temperature within the habitats. The presence of tadpoles (Ramsphaocephalu and Bu@ tmertpis) at a loca-
tion is indicated by dots and their absence by circles. The critical 0, tension (P,) for each species and 50% saturation level of dissolved oxygen are both indicated as a function of temperature. After Noland and Ultsch (1981).
terson and McIncktan 1989). Kana, on the other hand, breed in more permanent ponds that will tend to have lower DO levels, and the tadpoles compensate by breathing air during the lengthy develop~nentalperiod. Nie et al. (1999) also studied the effects of ambient PO, and temperature on the distribution of tadpoles (Rana catesbeiana) in Alabama. They found that during the summer, the tadpoles in one of the study ponds were frequently found in water with a PO, below their P, in spite of the lack of predatory fishes and the fact that 56% of the pond bottom had water with a PO, greater than the PCof the tadpoles. Tadpoles caught in submerged traps in the hypoxic areas drowned, which indcates that air breathing was obligate in those microenvironments. If a tadpole lives in shallow water to ensure being in a hgh DO environment or breathes air in hypoxic water, it is exposing itself to predation. Predation is probably the major cause of mortahty of tadpoles, especially in permanent ponds, and may be a major selective force that has resulted in many anurans breeding in temporary (fish are absent) ponds (see chaps. 9 and 10). Moreover, predation may determine anuran community structure (Britson and Kissell 1996; Cortwright and Nelson 1990; Heyer et al. 1975; Woodward 1983; see Axeisson et a[. 1997) and can elirninate entire populations of tadpoles (Cortwright and Nelson
1990; Sexton and Phillips 1986; D.C. Smith 1983; see Barreto and Moriera 1996). Some anurans that breed in temporary ponds have relatively unpalatable larvae (e.g., R. A. Griffiths 1986; Reading 1990; Voris and Bacon 1966; Wassersug 1971; Wilbur 1987; some Bafa), which would allow them to be exposed in shallow, well-oxygenated waters, but in general temporary-pond breeders have tadpoles that are more palatable than those of permanent-pond breeders (see chap. 9). Among anurans that breed in permanent ponds, tadpoles of those with extended developmental periods may also be less palatable than those with shorter developmental periods. Bullfrog tadpoles, wMe apparently not absolutely unpalatable, will be avoided by some predators if there are other anuran larvae available ( h s e and Francis 1977; Woodward 1983). The relationshius between behavior and air breathing have not been exteisively studied. The decreasing frequenG of air breathing with increasing water PO, (Crowder et al. 1998, Wassersug and Seibert 1975; reviews by Feder 1984, Burggren 1984) intjlcates that pulmonary respiration is an accessory means of gas exchange in tadpoles. Using lungs only when necessary shodd lower the predation risk associated with breathing at the surface (Feder 1983~).In addtion, when a tadp& does surface t* breathe air, ;he breath is taken quickly and followed by a rapid descent to minimize
PHYSIOLOGY
exposure time. A few reports of synchronous air breathing among aggregating tadpoles are known (e.g., R W. McDiarmid, personal commuriication, Leptodaczy~us;Altig and Christensen 1981, Rana heckscheri; M. S. Foster and McDiarmid 1983, Stuart 1961, Rhinophvynus domali; N. D. Richrnond 1947, Scaphwpus holbrookii);this aaivity has been interpreted as an antipredator behavior among fishes (Kramer and Graham 1976). Tadpoles lacking functionai lungs are not necessarily unable to benefit from atmospheric oxygen. "Air gulping" is a cornrnon behavior in fishes in hypoxic water (Ultsch 1989) that can increase blood 0, transport (Burggren 1982). Even in severely hypoxic water the upper few millimcters will be oxygenated, and if an aquatic animal can irrigate its gills with this water, it can use atmospheric 0, indirectly. S m d fishes with upturned mouths are weii adapted for this behavior (Kramer 1987; W. M. Lewis 1970).Bufi woodhousiz tadpoles appear to use the latter strategy, as they niove to the surface in hypoxic water but apparently do not gulp air (Wassersug and Seibert 1975).
Carbon Dwxide Eliminatwn andAcid-Base Balance The majority of CO, elirnination of d ampliibiails is cutancous, and tadpoles in normocarbic water would not be expected to be an exception (reviews by Burggren 1984, Burggren and Just 1992). This supposition was true for Taylorl Koiiros XVI-XIX (Gosner 4 0 4 1 ) bullfrog tadpoles in a flow-through respirometer, where 98% of the VCO, was aquatic (57% cutaneous, 41% branchiai) and only 2% was pulmonary even though 17% of the VO, I a s pulmonary (Burggrcn and West 1982). As with aquatic VO,, aquatic VCO, partitioning in resting tadpoles is not affeaed by developmental stage (and therefore body mass) throughout the premetamorphic stages. The dominant role of the skin in CO, elirnination that is characteristic of the adult is assumed when a larva cntcrs metamorphic clirnax at Taylor/Koiiros XX-XXV (Gosner 42-46; Burggren and West 1982). There is no reason to beiieve that the partitioning of VCO, between air and normoxic water would change sigd c a n t l y with an increase in pulmonary respiration. If the water becornes hypcrcarbic, a tadpole wouid have to increase its plasma PCO, in order to maintain an outward diffusion gradient for aquatic CO, elimination. Even a relatively siight environmental hypercapnia would be a potentidy severe acid-base chaüenge. The plasma PCO, of tadpoles is normaüy very low aiid closer to that of fishes than to that of other amphibians (reviews by Heisler 1986; Toews and Boutilier 1986; Ultsch 1996; see Busk et ai. 1997). According to the Henderson-Hasselbalch relation, an increase in blood PCO, of 3 mm H g in a tadpole such as Rana catesbeiana represents about a doubling from normal values. This would cause much more of an effect on plasma pH than wodd be the case for aquatic salamanders with a normal plasma PCO, 2-6 times that of a tadpole (Ultsch 1987, 1996). Normal acid-base variablcs among tadpoles resemble those of fishes that iive in normoxic water (Heisler 1986; Ultsch 1996; see Ultsch and Jackson 1996), aithough the
201
data are limited (Erasmus et ai. 1970-1971; HelE 1932; Tust et ai. 1973). Perturbations of acid-base status can be expected from the same sources as with fishes: exogenously from water aciddication and environmentai hypercarbia and endogenously froni accumulation of acidic metaboiites, especiaÚy lactate. The reactions of tadpoles to acidic precipitation and acid mine drainaee are disc;ssed below. ~ h effects e of water hvpercarbia oGadpoles have received almost no attention. H;percarbia eiicits an increased dcpendence on pulmonary resiiration in aquatic salamandêrs ( ~ a k e m & and Ültsch 1976), as was found for the late stages of bullfrog tadpoles (Infantino 1989); increasing water PCO, up to 12 rnm H g had iittle effect on rates of giil or lung ventilation in bullfrog tadpoles in Taylor/Koiiros IV-XV (Gosner 2 9 4 0 ) . A ventilatory response had developed by Taylor/Kollros XVI-XIX (Gosner 4 0 4 1 ) , when the frequency of breathing doubled and the frequency of giii irrigation reduced by half; these changes would be consistent with a pulmonary hyperventilation that would partidy conip~nsatefor a respiratory acidosis and a reduction in aquatic VOZthat might slow the rate of CO, entrance. For tadooles of earlier stages " with smaü lungs and for lungless species, this strategy is unavailable. Extraceiiular pH compensation would have to involve increases in pl&ma con~entratiorisof HCO;, a mechanism cornmon in fishes (reviews by Heisler 1986, Ultsch 1996) but lacking in the aquatic saiamandersAmphiuma and Siren (Heisler et al. 1982), which often inhabit hypercarbic urater. These salamanders d o w the extraceilular p H to f d during hypercapnia but defend intraceiiular p H by clevating intraceiiular concentrations of HCO;, partly by exchanging Clk for HCO; from the environment. With no field data on the upper iimits of PCO, in tadpole microenvironments, the leve1 of respiratory acidosis that might exist in natural populations is uiiknown. Tadpoles may lack effective mechanisms for coping with high CO, tensions and therefore avoid hypercarbic water. Thc accurnulation of lactate shouid present an acid-base chdenge.' and it is clear that laaate dões accumulate both during exercise and severe hypoxia (see above). Howcver, as with most other sources of acidosis among tadpoles, there are no data on mechanisms of acid-base comoensation to the acidosis that accompanies lactate formation. In aquatic nutles, lactate accumulation results initiaüy in both metabolic and respiratory acidosis, as HCO; will be titrated at a greater rate than the animai can eliminate the resdtant CO, (review by Ultsch 1989). In tadpoles, because of their multiple and efficient modes of CO, elimination and theit relatively s m d body size (and therefore favorable surfaceto-volume ratio for cutaneous CO, elimination), a significant contribution of respiratory acidosis is not to be expeaed when laaate accumulates; t h s wodd ameliorate the p H disturbancc. In bullfrog tadpoles, lactate can be eliminated by the gds, s h , and kidney, aithough elirnination is not important relative to gluconeogenesis in processing lactate that results from exhaustive exercise (Quinn and Burggren 1983). These paths of elimination might be irnportant during chroiiic laaic acidosis induced by long periods of anV
202
GORDON R. ULTSCH, DAVID F. BRADFORD, AND JOSEPH FREDA
aerobiosis such as might occur during ovemintering in hypoxic water.
Thermal Physiology Of all the physicai parameters in the aquatic environment, temperature is perhaps the most dramatic in its effea on the physiology, ecology, and behavior of anuran larvae. For example, environmental temperature dramatically affeas the time taken to reach metamorphosis, which can be criticai t o the survivai of an individual faced with a drying habitat or the onset of winter. Temperature aiso affeas differentiation and growth rates, body size at metamorphosis, mechanisms of gas exchange, rates of energy metabolism, and undoubtedly many other physiologicai parameters documented in other eaothermic vertebrates. Moreover, the limits of temperature tolerance and temperature-dependent life history traits of anuran l m a e are generally related to the geographic distribution of the species. The thermai environment of all anuran larvae is variable in space and time, often extremely so in shallow water exposed t o intense insolation. For example, tadpoles of Rana catesbeiana may encounter seasonai temperatures ranging from near 0" t o over 3S°C, and near-shore temperatures may increase by more ti~an20°C in less than 6 hr (Ldlywhite 1970; Menke and Claussen 1982). Water temperature adjacent t o tadpoles of some species in temporary ponds may regularly rise during the day to 42°C (H. A. Brown 1969; Dunson 1977). Anuran larvae have generally accornmodated to variation in the thermai environment by (1) possessing the physiologicai ability to function over a wide range in body temperature, (2) behaviorally regulating body temperature, and (3) physiologically adjusting to changes in environmentai temperature (i.e., acclimatization, or in the laboratory, acclimation). O n an evolutionary scale, variation in the thermai environment has resulted in natural selection for differences among anuran larvae in a number of temperature-dependent physiological or life history traits. Temperature Tolerante Lzmits The lirnits of temperature tolerance of an animal are commonly described by a criticai thermai maximum (R,) and criticai thermal rninimum (CT-). These usually are defined as the temperatures at which "locomotor activity becomes disorganized and the animal loses its ability to escape from conditions that wili promptly lead to its death" (Cowles and Bogert 1944). The CT,, for most anuran larvae, when compared at the same stage of development and at intermediate acclimation temperatures, is between about 38" and 42°C (table 8.2). Extreme vaiues are severai degrees higher (44.9"C, Bufo marinus; fig. 8.7; table 8.2), and CT,, is apparently often approached in nature. For example, Cyclorana cultrpes, C. piutyuphaiu, and Litoria mbella occur in Australian pools at 39.2"C (Main 1968), Lzmnonectes canwivovus at 42°C (Dunson 1977), Scaphwpw couchii at 39"40°C (Mayhew 1965), Pseudaois tmimata at 36.S°C (Hoppe 1978), Osteopzlus septentrionalis suspeaed at 42°C (H. A.
Acclimation temperature O 35°C A 30°C O 25°C
DEVELOPMENTAL STAGE Fig. 8.7. Critical thermal m b a (a), and critical thermal minima (arn) of larvae of Bufi marinus at three acclimation temperatures and variou stages of development. Dotted liries connect mean responses of larvae averaged over aii acciimation temperatures. Staging foiiows Gosner (1960). After Floyd (1983).
Brown 1969), and a number of Australian species at 35"45°C (Tyler 1989). CT,, of tadpoles appears to be related to the natural environmentai temDeratures to which the animais are ex~osed. Such a pattern is weli established for anuran embryos (Bachmann 1969; J. A. Moore 1949b). The highest reported CT,, vaiues for tadpoles occur in species thãt typicay inhabit shailow ponds exposed to intense insolation (e.g., Bufo marinus and other species, Gastrophryne caroliansis, and Limnonectes cancrivoms): Among twó species of hylids and two species of pelobatids (table 8.2), lethal temperature is directly correlated with the maximum temperatures likely t o be experienced in the field (H. A. Brown 1969). In Ascaphus &i,-a species inhabiting coo1 streams, CT,, may be exceptionally low, as tadpoles aiways avoid temperatures above 22°C in a thermai gradient (De Vlaming and Bury 1970). Pseudmi tmseriatain Colorado has a stgnificant& higher CT,, at low elevation (e.g., 38.6"C at 1530 m, Taylor/ Koiiros XX [Gosner 421) than at high elevation (3725°C at 2710 m; Hoppe 1978). Likewise, in R. sylvatica heat tolerante decreases with both increasing elevation and latitude
PHYSIOLOGY
203
Table 8.2 Preferred body temperatures (PBT, as mean selected temperature) and CT,, and CT,,for anuran l m a e at various stages and acclimation temperatures. In studies including more than one acclimation temperature or larval stage, an intermediate acclunation temperature and ,, o b s e ~ e dat any larval stage stage closest to Gosner (1960) stage 39 were chosen. Values UI parentheses are the extreme means of CT,,or a or acclimation temperature. FTP = final thermai preferendum, (i.e., acclimation temperature equals PBT; Reynolds and Casterlin 1979) and RT = room temperature.
Species
Stage
Acclimation Temperature ("c)
ASCAPHIDAE Ascaphus tnrei BUFONIDAE Bufi amwicanus
B. boreas
PBT
a,,
%
10
De Vlaming and Bury 1970
FTP 22.5 20 22.5
Dupré and Petranka 1985 Beiswenger 1978 Cupp 1980 Beiswenger 1978 Karlstrom 1962 Karlstrom 1962 Straw 1958 Beiswenger 1978 Floyd 1984 Floyd 1983 Heanvole et ai. 1968 Davenport and Castle 1895 Noland and Ultsch 1981 Sherman 1980 Cupp 1980
-
22.5 27 30 21 25 27 -
20 HYLIDAE Osteupilus septentrionalis Pseudaclzr regilia f?hiseriata
20
H . A. Brown 1969 H. A. Brown 1969 Dupré and Petranka 1985 Hoppe 1978 Cupp 1980
21
Heanvole et al. 1968
20
Cupp 1980
25 20 ETP -
LEPTODACTYLIDAE Lepto*lus albilabvk MICROHYLIDAE Gartruphvyne carolinensis PELOBATIDAE Scaphiopus couchii S. holbmokii Spea hammondii RANIDAE Limnanectes ca~tcrivwus R. cmcadae R. cutesbeiana
.'Incipient lethal temperature (i.e., m&um bLethaltemperature, dead in 1-2 hr.
25 18-20 26.5
H. A. Brown 1969 Gosner and Black 1955 H. A. Brown 1969
22-25 21 21 24 26.7 RT 15 20 20 4 20 FTP RT 27 FTP 20 20 22
Dunson 1977 W o h u t h et al. 1987 W o h u t h and Crawshaw 1988 Dupré et ai. 1986 Hutchison and Hiü 1978 Lucas and Reynolds 1967 Menke and Claussen 1982 Workman and Fisher 1941 Wiilhite and Cupp 1982 D. F. Bradford, unpublished data W o r h a n and Fisher 1941 Casterlin and Reynolds 1979 Lucas and Reynolds 1967 Noland and Ultsch 1981 Dupré and Petranka 1985 W o r h a n and Fisher 1941 Cupp 1980 Manis and Claussen 1986
temperature that 50% of the tadpoles can tolerate indelinitely).
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GORDON R. ULTSCH, DAVID F. BRADFORD, AND JOSEPH FREDA
(Manis and Claussen 1986). In contrast, no sigiiificant difference in CT,= was found benveen populations ofleptodmtylus albilabris at 15 and 570 m elevation in Puerto Rico (Heanvole et ai. 1968). The CT,,also appears to correlate with environmentai temperatures, although it has been determined for tadpoles of only a few species (table 8.2). In Rana muscosa, a species in which tadpoles ovenvinter in frozen lakes, CT,,is below -2°C. The CT ,, is near or below 0°C in R. catesbeiana, a temperate species that ovenvinters in some populations (Coiiins 1979), a n d h a p h w truei, a species inhabiting coo1 temperate streams. In contrast, the tropical Bufo marinus has a much higher Ct,, (i.e., 6.0°C or greater and dependent on acclimation temperature and larvai stage; fig. 8.7). Similarly, in the temperate species Scaphiopus holbrookii, which undergoes larvai development entirely during the surnmer, CT, is 8.5"C in larvae acciimated at 18"-20°C. The temperature tolerance range of anuran larvae is large in comparison to most eaothermic vertebrates. In species in which both CT,, and CT,,have been determined, the temperature tolerance range for a single stage of development and acclimation regime is 34°C in Bufo marinus, 37°C in R. catesbeiana, and 28°C in Scaphwpus holbrookii (table 8.2). This range is even greater if acchation effects are included. For example, B. marinus tadpoles at Taylor/Kollros VI (Gosner 31) can tolerate a temperature range of 39°C if acchated prior to exposures to the low and high temperatures (fig. 8.7; Floyd 1983; ais0 Abe and Godinho 1991). Data are not available for the temperature tolerance limits of tropical forest species that experiente relatively s m d variations in temperature. It might be expected that tadpoles of these species would have narrower temperature tolerance ranges than species exposed to wider temperature variation. However, among adult anurans, tropical species do not gene r d y have narrower temperature tolerance ranges in comparison to temperate forms, aithough their temperature tolerance iimits are higher than those for temperate species (Brattstrom 1968). The typicaiiy higher CT,, of tadpoles relative to adults is a striking difference in the thermai relations of larvai and adult anurans. This is the case for Bufo americanus, B. exsul, B. marinus, B. woodhousii, Gastrophlyne carolinensis, Rana catesbeiana, R. pipiens, R. sylvatica, and Scaphiopus holbrookii (Cupp 1980; Floyd 1983; Hathaway 1927; Sherman 1980; Straw 1958; compare data in table 8.2 with Brattstrom 1968). The only apparent exceptions to this pattern are Pseuh r i s tnjeriata, in which larvai m , appears to be similar to adult CT,, (Hoppe 1978), and B. canums, in whch larvai CT ,, is lower than adult CT ,, (Karlstrom 1962). The finding that R. pipiens tadpoles die more quickly at high temperature than adults (Orr 1955) may have been caused by differences in body size. The generdy higher a,,,, of tadpoles than adults may reflea the need for tadpoles to minimize the time to complete metamorphosis and escape inimicai environmentai conditions and aquatic predators (see below). Alternatively, this difference may reflect the greater iikelihood for tadpoles than adults to become trapped in warm surroundings. Adults on land continudy lose heat
by evaporation (Tracy 1976) and often have the option to move to aiternative thermai microenvironments (Lillywhite 1970). Both larvai and adult anurans regulate body temperature behaviordy by moving or changing posture among available thermal microenvironments (Brattstrom 1962, 1970). When placed in a thermal gradient in the laboratory, anuran larvae invariably selea a certain temperature or temperature range more frequently than others. The arithmetic mean of these selected temperatures is often defined as the preferred body temperature (PBT; Reynolds and Casterh 1979). Many biochemicai and physiologicai processes, such as active metabolic rate, maximurn sustained speed, growth rate, food conversion efficiency, and learning and memory capabilities, are optimai at or near the PBT (Huey and Stevenson 1979; Hutchison and Maness 1979). Among anuran larvae, important processes known to change as a function of temperature include dzerentiation rate, growth rate, body size at metamorphosis, mechanisms of gas exchange, and metabolic rate (see below). Clearly, temperature regulation aiiows maximization or control of diierentiation and growth rates (Smith-Giii and Berven 1979). For example, in Pseudacris ornata, Rana clamitans, and R. sylvatica, differentiation and growth rates increase with increasing temperature until an inhibitory temperature weli below CT,, is reached (fig. 8.8;
i1
Growih
TEMPERATURE ('C) Fig. 8.8. Temperature dependence of differentiation rate and growth rate for individual Ranapipiens. Growth rate is cornputed as the regression coefficient of body v o l ~ r n eon ~ .days ~ ~ up to Taylor/Koiiros XVII (Gosner 40). Differentiation rate is computed as the regrcssion coefficient of stage on days through Taylor/Kollros XX (Gosner 42). Lines connect geometric rneans at each temperature. After Smith-Giii and Berven (1979).
PHYSIOLOGY
uble 8.2; Berven 1982; Berven et ai. 1979; Harkey and Scmlitsch 1988; Smith-Gili and Berven 1979). Temperature ulection rnay be critical to a tadpole faced with a deterioratiqaquatic environment, the end of the growth season, or ni increased risk of predation. Behaviorai temperature reguhxion also rnay serve to rninimize exposure to deleterious mn-tures abd conditions. For ex&vle. PseudanZs ornata lan-;e have fewer deformities and greater average survivai a h e n raised at intermediate temperatures of 20" and 25°C tban when raised at 10" and 30°C (Harkev and Semlitsch 1988). In overwintering species, avoidance of the lowest mperatures rnay minimize the probability of entrapment in ice that rnay lead to death by freezing or anoxia (Bradford 1984b). A temporary elevation in PBT, termed behaviorai fever, occurs in d major groups of ectothermic vertebrates iNuger 1978). Behavioral fever can be induced in tadpoles by injection of kiüed Aeromonm hydrophih, a common pathopin fishes, ampiubians, reptiles, and mamrnals (Casterlin and Reynolds 1977). This response has an adaptive vaiue in some ectotherms by increasing survivai rate after infection a i & iive A. hydrophila (Kluger 1978). However, behaviorai kver in tadpoles rnay aiter their behavior and increase their nisceptibility to predators (Lefcort and Eiger 1993). The mechanisms of heat exchange involved in behaviorai thermoregulation M e r between l&al and adult anurans because only adults can thermoregulate on land where radiation and evaporation are important mechanisms of heat exchange (Liilywhite 1970; Tracy 1976). In water, conduction and convection predominate as heat exchange mechanisms. Consequently, the body temperature of a tadpole is determined alrnost entirely by the temperature of the surrounding nater. Neither tadpoles nor frogs are known to possess any physiologicai means of controhng heat flux when in water (Brattstrom 1979). Nevertheless, solar radiation rnay contribute direaly to the heat input of tadpoles in shallow water (see below). The PBT of most anuran larvae studied is between 28" and 32°C (table 8.2). These values are roughly 10°C below the CT,,for each species, aithough PBT does not appear to be well correlated with CT,, There is some evidence for a weak correlation between natural environmental temperature and PBT. For example, in Rana clamitans, R.pipiens, and R. sylvatiea in the northeastern United States, tadpole PBT is duealy correlated with the beginning date of the breeding season and the northernmost distribution of the species (J. A. Moore 1949a; Workman and Fisher 1941). Moreover, the two species with the lowest known PBT (table 8.2; Rrcaphus mez and R . sylvatua) inhabit the coldest environments (also see Miranda et ai. 1991). The precision of temperature selection varies considerably among species and larvai stages. For example, Pseudacris tris&ata and Rana sphevweqphala behave as weak thermai selectors, especidy early in larvai development, whereas Bu@ am'canus behaves as a strong thermai selector throughout development (Dupré and Petranka 1985). For the developmental stages showing the most precise temperature selection in these species, the standard deviation for seleaed tem1
205
perature in groups of tadpoles is 2.2"C in E triseriata, 2.1°C in R. sphevwcephala, and 1.6"C in B. amevicanus. The corresponding value in R. eatesbeiana, in which selected temperatures were determined for individuais rather than groups, is 0.7"C ( W o h u t h and Crawshaw 1988). In contrast to CT-, the PBT of tadpoles shows no general pattern in comparison to PBT for adults. Rana cmcaúue tadpoles have higher PBTs than adults ( W o h u t h et ai. 1987), R . pipiens tadpoles appear to have a similar PBT to adults (Casterlin and Reynolds 1979), R . catesbeiana have similar or lower PBTs than adults (Hutchison and Hdl 1978; Lillywhite 1970; Lucas and Reynolds 1967; Wollmuth and ~rawshaw1988), andRreaphhs m e i tadpoles have lower PBTs than adults (Claussen 1973; De Vlaming and Bury 1970). Data are not avadable for tropical forest anurans tha; experi'ence a narrow temperature range or iive in therm d y homogeneous habitats. It is possible that some species in these conditions do not behaviordy regulate body temperature like some tropical forest-dwelkg fizards ( ~ u and e ~ Webster 1976).
Ontogeny of Temperature Tobrance and Reguhtion The temperature tolerance limits of anuran larvae typically change considerably during ontogeny. The most striking and consistent change is a decrease in CT,, near the completion of metamorphosis (about Taylor/Koliros XXI-XXV [Gosner 43-46]; fig. 8.7), as in Bu@ amerieanus, B. marinus, B. terrestris, B. woodhousii, Gashopblynecarolinensis, Pseudacris triseriata, Rana sphevwctphah, and R . sylvatua (Cupp 1980; Floyd 1983; Hoppe 1978; Noland and Ultsch 1981; Sherman 1980). The only exception is R. catesbeiana, in which this pattern was evident at only one of two acclimation temperatures (Menke and Claussen 1982). Prior to metamorphosis, CT,, remains fairly stable over a broad range of stages in most species, although significant changes are sometimes apparent (above referentes; Gosner and Black 1955). Ontogenetic changes in the CT,has received iittie attention. In B u . marinus the change in CTm, with stage is pronounced and is largely the opposite of the change in CT(fig. 8.7). In determinations of CTminfor three groups of stages of R. catesbeiana, CTmi,was near 0°C and varied l i d e among the stages (Menke and Claussen 1982; see Dainton 1988, 1991). Based on these limited data, the temperature tolerance range of anurans (i.e., CT,, to CT-,) appears to be reduced during the final stages of metamorphosis, rather than shified t o a lower level, as postulated by Cupp (1980) and Floyd (1983). The characteristic reduction in CT,,,= and the apparent reduction in temperature tolerance range at the end of metamorphosis rnay be consequences of biochemical and morphologicai rearrangements occurring at this time (Sherman 1980). Floyd (1983) noted that the times of least tolerante to temperature extremes in B. marinus coincide with the times of greatest morphological and biochemicai rearrangement early and late in larval development. The thermai preference of tadpoles also changes during larval development. Throughout most of development, PBT generdy increases with larvai stage (e.g., De Vlaming and
206
GORDON R. ULTSCH, DAVID F. BRADFORD, AND JOSEPH FREDA
Bury 1970; Dupré et al. 1986; Dupré and Petranka 1985; Floyd 1984; Hutchison and Hdi 1978; Lucas and Reynolds 1967; Woiimuth and Crawshaw 1988; Wollmuth et al. 1987; Ascaphus truei, Bufo americanus, B. marinus, Pseudacris triseriata, Rana cmcaúae, R. catesbeiana, R. pipiens, and R. sphenocephala). However, in R. cascaúae and R . catesbeiana (Oregon), PBT declines substantiaily during final metamorphic stages (Woilmuth and Crawshaw 1988; Wollmuth et al. 1987), whereas it appears to remain high at this time in B. am.canus, l?tkeriata, R. catesbeiana (Oklahoma), and R. sphenocephala (Dupré et ai. 1986; Dupré and Petranka 1985; Hutchison and Hill 1978). Precision of temperature selection generaily increases throughout larval development, along with the increase in PBT (e.g., Bufo americanus, Pseudacrii triseriata, Rana catesbeiana [Kentucky], and R . sphenocephala; Dupré et ai. 1986, Dupré and Petranka 1985). Standard deviations of selected temperature in groups of tadpoles of these species range from about 4"-8°C in early developmental stages to about 2"-3°C in later stages. In R . catesbeiana, in which individual tadpoles were monitored rather than groups, PBT and the precision of temperature regulation also generaily increased during development (Wollmuth and Crawshaw 1988). However, both precision and PBT decreased at the end of development (i.e., Taylor/Koilros XXII-XXV [Gosner 44461). The standard deviation for selected temperature in this study varied among stages fiom 0.7O4.6"C. The adaptive significance of ontogenetic changes in PBT is not clear. Floyd (1984) argued that ontogenetic changes in PBT of B. marinus are correlated with changing thermal characteristics of the natural microhabitats, and PBT is not coupled to ontogenetic change in temperature tolerance. Dupré and Petranka (1985) argued that the general increase in PRT during development rnay reflea greater selection pressure for rapid development at the end of the developmental period; this is a time when larvae become increasingly susceptible to habitat deterioration (Wilbur 1980) and predation (S. J. Arnold and Wassersug 1978; Wassersug and Sperry 1977), and the growth season may be ending. Finaüy, ontogenetic changes in PBT may spatiaiiy segregate age or size classes and thereby potentiaily reduce competition or cannibahsm, or encourage the formation of size-specific, cooperative aggregations (Alford and Crump 1982; Dupré and Petranka 1985). Although age segregation ofR. mcadae occurred in the field, groups were in such close proximity that neither cannibahsm nor competition were likely to have been affected ( W o h u t h et ai. 1987).
son and Maness 1979; and references therein). In ali amphibian larvae examined (table 8.2), temperature tolerance limits are significantly affected by the temperature of acciimation. For example, an increase in acciimation temperature of Bufo marinus from 25" to 35°C resiilted in an increase in CT,= of about 2.5"C and an increase in CT, of about 1°C (fig. 8.7). Among five other species (Bufo,Gastrophryne,Pseuda&, Rana), an increase in acclimation temperature from 10" to 30°C resulted in an increase in CTm, of about 1"-3°C (Cupp 1980), and an increase in acclinlation temperature from 15" to 35°C in three species (Osteopilus,Scaphiopus, and Spea) resiilted in an increase in lethal temperature by about 4°C (H. A. Rrown 1969). Such effects are probably essential for surviving temperature extremes in natural conditions, as a number of species have been observed in the field thriving ,, (see above). The in water at temperatures near their CT effect of acclimation temperature on PBT is much less distinctive than its effea on temperature tolerance iirnits. InAscaphus truei and B u . marinus, there is no effect of temperature acclimation (De Vlaming and Bury 1970; Floyd 1984), whereas a complex interaction was found among acclimation temperature, stage of development, and PBT in Rana cascadae,R. catesbeiana, and R.pipiens (Hutchison and Hdi 1978; Lucas and Reynolds 1967; Wollmuth et al. 1987). The time required to acclinlate completely to a new temperature has not been documented for anuran larvae. In adult anurans about two to four days are required for CT ,, and CT,, to s t a b h e after a large change in acclimation temperature (Brattstrom 1968; D u e h a n and Tmeb 1986). Possibly as little as 24-36 hr are required in larvae, and t h s time has been used as the minimum required for measuring the "final thermal preferendum" (= the temperature uitimately selected regardless of previous thermal experiente; Casterlin and Reynolds 1979; Dupré and Petranka 1985; Reynolds and Casterlin 1979). In addition to acclinlation, which is a gradual process, tadpoles of Rana catesbeiana undergo heat and cold "hardening" (Menke and Claussen 1982). In this process tadpoles exposed briefly to near-lethal temperatures become more tolerant to subsequent exposure to these temperatures within 90 rnin.
Other Infuential Factors A number of faaors (e.g., time of day, season, iight intensity, photoperiod, and nutritional state) other than stage of development and thermal history (i.e., acclinlation) influente theri%oregulatory behavior or-temperature tolerance in anuran larvae ( D u e h a n and Tmeb 1986; Hutchison and MaTemperatureAcclimatwn ness 1979). The magnitude of the effeas of these parameters Over a period of hours to days in a laboratory setting, tad- on PBT and tempeiature tolerance lirnits gener&y is smail poles accommodate to changes in the thermal environment in comparison to the effects of thermal history. by physiologicaiiy adjusting to new temperatures (= temDiel and seasonal cycles in temperature tolerance and perature acclirnation; Hutchison and Maness 1979). When PBT have been found in manv eaothermic vertebrates. alsuch adjusunents occur in the natural environment, the pro- though it is not established whether ail cycles are t d y encess is cailed acclirnatization (K. Schmidt-Nielsen 1983). dogenous (Hutchison and Maness 1979). Among anuran' Temperature acclimation has been discussed extensively for larvae a diel Dattern in PBT was observed in Rana clamitans adult amphibians and for ectotherms in general (e.g., Dueli- and R. pipiek but not in Ascaphus truei (Casterlin and Reynman and Tmeb 1986; Hutchison and Dupré 1992; Hutchi- olds 1979; De Vlaming and Bury 1970; Wiiihite and Cupp
PHYSIOLOGY
207
1982). Seasonal differences in PBT have been found in R. during the daytime as water temperature increases. Tadpoles catesbeiana and R. pipiens (Lucas and Reynolds 1967; Woil- commonly select the warmest temperatures available (e.g., muth and Crawshaw 1988). In tadpoles of R. catesbeiana at Beiswenger 1977,1978; Bradford 1984b; Brattstrom 1962; Taylor/Kollros XI-XVI (Gosner 36-40), PBT was above Muilally 1953; Noland and Ultsch 1981; Tevis 1966; Woll30°C during surnmer and in the mid-20s during winter. In muth et al. 1987; Bu) boreas, B. canorus, B. hemwphlys, B. contrast, earlier stage tadpoles selected the same temperature punctatus, B. terresCm,,Rana c a s h , and R. muscosa). Overthroughout the year. Aithough the cues underlying this sea- wintering R. muscosa select the warmest temperature below sonal diierence in later stage tadpoles of R. catesbeiana are the thermocline in frozen lakes (i.e., 3"4"C; Bradford unknown, a seasonal dzerence in PBT would íunction to 1984b). For some anurans (e.g., Beiswenger 1977, 1978; minirnize rate of diierentiation at a time inappropriate for Brattstrom 1962; Noland and Ultsch 1981,Bufo a m a n u s , rapid development and metamorphosis (Woilmuth and PseudamS crucfer, Rana boylii, and R. sphevwcephala) surface waters become sufficiently warm that they are avoided or no Crawshaw 1988). Although tadpoles of many species are positively or neg- longer sought. A comparison of the thermal relations of Bufo terremi atively phototaxic (Dueliman and Tmeb 1986; Wolimuth et ai. 1987), daytime PBT does not diier significantly from and Rana sphenocephala in the field and laboratory demonnighttime PBT of Rana pipiens (Casterh and Reynolds strates relationships among tadpole temperature tolerance 1979). Many positive phototaxic responses may occur in an- limits, tadpole thermoregulatory behavior, and the therticipation of increasing water temperatures that foilow expo- mal characteristics of the environment (Noland and Ultsch sure to sunlight (Beiswenger 1977; Dueliman and Trueb 1981). Tadpoles of B. tememi typicdy select the warmest 1986). Photoperiod d e a s the PBT of second-year but not temperatures available in shaiiow water, which often results PBT increases when in body temperatures above 30°C. In contrast, R. pipiens first-year tadpoles of Ascaphus -i; photoperiod increases (De Vlaming and Bury 1970). Photo- avoids shaiiow water when temperatures become warm, and period affects CT,, and CT,,, in B. marinus tadpoles in a body temperatures are typicaiiy weil below 30°C. These way that appears to increase survival under potentially dan- dzerences correlate with a higher CT,, in B. temescris than gerous thermal conditions (Floyd 1985). At high acclima- in R. pipiens (table 8.2). Aiso, the body temperature of B. tion temperatures, a long photoperiod increases R,,and temesh-zj in the field more frequently is near the CT,, than at low acclimation temperature, a short photoperiod reduces R. pzpiens The conspicuous behavior that maximizes body CTmm. The magnitude of these effects in B. marinus is a s m d temperature in B. temesh-zj, a species that frequently breeds fraction of the changes in CT,, and CTm,,caused by ther- in shdow, temporary waters, is viewed as a strategy for mal history. shortening developmental time and thus increasing the Nutritional state affects PBT in many ectothermic verte- probabiiity of completing metamorphosis before the habitat brates, includiig aduit anurans. The increase in PBT that oc- dries. In contrast, R.pz;piensusudy inhabits more permanent curs when the animal is digesting food (Ldiywhite et al. habitats than Bufo and does not develop as rapidly. More1973) presumably maximizes rate of digestion and con- over, Rana habitats typically have lower ambient temperaserves energy when digestion is not occurring. This pattern tures than Bu$ habitats. may be irrelevant for many anuran larvae, which are virtudy Dense aggregations of a few to thousands of anuran larnever without food in the digestive tract. No data are avail- vae frequently occur (see chap. 9). Aithough a number of able to assess the effect of nuuitional state on PBT in tad- factors are involved in the formation and maintenance of poles. Nutritional state affects thermal tolerance limits in these aggregations, water temperature is often the dominant Bufo americanus and B. marinus by decreasing the range of factor (Beiswenger 1975, 1977,1978). For example, in Bufo tolerance during food deprivation (Cupp 1980; Floyd ametiuznus, dispersed tadpoles are activated in the morning 1985). However, the magnitude of the reduction in both by increasing light intensity and move to shdow water on species is s m d in comparison to the effects of thermal his- sunny days where they accumuiate in warm microhabitats tory on temperature tolerance h i t s . (Beiswenger 1975). Once tadpoles reach sufficient density in the lighter and warmer microhabitats, feeding and social Themzoreg~tlatwna n d h r e g a t w n Behavwr activities draw them into dense aggregations. At night as Aithough selection by tadpoles of a preferred body tempera- water temperatures decrease in the shdows, tadpoles return ture is evident in the laboratory, a host of factors (e.g., light to warmer, offshore water. Beiswenger (1975) argued that intensity, food availabiiity and quality, dissolved oxygen, aggregating is a way for tadpoles-to exploit food more popuiation density, presence of predators, and tadpole social efficiently, engage in certain social activities, and seek suitinteractions) other than temperature may d e c t microhabi- able temperatures more effectively. In contrast, Brattstrom tat selection in the field (Beiswenger 1975, 1977; Lemckert (1962,1970) and Woilmuth et al. (1987) argued that aggre1996; Noland and Ultsch 1981; Woilmuth et al. 1987). gations in B. boreas, Pseudacris crttcfer,l? regila, &na boylzi, Nevertheless, temperature is often the dominant factor de- and R. c a s h occurred because of, and to augment, the termining microhabitat seleaion, and thermoregulatory be- thermal characteristics of the local microhabitat. Clearlv. havior has been documented in a number of studies. dense aggregations in many species are often observed in the Tadpoles in many temperate ponds typicatiy lie offshore warmest niicrohabitats in a pond. at night in warmer, deeper water and migrate to shdows Brattstrom (1962) provided experimental evidence that
i'
208
GORDON R. ULTSCH, DAVID F. BRADFORD, AND JOSEPH FREDA
tadpoles aggregate, in part, because they absorb more solar crease from 13" to 23°C resuits in about a 10-fold increase radiation than the surroundmg water, which resuits in more in differentiation rate and a 6-fold increase in growth rate in heat being absorbed in water containing aggregations. Beis- Ranapipiens (fig. 8.8; Smith-Giii and Berven 1979). Similar wenger (1977) described observations both supporting and patterns are also found in R. chmitans and R. sylvatica (Berrefuting this argument. The use of white porcelain pans in ven 1982; Berven et ai. 1979). which much of the radiation rnay have been refleaed by the Environmentai temperature has a ~ronouncedeffect on white substrate is a limitation in evaluating the data in Bratt- length of the larvai ieriod by virtu; of its iduence on strom's (1962) paper. Further experiments are needed in differentiation and growth rates (Smith-Gill and Berven which the radiative properties of the substrate in the test sys- 1979). In some species, reducing the time to metamorphosis to a rninimum is critical because tadpoles must complete tem better represent those in the field. metamorphosis prior to drying of the habitat or onset of Temperatwe, Dzflerentiatwn, and Crowth Rate other inimical conditions. Behavioral temDerature selection The influence of temperature on differentiation and growth resuiting in maximal differentiation rate wouid be expected rates probably is the most dramatic effect of environmentai (e.g., Brattstrom 1962; Sherman 1980; Wolimuth et al. temperature on the ecological physiology of anuran larvae. 1987). The differential effea of temperature on differentiaThis influence determines larval body size and length of the tion and growth rates promotes emergence from ponds durlarval period (Reques and Tejedo 1995; Smith-Giii and Ber- ing the warm part of the year, particularly if ponds become ven 1979), which in turn are directly related to survivai and overheated during pond drying (Etkin 1964). The same reproductive success (Berven 1982; Berven and Gdl 1983; mechanism mhibits emergence during the inappropriate Berven et al. 1979; C o h s 1979; Crump 1989a; Harkey cold season. In some species and environments, temperature may be and Semiitsch 1988; D.C. Smith 1987). Typicaiiy, an increase in temperature resuits in faster rates of development sufficiently low to make ovenvinteriig of larvae obiigatory and growth, shorter time to metamorphosis, and smaiier (Berven et al. 1979; C o h s 1979; Coiiins and Lewis 1979; Smith-Giii and Berven 1979). Overwintering occurs in a body size at metamorphosis. A model that predicts the timing of metamorphosis based number of anurans at high elevation and latitude where averon differentiation rate has been proposed and tested in the age temperatures are lower and the growing season is shorter laboratory and field by Smith-Gdl and Berven (1979). In than at lower elevation and latitude. For examde. Rana Ranapipiens, differentiation rate (defined as the slope of the catesbeiana larvae in Louisiana rnay complete metamorphosis stage-age relationship) is strongly correlated (r2 = 0.95) in a few months, whereas individuals in Michigan may not with the length of the larval period, whereas growth rate is metamorphose untii their third summer (Coiiins 1979).Asconsiderably less correlated (rZ = 0.51). Growth rates of caphus trÜei tadpoles in subalpine sites in Washington require R. pipiens and R. sylvatica larvae in some circumstances show five summers to complete larval development (H. A. Brown no significant relationship to length of the larval period. 1990b). In R. ylvatica in montane environments, a oneGrowth pararneters are often poor predictors of timing of month difference in ovi~ositionresuits in nearlv, a vear , metamorphosis largely because growth and differentiation difference in completion of metamorphosis because larvae are affected differentiaily by environmental factors such as from eggs oviposited later must overwinter (Berven et ai. temperature and population density. Also, growth rate is 1979). At extreme elevations and latitudes, low temperafunctionaiiy dependent upon differentiation rate, whereas tures that Drevent metamor~hosismav be the factor h:tine the converse is not true. This is because growth and develop- the geographic range of a species (Smith-Giil and Berven mental rates are both functions of circulating hormone lev- 1979; Uhlenhuth 1921). els, which are in turn dependent upon thestage of differAmphibian larvae are typicaiiy larger when raised at low entiation reached. Nevertheless, growth rate frequently is temperature, a phenomenon that appears to be general for related to the duration of larval development (e.g., Wiibur larval ectotherms (Berven 1982; Berven and GU 1983; Berand Coilins 1973) because conditions favorable for differ- ven et al. 1979; C o h s 1979; Etkin 1964; Harkey and Sementiation often are also favorable for growth (Smith-Giil and iitsch 1988; Koiiros 1961; Smith-Gdi and Berven 1979; Uhlenhuth 1919). For example, R. pipiens raised at 13" and Berven 1979). Temperature is a major factor determining larvai differ- 23°C in the laboratory differ in body size by about 3-fold at entiation and growth patterns, although other factors such aii stages, including metamorphic climax (fig. 8.9; Smithas density, food abundance and quality, and water quality Gdi and Berven 1979). In R. sylvatica in the laboratory and are clearly important (Berven 1982; Berven and Giil 1983; in R. clamitans in both the field and laboratory, a 10°C deHarkey and Semiitsch 1988; Pandian and Marian 1985b; crease in temperature results in about a 2-fold increase in Smith-Giii and Berven 1979; Viparina and Just 1975; Wil- body size at ietamorphic clima (Berven 1982; Berven and bur 1980; Wdbur and Coilins 1973). As temperature in- Gil1 1983; Berven et al. 1979). Larger size at lower temperacreases, rates of differentiation and growth both increase ture can be attributed to the greater effect of temperature on until an mhibiting temperature is reached (Berven 1982; Be- differentiation rate than on growth rate (fig. 8.8; Berven rven et al. 1979; Harkey and Semhtsch 1988; Smith-Giii et ai. 1979; Smith-Giii and Berven 1979). Thus. iarvae at and Berven 1979). Such an increase is predictable based on low temperatures gain more mass and are larger at any given Arrhenius enzyrne lunetics. For example, a temperature in- stage, including metamorphic clima, than at higher temI
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,
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PHYSIOLOGY
209
fects of temperature, rather than genetic or maternal effeas. Nevertheless, significant genetic differences were found. For example, in R. clamitans genetic differences were found in the témperature at whch-dfferentiation and growth rates were maximal, in temperature sensitivity of differentiation and growth rates, and in stage-specific growth rates. These genetic dfferences were counter to the observed clinai Gariation. For example, in cold-temperature experiments designed to simulate mountain-top conditions, montane tadpoles developed faster and completed metamorphosis earlier and at a smder size than did lowland tad~oles.Thus. naturai seleaion in R. chmitans has favored the shortest possible larvai periods given the ambient temperature constraints. This pattern is viewed as a case of counter-gradient selection, in Ghich naturai seleaion favors genot$es that minimize the range of phenotypes potentidy induced by the environments aiong a gradient. A similar counter-gradient pattern exists between environmentai temperature and developmental rate in anuran embryos (H. A. Brown 1967; J. A. Moore 1949b). DEVELOPMENTAL STAGE Fig. 8.9. Body size of larvae of Ranapipiens reared at 13"and 23°C through metamorphic dimax (Taylor/Koiiros XX,Gosner 42). Vertical bars were not defined in original ieference. After Smith-Giii and Berven (1979).
peratures. A secondary consequence of larger body size in ~oplobatrachusti>erinÜs appeai-s to be increased énergetic efficiency in converting tadpole tissue into frog tissue (Pandian and Marian 1985b). The differentiai effeas of temDerature on rates of differentiation and " growth are evident in the field as weii as the laboratory. In Rana clamitans larvae that had not completed metamorphosis by September, differentiation ceased whereas mowth continued (Smith-Gill and Berven 1979). ~ v e n t u dthe i larvae ceased both differentiation and gowtk as temperatures dropped to below 10°C. In the foiiowing spring, growth commenced earlier, at a lower temperature, than did dfferentiation. Subseciuentlv. these larvae metamorphosed at a larger size than'those'that both grew and differentiated at faster rates during the previous surnrner. Larvae with the slowest growth and differentiation were largest at metamorphic climax (Berven et ai. 1979; SmithGill and Berven 1979). Clinai variation in larvai development and morphology associated with temDerature differences has both environmental and genetic components. In Rana chmitans (lowland and montane populations) and R. ylvatica (lowland, montane, and tundra populations), the relatively cold environments at high elevation and h g h latitudes shorten the available breeding seasons, slows tadpole developmentai rates, prolongs the larvai periods, and increases the sizes of larvae at d stages in comparison to the lowland sites (Berven 1982; Berven and Gill 1983; Berven et ai. 1979). Complementary field and laboratory studies (including reciprocal transplant and breeding experiments) demonstrated that this clinai variation is primariiy induced by environmentaiefI
TemperatureE$ects on Other Promsses Energy metabolism measured by rate of oxygen consumption of anuran larvae increases approximately exponentidy as a funaion of temperature, a pattern typicai of most ectothermic animais. Qlovalues are 1.6-2.2 in Rana berlandieri (Burggren et ai. 1983; Feder 1985), 1.9-2.4 in R. catesbeiana (Burggren et ai. 1983; Feder 1985), 1.8-1.9 (Noland and Ultsch 1981) and 2.6 (G. E. Parker 1967) in R. sphenocephafa, 1.2-1.8 in Bufo tmestns (Noland and Ultsch 1981), 1.3-2.0 in Xenopw h s (Feder 1985; Hastings and Burggren 1995), and 3.2 in Limnodynastesperonii (E. Marshd and Grigg 1980b). An overd Qloof 2.14 between 15" and 25°C has been derived from data for both anuran and caudate larvae (Gatten et ai. 1992). Thermai acclimation of 0, consumption occurs in larvae of three of the four species examined: Rana berhndieri, R pi@ns, and X. 1(Feder 1985; G. E. Parker 1967). The findings are s i d a r to those for many adult anurans and caudates (Feder 1985; Feder et ai. 1984a) and many fishes and invertebrates (Bdock 1955) in which thermai acclimation f i e a s rate of oxygen consumption. Comrnonly, eaothermic animais reared at coo1 temperatures have hgher metabolic rates at a given temperature than animais reared at warmer temperatures (Prosser and Brown 1961; K. Schrnidt-Nielsen 1983). Interestingly, tadpoles of the Australian leptodactylid Limnodynastesperoni show no thermai acclimation of metabolism at any temperature (E. Marshd and Grigg 1980b), and one has to ask if this trait may be a common feature of the larvae and adults of Australian anurans. Temperature f i e a s many other physiologicai variables that are ecologicdy relevant in a wide variety of eaothermic vertebrates. Examples are digestive efficiency and rates (Warkentin 1992a, b), sumivai of disease, maximum locomotor acceleration and velocity (e.g., Lefcort and Blaustein 1995), endurance, active metabolic rate (see Toloza and Diamond 1990a, b), and learning and memory capabilities (Huey and Stevenson 1979; Hutchison and Maness 1979; Kluger
GORDON R. ULTSCH, DAV I D F. BRADFORD, AND JOSEPH FREDA
210
1978). Presumably, many of these variables are iikewise affected by temperature in anuran lamae.
Osmoregulatory Physiology Our current knowledge of ion and water balance in tadpoles has come from three principie areas: comparative physiology, properties of adult and lamal frog skin, and acidiication of freshwater habitats by acidic deposition. The latter causes mortality of amphbian lamae (e.g., Ling et ai. 1986) primarily through the disruption of Na+ and C 1 regulation. Studies exploring the mechanisms of acid water toxicity have revealed much basic information about ion regulation in tadpoles (e.g., Pierce 1985; Pierce and Harvey 1987; Pierce et ai. 1984). Although osmoregulation in tadpoles has been studied from these different perspectives, our overaii knowledge stili remains incomplete in comparison with our knowledge of gas exchange in tadpoles or osmoregulation in fishes. Thus far, ion regulation in tadpoles appears to be similar to ion regulation in teleost fishes. Significant differences between tadpoles and teleosts include an active uptake of ions across the skin, giils that are less developed morphologicdy, and metamorphosis providing a gradual transition to air breathing. Many interesting detaiís regarding ion and water balance in tadpoles await discovery. In this section, our current state of knowledge is presented and promising areas for research are suggested. Body Compositwn The ionic composition of the plasma of tadpoles, like most freshwater vertebrates, is markedly hyperosmotic and hyperionic relative to the surrounding environment. Ions of Na+, CI- and HCO; (table 8.3) are the major constituents responsible for 50%, 30%, and 15% of the osmotic pressure of plasma respectively (Just et al. 1977). The concentration of Na+ in bullfrog tadpoles is much more dilute than in typical teleost fishes (90 and 150 mEq/liter, respectively). In the crab-eating frog (Lzmnonectes ~ a n ~ v m sNa+ ) , and C 1 are also the most important ionic constituents, but their concentrations are about 50% higher than in bullfrogs acciimated to similar conditions (table 8.3; M. S. Gordon and Tucker 1965). Limnonectescancrivorus inhabits braclush water ponds and both tadpoles and adults can survive prolonged exposure to füil-strength seawater. The plasma osmolarity of
spadefoot toad (Spea hammondii) tadpoles is also higher than that of bullfrog tadpoles, and Funkhouser (1977) hypothesized that this is an adaptation for sumivai in ephemerai ponds that exhibit high salinities caused by evaporation (also see Ferrari 1998). Little is known about the plasma ion concentrations of other species of tadpoles; as this information becomes available, it wiil be interesting to see if the concentrations of plasma electrolytes are correlated with the concentrations Ôf saits in theirhabitats. The osmotic pressure of tadpole plasma increases steadiiy throughout development and is highest during the later stages (Degani and Nevo 1986; Funkhouser 1977; J. E. Richmond 1968). Osmolarities of 160 mOsmol/liter in premetamorphc stages of Rana catesbeiana tadpoles increased to 259 mOsmol/liter at the end of metamorphic climax (J. E. Richmond 1968). Just et al. (1977) reported a much smder increase (181 to 198 mOsmol/liter) during development of R. catesbeiana. Spea hammondii tadpoles aiso experienced a similar increase in plasma osmolarity at metamorphosis (Funkhouser 1977). This increase is presumably because of the increase in concentrations of plasma electrolytes resulting from a characteristic dehydration that occurs at metamorphosis (Just et al. 1977). This phenomenon is in keeping with the general concept that aquatic animals benefit from lower plasma ion concentrations because of a reduction of osniotic and ionic nradients between the animal and the water. Hematocrit remains relatively stable during development and averages about 30% in R. catesbeiana tadpoles (Just et al. 1977). Few measurements of osmotic concentration and comDosition of tadpole blood have been reported for species other than large ranids. Because of this iimitation, many investigators have re~ortedion and water concentrations as wholebody concentrations, and large interspecific and intraspecilic variations exist (table 8.4). Caution must be taken when interpreting experiments that measure whole-body concentrations of ions and water because several factors influence their levels. The recent feedmg history must be considered because a large percentage of the mass of a tadpole is ingested material in the gut, and the ionic content of the food can directly influence the mass-specific ion content of tadpoles. The mass of the gut contents also can have an indirect effect on mass-specific ion content by infiuencing body mass. In addition, body ion and water content changes dramaticdy U
Table 8.3 Ionic cornposition, osmotic pressure and hernatocrit of the pla srna of tadpoles Ionic cornposition (mEq/liter) Species Limnonectes ~anrrivorus~ Rana catesbeiana
Na'
K+
CI-
HCO,
Osmotic Pressure (rnOsm/liter)
153 90 96-109
5 4 3 4
99 68 57-60
25 8-24
272 70-195 1-200
aLimnonectescanwivorus was acclimated to 100% freshwater.
Hernatocrit (%)
Referente M. S. Gordon and Tucker 1965 Alvarado and Moody 1970 Just et ai. 1977 S. C. Brown et ai. 1986 Funkhouser 1977 Funkhouser 1977
PHYSIOLOGY Table 8.4 Ion content and percent body water of five species of Rana tidpoles lon Content (p,Mol/g dry body mass) Species of Rana
catesbeiana clamitans muscosa pip'ens sylvatica 'units
=
Na' 573-1080 573 369 60-70' -
1365-1815 400-800
Body water
K+
Cat+
339-355
-
-
-
-
45-5 5'
30-35" 507 300-600
-
C1-
Referente
-
Freda and Dunson 1984 Freda and Dunson 1986 Freda and Dunson 1984 McDonald et al. 1984 Bradford 1984b Freda and Dunson 1984 Freda and Dunson 1984
-
-
-
-
3040' -
88-91
300-825
87-96
-
(%)
-
p,Eq/g wet mass.
as a tadpole develops. Freda and Dunson (1984) reported the body ion and water concentrations of wood frog (Rana ~lvatiuz)tadpoles every week from one week posthatching until metamorphosis. From days 7-14, body sodium concentrations increased from 400 to 800 pEq/g dry mass. This presumably occurred from a combination of active uptake across the skin and gds and the initiation of feeding. Body water also increased from 80% to 96%. The net result was that tadpoles gained weight very rapidly early in development because of the uptake of water. For example, dry mass increased by only 20%, whiie wet mass increased by 300%. This rapid increase in body mass early in development has ecological and physiological significance. Many predators (e.g., newts and salamander larvae; Brodie and Formanowicz 1983; C m p 1984) of tadpoles are gape-limited, that is, they feed on what they can fit in their mouths and swallow. Tadpoles should be most vulnerable to predation during early stages of development, and a rapid volume increase after hatching would tend to reduce predation. Throughout the remainder of development of R. sylvatica, body Na+concentration and body water gradually declined. Body Na+ concentration has been shown to be linked with tadpole size for other species. For R. catesbeiana, body Na+ concentration is negatively correlated with dry mass (body Na+ concentration = 255 g - 0.485, r2 = 0.94; Freda and Dunson 1986). Sidarly, Bradford (1984a) reported that the concentrations of body water and solute are negatively correlated with body mass, and Zamachowski (1985) found that percent body water deciined as R. temporaria tadpoles grew. The mechanisms causing this relationship are not known, but ifthe extracellular fluid space shrinks during growth and metamorphosis, body water and solute concentrations would be expeaed to decline. A second possibility is that as tadpoles grow, they contain a higher percentage of tissues (e.g., bone) that might reduce mass-specificconcentrations of water. McDonald et al. (1984) showed that body Ca" concentrations nearly triples in R. clamitans during premetamorphic and metamorphic stages. T h s presumably occurs as a result of limb development and increased cakification of the skeleton. Species comparisons are also confounded by environmental conditions (e.g., temperature, sahnity, and pH), which can have large effects on body ion and water composition (see below), and intraspeciíic variation in body ion
and water concentrations. For example, Freda and Dunson (1984; see Pehek 1995) reported that R. chmitans tadpoles coilected from an acidic bog and acchated in the laboratory to water with a pH of 5.8 had a body Na+ concentration of 369 pEq/g dry mass. McDonald et al. (1984) reported a body Na+ concentration of 60 pEq/g wet mass (= 600 pEq/ g dry mass, assurning 90% water) for R. chmitans tadpoles coilected from an undescribed pond (see M. Uchiyama and Yoshizawa 1992). Conclusions about any general effects of D Hreauire further studies because the different s~eciesthat I have been tested have not been of the same age or size or maintained under comparable conditions (see Bradford et ai. 1994; Schmuck et al. 1994; Verma and Pierce 1994). Water Balance As discussed in the previous section, the body fluids of most tadpoles are hyperósmotic and hyperioiic .relative to the freshwater habitats in which they iive. These osmotic and ionic gradients are the driving force for the continual osmotic uptake of water and d i i v e leak of plasma ions. As with freshwater fishes, tadpoles remain in ion balance by excreting copious quantities of dilute urine and by actively transporting ions across external epitheiia. Few direa measurements of unidirectional exchanges of water in tadpoles have been reported. This is surprising because the body water concentration of tadpoles changes during growth and development and is strongly influenced by temperature (Bradford 1984b). Water may be taken up across the gds, skin, or gut. Tadpoles drink the external medum, probably during the course of feeding. Alvarado and Moody (1970) reported d r i n h g rates (Rana catesbeiana) of 0.014 mi/g.h (see Territo and Smits 1998 for a discussion of physiological calculations based on various measures of body mass), ofwhich 0.006 ml1g.h is absorbed. S. C. Brown et ai. (1986) reported preliminary measurements of urine production to be 0.006 ml/g.h, and Mackay and SchmdtNielsen (1969) and B. Schrnidt-Nielsenand Mackay (1970) reported urine flow in R. clamitans at about 0.02 mi/g.h. Because the mass of these animais did not change during the measurements, urine flow rate approximated the uptake of water across the giiis, skin, and gut. Detailed studies ofwater uptake and loss across the gds, skin, gut, and kidney remain to be done.
212
GORDON R. ULTSCH, DAVID F. BRADFORD, AND JOSEPH FREDA
Ion Rt~uiution Tadpoles continuously lose Na+, CI- and other ions because of the large concentration gradient between their body fluids and the water. In addition, ions are lost in the urine. We are not aware of studies that quanti@ the relative importance of these different loss routes. Several studies reported loss rates of Na+ and CI- for Rana catesbeiana and R. clamitans (Aivarado and Moody 1970; Dietz and Aivarado 1974; Freda and Dunson 1984; McDonald et ai. 1984). Uptake of Na+ and CI- generaiiy exceeds loss so the animais remain in positive ion baiance. Possible routes of active uptake of ions include the gilis, skin, gut, and buccopharyngeal epithelium. Initially uptake was thought to occur only at the gilis because Na+ and CI- was lost from solutions used to perfuse the gilis, but uptake was not increased if the períüsate was aiiowed to contact the skin (Aivarado and Moody 1970). In addition, studies of isolated larval skin did not detect active uptake or a transepithelial potential (TEP; Aivarado and Moody 1970). In support of the notion of the lack of dermai transport, active transport and TEP across the skin abruptiy appear late in metamorphosis and are correlated with an increase in skm Na+-K+-ATPase(Boonkoom and Aivarado 1971; Kawada et ai. 1969; R. E. Taylor and Barker 1965). This conclusion has been challenged because stripping the skins from the underlying musculature caused considerable stress to the preparation. In addition, no specific precautions were taken to prevent edge damage. Cox and Aivarado (1979; see Aivarado and Cox 1985) developed techniques for the study of isolated larval skin that rninimized dissection and edge damage. They found that larval skin actively transports Na+ inward at a rate of 5%10% of that of adult skm. Their work suggests that the basal membrane in the skm of larval and adult anurans is similar. The difference in the rate of Na+ transport may be caused by the absence of amilorideinhibitable Na+ channels in the apical membrane of larvai skin. The addition of nystatin (forms cation-selective channels in lipid bilayers) to the outer bathing solution stimulated Na+ influx to rates comparable to untreated adult skms (Cox and Aivarado 1983; also Zamorano and Salibián 1994). The many factors that influente the active uptake of Na' include temperature, external ion concentration, water hardness, and pH. Interspecific differences may occur, but conclusive data are lacking. The uptake mechanisms for Na+ and CI- display typical saturation kinetics. The Km and V, for Na+ uptake in Rana catesbeiana tadpoles were 0.2 mEq/liter and 0.25 ~ E q / g - h(Dietz and Aivarado 1974). Freda and Dunson (1986) reported a Km and V, for Na+ transport in R. catesbeiana to be 0.28 mEq/liter and 13.4 ~Eq1g.hon a dry mass basis (= 1.61 p,Eq/g.h; assuming 90% body water). The chloride transporter was saturated over the range of 0.2-3.0 mEq/liter and the V, for C1- was 0.10-0.15 ~Eq1g.h(Dietz and Aivarado 1974). The location and type of ceils responsible for Na+ and C1- transport have not been identiíied. Na+-K+-ATPaseactivity in microsomal fractions of giil homogenate correlates weil with the intensity of Na+ transport (Boonkoom and Aivarado 1971). Na+-K+-ATPase
has also been measured in the skin of Rana catesbeiana tadpoles (Kawada et al. 1969). The transport of Na+ and CI- are independent. For example, acetazolamide inhbits the branchial influx of CIwithout affecting the influx of Na+ or the efflux of Na+ or CI- (Dietz and Aivarado 1974). The counter ions for Na+ transport are thought to be H + and NH,', while CI- is exchanged for HC03. These findings bring up another important ~ o i n t In . addition to their function in sait and water baiance, the gilis of tadpoles are also important sites of acidbase regulation and NH,' excretion. Dietz and Aivarado (1974) reported net NH,' excretion in Rana catesbeiana tadpoles of 260 nEq1g.h. McDonald et ai. (1984) reported net losses of NH; for Rana clamitans of 634 nEq1g.h. In addition, NH,' excretion in postmetamorphic animais was 12% of that in premetamorphic animais, indicating that the weilcharacterized switch from ammoniotely to ureotely had been completed. In the terrestrial BufO bufO, this switch starts at the time when forelimbs are developed under the operculum and accelerates with f o r e h b emergence but does not occur in the aquatic Xenupus luevis (Munro 1953).
Effects of Temperature When tadpoles are exposed to cold temperatures (e.g., 4"C), they rapidly increase in mass because of the uptake of water. The water content of Rana muscosa tad~oles increased bv 6% I after 1month of exposure to 4"C, after which water content remained stable for 7 months (Bradford 1984a). Between 7 and 12 months of exposure, water content again increased slightiy. During the first month of exposure, the osmotic pressure of the peritoneal fluid dropped by 14%, approached control values after 7 months, and then again declined at 12 months. It appears that water uptake is accommodated by the extraceilular fluid volume (ECF; Bradford 1984a). In a related study, S. C. Brown et al. (1986) studied the weight loss in cold-acchated (5°C) tadpoles after return to warmer temperatures. Rana catesbeiana tadpoles transferred to 11" and 18°C lost 7% and 10% of body weight after 5 days, whde plasma Na+ concentration increased by 28% and 21%, respectively. Daily treatment with ovine prolactin or growth hormone prevented weight loss or the concornitant increase in plasma Na+ concentration. Neither propylthiouracil nor arginine vasotocin had an effect. These authors concluded that the changes in plasma solutes reflected changes in ECF volume. The adaptive significance, ifany, of cold-induced edema in larval or adult anurans is not known. It would be interesting to know ifwater gain was simply because of an inhibition of osmotic regulatory mechanisms at low temperature, or if it is a specific physiological adaptation to winter conditions. Effects of Salinity Frogs occur in aquatic habitats that range widely in salinity. Many habitats are extremely dilute, such as soft-water bogs, rainwater fiiled temporary ponds, and water in granitic basins. Rana catesbeiana tadpoles can be reared in distiiled water (Aivarado and Moody 1970). Similar to frogs and fishes, exposure to distilled water or very dilute solutions stimulates
PHYSIOLOGY
the sodium transport system. Elevated V, for Na+ transport and an unchanged Km (Dietz and Aivarado 1974; Freda and Dunson 1986) may reflect an increase in the total number of transport sites. Freda and Dunson (1986) also found that exposure to high Na+ concentrations increased Km and depr&sed V,,,,. ~ h e s changes e in the characteristics of the transport mechanism would help maintain Na+ balance in dilute water and reduce energetic costs of ion regulation in water with high concentrations of Na+. It is not known whether branc6al or s h permeability is adjusted in response to water saiinity. Some amphibians occur in highly saline habitats such as ponds and streams d u e n c e d by saltwater spray or tidai movements and desert ponds as they evaporate. The majority of field studies have focused on the distribution of aduits with referente to salinity (Christrnan 1974; Ruibai 1959, 1962). Manv s~ecieshave been found in braciush salt marshes, and it appears that species vary in their tolerance to salinity. A few specialized species (Bufo viridis and Limnonectes cancrivoms) can survive in 40% and fuli-strength seawater, respectively (M. S. Gordon 1962; M. S. Gordon and Tucker 1965; M. Uchiyama et al. 1990). Very few studies of to habitat salinity the distribution of tadpoles with regard have been re~orted. The best:known euryhahe amphibian is the crab-eating frog (Limmnectescancrivoms) of southeastern Asia. The aduits and tadpoles may be found in braciush water ponds and mangrove swamps. The tadpoles can survive exposure to fdi-strength seawater (M. S. Gordon and Tucker 1965; M. Uchiyama et al. 1990; M. Uchiyama and Yoshizawa 1992) and have been found in ponds ranging from 16% to 75% seawater (M. S. Gordon and Tucker 1965; Dunson 1977). However, M. S. Gordon and Tucker (1965) couid not induce tadpoles to metamorphose in the lab if water salinity was griater than 20% Seawater, and the largest tadpoles were obsemed in the most saline ponds. These obsemations suggest that L. cancrivoms tadpoles cannot metamorphose at high salinities, but this suggestion awaits more rigorous verification. The adults are osmoconformers and are able to survive in highly saline waters by elevating plasma urea, which raises plasma osmotic pressure and thereby elirninates the driving force for the dehydration that would occur in saltwater. Larvae are osmoregulaters; ifwater salinity is increased from 100% freshwater to 100% saltwater (a more than 10-fold increase in osmotic pressure), plasma osmotic pressure only doubles (M. S. Gordon and Tucker 1965). Over d salinities (0%-100% seawater), 90%-100% of the osmotic pressure of plasma is caused by Na+. K+. and C1-. Similar to marine teleost fishes. these tadpeles osmoregulate in seawater by d r i n h g thé hyperosmotic medium and by excreting a s m d amount of isosmotic urine. Aithough it hai never bein verified, the tadpoles probably excrete salts by an extrarenal pathway such as Na+ transporters in the skin and giüs. M. S. Gordon and Tucker (1965) also found that tadpoles become osmoconformers as froglets (Taylor/Kollros XXV, Gosner 46). In 80% seawater, starting at Taylor/Kollros XX (Gosner 42), plasma osmotic pressure increased and plasma Na+, K+, and CI- concentra,
L
213
tions did not change. This pattern was presumably the resuit of the initiation of urea production. More detailed experimental data are clearly needed on the physiology of this interesting species.
Effects of LowpH Concern over acidic precipitation has stimuiated a great deal of recent research on the effects of acidic water on amphibians. Lowered rain pH over the northeastern United States, southeastern Canada and Europe has been implicated in the depression of alkalinity and pH of many freshwater habitats. Acidic mine drainage associated with coal and metal strip mining can also seriously impact freshwater habitats (Kinney 1964; Porges et ai. 1986). Aithough anthropogenic acidification has received much attention, it is generdy not realized that many freshwater habitats are acidic because of naturdy occurring humic acids or the biological activity of Sphapum (reviews by Gorham et al. 1985; Kilham 1982; see Rosenberg and Pierce 1995). Naturdy acidic waters have been described throughout the world: major branches of the Amazon and Congo rivers (Marlier 1973); boreal peat bogs of North America, Europe, and Asia (Gorham et al. 1985); many waters of the eastern and Gulf Coastal plain of the United States (Gosner and Black 1957%) and the southwest cape of South Africa (Picker 1985; Picker et al. 1993); heathlands of Great Britain (Beebee and Grifin 1977); swamps of Maiaysia (D. S. Johnson 1967); and ponds of northern Austraiia (T. E. Brown et al. 1983). Detailed discussions of the distribution of acidic waters in the United States, the relative tolerance of different species, and the ecological effects of acidic waters are reviewed by Freda (1986) and Pierce (1985). Tadpoles are more tolerant of low environmental pH than embryos but less so than aduits (Freda 1986). Amphibians as a group are much more tolerant than fishes. The primary toxic effect of low pH is dismption of Na+ and CI- balance (Freda and Dunson 1984; McDonaid et al. 1984). Acute exposure to lethal p H mhibits the active uptake of Na+ and C1- while causing a massive stimuiation in passive Na+ and C1- loss. InAux of Na+ is linearly related to pH and 100% inhibition occurs near pH 4.0. The loss of Na+ increases exponentidy just above the lethal pH. In d species tested, death occurs when body Na+concentration is reduced by about one-half. The increased efflux of Na+ and C1- at low pH is quantitatively responsible for the reductions in body ions, and variation in the rate of loss defines intra- and interspecific variation in acid tolerance (Freda and Dunson 1984). The inhibition of Na+ influx may be caused by direct competition of H + and Na+ for the carrier sites (which may not be the sarne for the two ions), as increasing the concentration of Na+ in acidic water elevates Na+ uptake (Freda and Dunson 1986). Ion loss presumably occurs across the s h and giils. In fishes it is thought that Na+ loss at low pH results from the leaching of calcium from the branchial epithelium, which opens up tight junctions and compromises the structurai integrity of the gdi epithelium (Freda and McDonald 1988; also see Suffler 1996). Chronic exposure to sublethal p H generdy causes a 20% decline in body Na+concentration and stimulates compensa-
214
GORDON R. ULTSCH, DAVID F. BRADFORD, AND JOSEPH FREDA
tory mechanisms to help maintain ion balance (Freda and Dunson 1984, 1985, 1986). The influx of Na+ in Rana pipiens tadpoles was first depressed but then exceeded conGol values during seven days of exposure to pH 4. 5. Efflux of Na+ was initidy stimulated but later declined to levels just above controls (Freda and Dunson 1984). Similarly, McDonald et al. (1984) reported that Na+ influx and efflux in R. ciumitans in closed chambers where the water was initiaiiy of DH4 . 0 4 . 2 returned to control values after 7 hr of emosde. Aithough the inhibition of influx is not significant during lethal exposures, restoration of influx during sublethal exposures is important in maintaining ion balance. Freda and Dunson (1986) showed that exposure to low p H exposure acts simiiarly to other salt-depleting conditions (e.g., distiiied and soft water) by increasing the V, for Na+ trans~ o r tThe . reduction in sodium efflux that occurs after molonged exposure h a s not been studied but presumably involves a reduction of Na+ permeability of the giiis, skin, or both.
Summary To understand the ecological physiology of tadpoles as a group, it is essential to examine phylogeneticdy diverse tâua and diverse environmental conditions. At present, most of the knowledge about tadpole ecological physiology is based on very iunited subsets of taxa and environmental settings. For example, most ecophysiological studies have been done with temperate zone species, rather than tropical species, yet the greatest diversity of taxa are tropical. Even within the temperate zone, the preponderance ofwork has been iunited to members of the Bufonidae and Ranidae. In part, this is because relatively few investigations have been conducted on amphibian larvae in comparison to aduit amphibians and other vertebrate groups. Also, these studies have often sought to understand how amphibian larvae d s e r from aduits and other vertebrates rather than to understand how tadpole biology M e r s among species and environments. Investigators have tended to work with local species or species easiiy maintained in the laboratory. Future ecophysiological studies should ask questions concerning the interaction of environmental parameters and the physiology of tadpoles in environmental settings that are
poorly known. Studies of ontogenetic differences wouid be helpful (e.g., Burggren 1984; Burggren and Fritsche 1997). Examples may be temperature relations of tadpoles in tropical forests with little fluctuation in temperature and gas exchange of tadpoles mhabiting bromeliads. To the extent possible, such studies should be designed to compare phylogeneticdy disparate taxa and different settings in order to distinguish between phylogenetic and environmentaiiy induced patterns. We shouid also attempt to understand the physiology of tadpoles in the context of the many considerations faced by the individual (e.g., obtaining food, avoiding abiotic and biotic hazards, and maintaining an internal environment within tolerable lunits; Feder 1992). For example, behavioral temperature regulation can expedite development, and air gulping can compensate for low oxygen levels in the water. In contrast, the former may lead to stranding, and both activities may render an individual more susceptible to predation (e.g., Lefcort and Eiger 1993). Our challenge is to understand the trade-offs between the physiology-driven processes and other considerations. This task should be interesting, although perhaps difficuit, because many amphibians can tolerate wide variations in some physiological parameters (e.g., body water, temperature, and osmolyte concentration) in comparison to other vertebrates, especiaiiy birds and marnmals (Feder 1992).This is exemplified for tadpoles of many species by their relatively wide temperature tolerance ranges (table 8.2). Aiso, many aspects of the physiology of tadpoles change during larval development. This apparently wide tolerance of some physiological conditions combined with ontogenetic changes in physiology may aiiow tadpoles considerable flexibility in accornmodating to the spatial and temporal variations in their abiotic and biotic environments.
ACKNOWLEDGMENTS We thank T. Dietz, A. Riggs, and R. J. Wassersug for editing parts of this chapter. Additional cornnients were provided by W. Burggren and M. Feder. Bradford acknowledges the environmental Science and Engineering Program at the University of California, Los Angeles, for support during the early stage of preparation of t h s chapter.
BEHAVIOR Interactions and Their Consequences Karin vS. Hoff, Andrew R. Blaustein, Roy W. McDiarmid, and Ronald Altig
I find studying the behaviour of animais in their natural surroundings a fascinating hobby. Tinbergen 1968:iii
Introduction A tadpole is an energy-gathering,growing, nonreproductive larvai stage in the biphasic anuran life cycle. Various authors (e.g., Wdbur and Cohns 1973) have modeled the impacts that different aquatic environments have on tadpole gr&th and feeding, and growing to the largest size in the shortest period remains a driving force for selection. Optirnizing growth enhances the probability of completing metamorphosis and reaching the reproductive stage. Forms of paedomorphosis that result in a larval individual capable of reproduction occur in saiamanders but are unknown in anurans. As a resuit, behaviors usuaiiy associated with sexual activity and species recognition (e.g., courtship displays) among reproductive adults are absent in larvae. Instead, the behaviorai repertoire of tadpoles is restricted to activities that augment development, growth, and survival to metamorphosis. Aggregations of tadpoles in nature are relatively common (see Duellman and Tmeb 1986; Lescure 1968; Lyapkov 1996; P. J. Watt et al. 1997) and may be interpreted broadly as ecophysiological, metamorphc, feeding, and social responses. Relative to aggregative behavior, we focus primarily on feeding and social interactions. Three basic subject areas provide the organization for this chapter: (1) aspects of general maintenance (feedmg, respiration, thermoregulation, and locomotion); (2) dispersion and social behaviors (habitat selection. social interactions. and kin recognition); and (3) sensory abilities (vision, cutaneous senses, olfaction, and chemical communication) and learning. Tadpole behavior is not weii studied, and we point out specific areas that need attention. i notations of developmental stages foilow the system of Gosner (1960; see table 2.1 and fig. 2.1).
General Maintenance Feedin~ Tadpoles usuaiiy are considered highly speciahzed, fiiterfeeding herbivores (e.g., Duellman and Tmeb 1986). Most ingest planktonic material from the water column, obtain organic materiais from pond sediments, or scrape material (i.e., aufwuchs, periph~on)from submerged substrates. Given the diverse and son~etimesbizarre morphology of their feeding structures, the variety of sizes and kmds of food items recorded in their guts, the absence of ceiiuiase for digesting plant materials, the diversity of microhabitats occupied, and our lack of basic knowledge of their diets determined from conventional gut content analyses convinces us that tadpoles are better thought of as opportunistic omnivores or detritivores.
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KARIN vS. HOFF, ANDREW BLAUSTEIN, ROY McDIARMID, RONALD ALTIG
Stimuli emanating from food sources that initiate locomotor or feeding responses (e.g., P. H . Harrison 1990) also have not been studied well. Svstematic and com~arative evaluations of the food habits of tadpoles are uncommon (but see Diaz-Paniagua 1985; Heyer 1973b; Inger 1986 and referentes therein) and generaily not very informative because many ingested items pass undanlaged through the gut, whiie other soft-bodied oreanisms and bacteria are not dea tected. Such observations have led some authors to suggest that the real sources of food for tadpoles may be dissolved inorganic and orgaxiic nutrients, bacteria, and viruses (Heyyr 1973b; Inger 1986). The contribution of these s m d itcms to tadpole diets remains unstudied in nature, and that part of thematerial that a tadpole ingests that is actually digeSted is not known. Items re~ortedfrom the Vm t s of tad~olesinclude sand. detritus, viruses, bacteria, smaii unicellular organisms (protists), algae (diatoms, filarnentous green, euglenophytes), plant fragments of assorted sizes, pollen grains, hngi, various kinds of s m d animals (axmelids, cladocerans, copepods, gastrotrichs, insccts, nematodes, rotifers, tardigrades, water mites), anuran eggs, and heterospechc and conspecific tadpoles (Costa and Balasubramaniam 1965; Diaz-Paniagua 1985; J. D. Harrison 1987; Heyer 1973b; Inger 1986; Lajmanovich 1994; Sabnis and Kuthe 1980; Sekar 1992). Tadpoles also are known to feed on fecal material (Steinwascher 1978a) and swldry typcs of carrion (= necrophagous group of Beiswenger 1975). In all cases, caution must be exercised in interpreting feeding habits and their possible correlations with morphology. A. Haas (personal communication) recently found intact ephemeropteran larvae in an unidentified ~oophistadpole from ~ a d a ~ & c aThis r . situation was unexpected in a suctorial tadpolc that lives in very fast water and maintains position with an exceptionaily large oral disc. Research has focused on evidence of food selection from several approaches: stomach content analysis (e.g., Jenssen 1967); comparative aspects of buccal anatomy related to feeding (e.g., Viertel 1985; Wassersug 1980); comparative mechanical restrictions on feeding behavior based on anatomy a i d limitcd experimentation(e.g., Wassersug and Hoff 1979); feeding dynamics of a smaii number of species in the laboratory (e.g., Sede 1980); and relationshps between feeduig modes and microhabitat use, oral morphology, diet, and phylogenetic groups (e.g., Altig and Johnston 1989; Diaz-Paniagua 1985; Heyer 1973b; Ingcr 1986). Warkentin (1992a, b) examincd the effects of temperatiire and Uumination on microhabitat use and feeding rates of Rana clamitans tadpoles. Most tadpoles feed by producing currents that carry particles into the bucal cavitv and across food entraDment surfaces. A tadpole opens its mouth (ser fig. 4.16), depresses the floor of the buccal ca~ityto draw in water, closes the mouth, and then elevates thé floor of the buccal cavitv to pump water across food entrapment surfaces and out through the spiracle(s) (e.g., De Jongh 1968; Gradwell 1972b, c; Kenny 1969b, c; Severtsov 1969a; Wassersug 1972). Tadpoles occur in countless aquatic habitats, feed at many
sites (benthic, midwater, surface) throughout the water column, and have characteristic morphologies and behaviors. To demonstrate t h s ecological and morphological diversity and to provide some background for reading this chapter, we illustrate two somewhat hypothetical larval comm~mities, one typical of a forest pond 9.1) and the other of a forest stream (fig. 9.2). VCTeselected our examples from the Neotropical region because that is a fauna with whch we are familiar. It also is broadly representative of faunas in other tropical regions, which are ecologicaily arid taxonomicaily diverse compared to tliose in comparable habitats in temperate zones. More detailed illustrations of these and other tadpole morphotypes are shown in figure 12.1, and their associated mouthparts are shown in figure 12.2. Heyer (1973b) described the microhabitat use, feeding and swimming behavior, and diet of pond-dwehlg tadpolcs of 1 7 species in a dry forest site in Thailand, and Inger (1986) a l d Ingcr et ai. (1986a) reported a comparable study for 12 stream and 4 nonriparian tadpoles of 16 frog species from a wet forest site in Borneo. Pond tadpoles of the African frog Xenupus laevis are typicaiiy positioned head downward at about 4S0, while those of&alychnis p w e l l i (Duellman and Trueb 1986) and otlier phyllomedusine hylids usuaiiy position thcmselves upward a t .about 45'. suspension-feediig microhylid tadpoles usuaiiy float horizontdy near the surface or in midwater, and tadpoles of Rbinopbvynus dorsalir usuaiiy swim horizontaiiy. The buccal purnping mechanism is similar in at least ail rasping tadpoles, but species d 8 e r in the efficicncy of entrapment based on the sizes (i.c., 0.126 in Wassersug 1972 to greatcr than 200 p.m in Seale 1980) of particles that are capGred. These differences in efficiency have been correlated with variations in skeletal elements of the purnp (Wassersug 1972; Wassersug and Hoff 1979) and density of the giil aters (Wassersug 1972). Tadpoles without keratiriized mouthparts (e.g., G ~ o p h l y n eandXenopus) cannot graze on plant material that is too laree " to fit into their mouths. and tadpoles lacking ultraplanktonic entrapment surfaces (e.g., Hymenocbirur) feed on items large enough to be retained without entrapment surfaces. Wassersug and Hoff (1979) noted specific behavioral correlates with buccal pump design. Deflcaion of the floor of the cavity by a levcr aaion of the ceratohyal causes the buccal cavity to act as a hydraulic pump. The area of the bucal cavity floor, the length of the lever, and the amount of deflection determine maximum buccal volume and maximum suction force (negative pressure) generated by the pump. Microphagous tadpoles tend to have large buccal volumcs and short lever arms and regulate fecding rate by frequency moduiation (FM) of pumping frequency (e.g., Xenopus laevzs). Tadpoles with relatively longer lever arms vary buccal volumes and pressures by amplitude modulation (AM)of the ceratohyal defleaion (e.g., Rana yl17atica). Suctorial forms that rely on buccal suction to adhere to surfaces (e.g., hcaphus) have large lever arms and smail buccal volumes to generate high pressurcs. Macrophagous tadpoles have large volumes and long lever arms. The validity of morphological modeling to predict feed-
(fig.
BEHAVIOR
Fig. 9.1. An ecological diorama of a hypotheticai composite tadpole community in and near a neotropical pond. The mdpoles of six species with distina morphotypes that might occur there are üiustrated exhibiting typical behaviors (e.g., feeding, swimming, hiding, etc.). Top center: Hyla b m m e l e (Hylidae), an arboreal (Tjp 1) tadpole that occurs in the central axil of a bromeliad. Top right: Hyla miroqhaíu (Hyiidae), a midwater macrophagous form with reduced mouthparts searching for s r n d crustaceans among stems of aquatic plants. Lower
right: Scinuxstuu@n (Hylidae), a nektonic midwater form with high fins that scrapes food from leaves and stems and other undenvater surfaces. Right center: Rhinophynushalk (Rhinophrynidae), a filter feeding tadpole that swims in large, midwater schools. Left center: Lcp t o ~ 1 w p e n t ~ L (Leptodactylidae), us an omnivorous benthic tadpole that often is carnivorous on hatchlings and small tadpoles. Lower left: B u . murinus (Bufonidae), a black, benthic, rasping tadpole that sometimes aggregates.
ing behaviors is supported by studies of feeding dynamics in 1997; aiso see Caidweii and De Araújo 1998 and Nguenga Ranu ylv& and Xempus laePrj (Sede et ai. 1982 and Sede et ai. 1997). In their review of arboreai tadpoles, Lannoo and Wassersug 1979; see feeding dynamics below) and aiso et ai. (1987) tabulated species known to consume frog eggs; is consistent with the suggestion (Wassersug and Seibert other hylids that breed in phytotelmata (i.e., bromeliads and 1975) that the buccal pump design of tadpoles refleas feed- tree holes), including Phrynohym resinzjhm (R. W. McDiaring more than respiratory needs (see Respiration below). mid, personal observation), Osteocephalus d.iqmeurii (R W. Polis and Myers (1985) tabulated 14 species fiogs McDiarmid, personal observation), 0.oophqgus (Jungfer and whose tadpoles ate conspecific tadpoles or eggs, and other Schiesari 1995); Anothecu spinosa (Jungfer 1996) and 0. species have been added to the list (e.g., Osteopilus ieptencvio- phniçeps (L. Haugen, personai cornrnunication) can be added dIj,Crump 1986; aiso see table 10.2). Crurnp (1986) dis- to that list. ChirUcdw etfingm' (Rhacophoridae)nests in tree tinguished between opportunistic cannibalism (such as oo- holes and broken or cut bamboo stems and has oophagous phagy and necrophagy, in which the prey does not attempt tadpoles (Ueda 1986; Karn et al. 1996). Tadpoles ofPhilautus to evade the predator, and cannibahsm, in which conspecifics sp. aiso found in a tree hole in Thailand apparently feed on are attacked, killed, and eaten (e.g., Summers and Amos frog eggs, likely their own (Wassersug et ai. 1981a).
9
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K A R I N vS. H O F F , A N D R E W B L A U S T E I N , R O Y M c D I A R M I D , R O N A L D A L T I G
Fig. 9.2. An ecological diorama of a hypothetical composite tadpole community in and near a neotropical stream. Likely occurring representative morphotypes are shown in different rnicrohabitats and exhibi ~ typical g behaviors (e.g., feeding, swimming, hiding, etc.). Top right: Thmopa miliari (Leptodactylidae), a semiterrcstrial tadpole that lives on the wet surface where rivulets of water flow over a vertical rock faces. Lower right: Cocbraí~~üugvanulosa (Centrolenidae), a fossoria1 tadpole that buries within leaf packs in stiU.water. Right center: O a > p ~ p y b u r n(Microhylidae), i a psamrnonic tadpole buried in sand
in shailow, slow-moving water. Left center: P h ~ h ~ u t t a(Hyt a lidae), a neustonic tadpole feeding from the surface film in shallow water with an umbeiiiform oral apparatus. Lower left: Hyh annata (Hylidae), a suctorial tadpole that attaches to rocks in fast water. Top left: Elcuthemda&u~ ridenr (Leptodactylidae), embryos of a &rem developing species that placa its eggs among fallen leaves that often accumulate in the axils of understory plants. Top center: PhynuLyll~resintjitm (Hylidae), an arboreal (Type 2), omnivorous, often times oophagous, tadpole that occurs in tree holes.
Cannibalism may be more common than reported, especiaiiy among tadpoles of frogs that breed in smaii, ephemerai ponds and phytotelmata (e.g., bromeliads and tree holes) that are subject to unprediaable drying or where resource shortages and overcrowding may be common and survivorship low (Bragg 1957, 1965; Crump 1986, 1990, 1992; Downie 1990b; see chap. 10). Cannibaiistic tadpoles most commonly eat conspecifics of different sizes or develop-
mental stages. Large tadpoles may eat eggs (Crossland 1997; Crossland and Aiford 1998; Heusser 1970a) and hatchlings (Crump 1983), and premetamorphic tadpoles may prey on metamorphosing individuais (Bragg 1957; C m p 1986). Heusser (1970a) speculated that conspecific oophagy may be yet another reason for synchronous oviposition, and this argument can be extended to synchronous metamorphosis. Reports of tadpoles eating conspecific tadpoles in the field
BEHAVIOR
have not aiwavs made it clear whether the orev were aireadv dead before they were eaten. However, conspecific tadpole cannibaiism has been observed in the field (Cmmp 1990, Hyhpseudupuma); Petranka and Thomas (1995) argued that explosive breeding in Rana sylvatica reduced egg and tadpole cannibalism. In laboratory studies, Cmmp (1986) dowed tadpoles of Osteopilus septencrionalis to me&norphose in aquaha with emergent surfaces to reduce the likehhood of drowning. The presence of these surfaces did not eliminate cannibalism by younger tadpoles in the sarne aquaria, and rnetarnorphosing tadpoles (Gosner 42-43) in both experimental treatments (i.e., those that were not eaten by conspecifics) climbed up the verticai glass waiis. Aii metarnorphosing froglets survived in the control treatments (i.e., those without younger conspecifics). It seems k e l y that cannibaiism, at least in this species, is active predation by younger (Gosner 36-39) tadpoles, perhaps siblings. Cmmp (1986) speculated that metamorphosing tadpoles were more vuinerable to predation because they had diminished locomotor capacity compared to either tadpoles without forelegs or froglets without taiis. Wassersug and Sperry (1977) aiso demonstrated that anurans in the middle of metarnorphosis (four legs and a tail) do not swim as fast as tadpoles younger - than Gosner 42 or hop as far as froglets older than stage 45. It may be that tadpoles prey preferentiaiiy on conspecific tadpoles when they are most vuinerable; t h s is the same stage at whch they are aiso preferentiaiiy preyed upon by other species (e.g., Tbamnuphis, S. J. Arnold and Wassersug 1978). Some tadpoles (e.g., Hymenocbims and Lepidobatracbus) are specialized for consuming large food items (Wassersug and Hoff 1979). and some are activelv , oredaceous on heterospecifics. The hypertrophied jaw serrations of the tadpoles of Otopbryne pyburni (Wassersug and Pyburn 1987) and Mantdu@ylus lu.ubrtr (R. Altig, personai observation) superficidy appeai to be specializa~onsfor carnivory but are probably used to sort particles during filtration processes. Wassersug and Pyburn (1987) suggested that the tadpole of Otopbrynepyburni feeds by passive aspiration caused by water flowing past the aperture of the elongate spiracle tube. An arnazing example of feeding behavior and parentoffspring com&unicas, R septentrionaks, Farel 1980, 1981, tadpoles) and other aquatic vertebrates and %nopus laePZr) that varied in siix and shape. Although (Grillner 1974, dogfish; Grillner and Kashin 1976, carp) the performances of size-matched tadpoles were broadly showed that ipsilateral axial muscles can contraa serially t o overlapping, the performance ranks correlated with the mus- ~ r o d u c ea wave of muscle activitv that travels with the bendcle mass; Rana septentriunalis was the fastest tadpole with ing wave. Examination of other swimming activities (e.g., 26% of its mass as axial muscle andxénopw laevis ( 3 . 5 4 . 0 starting, stopping, very slow and very fast swirnming) in cm TL) was the slowest with 16% of its mass as axial muscle. Rana catesbeiana showed that traveling waves of bending can Most fishes have greater amounts of axial muscle compared be produced when contralateral muscles are acting simultato any tadpole exarnined (Hoff 1988b). This disparity sug- neously and also can be transmitted passively (i.e., without gests that muscle mass alone is not what permits compara- muscle aaivity in the posterior tail) if the wave is initiated tively good burst swimming performance; overall body anteriorlv. It is not clear whether this rance " of locomotor shape may be an important factor. The maximum absolute mechanisms is specific to Rana catesbeiana or to anurans, or velocity recorded (Hoff 1986a, 1988b) was 104 cm/sec for if it is a general feature of vertebrates that use undulatory a largetadpole, and the hghest relative velocity was 29 body swimming. lengths/sec for a small tadpole (about 2 cm long). The range L. Muntz (1975) described five stages in the behavior of in locomotor performance was very large for a11 species, and B n q w larvae relative to trunk myogenesis: nonmotile many individuais did not respond by swimming rapidly. (NieuwkoopFaber 20-22; myotomic muscles start to Maximum electrically inducible speeds may not be indicative differentiate), premotile (stage 22-24; first striated fibrils of the utility of speed alone to evade predators. Even at these visible, contractions possible), early flexure (stage 24-27; re-
BEHAVIOR
flexes and peripherai nerves present), early swimming (stage 28-33), and free swimming (stage 3 2 4 6 ; coordinated swimming possible, muscle c e ~ ut&ucleate). s Muscle cells did not become multinucleate until metamorphosis (Nieuwkooppaber 48-50). The behaviorai development of leg muscles was similar but, as expected, occurred at later stages: nonrnotile (Nieuwkoop/Faber 48-52; diierentiation minimal, nerves present), premotile (stage 53-54; limb trembles and cell striations forming), motile (stage 55-58; lirnb can make stepping movements, celis striated and multinucleate), and fully funaionai (stage 60-63). Hughes and Prestige (1967) studied the behavior of the hind limb during development. Some tadpoles move in ways other than by swirnming. Suctorial tadpoles occur in a number of families and have large oral discs (e.g., Aitig and Brodie 1972; Ascaphus tmei). The l a r ~ edisc aiiows the tad~oieto move about and feed on rock substrates in hgh-energy streams without loosing contact (C. L. Taylor and Aitig 1995; C. L. Taylor et ai. 1996). Having the belly modified into a sucker (e.g., Ranidae: Amoiups, HuUt, and Meristoflenys; Bufonidae: Atelophryniscus, Ateiupus, some Bufo) apparentiy aiiows mhabitation of faster currents (Altig and Johnston 1989), but it is the extension-retraaion c d e s of the oral disc that ~rovide the locomotor force. ~ i k suctoriai e and other rheiphilous tadpoles, those with abdominal suckers can move across the substrate by extension-retraction cycles of the oral disc (= oral h i t c h g of Altig and Brodie 1972). Aithough some stream tadpoles can swim powerfdly (e.g., Formas 1972; Telmatobufi australis),there are no tadpoles that continuaiiy occupy &e water column in fast floGing water like somé fishes do. Some nonsuctoriai tadpoles that live in flowing water escape the current by hdmg within crevices, rocky substràtes, or leaf packs. These tadpoles often do not have the typicai morphÔlogy associated Gith stream inhabitants; they are often fusiform (= vermiform) with less robust tad muscles and low fins. It is &ely that tadpoles of this morphotype swim against currents ( ~ a s s e r s uand g Heyer 1983 and citations therein; R. Aitig, personai observation). Tadpoles of the family Centrolenidae are stream dweliers with fusiform bodes, long tads and low fins, poorly developed eyes, and highly vascularized and lightiy pigmented skùl. Vdla and Vaierio (1982) reported coliecting specimens in soft, spongy earth of a stream bank, in moist earth beneath a plant 3 m from the stream, and in leaf packs in the s u e m . They caiied them "fossorial" and speculated that the long tails were usem in pushing the fusiform body (= burrowing) into mud and leaf packs. We have coliected centroleGd tad~oiesof severai S~eciesand most often found them in dense leafpacks and decaying organic material aiong streams, sometimes above the waterline. The tadpole of Staurois nutator (Inger and Tan 1990; Inger and Wassersug 1990) is a morphologicaiiy similar burrowing tadpole from streams in the lowlands of Borneo. In addition to being strongly convergent on the centrolenid morphology, this tadpole has a large, uninflated lung (does not breathe air) and, like centrolenid tadpoles, probably relies heavily on cuV
227
taneous respiration; in this respect it differs from other elongate tadpoles. Other elongate tadpoles live in bromeliads and do very little swirnming (table 3 in Lannoo et ai. 1987). The tadpole of Osteopilusbrunneus has a tail to body ratio of 3.9 and probably is the most elongate tadpole known. Lannoo et ai. (1987) showed that 0. brunneus tadpoles swim very little, ineffectively (i.e., they have to beat their t& twice as fast as a Rana or Xenopus larva to achieve the same velocity), and with excessive lateral motion indicative of low kinematic efficiency. Three explanations had previously been offered to account for the very long tail of 0. brunneus tadpoles (and certain other arboreai, bromeliad dweliing forms as well): cutaneous res~iration.locomotion in a viscous medium. and an agitator to aerate the water. Lannoo et ai. (1987) reviewed each of these postulates and found them somewhat unsatisfactorv. As a result., thev offered a fourth: the tail of 0 . brunneus serves as a static posturai organ to keep the head directed upward and nearer the water surface. They suggested that the lungs serve for buoyancy and assist in this . . behavior. ~ u l m o n Grespiration is important to the tadpole of 0.bmnneus, and this posture saves the tadpoles energy by them not having to swim to the surface. Also a heads-up position could provide the longest tadpoles with an advantage in getting to eggs laid by femaies at the water surface (see previous oophagy discussion). Oldham (1977) described terrestrial locomotion in the tadpoles of two West African frogs, Chiromantis rufescens and Leptopelis hyloides (Hyperoliidae). Leptopelis deposits eggs in a "nest" dug up to 6 cm beneath the surface in moist, soil close to water; &ek the eggs hatch and the tadpoles wait for rain. When the nest area floods, frantic wiggling by the group of tadpoles creates a water-íiüed cavity. The roof of the cavity eventuaiiy coliapses and the tadpoles ccburrow"to the surface. The tadpoles have unusuaiiy long tads with many muscle bundies per linear unit and are able to reach water by wiggling like eels in very shaiiow water across the substrate (Oldham 1977). In contrast, Chiromantis ru@scens builds foam nests on vegetation, usuaiiy above water; when the nest disintegrates, tadpoles drop into the water and carry on as typicai pond larvae. Sometimes, the nest is not above water and the tadpoles have to make their way across wet soil to water. The tail of C. mfescens tadpoles is relatively shorter and less muscular. In a different scenario, CaidweU and Lopez (1989) reported that tadpoles of Leptodactylus mystaceus aiso make foam in their terrestrial nests to avoid dehydration. Under experimental conditions designed to duplicate hatching conditions, Leptopelis hyloides larvae traveled further and faster and aiways moved on their bellies while propeliing themselves with lateral undulations. Tadpoles of Chiromantis rufescens used less flexure in wiggling G d moved more rapidiy by landing on their sides and "fhpping" with tail movements much like a fish out of water, and some larvae of&ntiahtylus spp. also move effectively in this manner (R. Aitig, personai communication). Leptopelis larvae were able to survive and wiggle toward water longer than Chiromantisin the i
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KARIN vS. HOFF, ANDREW BLAUSTEIN, ROY McDIARMID, RONALD ALTIG
same trial conditions. Both species showed some ability to mo&@ the rate of movement with changes in surface moisture and relative humidity, and ú.ptope1isshowed some ability to move directionally, perhaps through geotaxis. The sinuous wiggling locomotion of lcptopelis larvae was correlated with the longer, more muscular tail and seemed to work better under the conditions tested. Oldham (1977) suggested that the probability of reducing aquatic predation on the defenseless egg stage and having a relatively large and weliadvanced tadpole arrive in the pond constituted the survival value of terrestrial eggs. In these experiments, the tadpoles of Bufo muculatm used for comparison had no ability to move on land. Wager (1986) reported that tadpoles of a related species from South Africa, Leptopelis natalensis, afier hatch& and emerging, moved towaid water as a group. Another pattern of locomotion characteristic of larvae with long, low-finned tails, weii-developed eyes and hind limbs, cryptic coloration, and unusual mouthparts (see chap. 12) we cail "tail flipping." This type of movement is associated with tadpoles d e d "subaerial" by Wassersug and Heyer (1983) and "semiterrestrial" by Altig and Johnston (1989):In mbst other situations, we wouldgive priority to the earlier name, but for obvious reasons we use "semiterrestrial" here. These tadpoles use their tails to flip around on wet, exposed rocks in streams, in films and trickies of water flowing over rocks or from seepages, and on stems and leaves and between axils of plants. Wassersug and Heyer (1983) examined the tadpoles of Cychamphw and Thmopa (Leptodactylidae) and noted their similar morphologies (e.g., elongate and relatively finless tail, depressed body and branchial baskets, compressed and deep jaw sheaths). These tadpoles are obligate air breathers found on vertical rock surfaces where water flow is negligible. Some of these have a flattened abdomen (a possible precursor to a beliy sucker) presumably to increase surface area for cohesion and as an adjunct to lung ventilation. Drewes et ai. (1989) descnbed the tadpole ofArthroleptides martiensseni (Ranidae) and commented on the striking morphological and ecological convergence between their Arthroleptiúes tadpoles and those of Cychamphus (Heyer 1983a, b) and Thmopa (Cocroft and Heyer 1988).Arthleptiúes martiemeni tadpoles were coliected from vertical or steev faces of smooth rocks in the stream but outside the 1 main current; many tadpoles were in fissures. These authors noted the large eyes of these tadpoles and found that the hind legs of this species developed much more precociously than those of tad~olesof Bufi or Rana. When disturbed. tadpoles moved hkphazardly by tail flipping, sometimes foi a distance of 1-2 cm per flip. The obvious convereences on the semiterrestrial morphology in tadpoles from several families are notable. Tadpoles of Nannophys q k i s (Ranidae; Kirtisinghe 1958) also are morphologidy similar to those of Arthrohpdes, Cyclmamph, and Thmopa and occur in shallow sheets of water in seeps. The strikingly similar tadpoles of Indirana bedahwi were described by Annandale (1918) as skipping rapidly over damp rocks.
Fig. 9.6. Semiterresmal mdpole of PetmpcdttEsparkcri (Ranidae).Tadpoles were found climbing on slime-covered rock faces along a road cut through a forest in Cameroon, West Africa.
Blommers-Schlosser and Blornmers (1984) noted that tadpoles of the Malagasy frogs in the M.antzahq1wpulcher group can move from one axil of Pandanw to another by violent wiggling; they also have elongate, depressed bodies and low fins on a long tail. Lawson (1993) reviewed the natural history of the tadpoles of the Cameroon species ofPetropedetes (Ranidae). In general, they are elongate tadpoles with long tails, weli-developed hind legs that apparently develop early in the larval stages and small heads. Lawson (1993) noted that eggs are laid on the undersides of leaves on low shnibs and trees along rock and pebble banks of seasonal streams. On hatching, the tadpoles squirm along the branches for some time before dropping to the ground below. In his figure 19, Lawson (1993) showed tadpoles of i? cameronensis on stems and a leaf and a tadpole of i? parkeri with well-developed hind limbs and a long tail sitting on a leaf; Pparkevi tadpoles were found crawling on slimecovered, vertical rock faces covered by trickling water (fig. 9.6), and Petropedetes tadpoles were found at several localities in the Korup National Park actively moving on the forest floor hundreds of meters from the nearest water. Kunte (1998) observed ecologicaily similar tadpoles in India that were probably Indivana kithii. These tadpoles tried to escape the predatory strikes of the snake Ahaetulla nasuta by hopping into cracks and depressions in the surrounding rocks. Tadpoles of H o p l o p w r0pn-iand H. ulugu~nsis(Noble 1929) live in the damp crannies between leaves of wild bananas or within split bamboo stems and have a bilateral pair of fingerlike, fleshy projeaions on the ventrolateral margin of the body at the posterior end of the buccopharynx. These projections move upon contraction of the subhyoideus muscle (chap. 3), and Noble suggested they give an added "kick" to assist the tadpoles as they wiggle from one moist axil to another. It is interesting that the tail of a weliformed embryo is longer than the head and body and wraps across the ventral surface of the developing embryo; hind limb buds are clearly visible in these tadpoles before they hatch but external gills are not (Noble 1929). Recently hatched larvae of H. u l t g u e have weli-developed, inflated lungs that extend two-thirds the length of the body
BEHAVIOR
cavity; their size implies that pulmonary respiration is important for these tadpoles (Noble 1929). It is interesting to speculate about the origin and adaptive nature of patterns of taii-flippingJsemiterrestnal locomotion. Undoubtedly, the precursor of this behavior can be found in more typical tadpoles but little information is avaiiable. M. A. Smith (1916) noted that the carnivorous tadpoles of Occidozyda and Phlyno~iussuslie quietly for long periods, seldom move with their taiis, and push themselves about with their precocial hind legs. Perhaps other examples are in the literature but have not been evaiuated in this regard. Our understanding of the evolutionary interplay between the breeding ecology of most frogs and the feeding and locomotion of their tadpoles is elementary. A cursory review of the literature on more specialized patterns of breeding (Dueiiman and Tmeb 1986), especially on frogs that deposit eggs in relatively small and potentially ephemerai habitats such as phytotelmata, suggests fniitfd areas of investigation. The convergent evolution of similar morphology (e.g., body shape, taii length, oral stmctures), physiology, locomotion, and feeding in different lmeages in similar habitats is strikmg. What are the trade-offs and patterns of convergentes between feeding and locomotion in these difíèrent habitats in whch tadpoles find themselves? For example, what is the evolutionary hstory of the independent trends toward increasing tail length, dependency on pulmonary respiration and development of semiterrestriai/tailflipping locomotion, and changes toward macrophagy as exemplified by carnivory, cannibalism, and oophagy? Surely, more tadpole watching wiü provide insight and answers to some of these questions and bring other morphologicai and behavioral correlates to light; we encourage such investigative .efforts. There is considerable information on the stmcture and funaion of hatching glands (chap. 3), but few observations have been made across species to identi5 potential differences in the timing and actual hatching process and behavior of the embryo (e.g., Bradford and Seyrnour 1985; Goiiman and Goiiman 1993a; Kothbauer and Schenkel-Brunner 1981; Lutz 1944a; Noble 1926a; Yoshzaki and Yamasaki 1991). Thrashing about by embryos may enhance hatching of other embryos in a clutch of eggs with h g h water turgor. Physicai features like pH (e.g., Dunson and Connell 1982) and oxygen tension (e.g., Petranka et ai. 1983) also influence hatching; one of us (R. Aitig, personal observation) has seen several cases where the surface-film eggs of Hyla cinerea became encased in a mat of aigae in a particuiarly eutrophic pool. These embryos died &er reaching Gosner 25 because they could not escape the jelly membranes. Behavior of hatchiings is largely unknown, but specific activities that have not been studied must occur in those frogs that have larvai transport or some other form of larvai brooding. Hatchlings of some endotrophs (e.g., G. J. Ingram et ai. 1975, Assa; Brauer 1898, Sooglossus secheliensis) and exotrophs with larvai transport (e.g., De Pérez et ai. 1992a, dendrobatids; Inger and Voris 1988, Inger et ai. 1986b, Limnonectes microdtrca) must respond by negative
229
geotaxis, pheromones, or a combination of these and other cues to arrive at the proper place in or on the parent.
Dispersion and Social Behavior Habitat Selectwn Numerous physical (e.g., distance from shore, oxygen concentration, substrate qualities, water depth and flow rate, site duration, and temperature; discussed by O'Hara 1981) and biological (e.g., presence and distribution of vegetation, other tadpoles, other organisms, and the phenology of ali organisms) factors influence the spatial and temporal distribution of tadpoles among microhabitats. Tadpoles may select habitats because of attraction to or avoidance of conspecifics and predators. Temperature often influences the behavior and ecology of tadpoles (review by D u e h a n and Tmeb 1986; chaps. 8 and 10). Temperature influences tadpole aaivity patterns, growth and development, metabolic rate, and the timing of metamorphosis (Kohos 1961; Srnith-Gill and Berven 1979; Wilbur and Collins 1973). Rapid growth and development are especially important for species that live in ephemerai habitats, such as in deserts where pools dry up quickly or at high elevations where ponds may freeze (A. R. Blaustein 1988; Hokit and Blaustein 1995; O'Hara 1981; Skelly 1996). In nature, the gathering of tadpoles (e.g., Bufo, Hyh, Pseudamis, Rana, and Scaphwpus) in the warmest thermai gradients suggests selection of favorable temperatures for rapid growth (e.g., Ashby 1969; Beiswenger 1972; Bragg 1968; Brattstrom 1962,1963; C. C. Carpenter 1953; Muiially 1953; O'Hara 1981; Tevis 1966). This assumption is supported by experimental studies (e.g., Beiswenger 1972; Beiswenger and Test 1966; De Vlaming and Bury 1970; Herreid and Kinney 1967). Few experimental tests have demonstrated that tadpoles selectively respond to key features of the substrate. Aitig and Brodie (1972) showed that tadpoles of Ascaphus tmei preferred smooth rocks above 55 mm in diameter. J. A. Wiens (1970.1972) showed that Rana aurora and R. cascada tadGoles could be conditioned to prefer certain substrates, although the two species displayed opposite preferences in identical experimental regimes. Rana aurora tadpoles reared over featureless or square-patterned substrates showed no preference for striped or square-pattemed substrates, but larvae reared on striped substrates preferred striped-patterned habitats. The preference for striped substrates was established during the first 14-17 days in the striped habitat. T h s preference was retained &er isolation from the substrate and could be reestablished in both young and old tadpoles. Rana cmcadae tadpoles reared in featureless or striped-pattern environments showed no preference for either square-patterned or striped substrates, but tadpoles raised in a squarepatterned environment showed a significant preference for that regime. J. A. Wiens (1972) suggested that the different responses were because of Werences in the substrates of the haGitats in whch these tad~olesare found. Rana aurora m i cally breeds in shallow ponds prone to surnrner drying and ,L
230
KARIN vS. HOFF, ANDREW BLAUSTEIN, ROY McDIARMID, RONALD ALTIG
in areas where permanent ponds have overflowed (Storm 1960; J. A. Wiens 1970). Branches, and stems of emergent plants that are characteristic of these habitats cast a pattern of linear shadows on the bottom. The strioes that larval R. aurora res~ondedto mav resemble the linear substrates and shadows {ound in their natural habitat. Methods similar to those of J. A. Wiens (1970, 1972) were used to test habitat selection in Iú*.loulapukhra ( P u m 1976) and Bufo americanus, Rana clamitans, and R. sylvatzca (O'Hara 1974). Iú*.loula tadpoles reared in striped habitats preferred stripes, those reared in square-patternedhabitats preferred squares, and those reared in featureless habitats displayed no preferences. Punzo (1976) suggested that tadpoles imprint on the habitat in which they were reared and that they select this type of habitat in nature. In contrast to studies by Wiens and Punzo, the rearing regime had no influente on the habitat choices of B. americanus, R. clamitans, and R. sylvatica (O'Hara 1974). Results obtained for Rana cascadae tadpoles by J. A. Wiens (1972) and by O'Hara (1981) are contradictory. O'Hara (1981) tested the responses of tadpoles reared on a smooth tank bottom versus natural substrates (e.g., sand, gravel, and rock). Tadpoles of Bufo boreas, Pseudacris regila, and R. cascadae preferred fine-grained over coarse-grained substrates. Tadpoles from different populations and wildcaught tadpoleS versus those reared &e laboratory environment behaved similarly. Rana cascadae tadpoles were influenced by the rearing regime in the study by Wiens, whereas in O'Hara's exoeriments thev were not. One must be cautious about interpreting results of experiments concerning habitat selection when the environment is quite artificial. Comparing experiments that used different techniques is difficult; theseresdts may reveai real ecoiogical ~ e r e n c e s in nature (see O'Hara 1974, 1981, and J. A. Wiens 1970 for discussions). Tadpoles may use visual, tacule, and olfactory cues to dist i n p s h among substrate types in field and laboratory tests (O'Hara 1981). Waringer-Loschenkohl(1988)showed that the presence of vegetation, as weli as other species, caused a significant shift in the distribution of European tadpoles from the bottom of aquaria toward the water surface. Experimental results (Pfennig 1990a, b) suggested that tadpoles of Spea multiplicata select their habitat by using diet-based environmend cues; tadpoles reared on similar diets aggregated with one another; he also argued that larvae have increased growth and survival when they were restricted to their natal environment. 1.A. Haii et al. (1995) found that larvae of Spea intemzontana did not prefer only cues of their natal environment but were able to react preferentially to nove1 stimuh (larvae raised on different diets) in forming associations. Social Interactwns Many aggregations of larval anurans form as a result of social attraction toward conspecifics or because of abiotic parameters. Through field observations and experimentation in the laboratory and field, the various moda of tadpole aggrega-
tive behavior have been assessed and classified (e.g. Bragg 1965; Caldweli1989; Downie 1990a; Dueliman and Trueb 1986; Lescure 1968; Wassersug 1973). Analyses of the geometric struaure of tadpole aggregations (e.g., L. C. Katz et ai. 1981; Pote1 and Wassersug 1981; Wassersug et ai. 1981b), the sensory bases by which individuals maintain contact with conspecifics (e.g., A. R. Blaustein and O'Hara 1982a; Waldman 1985a; Wassersug et ai. 1981b) and the selective pressures that may have influenced aggregation formation (e.g., A. R. Blaustein 1988; Waldman and Adler 1979; Wassersug 1973) have been investigated and discussed. Studies of the roles of competition and predation in aquatic communities in which tadpole aggregations are a significant component have provided important insight into how aquatic communities are structured (e.g., Morin 1981; Travis 198C)b;Wdbur 1972,1984; Woodward 1982,1983; chap. 10). Several authors (e.g., Beiswenger 1975; Bragg 1965; Caldweli 1989; Wassersug 1973) categorized tadpole aggregations qualitatively; Bragg (1965) described tadpole aggregations as being asocial or social and suggested that asocial groups form through association with environmental features (e.g., food patches or temperature gradients) that are attractive to individuals. Social aggregations form because of the attraction of individuals to conspecifics. Because of the difficulty in distinguishing between social versus asocial factors, Wassersug (1973) suggested a broad, functional classification of two types: a simple, taxic aggregation in response to some physical feature (e.g., temperature, iight, current) was equivalent to the asocial aggregation of Bragg (1965), and a biosocial aggregation (= school) was equivalent to the social aggregate of Bragg (1965). Either type of aggregate may be polarized (tadpoles oriented in same direction) or nonpolarized. Tadpole schools are biosocial aggregates that display some synchronized movement patterns, but the degree of polarization within a school varies. Also, some tadpoles form slow-moving, polarized aggregations within which individuals may iie on the bottom of the body of water or be suspended motionless in midwater. Beiswenger (1975) also proposed a functional classification of tadpole aggregations focused on moving (streams and schools) and stationary (feeding and metamorphic) patterns. Because of the difiiculty in assessing whether aggregations observed in nature were simple or biosocial, M. S. Foster and McDiarmid (1982), O'Hara (1981), Wassersug (1973) and Wassersug and Hessler (1971) conducted a series of controlied laboratory experiments to test rigorously how and if tadpoles of various species were sociaiiy attracted to one another. These studies consisted of placing one tadpole of a particular species within each of four sections of a glass or plastic tray (M. S. Foster and McDiarmid 1982; Wassersug 1973; Wassersug and Hessler 1971) or an aquarium (O'Hara 1981). Each section was separated from the others by water-tight, transparent partitions so that tadpoles in each section had visual but not chemical contact with one another (see M. S. Foster and McDiarmid 1982 for results of chemical contact with the same design). Each section
BEHAVLOR
was marked into four equai quadrants (fig. 1 of Wassersug and Hessler 1971). If visually mediated sociai interactions among test individuais were iandom, then it was assurned that tadpoles would not associate in one particular quadrant over another. If tadpoles were positively attracted toward one another, they would be found most ofien in the quadrants where they could be as close to one another as possible. If tadpoles were avoiding one another, tadpoles would be found more often in the quadrant farthest from other individuais. The tadpoles of a; least 10 species have been tested with these methods with variable results (see M. S. Foster and McDiarmid 1982 for a criticai evaiuation of these methods). Tadpoles known to aggregate in nature generdy preferred to associate in the quadrant closest to conspecifics (e.g., O'Hara 1981, Wassersug 1973, Bufo borem; O'Hara 1981, Rana cascadue; Wassersug 1973, Rhinophynus hrsalis and Xenupus laevts; Wassersug and Hessler 1971, Xenupus laevts). Tests of species that probably only occasiondy form aggregations in nature, such as thé r ~ i d Rana s boilii, R catesbeiana, and R. pipiens, displayed a random distribution among the quadrants (Wassersug 1973). There was one discrepancy between the results obtained by O'Hara (1981) and Wassersug (1973). Wassersug (1973) found Pseudacri's regillu tadpoles exhibited no biomutuai attraction whereas O'Hara (1981) showed that they were mutuaüy attracted to one another. I?regilla tadpoles form relativelfloose, intermittent aggregations in nature and their aggregating tendencies seem to differ between populations (A. R. Blaustein 1988; O'Hara 1981). The different testing apparati used by Wassersug and O'Hara rnay have accentuated the apparently discrepant results. Of the ranids tested, only Rana cascad~ tad~oiesdis~íaveda dear-cut biosocial attraction toward co&pecifics.L~/nature,R. cascadue tadpoles are one of the most social of the ranids and form small, cohesive aggregations in ponds and lakes (A. R. Blaustein 1988; Hokit and Blaustein 1997; O'Hara 1981). Tadpoles of Spea do not display an attraction for conspecifics (Wassersug 1973) even though they form aggregations in nature (aiso see J. A. Haii et ai. 1995). As Wassersug (1973) pointed out, these tadpoles rnay require more than visuicues in order to form aggregations or, as exemplified by Pseudacri's regilla tadpoles, the tendency to form aggregation rnay vary among populations. Based upon laboratory experiments and field observations, Wassersug (1973) described two basic modes of tadpole group formation (= schooling): the Xenupus mode and the Bufo mode, with comments on a t h r d mode made up of schooling tadpoles that occur in ephemeral breeding sites. H e judged that tadpoles within different famiúes generally fit into one of these basic modes of schooling behavior. In theXenupus mode, schools consist of clusters of strongly polarized individuais in midwater. and individuals avoid contact with one another. The B U . mode is characterized by schools being polarized or not and hundreds to thousands of relativelv slow swimrninp individuals in freauent contact 1 that "appear as dense black mats in shallow water or near the V
23 1
bottom" (Wassersug 1973:285). The ephemeral group was characterized by highly motile, strong swimmers that occur in very active, closely packed schools; these tadpoles are often ornnivorous in terms of food particle size and quality. Severai species of pelobatid frogs (e.g., Scaphwpw and Spea), Rhinophlynus hrsalis, Pyxictphalus dpersus, and many Australian species fit this mode. Many schooling species remain to be categorized. Tadpoles of Rana hechcheri (Altig and Christensen 1981) move about in imrnense schools of severai cohorts; tadpoles in front are feediig and those behind are moving and coming to the surface to breathe. A large school can be heard by the crackling noise caused by so many tadpoles surfacing. In laboratory tests, there was evidence of sociai faciútation in feediig. Tadpoles of severai species of Leptodactylus aggregate in nonpolarized schools that extend from the bottom to the top of the water, and these tadpoles also are stimulated to follõw smaü waves made bv the'ir attendant mother. Likewise, the nonfeedmg tadpoíes of Nectophyne afra foliow vibrations caused by movements of the attendant maie (Scheel1970). Tadpoles ofAubriasubsigiluta form tight football-shaped clusters that appear to roli across the bottom (Schi0tz 1963). Tadpoles of Pyxicephalus adspersus promptly move through channels dug by the attendant maies from drying parts of the habitat to remaining water (Kok et ai. 1989). Tadpoles of P~xicephalusrnay school with those of SchZrmademza (R. Altig, personal observation; aiso see R. A. Griffiths and Denton 1993). Caldweii (1989) suggested that it rnay be difficult to place tadpole schooling behavior in one of Wassersug's modes because of considerable variation within a s~eciesand potentiaily different modes displayed by other siecies. Because similarities in the behaviors that result in groups rnay occur in species that are not closely related, Caidweii (1989) suggested that these behaviors should be designated by types rather than by taxonomic names. According to her scheme, Type I behavior is iüustrated by tadpoles that form loosely aggregated schools in shaüow areas or on the bottom of ponds but rarely in midwater. These aggregations rnay or rnay not be polarized, and movement of the group is amoeboid and slow (e.g., Bufo and possibly some Leptodactylus). Type I1 behavior (e.g.,Xenopus, some species of Phyllomedusa and some microhylids), is characterized by weii-organized schools in midwater. and individuais are not in contact with one another. Movement is slow in these strongly polarized schools. Type I11 behavior (e.g., Hylageogaphica, some ranids and rhacophorids) involves weii-organized, polarized schools in the shape of a sphere; and tadpoles are aiways in physicai contact with one another. These schools are found throughout the water column, near the edge or on the bottom. Individuais continuouslv movinp; " toward the center of the school creates a roiiing effect. Comparable data on the structurai organization and sensory bases of fish schooling behavior (e.g., Partridge 1982; Partridge and Pitcher 1980; review by Pitcher 1986 and E. Shaw 1978) are not available for anuran larvae. Anaiysis of the geometric structure and sensory bases of schooling (L. C. Katz et ai. 1981; Wassersug et ai. 1981b) suggested
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KARIN vS. H O F F , ANDREW BLAUSTEIN, ROY McDIARMID, RONALD ALTIG
that schooling behavior of Bufo woodhousii and Xenopus l m ? than individuals in the early detection and avoidance of tadpoles is similar to that of fish. In the absence of other predators (O'Hara 1981). Theoretical, observationd, and cues, both Bufo and Xenupus larvae exhibited two features experimental evidence suggest that as prey group-size inof fish schools -oriented paraliel to and showed preferential creases early predator deteaion and probability of escape inbearing to their nearest neighbors. In spite of these similari- creases (e.g., S. J. Arnold and Wassersug 1978; Hamilton ties, most tadpole schools do not exhibit the mobiiity dis- 1971; Kenward 1978; G. V. N. Powell1974; P d i a m 1973; played by fish schools. Compared to those of fish, rnost tad- Siegfried and Underhill 1975; R. J. Taylor 1976, 1979; pole schools are relatively stationary and individuals in Treisman 1975; Vine 1973). Tadpole groups rnay efficiently schools are usualiy at random distantes fi-om their nearest swamp potential competitors. O'Hara (1981) and Olson neighbors. A preferred distance to neighbors displayed by (1988) occasionaliy observed aggregations of western toad fish is rarely observed in tadpole schools (Wassersug et al. (Bufo boreas) tadpoles displacing s m d groups of Pacific tree1981b). The mobile schooling behavior of Hylageographh frog (Pseuducris r@Lla) tadpoles. Intraspecific competition is an exception to the generalization that tadpole schools are rnay be mediated by aggressive behavior between individual relatively stationary (Caldweíi 1989); the same is true for tadpoles; apparent aggressive "butting" has been observed schools of Rhznophynus donalis (Stuart 1961; R. W. McDi- in Bufo americanus tadpoles (Beiswenger 1975; D.C. Smith armid, personal observation). Tadpoles of certain species, 1990 and referentes therein; Waldman 1982a). Groups of tadpoles rnay thermoregulate more efficiently such as Phyllomedusa vaillanti, rnay be evenly spaced when schooiing in midwater (Branch 1983; J. P. Caldwell, per- than individuals. An aggregation of black tadpoles rnay sonal cornmunication). Bufo and XÊnupus tadpoles differ in efficiently absorb solar radiation that raises the temperature some aspects of their schooiing behavior. The bearing rela- of the surrounding water (Caldweíi 1989; Guilford 1988; tionship of one individual changed with iiiumination inXen- Wassersug 1973).O'Hara (1981) repeatedly found temperaopus but not in Bufo. Aithough Bufo tadpoles in schools seem ture differentials of 2-3°C inside and outside of B. boreas agto be generaliy weakly polarized (Breden et ai. 1982), they gregations; he ascribed these to solar heat absorption and polarize more extensively in the field than in the laboratory possibly metaboiic activity. Aiso, tadpoles rnay accrue inclusive fitness by associating with related individuals. The con(Wassersug et ai. 1981b) L i e some fishes (e.g., Radakov 1973), tadpoles in cept of inclusive fitness (Hamilton 1964a, b, c) predicts, ali schools rnay orient toward individuals of similar sizes (e.g., else being equal, that individuals wiii cooperate with or aid Alford and Crump 1982; Branch 1983; Breden et al. 1982). related individuals over unrelated individuals. Aithough The magnitude of and the factors involved in size sorting not required, Hamilton suggested that an ability to discrimivaries arnong species. Phyllomedusa vaillanti larvae in Brazil nate between kin and nonkin (= km recognition) couid fa(Branch 1983) formed temporary schools of rnixed size cilitate this so-calied kin selection (Maynard Smith 1964) classes that eventualiy segregated into schools cornposed of process. different size classes. Unequal locomotor capabilities of size classes, social attraction of like-sized individuals, and prefer- &n Rewpitwn and &n Association ences for specific water depths rnay contribute to sorting by Tadpoles of many species are socialiy attracted toward and size in these schools (Branch 1983).Ranasphenocephala tad- form schools with conspecifics in nature, and tadpoles in poles of different size classes rnay iive in different habitats, schools rnay orient toward individuals of similar sizes. Aiso, and both interferente and exploitative competition rnay based on numerous laboratory. experiments that controlled contribute to intraspecific size sorting (Alford and Crump for body size, tadpoles of several species seemingly prefer to 1982). S m d R. sphenocephala tadpoles rnay be displaced by associate with relatives over unrelated individuals regardlarge ones. Aithough Bufo woodhousii larvae seem to associate less of body size (A. R. Blaustein 1988; A. R. Blaustein with individuals of the same size, the magnitude of size sort- et al. 1987a; A. R. Blaustein and Waldman 1992; Waldman ing is smaü (Breden et al. 1982). Both large and smaü indi- 1991; also see Cornell et al. 1989; Dawson 1982; O'Hara and Blaustein 1985; Waldman 1982a, 1986a). It seems vidual~rnay be found near one another. Group living has numerous benefits, including the possi- iikely, therefore, that tadpole schools of certain species are bhty of avoiding, detecting, and deterring predators, en- composed primarily of related individuals. Investigators have used variations of two basic rnethods, hancing foraging efficiency, accming benefits in competitive interactions, and increasing the efficiency of thermoreg- laboratory choice tests or laboratory open-field tests, to deulation (Aiexander 1974; Bertram 1978; Hamilton 1971; termine Ghether or not a tad~oiec k discriminate between o i cof e tadpoles of the Pitcher 1986; Pulliam and Caraco 1984; G. C. Williams kin and nonkin. ~ ~ ~ r e ~ a t i o n c htests 1964). Tadpoles that form aggregations rnay gain many of western toad (Bufo boreas), Pacific treefrog (PseudacrW rethese benefits (A. R. Blaustein 1988; Brodie and For- gilla), and the red-legged (R. aurma), Cascades (Rana casmanowicz 1987; O'Hara 1981; Waldman 1982a; Wassersug cadae), and spotted (R.prehosa) fi-ogs have been conducted 1973). For example, stirring of the substrate by groups of in the laboratory (review by A. R. Blaustein 1988; A. R. toad tadpoles results in suspending food that larvae can filter Blaustein and Waldman 1992; A. R. Blaustein and W d s from the water (e.g., Beiswenger 1972, 1975; Wdbur 1995) after test animals were reared in one of four regimes 197%). Tadpoles that form groups couid be more efficient (summarized in A. R. Blaustein and O'Hara 1986a): (1) km
BEHAVIOR
233
oniy, (2) kin and nonkin (mixed-rearing regime), (3) in colors, equai numbers of the two groups were placed in a isolation from an early embryonic stage, and (4) nonlun laboratory pool simuitaneously, and the distantes from each oniy. Association preferences were measured by allowing tadpole to its nearest s i b h g and nearest nonsibling were retest individuais to associate near members of two stimuius corded. Waidman (1985a, 1986a) also used choice tests in a groups within a rectangular tank (A. R. Blaustein and Y-maze to assess iun recognition in B. americanus tadpoles. O'Hara 1986a). Stimuius compartments that were separated In some of these tests, tadpoles were simultaneously prefiom the main portion of the tank by a screen were placed sented with water flowing from m o containers, each holdon opposite ends of the tank, and various numbers of tad- ing members of Merent s i b h g groups. In other tests, tadpoles that varied in genetic affinities were placed in each poles were simuitaneously presented with water flowing compartment. In most tests, the time out of 20 min that from a container holding siblings and one holding dechloritadkles spent in the h& nearest one stimuius group was nated tap water. Dawson (1982) used both choice tests and compared with the time that wouid be expected if associa- open-field tests to investigate lun recognition in B. ameritions were random. In other experiments, the time that tad- canus tadpoles. Like in experiments of Corneil et ai. (1989), ~ o l e sDent s in the thrd of the tank closest to one stimuius the test apparatus used by Dawson was much smaller than group, the third closest to the other stimuius group, or the the one used by A. R. Blaustein and O'Hara. The methods time spent in the middie third of the tank was compared and rearing regimes used by Dawson (1982) differed somenlth a random expectation. Resuits obtained by A. R. what fiom those used by A. R. Blaustein and O'Hara and Blaustein and O'Hara are difficuit to compare directly with Waldman, so again direct comparisons are difficult. similar tests of iun recognition done by Cornell et ai. (1989, Significant Merences in how tadpoles discriminated beR. ylvaticu) and Fishwild et ai. (1990, Pseudmris mcifer, R tween kin and nonlun exist among species (table 9.1), and pipns, and R. ylvatica) because rearing and testing proto- the different methods used by the various investigators cancols were different. not fuiiy explain the observed differences. DifTerences in disWaldman (1981,1984,1985b) and Waidman and Adier crimination between species were apparent even when iden(1979) conducted open-field laboratory experiments to test ticai rearing and testing regimes were used. For example, the kin recognition in B. americanus and R. sylvatica tadpoles three ranids tested and reared identically by A. R. Blaustein (alsosee Rautio et ai. 1991).After being reared under a vari- and his coiieagues displayed signhcant differences in how ety of regimes, members of two sibships were dyed different they discrirninated between iun and nonkin (table 9.1). Table 9.1 A summary of the results of kin recognition experiments involving various anuran tadpoles. ENC = experiment not conducted.
Species Bufonidae Bu@ americanus B. bweas Hylidae Pseuhris mtcijèr l?r@ih Ranidae Rana aurora R. cuscadae R. pipieru
Discriminates Siblings Frorn Nonsiblings
Identifies Half-Siblings
Yess Yes
Yesh Yesc
Dawson 1982; Waldman 1981 A. R. Blaustein et al. 1990; O'Hara and Blaustein 1982
No No
ENC ENC
Fishwiíd et al. 1990 O'Hara and Blaustein 1988
Early stages oniy Yesa
ENC Yesd
No
ENC
No Yes
ENC Yes'
A. R. Blaustein and O'Hara 1986b A. R. Blaustein and O'Hara 1981, 1982a Fishwiíd et al. 1990; O'Hara and Blaustein 1981 O'Hara and Blaustein 1988 Corneii et al. 1989; Fishwild et al. 1990; Waldman 1984
aCorroboratedin field experiments (O'Hara and Blaustein 1985; Waldman 1982a). bPreferencefor fuii siblings over paternal half-siblings; maternal half-siblings not distinguished from f di sibiings (oniy half-sibling categories tested). 0.05.
chemicals from injured conspecifics by increasing their over- iads of Aeshna umbrosa. Other chemical cues may originate all activity level and avoiding areas containing the substance. in predators. Petranka et al. (1987) demonstrated that Hyla Bufo boreas tadpoles captured by the water bug Lethocems ch~soscelistadpoles exposed to water conditioned by the fish americanus release chemicals that act as alarm substances Leponzis cyanellus spent more time in refuges than tadpoles in (Hews 1988). Other B. boreas tadpoles increased activity unconltioned water. Petranka and Hayes (1998) showed rates and avoided areas where tadpoles had been injured. that larval Buj%americanus and Rana sylvatica responded to Bufo tadpoles l d not respond to feeding by L. americanus water condtioned by the predatory odonate Anax junius by on tadpoles of other species. In another experiment, Hews reducing activity levels and moving away from the source (1988) showed that thls avoidance behavior was effective at of the odor. Larval B. americanus responded identically to decreasing the vulnerability of B. boreas to predation by na- conspecific tissue extracts, whde R. sylvatica larvae ignored
264
ROSS A. ALFORD
cies and B. americanus were unpalatable. The only species that regularly occur in permanent ponds and are palatable were A. glyllus and H. chlysoscelis. None of the temporarypond species or the unpalatable species spent significantly more time in refuges when exposed to water conditioned by fish. Tadpoles ofA.gryllusspent 86% of their time in refuges when fish were absent and 91% when fish-conditioned water was present, but the increase was not statistically significant. Larval H. chlysoscelis significantly increased time spent in refuges from 49% when water was not fish-conditioned to 82% when fish chemicals were present. Kats et al. (1988) suggested that the patterns were consistent with evolution of defenses against fish predation by species regularly exposed to it in nature. They also suggested that smd-scale geographic comparisons between popuiations exposed to differing predators might provide interesting information on the evolution of defenses in tadooles. I demonstrated that genetic variation for factors affecting vulnerability to predation exists in Hyla chlysoscelis (Alford 1986b). I reared 4 sibships of tadpoles, the offspring of a factorial cross of 2 males with 2 females. for 23 davs. I then exposed groups of 9 tadpoles to predation by male and female broken-lined newts (Notophthalmusv. dorsalis) in 24 x 30 x 12 cm plastic trays. Male and female parents had significant effects on tadpole growth at day 23. Male parent, and the three-way interaction of male parent, female parent, and newt sex had significant effects on the numbers of tadpoles remaining in the trays after 30, 60, and 120 min of exposure to predation. The least vulnerable families were not those with the largest bodies; this suggested that some geneticdv determined factor other than size had affected medation ;ate. This couid have been a difference in behkior or in levels of distastefd secretions. Semlitsch and Gibbons (1988) induced bodv size variation in larval H. chmsoscelis by rearing five sibships at three densities. When these were exposed to predation by bluegill sunfish (Lepomis mamochias), both tadpole body size and sibship controlied vulnerability to predation. In contrast, Semiitsch (1990) found no effects of sibship on the vulnerability of H. chlysoscelis tadpoles to predation by larval Tramea lacerta. D. C. Smith and Van Buskirk (1995) demonstrated that competition and predation interacted with the phenotypes of larval Pseudmi mtcifer and l? trileriata in predictable ways. Both species showed some alterations to their phenotyie when &sed in the presence of predators. l?crucifer, which normdy occurs with predators, responded less than l? mieriata, which does not. McColiuni and Leimberger (1997) and McColium and Van Buskirk (1996) showed that larval Hyla chlysoscelts and H. vmicolor raised in the presence of predators developed different morphology and color patterns than those raised alone. The changes were such that predation rates wouid be likely to decrease. Van Buskirk et al. (1997) examined the selective pressures exerted by predatory dragonfly (Anm)naiads on larval Pseudacris seriata and phenotypic responses by tadpoles to that pressure. They found that predation favored larvae with shdow, narrow bodies, high tail fins, and a wide tad muscle. Tadpoles exposed to Anax during development acquired higher tail ---
~
i
fins and wider tail muscles despite not showing greater activity, which suggests that this response may reflect morphological plasticity triggered by exposure to predator cues. Warkentin (1995) demonstrated that late-embryonic &alychnis callidryas respond to snake attack by hatching early, dropping into water, and avoiding the predator. The evolution of tadpole defenses against predation is an area that deserves greater attention in future work. The influente of predation on species interactions among tadpoles wdi be considered later in this chapter.
Composition and Ecology of Species Assemblages Conzpositwn and Ecology Species composition and habitat use in tadpole assemblages can be looked at in two ways. One approach compares ponds by examining which species co-occur and which do not and the factors that explain patterns of species co-occurrence. The resuits of this approach are often difficult to interpret in terms of tadpole ecology; the spatial distribution of tadpoles among ponds and their temporal patterns of occurrence resuit from the spatial and temporal distribution of reproductive effort by adult frogs, and aduits may respond to many factors in addition to the ecological requirements of their larvae. For exarnple, spawning site use may be constrained by aduit predation risk, predation or other mortaiity risk to eggs, or the quaiity of surrounding habitat for postrnetamorphic juveniles. Any of these factors, or many others, may cause tadpoles to occur in habitats that are not necessarily "optimal" for their growth and development but reflect compromises between the ecological requirements of tadpoles and other stages in the life history. Bradfield (1995) undertook a series of experiments and observations to examine this hypothesis with larvae of two species of rainforest tree frogs. Larval Litmiagenimaculata naturdy occur only in stream pools, and larval L. xanthomera occur in pools on the forest floor. Using transplant experiments, Bradíield showed that both species grew faster and survived at higher rates in forest pools than in stream pools. This suggests that L.genzmaculata are constrained to occur in streams by the requirements of other life history stages or by phylogenetic history. The second approach to the study of tadpole assemblages is to examine and attempt to explain the spatial and temporal distribution of tadpoles within ponds. This corresponds to the usual notion of a community study in which ecological relations among two or more co-occurring species are examined. Both approaches depend to some extent on examining patterns of reproductive habitat use by aduit frogs. Tadpoles have little control over the general habitat type (permanent or temporary, still or running water) they occupy. This is determined by the choice of spawning sites by aduits, which determines the range of species with which tadpoles may potentidy interact. The timing of frog reproduction determines the temporal distribution of tadpoles w i h sites. This affects the interactions each cohort of tadpoles experientes with other cohorts of the same species,
ECOLOGY
with other species of anurans, and with other vertebrates and invertebrates. The most diverse tadpole faunas occur in wet tropical regions. Detaded studies of spawning habitat use in the tropics include that of Cmmp (1974), who examined the spatiai and temporal use of reproductive habitats by 53 species of aquatic-breedmg anurans in a relatively aseasonai area at Santa Cecilia, Ecuador. She studied 8 breeding sites used by 26 species. The maximurn number of species breeding at any site was 16 and most sites were used by fewer species. Six of the 8 sites she studied were used by 7-13 species. The 2 most similar sites shared 56% of their species. Duellman (1978) further anaiyzed the tadpole communities at Santa Cecilia and found that no more than 10 species occurred at any site simultaneouslv. H e exarnined microhabitat use and iden&ed three broad habitat types: vegetation-choked areas, pelagic areas, and pond bottoms. A maximum of 7 species occurred in any microhabitat. Aichinger (1987) examined temporal and spatial use of seven reproductive sites by frogs in the seasonai wet tropics of Peru. A total of 34 anurans bred at his aquatic sites during 1 year of monitoring. Five of his sites were temporary and dried for long periods during the winter months. Twenty or more species of males caiied at four of the sites, but the maximurn nurnber observed at any time was 12 at a permanent pond site and eight at a temporary puddle site. Most species were reproductively active m a d y or exclusively in the wet season. No species reproduced at aii seven sites. Magnusson and Hero (1991) examined the distribution of tadpoles of 18 species arnong water bodies in a rain forest area in Amazonian Brazil; they found that site use appeared to be dictated by predation pressure exerted by anuran egg predators. Gascon (1991b) examined the phenology and reproductive habitat use of 25 species of frogs at 53 aquatic sites in rain forest in Brazhan Amazonia. He found considerable variation in the degree of reproductive seasonality shown by species and that activity by more seasonal species tended to be strongly aílected by rainfaii. H e used discriminant function anaiysis to determine the environmental factors that appeared to be responsible for determining the spatiai distribution of the 11most common tadpoles. A variety of factors were implicated, including the size and depth of water bodies, vegetation cover, and dissolved oxygen. Gascon did not find evidence for discrete structured assemblatzes " of co-occurring species; he concluded that each species responds individuaiiy to the environment in selecting sites for reproduction and subsequent larvai development. Gascon (1991a) examined the detailed responses of Leptoh$us knudreni to seasonal and annuai variation in rainfaii. Moreira and Lima (1991) aiso found that rainfaii was an important factor controlling reproduction and recruitment in f6ur species of Amazonian leaf-litter frogs, and Donnelly and Guyer (1994) reached a similar conclusion for an eight-species assemblage of hylids in Costa Rica. In the seasonaiiy dry tropics, Heyer (1973b) studied the tadpole communities of a series of ponds in Thaiiand. Ten species caiied at these sites and larvae of eight species were found. Six species started caiiing near the onset of the wet
265
season. wMe two s~eciesdelaved for 1-2 months after the onset of heavy rains. Species composition of the larval assemblages in his pools ranged from three to eight and was not correlated in any obvious way with diierences among the pools. He concluded that the species composition of the larvai assemblage at most ponds was largely caused by chance. In a similar study, Heyer et ai. (1975) studied larvai species assemblages in Costa Rican tropical wet forest and concluded that the tirning of oviposition and site selection by many species appeared to rninimize larval exposure to predation. Severai students and I are currently studying the use of reproductive habitats by frogs in seasonaiiy dry eucaiypt woodland in the Australian tropics near Townsvdle, Queensland. We have observed that adult frog density near ponds sometimes decreases temporarily after the first light wetseason rains, probably because frogs disperse to forage. Adult density increases dramaticaiiy, and most species begin &n after the first heaw rains of the wet season. A few species are attracted to very temporary habitats, such as flooded paddocks, creek overflows, and roadside ditches. These species also reproduce at less ephemerai sites such as dams and permanent water holes. For aii but the most ephemerai habitats, the species composition of larval assemblages early in the wet season does not appear to foiiow a strong pattern. The most reproductively catholic species is the introduced Bufo marinus, which reproduces at temporary or permanent water in any month of the year when there is rainfaii. Larvai B. marinus are distasteful to most fishes and to some dragonfly naiads (notably Orthetrum caledonuum, the most abundant species in many habitats) and larvai dytiscid beetles. This low vulnerability to predators may. minimize selection for s~ecializationb; site-or season. Reproductive tirning and site choice have also been studied in detail in temperate anurans. Detailed analyses of reproductive timing and sites are avadable for many temperate species but fewer entire species assemblages. Some of these are at least as diverse as the seasonai tropical communities; H . M. Wilbur (personai communication) observed 18 species of anurans calling at a single pond in the Sandhillsregion of North Carolina. Most of these species breed in the two months after the first heavy rains in the spring. Utsunomiya et ai. (1983) examined the timing and spatial distribution of reproduction by five species of Rana in a wooded mountain stream in Okinawa, Japan. They observed a greater than normal degree of pattern; none of the species overlapped in reproductive habitat use. Four used mutuaiiy exclusive habitats. The fifih overlapped with one of the first four in habitat but differed in season. Strijbosch (1979) documented reproductive habitat selection by six frogs in fen ~ o o l sin The Netherlands. H e found that ranids were the Lost selective species and bufonids the least selective. Most species avoided very oligotrophic or acidic sites. Thuty-three ~ o n d in s desert habitats in New Mexico (Woodward 1983) had six anuran species present. Four species (one Bufo, three Scaphwpus) occurred primarily in temporary ponds, while two Rana used only permanent ponds. H e suggested that this dichotomy was caused prirnarily by differing vulnerabiliV
ROSS A. ALFORD
266
Table 10.4 Records of frogs calling in a seasonal tropical eucalypt w o d a n d near Townsviile, Queensland, Australia. Perm Temp = temporary water.
=
permanent water,
--
T i g in Wet Season Mxd-
Early Taon
Bufo marinus cn1 ' zia desertzcola GYCI~RIUZ brkpes mmhoUandtm Limnudyastes omatzrs t~sm~niensis Litm aibo~uttata biufior rarmlea fdfrw: griuhta
Post-
Temp
Perm
Temp
Perm
Temp
Perm
Temp
Perm
X
X
X
X
X
X
X
X
X
X
X
X
X
X
X X X X
X X X X X
inem aaszrta rothi rubella Upemha lithmda mimula
Late
X X X X X
X X
X X X X X X X X X X
X X X X X X X X X X
X X X X X X X X X X
X X X X
X X
ties of larvae to predation; the temporary-pond species were more vulnerable to permanent-pond predators than were the avo Xana species. Sernlitsch et al. (1993) examined the facthe reproductive phenology of salamanders tors in South Carolina. Their study is remarkable for the large number of marked individuals used and the availability of data collected over an extended ~eriod. More detailed studies of the cues governing reproductive habitat selection have been performed for many indvidual species. Of 75 rock pools on the west coast of Sweden (Andrin and Nilson 1985), Bufo wtlamitu reproduced in 31 of them. The rate of use by toads was positively correlated with flatness of shorehe, height above sea level, and distance from the sea. Use by toads was negatively correlated with maximum water denth and nool size. The correlation with shoreline flatness may primarily reflect adult toad preferences; flatter shorehes make better calling sites and simplify entrv and exit from the water. The other correlations nrobably primarily reflect larval habitat requirements; increasing &stance from and elevation above sea level reduce water salinity, whlle snlall, shallow pools reach greater temperatures which allow faster growth and development. They suggested that choice of pool size was a compromise between avoidance of drying and attainment of maximum growth and develo~mentrates. Some species appear to be capable of evaluating the state of the aquatic community in small pools and adjusting their oviposition behavior accordingly. Adult HyIa ch?ysoscelk in North Carolina (Resetarits and Wilbur 1989: see 13etranka et al. 1994) discriminated among experimental pools for
calling and oviposition based on the presence of aquatic predators and conlpetitors, including H; chysosceEis belonging to earlier cohorts. The experinlent by Resetarits and Wilbur (1989) was criticized by Ritke and Mumme (1993), who suggested (among other things) that their experimental ponds were too small and close together, and that salamanders in one of their predator treatments may have consumed large numbers of eggs before they cotlld be counted. Even so, R. W. McDiarmid (personal communication) observed a similar pattern of oviposition by Smiliscaphaeota on the Osa Peninsula, Costa Rica, and Hylapseuhpunza also appear to be able to choose oviposition sites based on the condition of the habitat. Crump (1991) showed rhat they are capable of discriminating based on water depth and the presence of potential egg predators. Frogs may select reproductive habitats based on the presence or absence of other frog species. Gascon (l992b) showed that adult Pipa arrabali greatly decrease the survival of eggs and larvae of OsteocephaEw taurinus; he suggested that the species may coexist because 0,taurinus choose to spawn in sites in whichl?arrabati are absent. Pearman and Wilbur (1990) used computer simulations to show that increased patchiness of oviposition may increase population stability. Anurans are not always successful in choosing breeding habitats; Tevis (1966) documented repeated reproductivefailures, most caused by drying of aquatic habitats, in a population of Bu@pu72~tatus,and Laurila and Aho (1997) showed that Ram temporuria d ~ d not avoid depositing eggs in rock pools containing predatory fish. Most of the studies cited so far concentrated on choices of calling and spawning sites by adult frogs. Characteriistics
ECOLOGY
of the chosen sites and spawning phenology affect the ecology of tadpoles by defining whch species of competitors and predators are likely to be present and whether the habitat rnay dry before the end of the larval period. Species that spawn very early in the history of a temporary pool rnay gain an advantage for their larvae from the flush of primary productivity that arises from the high levels of dochthonous nutrients available early in the hstory of such pools. Their larvae rnay also gain size refuges from gape-limitedpredators and gain a size-mediated advantage in competition with other herbivores. Larvae of early spawners in permanent water bodies rnay gain simdar advantages against the larvae of fish and insects (e.g., Majecki and Majecka 1996) that use these sites. Several disadvantages are balanced against the advantages; spawning before temporary pools have completely filied rnay increase the risk of desiccation for tadpoles, and spawning early in the summer season in permanent water rnay lead to slow growth and development caused by low water temperatures. Such slow growth can increase the period of exposure to size-limited predators and decrease sizemediated competitive ability. With such complex possibilities, it is not surprising that frog reproduction follows a variety of phenological patterns. Blair (1961) summarized the reproductive phenology over a four-year period of seven species of anurans that bred at several sites near Austin, Texas. One species bred p r i m d y in winter, four in summer, and two in spring and autumn. Six species cded for more than 1month. The c a h g activity and initiation of first calling of all species was in response to heavy rains. After initial calling, some species continued to call any time that it rained or even with no rain, whiie others lirnited calling activity to periods of heavy rainfaií. The sequence of c&ng and spawning by the species varied considerably among years. Temporal separation of caiiing and spawning activity of adult frogs inhabiting a temporary pond in Mexico was documented by J. R. Dixon and Heyer (1968); they suggested that this phenology enforces temporal habitat segregation and resource-use differences in the tadpole assemblage. Seasonal occurrence of tadpoles and salamander larvae was documented at a site in Maryland over a 2-year period by Heyer (1976a). He found that the phenology and density of some species was very similar between years, while considerable pattern changes of other species in the same pond produced large changes in the total species assemblage. The same pattern continued over a further two years of monitoring at the same site (Heyer 1979). Brook (1980) identified three seasonal patterns of c&ng and spawning by frogs in Victoria, Australia: frogs with 4-6 week reproductive seasons occurring at roughly the same time each year regardless of precipitation hstory, frogs with short reproductive seasons (2-3 days) apparently initiated by heavy rainfaií, and frogs with extended reproductive seasons. The frogs breeding for 4-6 weeks began c a h g at different times depending on the genus; Litoria, Philoria, and Uperoleia initiated caiiing in early sumrner, while Pseudophryne started in late summer. Eggs or amplectant pairs occurred in more than 1month in 20 of 33 species. Diaz-Paniagua (1986, 1988) studied the reproductive
267
phenology of seven anuran species at Donaiía, Spain, over four years. The heaviest rains usuaiíy fell during the autumn and early winter months. Pelobates and Pelodpes had short re~roduc&eseasons associated with heaw kinter rains. Four other species bred over longer periods during early spring, and Ranaperezi had an extended reproductive season during summer. Temporal overlap in pond occupancy of larvae varied considerably among years; in 1978-1979, the heaviest rains arrived in mid-winter, and most species reproduced almost simultaneously. Temporal overlap varied less among the other three years of the study. Timed tape recorders were used (W. Martin 1991) to examine details of the caiíing phenology of frogs in seasonaiíy dry eucalypt woodland in the Australian tropics near Townsd e , Queensland (table 10.4; see Pearman 1995 and C . L. Rowe and Dunson 1995). He used daily c a h g data to construa simdarity matrices for c&ng patterns among species within sites. Classification analvses of these matrices revealed only two clearly delineated phenologies; Cyclorana brmpes and C. nuvaehollandiae caií early in the wet season in response to heavy rainfaií, whde aií other species have extended c a h g seasons with peaks in activity often corresponding to heavy rains. Although the classification analysis did not reveal clear phenological groups within the second category, Mantel tests comparing the similarity matrices among sites showed high degrees of correlation, implying that interspeciíic similarities in caiiing pattern remained constant between sites. This suggests that the large group of species with extended calling seasons contains a complex set of subgroups with slightly different phenologies. The longest series of data available on reproductive phenology for a single species (Terhivuo 1988) involves locations and dates of spawning by Rana temporaria in Finland between 1846 and 1986, with an extremely detailed supplemental data set for 1983. Terhivuo found that the date of the onset of spawning correlates well with temperature at any site. Populauons in southwestern Finland (60°N) spawn earliest, and spawning proceeds north and east as temperatures increase. The northernrnost populations (70°N) spawn an average of 35 days later than the southernmost ones. Unfortunately, data include only the onset of spawning, not its duration. Semlitsch et al. (1996), in their analysis of 16 years of detded data from a natural pond, showed that late spawners rnay sometimes gain a strong advantage: Scaphiopus holbrookii and Gas~r~bhrvne carolinensis were most successfd I when they spawned afier the pond had filied and dried earlier in the season, leading to low densities and diversities of competitors and predators. Larval anuran species assemblages are frequently complex but often less complex than adult species assemblages in the same geographical region. D u e h a n (1978) reports 10 species of tadpoles found in a single habitat simultaneously in an aseasonal tropical region with at least 53 species of aquatic-breedmg anurans, and Hero (1991) found a s d a r number in Brazil. In Madagascar, Blommers-Schlosser and Blommers (1984) found 15 species in one brook, and R. Altig (personal communication) collected 1 3 species within an area of about 2 m2 in a stream in Madagascar. Nearly as iI
268
ROSS A. ALFORD
many species have been found simuitaneously in seasonal tropical and temperate habitats with much lower aduit anuran species richness. This apparent low limit on the nurnber of simuitaneously occurring species may be caused in part by competition. Temporary pools are relatively unpredictable in space and time and contain a relatively unpredictable set of competitors and predators. This may limit the degree of specialization in resource use attainable by tadpoles. Because most tadpoles are relatively unspeciahzed filter-feeders, most species in a pond may be potential competitors. Differentiation of site selection and reproductive phenology by aduit frogs may serve to decrease the levels of competition experienced by larvae to tolerable levels.
Density and Resouvce Use Relatively few studies describe or explain the composition of tadpole species assemblages in the field. Although R. M. Savage (1952) did not set out to produce a community study, the detailed studies of the autecology of two species in the same ponds can be interpreted as one. Heyer (1973b, 1974) examined species distributions among and within ponds at a seasonai tropical location in Thaiiand, examined gut contents and relative gut lengths (Heyer 1973b), and calcuiated niche breadths and overlaps (Heyer 1974). His quantitative microhabitat use and niche measurements are based entirely on species occurrence in sweep net samples taken as an indicator of rnicrohabitat usage. H e found a broad range of overlap vaiues, as might be expected from a community containing 8 species and thus 28 possible species pairs. He examined the food particle sizes used by species pairs showing the greatest spatiai overlap and found little indication that food might be partitioned based on particle size. He suggested that differences in feeding mode overlooked by his relatively coarse-grained sampling techruque, for example surface-íiim versus midwater versus bottom feeding, might separate some of the more overlapping species (see Bowen 1980). Heyer (1973b) also reported a series of qualitative observations on microhabitats that include the observation that different cohorts of some species may occupy ddferent microhabitats. Heyer (1976a) studied habitat use and partitioning by tadpoles at sites in Maryland and on Barro Colorado Island, Panama. He defined habitat partitioning as including use of breeding ponds by adult frogs, microhabitat use by tadpoles within ponds, and temporal occurrence within ponds. As discussed earlier, I would suggest that habitat partitioning of the first type is better viewed as a consequence of aduit breeding biology rather than as a component of tadpole ecology. Heyer examined rnicrohabitat use at his Maryland site by dividing the available habitat into surface film, rnidwater, and bottom. Heyer sampled tadpoles of six species during 1974 and 1975. AU species for which sample sues were reasonably large showed evidence for microhabitat preference. The microhabitat of Pseudmk cmcifer larvae changed as they grew; larger larvae occurred relatively more ofien in deeper water. Indices of microhabitat overlap between species generally changed markedly between years. Oniy three species pairs maintained consistent overlaps in
both years. Heyer suggested that overlap values for most species pairs indicated that competition was unlikely. He also noted that most species experienced very different environments in the two years. The study on Barro Colorado Island (Heyer 1976a) cbncentrated o i examining species occurrences in a series of smaller streambed pools. Most pools contained only one species of tadpole. This might be caused by temporal or spatial partitioning of reproductive habitat by aduits or by a variety of other factors including interspecific egg predation or its avoidance. Heyer (1979) summarized the results of two additional years of monitoring tadvole habitats at the Marvland site. H e found considerable between-years variation in habitat use, popuiation sue, and recruitment. H e suggested that this variation resuited from complex interactions among causative factors including adult reproductive pattern, food resources, intra- and interspecific competition, physical-ciimatic factors, and predation. Turnipseed and Altig (1975) looked simultaneously at the density and age structure of Acrisgryllus, Hyla avivoca, and H. cinerea in a 4,000 mZfarm pond in Mississippi. They took weekly samples over 1 7 weeks starting on 14 A p d . Two samples were taken along each of four sections of the pond bank with a quadrat sampler placed at the waterline. Captured tadpoles were counted, staged, and weighed. Their collection methods allowed a more quantitative examination of spatial and temporal variation habitat use than previous studies. They found thatA.gryllus made up 95.7% of the tadpoles in the area sampled, and the spatial distribution of Acris tadpoles showed a consistent bias away from one area of the pond. The density varied through time, indicating some combination of changes in their propensity to remain near the shore and changes in total population size. The stage composition of the Acris population changed as cohorts developed and new cohorts were added by reproduction. The populations of both Hyiu species were apparently more evenly distributed spatially but showed temporal patterns similar to Acris, which suggest that they were responding to the same environmental stimuii. In 1980 and 1981. I used a circular auadrat samvler to examine the size structure and spatial distribution of populations of tadpoles in a pond in northern Florida. In March 1980, oniy larval Rana sphenucephala were present, but they were divided into three sue classes that were distributed differently in the pond (Alford and Crump 1982). An experiment in an aauarium showed that habitat use difíerences I among the size classes persisted in a simplified environment. In 1981, I sampled the pond from just after h a t c h g of the first species of frogs that used it until it dried (Alford 1986a). Larvai Pseuducris m a t a and R.sphenucephaiu were present throughout the sampling period. B u . americanus and Pseuducris ocularis appeared after sampling began. AU species persisted until the pond dried, and B. americanus, PseudaEms ocularis. and l?&ata vroduced metamorvhs. I selected sampling lócations haph&ardly within severi habitat types and sampled most areas of the pond which was at most 60 cm deep (table 10.1; see Wiid 1996). I found R. sphenoeephaiu at densities of up to 3.l/liter early in the season and at densi-
ECOLOGY
ties as high as 8.0/liter as the pond began to shrink. Tadpoles of B. americanus, which often form dense aggregations, reached densities as high as 47.31liter on 17 April. I measured a number of physical and biotic environmentalparameters, includiig plant cover, substrate type, temperature and water depth. Tadpoles of B. americanus, Pseuducris ocularis, and R. sphenocephala showed differences in spatial use between individuais of Merent sizes within sampling dates, which suggest that habitat use changes ontogeneticaiiy and that cohorts of different ages may function as separate "ecological species" (Polis 1984; Wemer and Gilham 1984). Kehr (1997) also showed stage-speciíic shifis in microhabitat use by l?ocularis. In rny study, aspeas of the spatial distribution of ali four species responded to one or more environmental parameters. Spatial distributions of some species pairs were correlated, which suggest that habitat use might, in part, be caused by behavioral responses of species or cohorts to one another. I evaluated this hypothesis with a laboratory experiment in an environment devoid of asymmetrical spatiai features. Rana sphenocephala tadpoles tended to be overdispersed with respect to other species. This may have been caused by other species avoiding Rana which were the largest tadpoles. Overaii, this study suggested that tadpole habitat use is species-spechc,changes ontogeneticaiiy within species, and may be plastic with tadpoles responding to short-term factors such as the presence of larger tadpoles. This complexity is not surprising given the great environmental variability encountered by temporary-pond tadpoles of each species during their evolutionary history. Diaz-Paniagua (1987) and Loschenkohi (1986) studied tadpole habitat use in Europe. Loschenkohi examined microhabitat, resource use, and seasonal diflerences among five species in the same pond. Four species (Hyh arborea, Pelobates jkcus, Rana dalmatina, and R. ridibunda) overlapped seasonaiiy. The f i f i , Bufo bufo, reproduced earlier in the year, and most Bufo tadpoles had metamorphosed before the other species bred. The four seasonaiiy overlapping species had very similar gut contents but Mered in their distributions among microhabitats. Waringer-Loschenkohi (1988) examined Merences in the use of three depth strata in experimental aquaria. Aquaria were established with diflerent population densities, vegetation, and species composition. The results showed that the species differed in microhabitat use within the aquaria. Tadpoles of B. bufo always preferred the bottom and those of H. arborea preferred the surface. Tadpoles of R. dalmatina preferred the bottorn when alone but altered this preference when other species were present, and Pfùscus preferred the bottom when alone but was distributed more widely when Hyh were present. Tadpoles of R. rzdibunda preferred the bottom of a bare aquarium, but this preference disappeared when the aquarium contained rnacrophytes. Diaz-Paniagua (1987) defined five vegetation mnes w i h ponds: (1) grass, (2) short floating vegetation, (3) ernergent vegetation, (4) subrnergent vegetation, and (5) no vegetation. Samples frorn 16 ponds showed that aii tadpoles avoided mne 5. Hyh meridwnalis tadpoles were found pri-
269
marily in zone 4 and some were in zone 3. Tadpoles of Bufo bufo were found mostly in mnes 1and 2. Bufo calamita, Disco&sus~a&anoi, and Ranaperezi tadpoles were distributed widely in zones 1 through 4. Diaz-Paniagua suggested that diflerences in zone use were related to Merences in feeding method among species. Degani (1986) found tadpoles of Bufo viridis, Hyla arborea, Pelobates syriacus, and Rana ridibunda in a 40 X 60 m temporary pond in Israel and examined their microhabitat use in aquaria. He recorded the proportion of time spent in seven depth strata and in areas with and without macrophytes. ALI species except B. viridis spent 60%-70% of their time near macrophytes, while Bufo spent only 45% of their time there. Bufo and Rana tadpoles spent most of their time at or near the bottom, Hyh tadpoles were distributed nearly evenly among depth zones, and Pelobates tadpoles were bimodaiiy distributed between the surface or near the bottom. Degani used an experirnent to determine whether these microhabitat preferences aífeaed tadpole growth rates. He foiiowed the growth of each species in three cages placed near the surface and three on the bottom. Results agreed with the habitat preference study; Bufo and Rana grew best in cages on the bottom, whde Hyh and Pelobates grew equaiiy well at either depth. Barreto and Moreira (1996) dernonstrated differences in microhabitat use among the larvae of six species of frogs breeding in a pond in central Brazil. Aü of the studies above were carried out in still water environments, many in highly productive temporary pools with relatively high nutrients. A few studies have examined rain forest stream environments, which are generaiiy thought to be relatively low in nutrients and rates of primary production (Bishop 1973). Inger (1969) comrnented on tadpole habitat use by frog communities along smaii rain forest streams. Odendaal et al. (1982) documented S e r ences in habitat use between Crinia riparia and C.s&nifera in streams of South Australia. In laboratory experiments they showed that the habitat preference of C. stgnijiera shified to reduce overlap when C. riparia was present. Inger et ai. (1986a) documented differences in microhabitat use among 29 species of tadpoles collected in streams in prirnary rain forest in Borneo. They identified four taxonomicaiiy heterogeneous groups: leaf-pack, pothole, riffle-shingle-openpool, and side-pool pothole species. Variation in species composition was greater between than within sites over aíl of their sampling. Species composition was least variable in the leaf-pack habitat. They suggested that little evidence for cornpetition existed and that most diflerences in microhabitat use probably were because of diflerences in adaptations for coping with the physical environment. Trenerry (1988) examined habitat use by four species of tadpoles living in a tropical rain forest stream in northern Queensland, Australia. He divided the habitat into pools, riffles, and runs. Litoria~enimaculataand Mixophyes schevilli primarily lived in pools, and L. nannotis and Nyctimystes dayi inhabited only riffles. Runs were not regularly censused but appeared to be inhabited at low densities by pool species. Both r f i e species were suctorial, while the pool species had
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typicai lotic body forms. Population densities reached relatively high levels in summer months. In a pool measuring about 10 x 6 m with a mean depth of 40 cm, he estimated a population of 621 14 M. schevilli (l/m2; 0.0025Jliter) and 9162258 L.~enimaculata(15.3/m2; 0.04Jliter) in late summer. Hawkins et ai. (1988) presented s d a r information for tadpoles ofRccaphus.
Interspecific Competition and Predation Field Studie~ Field studies cited above have shown that, regardless of habitat, species usudy overlap broadly in diet and microhabitat use and that tadpoles often reach high densities. Many tadpole habitats show a great deai of year-to-year and siteto-site variation in seasonai availability, duration, and size. Species composition of tadpole assemblages varies sidarly. This spatial and temporal variation probably reduces the degree of permanent niche differentiation among species. The combination of high population densities and relatively low niche dserentiation suggests that interspecific competition may be relatively common in tadpole assemblages. Interspeciíic competition has been studied by the same general approaches used for intraspecific competition; populations have been monitored in the field, experiments have been performed in field enclosures and large-scale artificial communities, and experiments have been performed in laboratory systems. Few field experiments have examined interspechc com(1964) used a field experiment to expetition alone. amine possible competitive exclusion between Rana pipiens and R. pretwsa. The percentages and numbers surviving contradict the numbers that he introduced, so the foliowing is mv intervretation of his methods and results. H e remoied allJtadpoiesfrom 4 s m d natural ponds and then introduced 400 Ranapretiosa to 1 pond, 400 R. pipiens to another, and mixed groups with 200 individuais of each species to the other 2 ponds. Nine weeks later, 44% ofR. pretwsa and 39% of R. pipiens had survived in the single-species ponds. In the mixed-species ponds, survival of R. pipiens was 86% and 84%. while R. pretwsa survived at rates of 38% and 52%. resp&tively. H: suggested that these results indicated tha; R. pipiens was capable of expandrng its range and displacing R. pwtwsa. Wiibur (1977a) examined the relative strengths of intraspeciíic and interspecific competition by raising Bufo americanus alone and with larvai Rana palustrw in 6 1 X 6 1 X 244 cm pens placed in a pond. Bufo alÕne were at densities of 67, 101, 134, 202, 336, and 605/m2 (0.44, 0.67, 0.88, 1.33, 2.22, and 4.00Jliter). Bufo raised with Rana were aiways present at a constant density (100 per pen; 67/m2; 0.44/liter). Rana densities were 0, 17, 34,67,134, and 202/m2 (0, O. 11, 0.22, 0.44, 0.88, and 1.33Jliter). Each treatnlent was replicated twice. A reanaiysis of his means for treatnlents with 100 Bufo larvae raised with 50,100, and 200 Bufo and 50, 100, and 200 Rana suggests that there was no effect of density (F2,6 = 0.08, P = 0.922), competitor species (F2,6 = 0.02, P = 0.900) or the interaction of density and
umas
competitor species (F2,6 = 0.02, P = 0.980) on mass at metamorphosis ofBufo. There were aiso no significant effects on arcsine-transformed proportion survivai. When these treatments are compared to the treatment with 100 Bufo raised aione, there is some evidence for reduaions in proportion surviving and mean mass at metamorphosis, but the reductions caused by Rana appear to be equivaient to reductions caused by Bufo. Wiitshire and Buli (1977) used a field enclosure exveriment to examine competition between Pseu4hlyne bibronii and l? semimamata, which have narrow zones of geographic overlap in southeastern Austraiia. They evaiuated the hypothesis that the observed geographic distribution might be maintained in part by competitive exclusion. They colleaed eggs of both species from allopatric populations, hatched them in the laboratory, and introduced hatchlings into experimental enclosures (30 X 30 X 130 cm) placed in a pond in the range of l? bibronii. Tadpoles were raised at 40 or 80 individuais per enclosure (116 or 232/m2; about 1.5 or 3.0Iliter). At densitv 40 there were 3 treatments: E bibronii Ao&, I? semimakarata aione, and 20 of both species. At density 80, there were 3 similar treatments that were repeated with and without supplemental food. Survivai of l? semimamorata was lower than survivai of E bibronii in ali treatnlents. When both species were present without food supplementation, no l?semimamorata survived to metamorphosis. With supplementai food, the presence of l? bibronii reduced the mass of E semimamorata metamorphs. Wiitshire and Buil suggested that under their experimental conditions E bibmnii outcomveted I? semimamorata and that larvai competition might partidy explain the narrow geographic overlap between the species (aiso see Kupferberg 199%). Interaaions between another species pair with primarily dopatric distributions were examined by Odendaal and Buil (1983). Crinia signifera typicdy occupies creeks with slow flow rates, and C. riparia lives in faster moving water. They measured growth and survivai of both species in enclosures placed in a creek in the range of C. signifera, in the range of C. riparia, and in an overlap zone. Tadpoles were captured in the field and relocated to cages measuring 100 x 50 x 40 cm high. Densities placed in the experimental cages ranged from 124 to 222/m2 (0.62-l.ll/liter). Some cages were shielded from stream flow while others were exvosed. In general, both species grew and survived s i d a r l y i; shielded cages; but in unshielded mixed cages, Crinia riparia grew and survived better than C. sgnifira. The results from the shielded and single-species caies-indicated that C. sgnijira could survive in areas normdy occupied by C. riparia, but the results from the mixed, unshielded cages show that tadpoles of C. signifera are at a competitive disadvantage when C. riparia occur with them in those areas. Odendaal and Bull suggested that competition was unlikely to be caused by exploitation but was more hkely a result of interspeciíic avoidance behavior. Tadvoles of C. ribaria were more active in laboratory experiments and were more capable of maintaining position in flowing water. Their movements may disturb C. signifera when both species occur in high flow-rate environI
ECOLOGY
ments and reduce their abilitv to remain settled on favorable substrates. This could result in C. signifera being swept away by currents or could simply reduce their growth and survival rates by forcing them to expend greater proportions of their energy in returning to sheltered sites. An experiment by Woodward (1982) exarnined potential competitive interactions between temporary and permanent pond tadpoles from a desert anuran cornrnunity. He excavated an array of 124 (1 x 1 x 0.4 m) pools in a flat field; each pond contained 227 liters of water. He used these ponds to perform pair-wise conipetition experiments involving tadpoles of Bufo woodbousii and Rana pptens, Scapbiopus m b i i and Spea multiplicata, R.pipiens and Scapbwpus couchii, and large and smail R. catesbeiana and Scapbicrpus couchii. Total tadpole densities were between 50 and 200 individuals per pond (50-200/m2; 0.22-0.88fiter). Tadpoles of Spea multiplicata eliminated R. pipiens, apparently via predation. B. americanus and Scaphiapw couchii had negative effects on one another, with the effect of Scapbwpus on Bufo stronger than the reverse. Scaphwpus couchii also negatively affected R. p p n s while R. pipiens had oniy a slight affect on S. couchii. R. catesbeiana of both sizes had negative effects on S. couchii while being affected rather little themselves. Woodward suggested that most of the competitive effects he observed were because of ex~loitationconi~etition.His results also indicated that in most cases, pernianent pond species could be excluded from temporary ponds by competitively superior temporary pond species. The tadpoles of R. catesbeiana, the oniy permanent pond species able to hold its own in competition with Scaphwpus, rnight be excluded from temporary ponds by its normdy extended larval period. Morin and Johnson (1988) examined competition between Pseudacris m c i f e r and Rana sylaatica in G i c i a l pond communities. They raised tadpoles of Pseudacris alone at 83 and 166/m2 (0.15 and 0.30/iiter), Rana aione at 83 and 166/m2,and PseudaEris and Rana mixed 1:1at a total density of 166 and 332/m2 (0.30 and O.óO/liter). These treatments ailowed an independent examination of the effects of intraspecific and inteispecific competition and compared the interspecific effects of both species with each other. Phytoplankton standuig crops were examined at intervals, and water from the ponds were assayed for inhibitory effects on the growth of Pseudacris tadpoles in the laboratory. The mean mass at metamorphosis of both species decreased when density changed from 83 to 166/m2. The effect on Rana was about twice as " areat as that on Pseudacris. The soecies d8ered greatly in their interspecific effeas; Pseuúamis had very little effect on Rana at either density, while Rana strongly affeaed most responses of Pseudanw at both low and high densities. The interspecific effea of Rana on Pseuducris was greater than the intraspecific effect of a similar number of PseudaEris. Rana tadpoles had a greater effea on the standing crop of periphyton;han did Pse&acris tadpoles. The assays for growth inhibitors suggested that interference competition through inhibition did not occur. They suggested that the greater effeas of Rana were likely because of their greater body size and effect on the availability of resources.
271
Trenerry (1988) used a reciprocal-transplant enclosure experiment to evaluate the potential for competition between larval Litoria genimaculuta and Nyctimystes ahyi in tropical rain forest streams. Tadpoles of L.genimaculuta norm d y occur in slow-flowing pools, and N. dayi tadpoles are suctorial and primariiy occupy f i e s . Both species are found in runs with intermediate flow rates. He measured and staged tadpoles, placed them in 3.5-liter plastic jars with screen wire sides, and anchored the jars in the stream. Nine jars were placed in a pool and nine in a riffle: 3 containing 6 L.genimaculuta (390/m2; 1.7/l1ter), 3 containing 6 N. dayi, and 3 containing 3 tadpoles of each species. After 34 days, he measured the mean growth increments of tadpoles and the number surviving in each jar. Both species showed significant increases in body length oniy when they were alone in their normal microhabitat. The data also suggested that mortality of each species was lower in its normal rnicrohabitat. Results indicate that L. fienimd~ulataand N. dayi are suffciently specialized that they perforni poorly in each other's microhabitats. The fact that presence of the other species caused theni both to perforni poorly in their normal microhabitats indicates tha; thts s~ecializátionmav be remforced by competition when they co-occur. Penned populations in the field are cornmonly used to examine competitive relationships. For example, R. A. Griffiths (1991) found that R. temporaria increased the larval period and decreased the growth rate, mass at metamorphosis, and survival to nietamorphosis of B. calumita even when the species were not dowed physical contact (see Bardsley and Beebee 1998). Likewise, R. A. Grfiths et ai. (1991) found that the growth of larval B. calamita was inhbited by co-occurring R. temporaria, and by R. temporaria feces alone. The effeas of pond drying and competition between tadpoles of Bufo calumita and Hylu arborea and either Rana esculenta,R. bssonae, or R. a b u n d a were exarnined by Semlitsch and Reyer (1992b). Rana esculenta is a hybrid species that is a sexual parasite on the two nonhybrids. In outdoor artificial ponds containing 1,100 liters of water, they used a 3 (Rana species) x 2 (interspecific competitors presentlabsent) x 2 (ponds dry/do not dry) factorial design. Each tank contained 40 tadpoles of one Rana species. Haif of the tanks also contained 35 Hylu and 100 Bufo. Haif of the tanks in each conibination-of Rana specie~/competitiontreatment dried completely in 60 days; remaining tanks had a constant water level. The tadpoles of R. ridibunda survived at low rates in d treatments: There was a significant interaction between the effects of species and drying regime on the proportion of tadpoles that metarnorphosed in 60 days. Several other interactions involving species identity that appear in their figures 1-5 were not statisticdy significant. Competition and drying regime also had significant main effeas on percentage of individuais metamorphosing and on mass at metamorphosis. Days to metamorphosis was significantly affected oniy by competition. Tadpoles of R. esculenta performed better under poorer conditions than either of the nonhybrid species, whde the nonhybrid R. lessonae outperformed R. esculenta under favorable conditions. Sernlitsch and Reyer suggested that environmental heterogeneity may
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be an important factor in maintaining popuiations of aii the species necessary for the stabiiity of this hybridogeneticcomplex (see Schrnidt 1993).
Laboratory Studies Compared to the large number of laboratory studies of intraspecific competition, relatively few have examined interspecific effects. Some experiments, such as those ofAiun (1966) and Licht (1967), have already been discussed with reference to growth inhibition. Smith-Gill and Gill (1978) examined interferente competition between Ranapipiens and R. ylvatzca and fed the tadpoles boiied lettuce ad libiturn. The effects of conspecific density on R. ylvatica were curvilinear and R. pipiens had iittie effect on R. ylvatica. Conversely, the effect of R. ylvatica density on R. pipkns was greater than the conspecific effect of R. pipiens. The interspeciíic effect of R. 91vatica on R. DiDiens was also curvilinear (i.e.. increased more rapidly thanLiensity).They also found ekdénce for positive effects of increasing density at lower densities. They concluded that the intensitv and even the sign of intersoecific competition coefficients may depend on density and that extrapolation from single-densityexperiments to predict interactions over a wide ranp.e of densities is unlikelv to resuit in realistic predictions. It wouid be interesting to perform a similar experiment under conditions where exploitation competition was likely to be dominant as it usually is in nature (Petranka 1989). Travis (1980b) examined the responses of Hyhgratwsa larvae belonging to six sibships to competition with H.femoralis lamae from a single sibship. Six of 7 experimental treatments included 20 individuais from 1H.gratiusa sibship and 20 H.femralis sibships, and the final one included 4 H.gratiosa from each of 5 of the sibshios olus 20 H. fimmalzs. The initial densities in aii treatments were equal with 40 individuals in a plastic pan holding 6 liters of water (555/m2; 6.661 iiter). His analysis indicated that H.~ratwsasibships differed in their compe&tiveeffects on ~.fet&raliswhose mass at day 47 of the larval period varied from means of 125-185 mg depending on the H.gratwsa sibship with whch they were competing. The H.gratwsa families also differed in their responses to the combination of inter- and intraspecific competition. The treatment that included H.g~atiosafrom a mixture of famiiies showed responses intermediate between, but more variable than, the sGgle family groups. The laboratory experiment of Aiford (1989b) was designed to determine whether variation in reproductive phenõlogy of aduits might interact with gene6c variation for factors deterrnining competitive abhty in larval H. chlysoscelis. I designed a 2 x 2 x 3 factor experiment in which the first 2 factors were male and female oarentage and the third was competitive regimen. Crossing two males with each of two females gave four sibships of tadpoles. I raised these in 3 competitive regimens: individuais alone in plastic boxes containing 250 ml of water (83/m2; 4/iiter), 1 H. chlysoscelis with 4 R. catesbeiana introduced simuitaneously (4 15/m2; 20/iiter), and 1 Hyh with 4 Rana introduced on dav 11 of the Hvh larval oeriod. These treatments simuiated variation in the relative tirning of reproduction of Hyh and V
D
I
I
V
Rana similar to that encountered in monitoring of field popuiations. I suppiied food to ali containers at the same dady rate and evaluated the effects of competition on the H. chlysoscelis tadpoles by weighing them o i day 41 of their larval periods. The presence of R. catesbeiana significantiy reduced the mass of Hyla tadpoles. The four H. chlysoscelis sibshps responded differentiy to competition, and the offspring of different females differed signiíicantly. Offspring from different male parents Mered significantly, but their raniung from large to s m d changed depending on whether competing Rana were introduced simuitaneously or later. These results suggest that seleaion caused by phenological variation may be a factor leading to the retention of genetic variation in the competitive abiiity of tadpoles because different suites of characters may be advantageous depending on when competitors reproduce. In anothercase (pers&xd observation), I examined competitive effects of tadpoles of Limnudynastes ornatus and Litoria inermis from Australia on lamae of the exotic Bufo marinus. I raised tadpoles in 10-cm diameter x 7-cm deep plastic containers holding 250 ml of water and suppiied food at 1 and 6X. As part of the experiient, I used 5 experimental treatments to examine interspechc competition: 1Bufo tadpole raised alone with 1X food, 1 Bufo raised alone with 6X food (density 127/m2;4/iiter), 1Bufo tadpole raised with 5 L. inemzis (762/m2;24/iiter), 1 Bufo with 5 L. ornatus, and 6 Bufo tadpoles. There were large differences in relative'effects of each species on Bufo growth rate. Tadpoles of L. inemzis had very iittie effect on growth rates of Bufo, which grew at nearlv the same rate in comoetition with five L. inermis as they 'did when raised alone. btraspecific competition from Bufo had an intermediate effect, while competition from L. ornatw had the greatest effect; Bufo raised with L. ornatus grew very slowly and ali died before metamorphosis. These results are consistent with what is known of the basic biology of tadpoles of each species. Limnudynactes are specialized for rapid growth in extremely ephemeral pools; they hatch from relatively large eggs with large yoik suppiies that d o w them to reach large sizes within 2 days posthatchmg. They are voracious feeders and behavioraiiv interfere with the access of other tadpoles to food sources by butting and can reach metamorphosis in as iittie as 13 days (personal observation). ALI of these characteristics suggest that L. ornatus tadpoles shouid be strong competitors. Tadpoles of L. inermis, which normaiiy occur in semipermanent or permanent dams and water holes, hatch from much smaiier eggs than L. ornatus and at a much smaiier sizes, grow more slowly posthatching, and appear to be less aggressive (personal observation).Bufo marinus are intermediate in aii characters except aggression while feeding; they appear to be as aggressive as L. matus, but because thev are usuaiiv smaiier after hatching and thek relative size decieases withke passage of time, L. ornatw iarvae can outcompete them for macroscopic food items. Semiitsch (1993) examined competition between tadpoles of species of the hybridogenetic Rana esculenta complex and showed that interspecific competition exists, with the hybrid R. escuienta a somewhat stronger competitor than R. iessonae.
ECOLOGY
Competitwn of Tadpooles with Other Organhms Aithough it seems likely that tadpoles and many other groups of primarily herbivorous aquatic organisms overlap in their food requirements, very iittle inforrnation is available on competition outside the tadpole guild. In her laboratory study of interspecific growth inhibition, Akin (1966) found that water conditioned by other taxa did not inhibit the growth ofRanapipiens tadpoles. Morin et ai. (1988) examined the responses ofHyh andersonii tadpoles to competition from Bufo woodhousii folaeri and an assemblage of aquatic insects. Twelve artificial ponds containing H. andevsonii tadpoles at a density of 83/m2 (0.151iiter) were used. Six ponds also contained B. w.fmleri tadpoles (83/m2).They dowed aquatic insects to colonize three of the ponds with both tadpole species and three with only H. andersonii. Both Bufo and inse&s reduced the mean metamorphic mass of H y h tadpoles. The combined effeas ofBufo and inseas were similar to the effeas of either group aione. Competition had no effea on larvai ~ e r i o dor survivai rate of Hvh. Bv measuring the standing crop of periphyton on glass slides on a single date, they found that inseas reduced the standing crop and presumably the availability of periphyton for tadpole consumption. They suggested that in naturai temporary ponds lacking vertebrate predators, competition with inseas rnay be at least as important as competition within the tadpele guild. competi2on of tadpoleskith other taxa has aiso been shown by Alford (1989c, newt larvae), L. Blaustein and Margalit (1994, 1996; mosquito larvae), Bronmark et al. (1991, snails), and Kupferberg (1997b, insect lamae). These results strongly indicate that such effeas should be considered in hture synthetic studies of tadpole ecology. Interactwns between Competitwn and Predatwn Competition and predation can have strong effeas on the development, growth, and survival of tadpoles. In naturai systems, tadpoles are commonly exposed to both of these factors, which rnay often interact. Predation obviously affeas competitive interactions by aitering the density of competing species. DXerences in palatabhty or predator avoidance among species rnay interact with differences in competitive abhty; species with better antipredator mechanisms rnay suffer less from interspecific competition as predators redúce the numbers of their com~etitors.The iniensitv of competition rnay affect predation rates and cumulative risks of predation by changing the time periods that prey spend at sizes that are vulnerable to particular predators (reviewed by Sih et al. 1985). The complexity of these possible effeas makes it necessary to experimentaily evaiuate their importance. DeBenedictis ( 1974) examined cornwtition between larvai Ranapipiens and R. rylaaticu in pens placed in a pond (101-806 individuals/m2;0.67-5.36/iiter) over a 2-year period. In the first year, density did not appear to lumt growth or sumivai of either species in any experimental treatment. He suggested that this indicated that the experimental densiof the environment. ties were below the carrying capacity . In the second year, there were strong effects of density and
2 73
evidence for interspecific competition with inter- and inuaspeciíic competition having about equal effects. Predators (fish, leeches, and odonate naiads) reduced sumivai and increased metamorph size of both species. Many of the results of DeBenedictis are difficult to interpret because of highly variable repiicates. Artificial pond communities generally exhibit less variation among replicates than pond enclosures and therefore ailow complex experiments with interpretable results. Interactions between competition and predation were first examined in artificial pond communities by Morin (1981). He established 16 experimental ponds containing adult brokenstriped newts (Notophthalmusviridescens donalis) at densities of 0,2,4, or 8 per pond (0, 1.1,2.2, or 4.4/m2). Five days later he added hatchluigs of Pseudmi crttcifeer,Rana @emcephah, and Scaphiopus holbrookii at densities of 0.2,0.3, and O.l/liter (110, 165, and 55/m2), respectively. The community was completed 36 days later with the addition of Bufo tewestris hatchlings at a density of 0.3/liter (165/m2).Morin found that ScaphUIpushad very high sumival to metamorphosis in the absence of predators (3 = 93%). Bufo ais0 survived at a relatively high rate when predators were absent (3 = 40%). Morin attributed the low survival of Pseudacris when predators were absent (2 = 4%) to interspecific competition. The survival rates of BujÒ and Scaphiopus deched with increasing newt density and reached means of 8% and 18%, respectively, at the highest newt density. Survival of Pseud m i increased to 28% at a newt density of l.l/m2 and remained constant at higher newt densities. Mean body mass at metamorphosis of Pseudmi increased frorn 72 mg at a newt density of 1.l/m2 to 211mg when 4.4 newts/m2 were present. Data from his table 1suggest that total metamorph biomass produced per pond deciined from about 93 g when newts were absent to about 46 g when 4.4 newts/m2 were present; this suggests that some competition rnay have been caused by interferente. Aiternatively, this result could have been caused by increased S U N ~ Vand ~ competition from larvai Rana that did not metamorphose during the period covered by his anaiyses. Morin (1981) demonstrated that predation could aiter the competitive hierarchy in a temporary-pond system but suffered from some lack of realism by includiig only a single predator. In a second overlapping experiment, Morin (1983) manipulated the abundance of a second predator, larval tiger saiamanders (Ambystoma t@rinum). Newts were established at the same densities (0,2,4, and 8 per pond) used in the first experiment. Two additional treatments were added: one with four adult N. v. dorsalis per pond and four A. tigrinum per pond and one with only four A. tigrinum per pond. Hatchling anurans were added in the sequence and densities previously outluied in Morin (1981). Twenty-two days after the introduction of Bufo tewestris, Morin added Hyla chrysoscelis and H. ~ratiosaboth at densities of 83/rn2 (0.15/liter). Larval A. tt&rinurnrernoved nearly d tadpoles from d ponds they occurred in. The effeas of newts on the tadpole metamorph assernblage were similar to those reported in Morin (1981), although the obsemations were over a longer period. Indusion of data on H. chrysosdlts and
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H.~ratiosashowed that total metamorph biomass did not decrease consistently with increasing newt density, which in&cates that competition was probably caused by exploitation of resources. Correlational analysis of interspecific competition suggested that it was strongly asymmetrical, with B. tewestrs, H. chlysoscelis, R. sphenocephah, and S. holbrookii negatively afFecting the growth and survival of H. ~ratwsa and l?mzrcqer, whiie not being affected by them. Morin suggested that H. jratwsa and l? crucqer may depend on reduction of the density of competing species by predators for their persistence in anuran communities. He also &scussed the possibility that some of the asymmetry in competitive effects may have been caused by the phenology of introduction of species. In both of his experiments, Morin (1981, 1983) could infer competition only through retrospective correlations of metamorph abundances with performance. Wilbur et ai. (1983) addressed this problem with an artiúciai pond experiment by manipulating the abundances of adult newts and tadpoles simultaneously. Newt densities were 0 , 4 , or 8 per pond (0,2.2, or 4.4/m2), and Bufo woodhousiifmleri tadpoles were introduced to ali ponds at a constant density of 1651 m2 (0.3Jliter).Three other species were introduced to low-, medium-, and high-densityponds as follows: Bufo tewestris (55,110, or 220/m2; 0.1,0.2, or 0.4/liter), Ranasphenocephala (28, 55, or 110/m2;0.05,0.1, or 0.2/liter), and Scaphwpus holbrookii (55, 110, or 220/m2; 0.1,0.2, or O Alliter). Total tadpole densities in the ponds were: low = 138/m2(0.251 liter), medium = 275/m2 (0.5/liter), and high = 550/m2 (l.O/liter). Bufo species were competitively dominant at medium and high densities when newts were absent. Scaphqus had low survivai rates, which was attributed to their inability to feed on the íilamentous aigae that dominated the ponds. Rana appeared to be strongly afFected by interspecific competition at the high density. When newts were present, they eliminated ali S. holbrookii. Newts at 2.2/m2 greatly reduced survivai of both Bufo species, and at 4.4/m2 they eliminated ali Bufo from 8 of 9 ponds. Newts also greatly reduced the survivorship of R. sphenocephah, but some Raha survived in most ponds with newts. Surviving Rana benefitted from reduced inter- and intraspecific competition and metamorphosed at mean body masses at least twice as large as Rana from ponds without predators. Wilbur et ai. (1983) suggested that R. sphenocephah was the oniy species capable of attaining a size refuge from newt predation and that predation rnight be the dominant organizing factor in many tadpole assemblages. Other studies focused primariiy on interactions between competition and predation as influences on tadpole ecology. Van Buslurk (1988) examined whether effects of multiple predators can be reiarded as additive. He studied predatLn by dragonfly naiads on a tadpole assemblage in artificial ponds by independentlyvarying the densities of Tramea carolina (O or 9.9/m2; O or 0.019Jliter) and A n a juniw (O or 2.2/m2; O or 0.004/liter). The tadpole assemblage consisted of Bufo americanus (138/m2; 0.26/liter), PseudanZs mzrcqer (39/m2; 0.07/liter), l? triseriata (50/m2; 0.09/liter), and Rana sphenocephala (83/m2; O.ló/liter). The composition of
the metamorph assemblage was afFected strongly by predators. Rana were almost eliminated from ponds with no predators, but about 10% survived in ponds with one species of predator. Rana survival decreased to 2% when both predators were present. Bufo and l?mzrczyer were afFected similarly by A. junius, which reduced their survival rates from 74% and 62%, respectively, to 30%. Tramea carolina afFected l? cmcqer and Bufo differentialiy with 0% and 35% surviving when Tmmea were the oniy predators. When both predators were present, their effects on Bufo appeared additive, with about 19% of Bufo reaching metamorphosis. The survivai of l?triseriata was afFected strongly by both dragonfly species by declming from 62% when predators were absent to about 10% when either predator was present and 0% in the presente of both. Predation benefitted surviving B. americanus and l? triseriata by increasing their growth rate and decreasing their larval periods; it did not afFect the performance of the other tadpole species. Van Buslurk concluded that the effects of predators on the tadpole assemblage were essentialiy additive and aliowed the effects of both species together to be predicted from the effects of each one alone. This offers some hope for the eventual construaion of models of species interactions in complex communities. Cortwright (1988) exarnined interaaions among predators and the effects of predators on their prey in 1 x 2.5-m pens placed in a permanent pond. His predators were adult Ambystoma *um and larval A. jefiersonianum, and A. macuhtum. The presence or absence ofA. opacum (O or 4.4/m2) was crossed with 3 initiai densities (17, 34, or 67/m2) of hatchling A. jeffeersonianurn. Other species were added at equal initial densities to ali pens: hatchling A. macuhtum (34/m2),hatchlmg Hyh chlysoscelis (92/m2),hatchling Rana sylvatica (200/m2),and year-old ovenvintering Rana clamitans (12/m2).Cortwright found that the yearling R. chmitans were not vulnerable to salamander predation presumably because of their large body size. Hyh chlysoscelis were virtualiy eliminated from ali pens with a maximum survival rate of 0.2%. The fate of R. sylvatica depended on the presente ofA. opacum; when these were present, R. syltatica were almost eliminated. WhenA. opacum were absent, about 10% of R. sylvatua survived to metamorphosis. There was some evidence that surviving R. sylvatica benefitted from reductions in conspecific density when the initial density of A. j@eersonianum was higher. Cortwright and Nelson (1990) report on additional results from this experirnent. Wilbur and Fauth (1990) examined competition and predation in a mo-predator, two-prey system in artificial ponds. Their experiment crossed the presence and absence ofAnax junius naiads ( m o per pond) and adult newts (Notupbthalmus virihscens; m o per pond) with the presence and absence of tadpoles of Bufo americanus and Rana palustrs, both at 276/m2 (0.5Jliter). When predators were absent, there was significant intra- and interspeciúc competition. The leve1 of competition was reduced when predators lowered survival rates. The survival of both species was reduced in ponds with one predator and one prey species but to a species-specific extent; Rana were more strongly afFected by Anax than were Bufo. When one or two predators and both prey were pres-
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changes in priority of reproduction by Bufo americanus and Rana sphenocephala in artificial pond systems. We crossed three Rana treatments (absent, 100 [55/mZ,O. l/liter] introduced on day 0, and 100 introduced on day 6) with three Bufo treatments (absent, 500 [275/m2, 0.5/liter] introduced on day 0, and 500 introduced on day 6). For each species, these treatments yielded ponds with no interspecific competition and ponds with interspeciíic competitors introduced simultaneously, 6 days earlier, and 6 days later. The treatment with neither species introduced was used in a separate esperiment (Wilbur and Alford 1985; see below). Both species performed best in the absence of interspeciíic competition. Both species aiso performed better when they were introduced on day 6 of the experiment than when they were introduced on day 0. The effect of Rana on Bufo appeared to increase when thev were introduced earlier than Bufo and to decrease when they were introduced later than Bufo. This result was consistent with the idea that the effects of interspecific competition are size-specific, with larger animais having greater competitive effects. Rana actuaüy performed better when Bufo preceded them into ponds and worse when Bufo foilowed them into ponds. This may have been caused b i a reduction in the number ofBufo competitor days esperienced by Rana when Bufo preceded them into the ponds. The performance of tadpoles can depend on the absolute fine timing of reproduction by adult frogs and on the relative timing of reproduction by competing species. L. Blaustein and Margaiit (1995) have demonstrated similar effects of smaü changes in priority on the interactions between larval Bufi viridis-and mosquitoes (Culisetalongiareolata). The study of Alford (1989a) was designed to examine the effects of short-term variation in reproductive phenology in greater detail than had been revealed in the preceding esperiment (Aiford and Wilbur 1985). I used 9 experimentaltreatments to examine the responses of tadpoles of Bufo americanus and Rana palus~rz'rto 7 relative timings of introduction of the other spe& that spanned a range õf 11days preceding to 11days foiiowing. AU treatments included both species at the same initial densities of 55 Rana/m2 (O.l/liter) and 274 Bufolm2 (0.51liter). Growth and survival of both Effeets of Environmental Uncertainty species failed ;o resbond to &e timing of introduction ofthe Environmental uncertainty has been featured prominently other species. Correlations between growth rates and numthroughout this chapter. Reproductive site choice by frogs, ber of metamorphs indicated that both species responded and thus possible tadpole community composition, is d u - to their own densitv. but there was little êvidence of interenced by a complex interaction between environmental specific competition. These species frequently co-occur in quaiix environmental uncertainty, life history, predation North Carolina ponds, and I suggested that the lack of interrisk, and resource availabiiity. Tadpoles are capable of re- specific competition might reflect co-adaptation to avoid sponding to alterations in the environment, both physical competition and that the effects of phenological variation on and biotic, by aiteritig their behavior and physiology and species interactions depend on the species being examined. Effects of short-term variation in reproductive phenology changing their relative rates of growth and development. As Morin and Johnson (1988) pointed out, competition be- were also explored by Gascon (1992a) and S. E Lawler and tween species of tadpoles is ofien asyrnmetrical and may de- Morin (1993). Gascon examitied competitive relations bepend on relative body sizes. Relatively recently, a number of tween the early reproducing Osteocephalus taurinus and the field experiments have attempted to evaluate how environ- later-reproducingEpipedobatesfemoralir and Phyllomedusa tomental uncertainty of several types effects ecological rela- mqptema i11 Amazonian Brazil. He conducted three experitions within and between species of tadpoles. ments in 45-cm diameter x 19-cm deep basins placed outAiford and Wilbur (1985) were interested in determining doors in the forest. Neither of the late-breeding species whether the outcome of competition was dected by smaü dected the early species, but the early species deGed both ent, the prey survived at higher rates than when they were alone with the predator; they appeared to share the rise of predation so that each species benefitted from the presence of the other. When both predators were present with one prey species, the prey suffered about additive mortaiity from both predators-the survival rate of prey in two-predator, one-prey systems could be predicted from their survival in one-predator, one-prey systems. Wilbur and Fauth exaniined their results further with several models of multispecies interactions. Fauth and Resetarits (1991) reported on the results of an experiment in which newts (Notopbthalmusvirideseens) and sirens (Siren internedia) preyed on a five-species tadpole assemblage. They found that newts acted as keystone predators, altering the composition of the tadpole assemblage, while sirens were nonselective. The predators interacted, apparently through predation by sirens on newts. Peacor and Werner (1997) found complex interactions between competition, predation, and behavioral antipredator mechanisms in experimental systems containing two size classes of larvai Rana catesbeiana, larval Rana clamitans, and ~ W O odonate predators. These field experiments demonstrate that competition and predation interact in a complex mamer in determining the success of tadpoles. Some species that have effective antipredator mechanisms (e.g., Pseudacns cmcifer) may benefit unambiguously from predation on competing species. Surviving individuais of many species may benefit from increased growth rates and body sizes at metamorphosis caused by reductions i11 the levels of inter- and intraspeciíic competition. The extent of these benefits may depend on interactions between freeing of resources by the thinning of competitors and the costs of antipredator mechanisms such as reductions in rates of movement (Van Buskirk and Yurewicz 1998). Whether the advantages outweigh the disadvantages of decreased survivorship for species with poor defenses probably varies from time to time and place to place depending on the densities of competitors and on the presente of other mortaiity sources such as pond drying. Some of these questions are addressed in the next section.
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of the late-breeding species. The relative tirning of introduction altered the effects of 0. taurinw on l?tomoptema; they were reduced when both s~ecieswere introduced simultaniously. Relative tirning did not alter the competitive effect of 0. taurinus on E. fenzoralis. S. P. Lawler and Morin (1993) used artificial pond experiments to determine how Bufo woodhousii and Pseuducris crucqer larvae responded to O, 7, and 14 day lags in tirning of reproduction. They found that the species responded asymmetricdy; Pseudacvis were affectedmore strongly by Bufo when Bufo were introduced 7 days before them, while Bufo were not affected by Pseudacvis. They concluded that the usual pattem in nature, in which Pseudami's reproduce very early, probably maxirnizes the success of this competitively inferior species. Competition may be direct, through the use of the same resources or behavioral or chemical interferente, or indirect, through alterations to the physical or biological structure of the environment. Wilbur and Alford (1985) demonstrated that tadpoles may affect other species through persistent effects on the environment. We examined the effects of pond history and competition on the performance of ~ ~ l a h r soscelis larvae. Hyh were introduced at a density of 274/m2 (0.5lliter) to the artificial ponds used in a separate experiment (Alford and Wdbur 1985. discussed above) 80 davs after &e ponds were initiaiiy filléd. They were alsó raised in a set of ponds that had been filled only 15 days previously and had never been occupied by other tadpoles. This led to H. chvsoscelis tadpoles experiencing ponds with 10 different hstories: 15- and 80-day-oldponds that had never been occupied by tadpoles, 80-day-old ponds that had been occupied by Rana sphenoc~.phalaor Bufo americanus for 66 or 72 days, and 80-day-old ponds that had been occupied by both Rana and Bufo for various combinations of 66 and 72 days. Most Bufo had completed metamorphosis before any Hyla were introduced to the ponds; effects of Bufo on Hyla thus were caused by environmental alterations rather than direct competitive effects. Growth and survival ofH. chrysosceliswas greatest in 15-day-old ponds. Eighty-day-old ponds that had never been occupied by other tadpoles produced the next best Hyh performance. The presence of Bufo or Rana decreased the performance of Hyla metamorphs, which was also iduenced by the order in whch Bufo and Rana had been introduced. Indirect effects between tempordy separated species were examined further by Morin (1987), who introduced Pseudacvis crucifer tadpoles to experimental ponds at 55, 110, and 220/m2 (0.1, 0.2, and 0.41hter). These were crossed with densities of the predatory newt Notophthalmw viridescens at 0, 2, or 4 per pond (0, 1.1, or 2.2/m2). Forty-three days later, about 1week before Pseudacri's began to metamorphose, Morin added hatchling Hyh versicolor to d ponds at a density of 110/mZ(0.2lliter). Newts had little effect on the growth .and survival of Pseudacri's, but increasing newt density strongly decreased the survival to metamorphosis of Hyla. When newts were absent, the total froglet biomass exported from ponds was relatively constant (about 75 g). The proportion of that biomass attributed to Hyla depended strongly on the initial density of Pseudami's; although d
Pseudacvis completed metamorphosis early in the Hyh larvai period, there was a significant negative correlation between Pseudumis biomass and Hyla biomass exported from ponds. Hyla versicolor growth and survival rates also decreased with increasing densities of Pseudacris. Morin pointed out that this pattern is consistent with a hypothesis of preemptive exploitation competition for resources; a limited total quantity of nutrients is avadable when the pond fills and the export in metamorphs of early breeding species may reduce the avadability to later reproducers. He also noted that Pseudacri's appeared to be competitively superior to Hyh and that their temporal separation might not preclude competitive exclusion under some conditions. Warner et ai. (1991) examined interactions among the effects of density, long-term reproductive priority, and pH on the larvai biology of Hyhfemoralis and H.gratwsa in outdoor ta&. M remaining H.gratwsa were removed before the introduction of H. fenzoralis 108 days after H. gratiosa had been introduced. They found that H.gratwsa larvae had longer larval periods and lower metamorphic body sizes densities were higher. Lower environmental p H inywhen creased the effects of intraspecific density on H. gratiosa. Hyhfemoralis responded similarly, but the effects of pH did not interact with the effects of density. H. femmalis introduced to ponds that had previously contained H. gratwsa performed better than ones in ponds with no previous tadpole occupants. Warner et al. (1991) suggested that this facilitation might have been caused by effects of H.gratiosa on resources; their grazing may have changed the abundantes of aigae, favoring types with better nutritive quality, or may have enhanced nutrient cycling or reduced the prevalence of some toxic substance. The consequences of variation in reproductive tirning within a species were examined by Morin et al. (1990). They introduced a second cohort of Hyh andersonii tadpoles at a density of 55/m2 (O.l/liter) to 12 artificial ponds used in an experiment discussed earlier under competition with other taxa (Morin et al. 1988).The second cohort was introduced 34 days after the first. Their resuits indicated that the second cohort experienced longer larval periods and reduced growth rates and survival to metamorphosis when compared to the first cohort. Mean masses at metamorphosis were similar between the cohorts except when interspecific competitors and predators were excluded; in that treatment, the earlier cohort reached metamorphc masses nearly twice as great as the later cohort. Hearnden (1992) demonstrated similar effects in Australian popuiations of Bufo marinus, with the additional factor that when a second cohort was introduced as eggs, the earlier cohort preyed upon them, adding predatory reductions in survival to competitive effects. The precediig experiments showed that the reproductive phenology of frogs can affect ecological interactions among tadpoles. Variation in reproductive phenology has the potential to alter the outcome of competition between some species. Variability in the persistence of ephemeral ponds is probably another aspect of environmentai uncertainty that is important in tadpole ecology. Wdbur (1987) examined interactions between competition, pond drying rates and pre-
ECOLOGY
dation in experimental pond communities. He hypothesized that predation may benefit some tadpoles in temporary habirats by reducing interspecific and intraspecific competition by aiiowing sumivors to grow more rapidly and leave ponds before they dry. He tested this hypothesis with an artificiai pond experiment including three rates of pond drymg: connant water depth of 50 cm, drained after 50 days, or drained afier 100 days. H e aiso included 2 predation regimes of adult Notophthalmus viridescens dorsalis (absent or present at a density of 2.2/mZ [0.004/liter] and low and high tadpole densities (totals of 242 and 970/m2: , , 0.44 and 1.76Ilite1-). The tadpoles included in each pond were Bufo americanus (110 or 441/m2; 0.2 or 0.8/liter), Hyia chrysoscelis (69 or 276/m2; 0.125 or 0.5/liter), Ranasphemcephaíu (28 or 1101 m2; 0.05 or 0.2/liter) and Scaphiopus holbrookii (36 or 1431 mZ;0.065 or 0.26lliter). The composition of the metamorph assemblage was d u e n c e d significantly by predation, drying time, density, and their two-way interactions. Scaphiopus appeared to be the dominant competitor. Rana negatively atfected the growth of ali species except Scaphiopus. Bufo and H+ appeared to have negative effects only on themselves. ,it low initial densitv. newts elimnated nearlv aii tad~oles. -it high density, si&& total numbers of tadp61es metamorphosed regardless of newt presence, but the composition of the metamorph assemblage changed; newts reduced the dominance of Scaphzupw and aiiowed other species to metamorphose in greater numbers. This effect was more pronounced in ponds that dried. With predators absent, only Scaphiopzw eherged from ponds thatdried in 50 days, b i t mith predators present, both Bufo and Scaphzupus metamorphosed. Sirnilarly, only Bufo and Scaphiopw emerged in any numbers from ponds that dried in 100 days when predators n-ere absent, b;t the presence of predatois allowed significant numbers of Hyla to metamorphose as weli. There was aidence that tadpoles responded directly to pond drying by initiatinp: metamomhosis earlier. Wibur inter~retedhis results as indicating that competition and desiccation probably dominate the dynamics of populations exploiting very ephemeral habitats, with predation possibly acting as a moderating influente. The importance of predation should increase as habitat duration increases. Harris et ai. (1988) documented the temporal patterns of abundance of adult and lamal newts (N. v. dorsalis) in a pond in North Carolina over a 3-vear period. We showed that the riming of newt arrivai and depkure and the duration of newt presence varied among years. This variation was not nreli correlated with variatiõn in the tad~oleassemblage (personal observation). Ali of the experimental studies cited thus far which examined predation did not explicitly d o w for the fact that predators typicaiiy foliow their own phenologicai patterns. I conducted an artificial pond experiment (Alford 1989c) to examine the effects of predator phenology and phenologicai variation. My experiment was combined with the one reported bv Wilbur (1987). The same four anuran species were introduced at the same two densities. I established 4 predation regimes that included 2 extreme treatrnents in which adult Notophthalmw at a density of 2.21 m2 (0.004/liter) were absent or continuously present. Two 0
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additional regimes mimicked the extremes in newt departure time obsemed by Harris et ai. (1988)-newts initiaiiy present but removed from ponds on 1 Aprii and newts initially present but removed on 13 and 14 May. A correlation analysis suggested that interspecific competition foliowed a hierarchy with S. holbrookii being the dominant competitor foiiowed in order by R. sphenoczphaia, B. americanus, and H. chrysoscelis. The presence of predators for any length of time aitered the composition of the metamorph assemblage. The anurans that reproduced earliest (Rana and Scaphzupus) were affected most negatively. When newts persisted for longer periods, they aiso affected later reproducers. The abundance and contribution to metamorph biomass of Bufò declined when newts persisted until 13-14 May, while Hyia increased. The relatively abundant Hyia in this predation regime appeared to have competitive effects on the other species, which suggests that interspecific competition may not be completely described by the simple hierarchy postulated earlier. Forcing newts to remain in the ponds through the summer reduced the abundance and biomass of Hyla by increasing the relative contributions of the other species to the metamorph assemblage. Bufo, Rana, and Scaphzupustadpoles appeared to reach size refugia after which newt removai did not aiter their sumivai patterns. There was strong correlationai evidence for negative effects of increased tadpole density on the performance of newt lamae. Because the primary resource of tadpoles is plant materiai and newt larvae feed primarily on zooplankton, this negative effect probably was caused by diffuse competition through two intermediate levels of the trophic web; tadpoles aitered the aigai community, which altered the zooplankton community, which affected the performance of newt larvae. This experiment confirms that incorporating predation into models of temporary pond and other communities requires some knowledge of predator phenology in addition to predator abundance.
Summary The avaiiable information on the ecology of tadpoles has increased greatly since Wilbur's (1980) review. Tadpoles have proved to be a valuable model system for investigation of many aspeas of population and cornmunity ecology. In the course of these investigations, it has become clear that a iÜii understandmg of the ecology of any tadpole assemblage requires data of severai types. First, there must be information on reproductive habitat choice and phenology of the frog species mhabiting that region. Choices of reproductive habitats by frogs set the range of possible tadpole assemblages that may develop. Reproductive phenology can predetermine the outcomes of interactions between tadpoles and their competitors and predators. Second, mformation on the reproductive habitat use and phenology of potential predators is necessary for the same reasons. I suggest that information on potential competitors belonging to other phyla will aiso be needed. Third, it is necessary to have mformation on tadpole, predator, and probably interphyletic competitor densities. Finaiiy, information on resource availabhty, habi-
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tat stnicture, behavioral responses of tadpoles to competitors and predators, and the previous history of the habitat may be needed. A lack of any of this information may lead to incorrect predictions about the course of interactions in any tadpole assemblage. Extrapolation from ecological interactions experienced by tadpoles to their effects on the population biology of frogs requires much more information on the biology of metamorph and juvenile fkogs than is currently avadable for nearly d species. This complex picture is far from the optimisticdy sirnple views of community ecology that prevailed in the early 1970s (see May 1974). It is also far from the nondeterminism espoused by some authors (see Strong 1983). Rather, it appears that tadpole assemblages, and probably complex assemblages of other species, are highly deterministic but that a great deal of information is needed to unravel the sources of that determinism. I identified several areas that are in particular need of h r ther investigation. To fully understand the autecology of tadpoles, detaded studies on their foods, feeding rates, and assimilation efficiencies must be initiated. Such studies also would aid in understandmg the role of tadpoles in communities. Although the evidence is sparse, tadpoles may provide a major source of íine particulate organic matter for detritivores. Studies of interphyletic interactions between tadpoles and other aquatic herbivores would also aid in examining this connection. Despite the comparatively great amount of work that has examined the relative imponance of interference and exploitation as competitive mechanisms in tadpoles, some good areas for investigation in these fields remain. Combining the quantitative genetic approach with ecological experiments
designed to separate interference and exploitation may lead to some insight into the evolution of these competitive mechanisms. The extreme competitive mechanism of carnivory or cannibalism, which often appears to be facultative in tadpoles, also should be looked at more extensively with quantitative genetic analysis. Interactions between tadpole behavior, inter- and intraspechc competition, and predation risk also have been explored only preliminariiy. I suspect the reader wiii have arrived independently at a iist of research needs that differs from mine. T h s should emphasize the fact that although much more is known about tadpole ecology in 1998 than was known in 1980, much more remains to be discovered.
ACKNOWLEDGMENTS I would Me to thank S. J. Richards for h s considerable assistance in reading and commenting on drafts of the manuscript and for access to h s comprehensive reprint collection. R. Altig and R. W. McDiarmid provided imrnense assistance in keeping up with developments in the field during the prolonged gestation of the book and made many invaluable editorial comments and corrections. I would also like to thank L. J. Alford and M. N. Hearnden for comments on the manuscript and my students K. S. Bradfield, M. R. Crossland, W. Martin, and M. I? Trenerry for discussions and access to their data. Support for my research was provided by several Australian Research Council grants, the Council of Nature Conservation Ministers, and the Cooperative Research Centre for Tropical Rainforest Ecology and Management.
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the evolutionary of interest is that the larvai stage . hypothesis .is where adaptations to maximize growth rate are expected. Evidence consistent with this hypothesis would include the presence of nonadditive genetic variation for growth rate &d a response to naturaiselection on genotype< that M e r in growth rate. Trade-offs between growth rate and other traits, such as competitive ability or antipredator mechanisms, might aiso be expected (Aiford 1986a, 1989a, b). If the gowth rate maximikon hypothesis is correct, selection has favored growth over other traits to the degree that any confia among fünctions exist. Rapid g r o d rate d o w s a tadpole to reach a sue refuge from many gape-limited predators and achieve a large body size at metamorphosis. Aiso, larvae quickly attain the minimum size needed for metamor~hosisand have the o ~ t i o n to metamorphose if the pond kgins to dry or if pre&on pressures increase. Body size at metamorphosis can be negatively correlated with age at first reproduction and positively correlated with sue at first reproduction (Berven and Giii 1983; D.C. Smith 1987). Thus, a high larvai growth rate is also of potential value in terrestrial survival, fecundity, mating success, and age at first reproduction. Predator avoidance and resistance to parasitism are other important traits that can be disassociated from growth rate and may be involved in phenotypic or genoment, the h o t h e s i s that direct development can facilitate' a phenotypic divergente between iife stages remains testable should suitable fossil material be found. The argument that a complex life cycle cannot be derived from direa development seems to be false as a general d e . Some members of the hemiphractine genus G ~ o t h e c aapparently evolved a complex life cycle from ancestors with direa development ( D u e h a n 1989; Wassersug and Duellman 1984). It is unclear ifa primitive complex life cycle reappeared or if the complex life cycle is in some way derived. If' ~ u e h a n ' phylogenetic s hypithesis is supported, it suggests that several pathways are possible in the evolution of anuran developmental modes. I stress that the suggestion of direa development being I
T H E ANURAN TADPOLE
a primitive feature of "protoanurans" is a hypothesis based
29 1
ponds ddfer in mean phenologies of primary productivity cannot be adequately addressed with current information. Predation pressuie on tadpoles rnay be less in recently filled ponds than in permanent ponds (Wilbur 1980,1987). Upon filling, a temporary pond rnay be a relatively predator-free environment. Fish wouid be absent, but saiamanders and other ~redatorsmight be important. In western " Virginia, newts (Notophthalmusvi&scens) migrate to srnd montane ponds in time to eat hatchlings of the wood frog (GLU1978, Rana sylvatica; personai observation). IndividuMaintenance of the Complex Life Cycle ais of a species of ~ i r e n(caudata: Sirenidae) emerged from food-rich aquatic habitat, a hgher probabiiity that free- a dried pond bed in the southeastern United States within living larvae wdl escape predation or parasitism better than two days of refiiiing (personaiobservation) and began eating embbos of direct deGelbping species, -and the increased op- tad~oles.Predaceous insects mav be scarce in a recentlv N e d portunity for kin selection in free-living larvae compared to temporary pond, but predators of s m d tadpoles, such as embryos in an egg mass can be associated with high larvai diving spiders, rnay colonize quickiy. Unless saiamanders growth and survivai and therefore might promote the reten- and insects are much less efficient Dredators than fish. it is tion of the larvai stage. It has been suggested that the mod- not clear that recently filled temporary ponds are characterem tadpole rnay be an adaptation to exploit abundant but ized by lower predation pressure than permanent ponds. ephemeral resources found in temporary pools (Wassersug More study is needed to compare predation on tadpoles and 1975; Wibur 1980; Wilbur and Colhs 1973). Indeed. the embryos in temporary ponds, permanent ponds, and terspecies diversity of anurans is higher in temporary ponds restriai habitats. If predation pressures vary systematically than in permanent ponds in the southeastern United States among temporary ponds, perrnanent ponds, and terrestriai (Wilbur 1987; personal observation). Free-living larvae rnay settings, then predation can be invoked as an evolutionary have enhanced survival in the presence of predators because factor that selects for larva1 habitat. Pond size is an important they can attain a size refüge f;om predat&-sand aiter their variable; extremely srnd temporary pools (e.g., the size of activity level to avoid detection by predators (Skeiiy 1990, cow hoof print) wiü not contain fish or salamanders but wiii 1991). Aithough the increased opportunity for kin selection retain waier long enough for some species of tadpoles to caused by behavior of tadpoles has not been suggested as a metamorphose (e.g., Gastrophiyne carolinensis and Physaluereason for the maintenance of a complex life cycle, behav- muspustulosus). ioral ada~tationswouid have the effect of increasing: the fitDirect development rnay be favored when predation or V ness of individuais or family groups that retain the complex parasitism is higher on free-livingtadpoles than on direct delife cycle. Kin selection aiso acts on antipredator responses velopers (Dueliman and Tmeb 1986; Lutz 1948; Magnusson and Hero 1991). Parentai care can interact with direct (chap. 9). Aithough some have asserted that temporary ponds pro- development to deter predation and lower the incidente of vide a flush of primary productivity as they fill and recently parasitism (McDiarmid 1978). Criticai data on these points faiien leaves and organic matter become saturated and re- are lacking and a need exists for fürther investigation. Direct lesse nutrients (Wassersug 1975; Wilbur and Collins 1973), development is more prevaient in the tropics and might be little limnologicai evidence supports their claim. Nutrients related to the intensity of aquatic predation. Average presurely are released upon pond fiiiing (Osborne and McLach- dation rates in temporary ponds in tropicai and temperate lan 1985); but the rate of that release, and the relationshp zones rnay be so different that a comparison wouid be between the release rate and ~rimarv~roductivitvavdable profitable.- Vermeij (1976) compared predation on gastroto tadpoles, is debatable. In faa, larvai resources might be at pods in the Pachc and Atlantic Oceans, and both prey and their highest level as the pond dries. At that time nutrients predators in the Pacific have evolved stronger defenses and become concentrated, and a flush of primary produaivity predatory abiiities, respectively. An increased opportunity for kin selection rnay favor the rnight occur. Before the hypothesis thai a cokpiex life cycle is an adaptation to exploit a flush in primary produaivity can retention of a complex life cycle. An individuai's inclusive be addressed criticdy, studies on the phenology of primary fitness is composed of its individual fitness and its effect on productivity and its avaiiabiiity to tadpoles in temporary the fitness of other related individuais (Hamilton 1964a). ponds are needed. Kin selection among embryos in a terrestriai egg rnass might Conversely, Wassersug (1975) argued that the larvai stage lead to the evolution of a communaiiy produced toxic subrnight be abandoned when ponds do not have a predictable stance. However, I argue that the opportunity for kin sein productivity. ~ r o ~ i ponds & l rnay lack a predictable leaion is greater among free-living tadpoles because the bepulse in productivity, and that rnay have been one selective haviorai repertoire is greater. Options such as schooling pressure for direct development in the tropics. Data on the behavior and release of aiarrn chemicais are not avaiiable to phenology of productivity of tropicai ponds aiso are l a c h g , ernbryos restricted to an egg mass. Enhanced behaviorai posso a meaningfui comparison with temperate ponds is impos- sibilities can increase an individuai's inclusive fitness by aisible at this time. The hypothesis that tropicai and temperate lowing individuais to aid related individuais. Kin selection on a sirnple genetic model (sensu Faiconer 1989) of the evohition of morphologicaiiy divergent life-history stages. A broad anaiysis of morphologicai transitions among a variety of metarnorphic and direct developing anurans is needed. Combining this anaiysis with a weii-supported phylogenetic scheme will be essentiai in resolving whether direct development is a primitive or derived trait in the Anura.
i l
i
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has played an important role in the larvai biology of many pended aigae. How resource concentration would interact species (chap. 9), and this rnay lead to an overali increase in with relative size of the filtering surfaces to affect size-specific fitness to the individual with a complex life cycle in environ- growth rate needs investigation. ments that aliow it. A comparison of size-specific growth rates of ranid tadComplex life cycles have been stable over long periods poles tends to support the hypothesis that a large body size of evolutionary time (Bolt 1977; Wassersug 1975). A theo- decreases the efficiency of suspension feeding. Werner reticai model by Istock (1967) suggested that such stability (1986) reviewed data for severai species of&na and found is unexpected, thus creating Istock's paradox. A critical as- that size-specific growth rates increase and then decrease sumption of Istock's model was that no genetic correlation over the larvai period. The decrease in growth rate as body exists between traits in both stages thereby allowing inde- size increases late in the larvai period is not associated with pendent evolution. This leads to the suggestion that stages the typicai depression in growth rate at metamorphosis. d differ consistently in rates of adaptation. Genotypes as- These data are consistent with a mechanistic explanation of sociated with a reduction or elimination of the less adapted decreasing efficiency of tadpole feeding as body size instage wiil be favored. The assurnption of genetic correlition creases and with the hypothesis that larvae (see above) d o has been evaiuated in only two studies with anurans (Blouin cate greater proportions of energy to development late in the 1992b; Emerson et ai. 1988) and is discussed below. Istock's larvai period. However, some species can grow exponenparadox can be resolved with the foliowing three explana- tially throughout their larvai period if resources are adequate tions: functionai constraints, fluctuating selection, and ge- (e.g., ALford and Harris 1988, Bufo woodhousiifwleri). Exponentiai growth implies a constant size-specific growth rate netic correlations. Functionai constraints of tadpole morphology and physi- throughout the larvai period (see eq. [I]). ology rnay lead inevitably to metamorphosis. Anuran tadUnder some ecologicai conditions, aquatic growth as a poles become less efficient feeders as they grow. Wassersug large larva, with its relatively smalier filtering surfaces, rnay (1975) argued that the surface area-to-volume ratio of the stili carry a higher fitness than metamorphosis to a terrestrial filtering surfaces of a tadpole decreases as biomass of the tad- stage at a smder size. This would select for paedomorphosis pole increases, and this creates less efficient feeding at in- or the relative lengthening of the larvai stage. An unfavorcreasing size. This ratio creates an upper limit to the size of able terrestrial environment would create such a selective rethe branchiai basket in tad~olesof ali s~ecies.In order to gime. More snidies that integrate the relationship of larvai overcome this constraint, evolution in the tadpole would size to filtering efficiency, assimilation percentage (Aitig and have to proceed via a peak shift (an ontogenetic change in McDearman 1975), metabolic costs of feeding, and specific trophic morphology and behavior tantamount to a meta- growth rates are needed. For example, tadpoles of species that metamorphose at a small body size (e.g., Bufo) apparmorphosis; S. Wright 1931). Morphological anaiyses provide an explanation for the ently can maintain a constant size-specific growth rate while decreasing trophic efficiency hypothesis. Oral trophic stmc- those of species that metamorphose at a large body size (e.g., tures show isometric growth or negative dometric growth Rana) cannot. Functionai constraints in the form of decreasing trophic with body size (Wassersug 1976a). In the latter case, feeding structures become relatively smder as the tadpole increases efficiency with increasing larvai body size can provjde a parin size. A positive allometsr of filtering surfaceand body size tiai resolution of Istock's paradox. The tadpole stage is would lead to a tadpole with an increasingly crowded body thought to be an adaptation to exploit ephemerai but favorcavity. Wassersug (1975) suggested that there rnay be an up- able growing conditions, aithough the isometry of filtering Der limit to the size of the branchiai basket: the branchiai surfaces to body size rnay lead to a slowing of further growth I baskets of large Pseudis paradoxa tadpoles are no larger in (Wassersug 1976a). Wassersug's argurnent leads to the sugabsolute terms than those of &na catesbeiana larvae. gestion that the adult stage wiil displace the larvai stage over Wassersug (1975) tested the hypothesis that large body evolutionary time because the rate of adaptation slows in the size decreases the relative size of the filtering surfaces and larval stage (i.e., larvae are as "adapted" as they can get bethus decreases feeding efficiency. He found that 12 smali cause of allometric constraints) but not in the adult stage. Ranapipiens tadpoles cleared their guts more rapidly than This resolution rests on the assumption that large size in a three large tadpoles of the same combined weight. Wasser- tadpole is always adaptive. The existente of species that typisug (1975) did not measure the metabolic costs of feeding caliy metamorphose at a smali size, such as Buf, suggests in small and large individuais. Large tadpoles rnay be less that metamorphosis at a smali body size can be an adaptaefficient feeders, but they rnay spend less energy feeding. If tion. Furthermore, the rate of larvai adaptation can proceed true, the net energy return per unit time rnay have been aiong numerous other axes, including the evolution of greater in the large tadpoles. Further experiments with a va- mechanisms of predator avoidance, increased competitive riety of species with the same and different feeding modes abdity, and digestive efficiency. need to be conducted to test W y the hypothesis. For exWassersug (1975) considered life-cycle evolution in diample, R. pipiens has keratinized mouthparts, which suggests chotomous terms: either the population retains or eliminates that the species rnay not function primarily as a fiiter feeder a stage. It seems more likely that selective pressures wiil op(R. Aitig, personal communication). Sede and Beckvar erate to increase or decrease the relative durations of a stage. (1980) and Sede and Wassersug (1979) showed that tad- If selection favored the larvai stage for a long period, two poles can adjust filtering rates to the concentration of sus- outcomes are conceivable. One would be the elimination of
THE ANURAN TADPOLE
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the adult stage (paedomorphosis). As Wassersug noted, this relation between lengths of the two stages is of interest. If would require a reworking of the tadpole body plan to make longevity is constant among individuais, then the length of space for eniarged gonads, to aiter amplexus or other mating larvai and adult stages necessarily are negatively correlated, behaviors, and to overcome a lack of emetic behavior that is but longevity in the larvai and adult stages might be posirequired for oviposition and sperm extmion (Naitoh et ai. tively geneticaiiy correlated. Individuals with longer larval 1989). Paedomorphic tadpoles may not be an evolutionary periods might aiso live longer after metamorphosis. If there possibility. This is a consequence of the high degree of diver- is no genetic correlation between length of larval stage and gente between life stages. The same phenomenon occurs in length of adult stage then persistent or fluctuating variation insects; the oniy truiy larvai reproduction in insects is asso- in length of larval period wdi have iittle effect on evolution ciated with par;henogenesis (H. F. Nijhout, personal com- in the adult stage and therefore persistence of a complex iife munication). Wassersug's question, "Why there are no pae- cycle. This has not been estimated in anurans, and its estimadomorphic tadpoles?" could be foliowed by the question, tion in a variety of species would be of interest. "Why are there no parthenogenetic tadpoles?" The occurrence of genetic correlations for Me-history The relative lengthening of the larvai stage, resulting in traits across stages provides a t h r d resolution of Istock's para single breeding period shortly after metamorphosis (e.g., adox. The possibility of antagonistic pleiotropy (M. J. Rose ephemeropteran insects; Istock 1984) is another possible 1982) could explain the maintenance of a complex Me cycle. evolutionary outcome of a highly adapted larvai stage. This If the genotype that codes for a complex of adaptive adult hypothesis could be tested by geographical comparisons. For traits does not code for the most favorable complex of adapexample, one might expect that populations that occupy fa- tive larvai traits, then genetic variation for those traits and vorable adult environments but consistentlv use IDoor larval the concornitant complex life cycle could be maintained. A environments should have a relativelv short larvai period. polymorphism would be achieved as two solutions come to Populations from the center of a geographical range may oc- an equilibrium: less adapted larvae and more adapted adults cupy equally favorable larval and adult habitats. Populations versus more adapted larvae and less adapted adults. If geat the edge of the range iikely exist in a poor larvai or poor netic correlations across life-history stages exist, it would be adult habitat. The goal would be to identi@ areas where the unlikely or impossible for one stage to evolve at a faster rate. environment was iimiting only on the larva or only on the This hypothesis could be tested with a conventionai quantiadult. A geographical comparison of the relative durations of tative genetic anaiysis, such as a haü-sib design that foliows larvai and adult periods would be of great interest. Indeed, tadpoles into adulthood and measures trait values for both Berven et ai. (1979) found that montane populations of stages (Faiconer 1989). Additive genetic correlations beRana clamitans have evidence of past selection for a shorter tween larvai and adult Me-history traits could be estimated larval period relative to lowland populations. The montane (e.g., Emerson et ai. 1988). Selection experiments on larvai ponds arguably are poorer larvai environments than lowland and adult traits with an assay for correlated selection reponds. The techniques of common garden (e.g., Berven sponses of larvai and adult traits aiso could be used. The long et ai. 1979) and reciprocal transplant experiments could be generation time of many anuran species would make selecemployed to test whether any observed differences have a tion experiments problematic. Species with generation times genetic basis. Because of the long generation times of an- of one year would be good candidates for a test of the antagurans, these experiments would be far more practicai than a onistic pleiotropy hypothesis. As argued above, anuran evoselection exper&ent. lution probably has been characterized by a genetic or develIstock (1984) postulated another resolution of Istock's opmental independence between stages. Such independence paradox: persistent genetic variation in length of larvai pe- would allow divergence of stages and would allow each stage riod could preserve a complex Me cycle. When ecological to adapt to different environments. If true, the antagonisfactors periodically favor lengthening the larvai period via tic pleiotropy hypothesis is unlikely to provide a resolution fluctuating selection, genetic variation for the length of the to Istock's paradox. Viability selection acts on the larval larvai period is maintained. If length of the adult stage is stage before viability selection or fecundity selection acts inversely related to length of the lakal stage, then such selec- on the adult. Whether this could create a differential rate of tion would concomitantly decrease the length of the adult adaptation in favor of the larval stage is unclear because stage. Fluctuating selection might aiter the relative lengths such difficult models have not been constructed (Hartl and of the two stanes. but neither stane would be eliminated if Clark 1989). the larval period were periodicaiiy favored. Fluctuating selection is one factor that leads to the maintenance of genetic Experimental Approaches to the Evolution variation (Hartl and Clark 1989), in this case for length - of of the Complex Life Cycle larval period. ~ h fluctuating-selection e explanation could be addressed Quantitative Genetics first by surveying populations for genetic variation for A central characteristic of the anuran complex Me cycle is a length of larval period. Such genetic variation has been phenotypic divergence between larval and postlarval stages. found in some populations (Berven 1987; Blouin 1992b; I have argued that uncorrelated developmental programs are Newman 1988b; P h c z et ai. 1984; Travis et ai. 1987). Sec- necessary for such divergence to have evolved. Support for ond. the assum~tion that the leneths of the larval and adult this hypothesis would be a quantitative genetic analysis that I periods are inversely related could be examined. Genetic cor- estimates no genetic correlations between a trait in the larval i
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stage and the same trait in the addt stage. An analysis of this kind has not been performed, although genetic correlations between larval iife-history traits and postlarval morphological traits have been estimated. Emerson et al. (1988) showed that time to metamorphosis and growth rate of larvae were not correlated with hind iimb shape of metamorphs, and Blouin (1992b) demonstrated that growth rate of larvae was not correlated with head width. These resdts suggest that larval life-history traits and postlarval hind limb traits are able to evolve independently. The generality of these resdts require further study. Estimations of the genetic correlation between values of the same trait in larval and postlarval stages are avenues for future study. One such trait is body shape in the tadpole and in the metamorph. For example, if selection is imposed for a narrower tadpole, will there also be a response to that selection in the postiarval stage? Lack of an additive genetic correlation wodd suggest that independent evolution is possible. Estimation of genetic correlations between traits in larval and postlarval salamanders wodd be an interesting companion study. I hypothesize that correlationsin salamanders wili be large, whde correlations in frogs will not be significant. If true, this wodd help to explain the far greater phenotypic divergence between stages in anurans. Lack of genetic correlations between stages wodd also explain why paedomorphosis is cornmon in caudates and not in anurans. The abiiity of a species to reproduce in a larval morphology (paedomorphosis) is inversely related to the degree of phenotypic divergence between stages. A lack of developmental flexibility (e.g., loss of possibility of paedomorphosis) has adverse macroevolutionary consequences (higher extinction rates) in benthic marine invertebrates (Valentine and Jablonski 1983). Such a pattern is unsnidied in anurans.
ceiis in a variety of species and assaying their fates across metamorphosis wodd be of great interest.
Summary
The complex iife cycle of anurans is characterized by a phenotypic divergence between larval and postlarval stages. Selection for specialization of one stage in protoanurans may have been accompanied by seleaion for uncoupling of traits in the other stage. Genetic and developmentalindependente is expected between stages that d o w independent evolution.-~irectdevelopmen; may have facilitated the origin of a divergent complex life cycle by dowing greater initial addt specialization. The divergent larval stage (tadpole) seems to be specialized for growth. Adaptations that promote rapid growth and provide an optirnal timing of metamorphosis are expected and have been examined by many workers. The evolutionary stability of a complex life cycle has been questioned (Istock 1967), and several solutions have been discussed. Once highly divergent life cycles evolve, elimination of the addt stage may be impossible without parthenogenesis. A parthenÕgene;ic solu6on has been exiloited by insect groups (H. F. Nijhout, personal cornrnunication) but not by anurans. However, the relative lengths of the anuran larva17andaddt stages can be adjusted. In Gurans, the length of larval period is under genetic control, but genetic control of addt longevity is unknown. By i d e n e i n g larval and addt environments that d a e r in auaiitv. it shodd be DOSsible to test the hypothesis that le&h &f larval has been adjusted accordingly. For example, a consistentiy lush larval habitat surrounded by a harsh terrestrial environment wodd select for ~aedomorbhosisin saiamanders but codd select for a long?arval period and short addt iife span in frogs. Further work is needed in several areas. Mor~hometric and phylogenetic anaiyses are needed in a variety of species An aiternative to the quantitative genetic methodology is to assess phenotypic correlations of traits across metamorrooted in descriptive histology and developmental biology. phosis. The case of Leiopelma is of particular interest in that Using this approach, Aiberch (1987) identiíied two devel- it is unclear if the earlysize-shape kajectory of the embryo opmental pathways that led to the formation of the larval resembles a tadpole (fig. 11.2D), an ancestral salamanderand postlarval epibranchial in the saiamander Eulycea. The like larva (fig. 11.2C), or neither (fig. 11.2B). Quantitative unique formation of the epibranchial cartilage during the genetic analises coupled with ecoGgical information are embryonic and larval periods is a primitive pattern. During invaiuable for testing hypotheses about current seleaion metamorphosis, larval chondrocytes can undergo ceii death on anurans. Such analyses aiso can test the hypothesis that or remain static. The compartmentalization of the precur- tad~oieand addt traits are eeneticdv uncorrelated. Develsors to larval chondrocytes (neural crest cells) into prospec- opmental biology wili become increasingly important in tive larval and addt ceiis is the derived pattern. Whde some addressing the general issue of uncoupling of iife-history neural crest ceiis differentiate into the larval epibranchial, stages (Alberch 1987). The combination of morphological, others remain quiescent. At metamorphosis, undifferenti- ge&ic, ecological, developmental, and phylo&netic apated cells develop into the postlarval epibranchial and the proaches surely wdi clarie our understanding of iife-history larval chondrocytes die. The derived compartmentalized de- evolution in anurans. velopment d o w s for independent evolution of larval and postlarval stages. Anurans also are expected to have compartmentalized de- ACKNOWLEDGMENTS velopmental programs (Aiberch 1987). The greater &ver- I thank R. Aiford, J. Hanken, S. Marks, and G. Wyngaard gence between stages in anurans perhaps is explained by a for helpful comments on the manuscript. James Madison greater number of compartmentalized developmemai path- University provided me with a research leave during which ways. A research program involving the marking of larval I developed the ideas presented in this chapter. V
DIVERSITY Farnilial and Generic Characterizations Ronald Altig and Roy W. McDiarmid
Tadpoles are ". . . highly specialized, and seerningly unlimited variation shows iittle organization on preiiminary study." Orton 1953:68
Introduction Orton (1953) clearly recognized the impedirnents that commoniy are encounteied w k n attemptGg to i d e n t q anuran tadpoles. If it were oniy the inherent morphologicai traits characteristic of the larvae of different species that were holding back our understanding of tadpole diversity, we would have made considerable progress over the past 45 years. Unfortunately, the tadpoles of many species remain to be identified, and we have oniy meager understanding of the nature of ontogenetic, geographic, &d metamorphc~variation(e.g., Cei and Crespo 1982; Goiiman and Goiiman 1991, 1995, 1996; Inger 1966; Korky and Webb 1996; L a d a 1984b; J. M. Savage 1960). Our abiiity to recognize and identq new forms progressively improves with each description, but many factors, including a chronic lack of detail in many descnptions, inadequate collections, and too few workers, harnper progress. Intangible insights come from looking at manY tad~olesof many s~ecies,and through such exPosure one begins to develop an understanding of their morphologicai diversity. Having a readily available surnmary of the known morphological diversity of tadpoles aiso would be beneficiai. At times, interspecific variation seems to be slight or absent; whether such Gariation simply is not recogni&d (e.g., Bufo)or poorly understood (many taxa) remains to be shown. Phenotypic plasticity, especiaüy of pigmentation and fin shape, is confusing. Conspecific tadpoles collected from turbid versus clear water vary tremendously in color, and cultured tadpoles often have aberrant mouthparts compared to wiid-caught individuais of the same species. Tadpoles of the same siecies may dXer in shape in Still versus flowing water (R. D. Jennings and Scott 1993; Van Dijk 1966), and ontogenetic changes in color and oral morphology are occasionaüy profound. Improper fixation and storage (chap. 2) tend to complicate aü other issues. Examination of the smaü, complex oral apparatus of a tadpole provides the major characteristics for species identifications but often is fmtrating. The discovery of a simple method for properly preserving a tadpole with its oral disc wide open and without distortion would facilitate consistent observations and be a major advance. In s ~ i t eof manv tzains. we stiü find ourselves in the realm of k e "prelimk& studyn mentioned by Orton (1953). Because research on tadpoles is increasing rapidly, the need for properly identified tadpoles is becoming more common. Researchers are reaiizing that sampling tadpoles usuaüy is an efficient, viable means of assessing local biodiversi+. Tadpoles are present in aquatic hab:itats for longer periods than breeding adults and are often more easily collected. H . B. ShafFer et ai. (1994) presented useful ideas in
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this regard, but Wassersug (1997b) raised some interesting counterpoints. The importance of understanding ontogenetic variation and patterns of development has been aiscussed previously (chaps. 2 and 3), and-the need for colleaions of ontogenetic series is even more apparent. Developmental data provided an understanding of the differences between the duai lateral spiracles of pipids and rhinophrynids and those of Lepidobatvachus (Leptodactylidae; Ruibai and Thomas 1988; see Nieuwkoop and Sutasurya 1976). Even so, morphologicai data of tadpoles have seldom been gathered or examined to answer question about character homology. The use of larvai data in systematic studies has been debated, and tadpole features have been used to various degrees (e.g., Diaz and Valencia 1985; Donneliy et ai. 1990a; Dueiiman and Trueb 1983; I. GriíKths 1963; I. GriíKths and De Carvalho 1965; Inger 1967; Kluge 1988; Kluge and Farris 1969; Kluge and Strauss 1985; Noble 1926b; 0 . M. Sokol1975; Starrett 1973; Yang 1991). Disagreements relative to the use of tadpole characters in systematic analyzes seemingly resuit from incomplete understanding of charaaer states and their distributions arnong taxa (e.g., Wassersug 1989b). When appropriate traits have been investigated, issues relative to character homology, functional capacities, and both geographic and ontogenetic variations can ofien be confronted. We reviewed the morphologicai diversity of tadpoles in chapter 3, and Harris discussed the evolution of the tadpole as ;life-history stage in chapter 11. In this chapter we &marize the known larvai morphology of pertinent taxa, and discuss the limitations of current knowledge. Two data sets are needed before meaninfl advances in understandmg the interactions of tadpole ecomorphology and phylogeny can be made. We must have a more detailed phylogeny of the farnilies and genera of anuran amphibians and a better understanding 6f the origin and m~;~hology of the primitive tadpole (see chaps. 4 and 11). Once this has been achieved, we shouid be able to examine the distribution of larvai traits amonp: " the severai clades of modern anurans and s~eculate on their evolution. The moduiators of growth and metamorphosis and their combined effects on tadpole ecology (e.g., Wiibur and Collins 1973) need to be considered, as do minute differences in developmentai patterns, if we are to expand the current notions of character homology and better understand the evolution of larva1 traits. We must be able reiiablv to distineuish between those features that are more " labiie in response to ecologicai pressures (i.e., result in ecomorphologicai convergences among lineages) and those that hold reliable phylogenetic information. For example, morphology of the chondrocranium (chap. 4 and citations therein), position of the front iimbs relative to the buccopharyngeai structures (Starrett 1973), and patterns of formation and position of the spiracle(s) might be expeaed to carry strong phylogenetic signai, whiie certain features of the oral apparatus more likely reflect ecologically pertinent seleaion. In the same light, the distribution of some oral features among lineages-seems to indicate lineage-specific constraints. From our perspective the majority of tadpoles fall within
boundaries that typicdy coincide with the phylogenetic patterns derived from aduit frogs, but the extremes in ecologicai and morphologicai diversity among anuran larvae (figs. 12.1-12.2) seem truiy astounding. Some of this diversity is captured in the composite of microhabitats and morphoTable 12.1 Guide to select literature on tadpole faunas and regional treatments of groups. Referentes with keys are indicated with asterisks. Europe General: Boulenger 1892*, E. N. Arnold and Burton 1985*, Nollert and Nollert 1992*, Berninghausen 1997" Austria: Grillitsch et al. 1983*, Lower Austria Belgium: De Witte 1948* France: Ame1 1946* Germany: gerninghausen 1994*, Brauer 1961*, Engermann et al. 1993" Italy: Lanza 1983* Portugal: Serra and Aibuguerque 1963* Russia: Terent'ev and Chernov 1965" Spain: Salvador 1985+ Turkey: Basoglu and Ozeti 1973 Africa East f i c a : Schiotz 1975, hyperoliids South Africa: Van Dijk 1966*, Wager 1986 West Africa: Rode1 1996, Schiotz 1967, hyperoliids Cameroon: Mertens 1938 Madagascar: Blommers-Sdilosserand Blanc 1991, Glaw and Vences 1992* Natal: Lambiris 1988aX,b* Zimbabwe: Lambiris 1989* Asia Southeast Asia; Bourret 1942* Borneo: Inger 1966*, 1985* China: C.-C. Liu 1940, 1950 Japan: Okada 1931, Maeda and Matsui 1989 Java: Schijfsma 1932 Malaysia: Berry 1972 Pakistan: Khan 1982aX Philippines: Inger 1954 Russia: Terent'ev and Chemov 1965* Taiwan: Chou and L i 1997" Thailand: M. A. Smith 1916a, 1917 Australia/New Guinea Australia: Watson and Martin 1973, Tyler 1989*; Queensland: Retallick and Hero 1988*, rainforest streams in one area North America Canada: Orton 1952*, genera, Aitig 1970*; British Columbia: Corkran and Thoms 1996"; Aiberta: A. P. Russell and Bauer 1993" United States: Orton 1952*, genera, Aitig 1970", Wright 1929*; Eastern United States: A. H. Wright and Wright 1949*; Florida: Fanning 1966*, Stevenson 1976*; Louisiana: Siekmann 1949*; North Carolina: Travis 1981ar; Oregon: Corkran and Thoms 1996"; Washington: Corkran and Thoms 1996* Middle America General: Dueilman 1970, hylids Costa Rica: J. M. Savage 1968*, dendrobatids; 1980ar, Lips and Savage 1996" Honduras: L. D. Wiison and McCranie 1993* Mexico: Aitig and Brandon 1971", genera, Aitig 1987" Panama: J. M. Savage 1968*, dendrobatids South America Argentina: Cei 1980, 1987; Kehr and Wfiarns 1990 Brazil: Hero 1990*, Manaus; Heyer et al. 1990, Boracéia Chile: Cei 1962 Ecuador: Dueilman 1978*, Santa Cecilia/üpper Arnazon Basin
DIVERSITY
types depicted in figures 9.2-9.3. The charaaerization of t-adpolesb y taxa pre&entedin ths chapter pinpoints some of the a c u l t i e s associated with species identifications, iilustrates gaps in the data, provides a point of departure, and lists ~ertinentreferences to im~rovethe likelihood of IDroDer I identiíication. In our experience, larval morphology is often concordant with accepted systematic treatments (e.g., Bufo vevaguensis, Hylu leucophyllata, and H. pam'ceps groups) and in other instances likely signals the need for adjustment (e.g., species in the Scinm vostrata group and Scarchyla). The literature that has proven useíüi for identiíication of tadpoles generaliy is scattered. In this chapter we review the sources of major keys and other large works that include considerable tadpole dormation (table 12.1). As we have noted previously, makmg correa identifications of tadpoles often is a c u l t . In table 12.2, we list citations that correctiy ident* previously misidentiíied tadpoles and in table 12.3 we provide identifications and references to tadpoles that were described orinindv without a name. Mouth~artsof tadpoles are admit;dly Ldd l o o h g structures without an obvious orientation, and they are sometimes printed upside down; known examples include Pseudis pavahxa (Dixon et al. 1995);Hylazeteki (Duehan 1970);Bufó bufo, Kaloula m&2eva, and Rana japonica (C.-C. Liu 1940); and Mimobatrmhella sp. (Wager 1986). The tadpole described as Centrolem bucklevi bv Rada de Martinez (1990) either is misidentified or deviates strongly (e.g., complete marginal papiilae and many more than 213 tooth rows) from the conservative centrolenid morphotype; her description of Scinm rostrata also seems in error. The primitive tadpole presurnably was some sort of benthic inhabitant of a pond-type environment, perhaps ephemeral in nature. It likely fed by rasping food materials from submerged surfaces with keratinized mouthparts. Bogart (1981)and others have presented alternative ideas (see chap. 11). As previously noted, suggestions regarding the evolution of specific characteristics among anuran larvae are rare and usudy weakly defined. Given the state of knowledge, the concepts of ecomorphological g d d s (Altig and Johnston 1989) or similar designations of ecologicdy hnctional larval groups (Van Dijk 1972) at the moment appear to be the best summaries of morphological diversity among lineages. 2
,
Familial and Generic Characterizations
297
Table 12.2 Identiíications of previously misidentified tadpoles. Names are arranged alphabeticdy by initial genus and species. Original Identification Citation
Bufo campons Korky and Webb 1973 Chinjcalw vittatus Pope 1931 Chimmantisnrfeswns Guibé and Lamotte 1958 Colostethushaydeeae Rivero 1976 Colostethw subpunctatus Cei and Roig 1961 Gephyromuntis methueni Razariheiisoa 1973b HetenXdus amoulti Razarihelisoa 1979 H-vhloyuaxa Duellman 1970 Hyh siopeh Caldweii 1974 Hyh sp. Stuart 1948 Hyperoliuspicturatus Ai111931 Kivsina sengaiensis Lamotte and Zuber-Vogeli 1956 Leptobrachium hmelti Wassersug 1980 Leptobrachiumgracili~raciliP Inger 1966 Mantuúictylus alutus Arnoult and Razarihelisoa 1967 Manttdactylus brevipalmatus Razarihelisoa 1973a Mantidaqlus ulce-rosus Razariheiisoa 1969 Nyctimystes montana H. W. Parker 1936 ?-Tvmmmystes duyi Czechura et al. 1987 Microhyh bmeensis H. W. Parker 1934 Otophlyne robusta Wassersug and Pyburn 1987 Paratelmatobiw lutzi Heyer 1976b
Understanding the diversity of tadpole morphology (figs. Phiíuutus vanadilU 12.1-12.2; also see chaps. 2 and 3) is a requisite of successfül Annandale 1919 identiiications. Appreciating how those morphologies are Pseudami brachyphona Green 1938 distributed across taxa and which tad~oleshave been described in each group also is invaluable. Because of gaps in Ptmhylafodiens D u e h a n 1970 our knowledge and the general conservativeness of tadpoles, Ptychadena oxyrhyachw some tad~olesare more difficult to characterize. and therePower 1927b fore idem+, than others. These obstacles may be at the ge- Rana hosii Van Kampen 1923 neric (e.g., ali centrolenids, most dendrobatids, Hyla vs. Osteocephalus, Scaphwpus vs. Spea) or specific levels of organi- Rana [= Limnonectes] macrodon zation (e.g., species of Bufo and the Ranapipiens complex, Flower 1899 HlLLis 1982; Scott and Jennings 1985; Wassersug 1976~).
Corrected Identification Citation
Bufo mucromistatus Mendelson 1997 ChinXal1*rdonae Heyer 1971 Phlyctr'mantU ieonardi Schietz 1975 HyhpWdaqh La Marca 1985 Colostethussemiguttata J. Faivovich, personal communication Manttdactylus bicaisuratus Blommers-Schiosser and Blanc 1991 HeteruCdus betsileo Blommers-Schlosser 1982 Unidentified Rana R. Altig, personal observation Hyh whta Toal and Mendelson 1995 Piemhvh teuchestes ~ u e h a and n Campbeii 1992 Rana albolab* Schietz 1967 Kivsina macuhta Schietz 1967 Leptobrachium hendhcbsonii Inger 1983 Leptobrachella mjobergi Inger 1983 Heterklw betsibo Blommers-Schiosser 1979a Mantdmtylw aenrmnalir Blommers-Schiosser and Blanc 1991 Manttdactylw curtus Blommers-Schiosser 1979a Nym'mystes cheesmanae Davies and Richards 1990 Litoria nyakaiensis S. J. Richard~1992 Kalophlynus sp. Inger 1966 0tophynepyburn.i Campbeii and Clarke 1998 Unknown W. R. Heyer, personal communication Nyctib&acbuspygraciliPmaeus Piüai 1978 Probably Ranapipiens R Altig, personal observation Rana@eri R. Altig, personai obse~ation Ptychadena anchietae Van Dijk 1966 Unknown Inger 1966 Unknown Inger 1966 (continued)
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RONALD ALTIG A N D ROY W. M c D I A R M I D
Table 12.2 wntinued
Rana [= Limnanectes]w o d a n Inger 1956 Rana microdiscapalavanensis Inger 1956 Rana nicobariensis M. A. Smith 1930 Ranapleske6 Annandale 1917 Rena vertebral& Hewitt 1927 Rhacophorzls leucomystm Inger 1956 Staurois natatm Mocquard 1890 Staurois latopalmatus Inger 1966 Rhqhoncs bimacuiuta Inger 1985
Limnanectes microdisca Inger 1966 Limrumectesparamuçrodon Inger 1966 Unknown Inger 1966 Perhaps Scutiger naumnauta Boulenger 1919 Rana umbraculata Van Dijk 1966 Polypedutes m m ~ Inger 1966 Unknown Inger 1966 R h q h w w bimaculatus Inger 1985 Rhqhwusgauni Inger and Tan 1990
aSeeJ. C. Lee 1996 for correct description. bToothiess. 'See C.-C. Liu 1950. Table 12.3 Identiíication of tadpoles originaliy described without a name. Names and citation are presented in alphabetical order by initial genus and species. Original Identification Citation
Corrected Identification Citation
Amo@ sp. A Inger 1966 Amo@ sp. B Inger 1966 Rhqhorus sp. B Inger 1966 Unknown Pyburn 1980 Unknown hylid Stuart 1948 Unknown E. H. Taylor 1942 Unknown Inger and Wassersug 1990
Merktgenysphaeomms Inger and Gritis 1983 Me&o~enyspoecilus Inger and Gritis 1983 Rana luctuosa Inger 1985 Otophynepybumi Wassersug and Pyburn 1987 Rana maculata Hiiüs and De Sá 1988 Rhinophrynw h a l & Orton 1943 Staurolc natatm Inger and Tan 1990
The apparent lack of daerentiating characteristics among species in some genera or inadequate study of certain groups sometimes forces workers to key tadpoles oniy to the species rank. In ths regard considerable work is needed on enigmatic taxa such as Buf, aii centrolenids and dendrobatids, Leptod&us, some ranids, and Telmatobius. Attempts to diagnose larvae above the species level with morphologicai
(e.g., Lavilla 1985, 1988) or anatomical (e.g., Viertel 1982) data are uncommon, and ecomorphological gurlds (Altig and Johnston 1989) do not reflect phylogenetic relationIn ths chapter we provide the first summary of familiai and generic characterizations of tadpoles based on a common terminology. The taxonomic arrangement of D. R. Frost (1985), updated through 1996, was foiiowed and includes most of the ranoid arrangement proposed by Dubois (1987,1992; see comments by Inger 1996). Representative, but usuaiiy not exhaustive, citatiois concerning each genus are provided. Subfamiiies are included primariiy to separate groups of genera. The Gosner system (1960) of staging was used throughout. Afier each f d y , the number of genera and species, geographic range, major ecomorphologicaidivisions of Aitig and Johnston (1989), and other characteristics are given; for mono~eneric farnilies or subfamiiies. the com~arabled o r " mation is presented only under the higher category. Character states common to aii genera within a famiiy or subfamiiy are not repeated at the generic level. The state of a character for whichdata are lack&p: " is indicated with a dash. Mor~hological traits are given only for exotrophic (i.e., feeding; see chap. 7 for endotrophic forms) forms; genera, aii of whose species are entirely endotrophic, are included oniy to provide a complete listing (see aiso chap. 7). Character abbreviations used in the compiiation are'CO, COmposition (famiiy/subfdy: number of genera/number of species; genus: number of species); GR, Geographic Range; EMG, EcoMorphological Guild; LTRP, Labial Tooth Row Formula (see chap. 3; ontogenetic and other variations not included); OA, Oral Apparatus (typicai oral disc with labial teeth and jaw sheaths regardless of coníigurations: position descriptor); MP, Marginal Papiilae (distribution: arrangement); SUP, SUbmarginal Papiilae; DEM, Disc Emargination; NA, Nares; VT, Vent Tube; EP, Eye Position; SP, Spiracle; UJ, Upper Jaw sheath (width notation, descriptor of shape of serrated edge); LJ, Lower Jaw sheath (width notation, descriptor of shape of serrated edge); DP, Dorsai Fin (general height descriptor, anterior site of origin, tip descriptor); BS, Body Shape (dorsai view/ lateral view); CP, Color and Pattern; TL, Total Length/ Stage; NO, Notes; and CI, Citation(s). Generalized drawingi of representative morphotypes appear immediately before the pertinent taxon, and data on the specimens used in the preparation of these drawings foiiow.
Fig. 12.1. Representative body shapes and fin configurations among anuran tadpoles. (A) Ranupalmipes (Ranidae, dasping). (B) Mgophys m t a n u (Megophryidae, neustonic). ( C )S c i m mbulosa (Hylidae, nektonic). ( D )Hyh vimduris (Hyiidae, suctorial). (E) Atclopw &nesm (Bufonidae, gaswmyzophorous). (F) Coiustcth nubicoh (Dendrobatidae, neustonic). ( G )Thmopapmopolitana (Leptodactylidae,semitemesmal). (H) LeptopclU byluih (Hyperoiiidae, benthic). (I) Hyh b?vmeliaiu (Hyiidae, arboreal Type 1. (J) Gashvphynecuwli& (Microhyiidae, suspension feeder). (K) Hyh nrinocephala (Hyiidae, macrophagous). ( L )Oudmy~aLISrna(Ranidae, macrophagous). (M) Hyh li& (Hylidae, suctorial). (N) DucUinamclyh ummchvoa (Hylidae, adherent). (0)CochvamUap$thsi (Centrolenidae, fossoriai) ( P ) Anotheaí pinosa (Hylidae, arboreai Type 2). (Q) Cmaqhrys m u t a (Leptodactyiidae, camivorous Type 1). (R) Sttphop&amclr (Bufonidae, arboreai Type 3). From Altig and Johnston (1989), after Dueiiman and Tmeb (1986); original drawings by and Tmeb. L i d a Tmeb. Reprinted by permission of HevpetoIo~gicalMm~raphs
Fig. 12.2. Representative configurations of the oral apparatus among anuran tadpoles. (A) Ranapulrn* (Ranidae, dasping), (B)Megopby muntuna (Megophryidae, neustonic), (C) Hyla riarlarLr (Hylidae, suctorial), (D)Atehpa & n e s m (Bufonidae, gastromyzophorous), (E) Hyla micmcephaia (Hylidae, macrophagous), (F) Cem&phtys m u t a (Leptodactylidae, camivorous Type l), (G) Hyla l i h (Hylidae, suctorial), and (H) DueUmumbh uranucbroa (Hylidae, adherent). From Altig and Johnston (1989) after D u e b a n and Trueb (1986); original drawings by L i d a Trueb. Reprinted by permission of H"pctob@ulMmpphs and Trueb.
DIVERSITY
301
ALLOPHRYNIDAE: CO: 111. GR: Guyana-Brazil. Tadpole unknown. Allophvyne: CO: 1.GR: Guyana-Brazil. Tadpole unknown. ARTHROLEPTIDAE: CO: 6/77. GR: sub-Saharan Africa. EMG: exotroph: lotic: adherent, neutonic, suaorial; lentic: benthic; endotroph. LTRF: several variations between 010 and 9/11. OA: typical: anteroventral, terminal, umbeiiiform. MP: absent, medium to wide dorsal gap, complete: uni- and muitiserial. SUP: absent, single row distal on lower labium, oblong papdae arranged radidy to mouth. DEM: absent, lateral. NA: nearer snout than eye. VT: medial. EP: dorsal, lateral. SP: sinistral. UJ: wide, smooth arc to V-shaped, sometimes serrations coarse and medial ones may be enlarged. LJ: similar to upper sheath. DF: low, originates on taii muscle posterior to the dorsai tail-bodyjunction, tip round to pointed. BS: oval to elongate/depressed. CP: uniformly dark to mottied. TL: 29-80136. Arthroleptinae: CO: 2/52. GR: sub-Saharan Africa. Arthroleptis: CO: 35. GR: sub-Saharan Africa. EMG: endotroph. Cardwglossa: CO: 17. GR: westem Africa. EMG: exotroph: lentic: benthic. LTRF: 010. OA: typicai: anteroventral. MP: wide dorsal gap: uniserial, long and widely spaced ventrdy. SUP: single row distal on lower labium. DEM: absent. NA: s m d , nearer snout than eye. VT: mediai. EP: dorsal. SP: sinistral. UJ: wide, smooth arc, coarsely serrate. LJ: wide, coarsely serrate. DF: low, tip rounded. BS: oblong/depressed. CP: unifonnly dark. TL: 29/36. NO: ventral íin originates on tad muscle. CI: Lamotte (1961). Astylosterninae: CO: 4/25. GR: western Africa. Astylostemus: CO: 12. GR: Sierra Leone-Zaire. EMG: exotroph: lotic: adherent. LTRF: 011, 3(2-3)/3(1-2). OA: typical: aimost terminal, anteroventral. MP: medium to wide dorsal gap: uniserial. SUP: row distai to distal most lower row. DEM: lateral, absent. NA: nearer snout than eye, s m d medial tubercle at margin. VT: dextral. EP: lateral. SP: sinistral. UJ: narrow to wide, smooth arc with single large, medial serration. LJ: exceptiondy wide, V-shaped, coarsely serrate. DF: low, tip pointed. BS: oblonddepressed. CP: uniformiy dark. TL: 80137. NO: ventral íin originates posterior to origin of dorsal fin; body with lateral sacs of variou degrees of development, function unknown (Arniet 1970, 1971). CI: Amiet (1971); Lamotte and Zuber-Vogeli (1954b). Leptoahctylodon: CO: 11. GR: Cameroon-Nigeria. EMG: exotroph: lotic: neustonic. LTRF: 010, but with ridges that suggest a 011-2 arrangement. OA: typical: umbeiiiform. MP: absent, margin crudely crenuiate. SUP: oblong papiiiae arranged radidy to mouth and scattered throughout disc. DEM: absent. NA: smd, about equidistant between snout and eye. VT: dextral. EP: lateral. SP: sinistrai. UJ: massive, d serrations large, especidy laterdy. LJ: massive, similar to upper sheath. DF: tip rounded. BS: ovai/depressed. CP: uniformly dark, mottied on tail. TL: 50136. NO: a tooth ridge-like ridge occws immediately distai to the lower jaw sheath; body with lateral sacs of various degrees of development, function unknown (Amiet 1970, 1971). CI: Amiet (1970). Scotobíefs: CO: 1. GR: Nigeria-Gabon. Tadpole unknown; see Lawson (1993). Trichobatrachus: CO: 1. GR: Nigeria-Equatorial Guinea. EMG: exotroph: lotic: suctorial. LTRF: 9(7-9)/11(1-2). OA: typical: ventral. MP: complete: rnultiserial. SUP: absent. DEM: lateral. NA: equidistant between eye and snout. VT: dextral. EP: dorsal. SP: sinistral. UJ: medium, strongly V-shaped. LJ: medium, V-shaped. DF: tip rounded. BS: oblongldepressed. CP: uniformly dark. TL: 91/36. NO: large subbranchial muscle along anterior two-thirds of body gives ventral sdhouette a distinctive shape; body with lateral sacs of variou degrees of development, h c t i o n unknown (Amiet 1970, 1971). CI: Mertens (1938). ASCAPHIDAE: CO: 111. GR: northwestern United States-adjacent Canada. EMG: exotroph: lotic: suaorial. LTRF: 2-319-ll(1). OA: typical: suctorial. MP: wide dorsal gap, but anterior lip fleshy and crenuiate: uniserial. SUP: muitiserial distal to distaimost lower row. DEM: absent but folds present. NA: nearer eye than snout, prominent tubuiar extensions. VT: medial. EP: dorsal. SP: midventral on chest, no dorsal w d . UJ: large, platelike lying aimost pardel with substrate, sometimes with medial break. LJ: minute, U-shaped. DF: low, originates at dorsal taii-body junction, tip broadly rounded. BS: ovalJdepressed. CP: rockiike mottling, tad tip typicdy white bordered by black. TL: 60136. NO: prominent s m d skm glands present ventrdy; LTRF A-1 and most distal posterior row rnultiserial.
Trichobatrachus
Ascaphus
RONALD ALTIG AND ROY W. McDIARMID
RFcaphus: CO: 1. GR: northwestern United States-adjacent Canada. CI: Altig (1970); H. A. Brown (1990a); Metter (1964, 1967); Stebbins (1985).
Bombina
BOMBINATORIDAE: CO: 218. GR: Eurasia-Philippines-Borneo Barboumh: CO: 2. GR: Philippines-Borneo. EMG: Tadpole unknown, perhaps endotrophic. Bombina: CO: 6. GR: Eurasia. EMG: exotroph: lentic: benthic. LTRP: 2/3[1], biserial. OA: typical: anteroventral. MP: complete: uniserial. SUP: row ventrolateraiiy. DEM: lateral. NA: nearer eye than snout. VT: medial. EP: dorsal. SP: low on left side. UJ: medium, straight area mediaiiy, coarsely serrate. LJ: narrow, V-shaped, coarsely serrate. DE: low, originates near dorsal taii-body junction, tip rounded. BS: oval/depressed. CP: melanophores form network pattern in skin. TL: 30-38136 CI: Boulenger (1892); Lanza (1983). BRACHYCEPHALIDAE: CO: 214. GR: Brazil. EMG: endotroph. Br1u:h~ephalus: CO: 2. GR: Brazil. EMG: endotroph. Psyllophlyne: CO: 2. GR: Brazil. EMG: endotroph.
Ansonia
BUFONIDAE: CO: 331381. GR: widespread except Australia. EMG: exotroph: lentic: benthic; lotic: benthic, suaorial, gastromyzophorous; endotroph. LTRF: 2/3,2(2)/3, 2(2)/ 3(1), 2(2)/2. OA: typical: anteroventral, rarely ventral and suaorial. MP: wide dorsal and ventral gaps, complete: uni- and biserial, wide dorsal gap only. DEM: lateral, absent. NA: often large, often not round and with mediai papilla, sometimes smaii and rounded, doser to eye than snout or reverse. VT: mediai, dextral. EP: dorsal. SP: sinistral. UJ: usuaiiy narrow and broadly arched. LJ: usuaiiy narrow and broadly V-shaped. DE: low, originates near or posterior to dorsal td-body junction, tip round to slightly pointed. BS: oval to roundldepressed. CP: typicaiiy uniformiy black; td muscle sometimes bicolored or banded. TL: 1540136. Ahiphlynoides: CO: 1. GR: Ethiopia. EMG: endotroph. Andinophlyne: CO: 3. GR: Ecuador-Colombia. EMG: endotroph. Ansonia: CO: 19. GR: India-Borneo-Philippines. EMG: exotroph: lotic: clasping, suctorial, gastromyzophorous. LTRP: 213. OA: typical: ventral. MP: smaii, with medium to wide dorsal gap, complete: uniserial. SUP: row(s) distal to P-3, few lateraiiy. DEM: lateral, absent. NA: smaii, nearer eyes than snout. VT: medial. EP: dorsal. SP: sinistral. UJ: narrow to medium, divided, absent. LJ:narrow, very open V-shaped. DE: low, originates on t d muscle or near dorsal taii-body junction, tip bluntiy pointed. BS: ovalldepressed. CP: uniformiy dark, with rniddorsal stripe. TL: 18-35/36. NO: large variations in oral morphology within genus; anterolaterai terrninus of abdominal sucker of A. "sucker" of Inger (1992a) has fingerlike projection. CI: Inger (1966, 1985, 1992a). Atelophlyniscus: CO: 1. GR: Honduras. EMG: exotroph: lotic: gastromyzophorous. LTRP: 213. OA: typid: ventral. MP: wide dorsal and smaiier ventral gaps: uniserial ventraiiy, biserial dorsally. SUP: few anterolateraiiy. DEM: absent. NA: s m d , nearer eye than snout. VT: medial, not attached to ventral fin. EP: dorsai. SP: sinistral. UJ: narrow, without serrations, V-shaped. LJ: narrow, V-shaped. DF: low, originates slightly posterior to dorsal taii-body junction, tip rounded. BS: oval to round/depressed. CP: black t d muscle boldly banded; other white marks on body. TL: 26/37. NO: ventral fin originates on t d muscle; resembles tadpoles ofAtelupus. CI: McCranie et al. (1989). Atelopus: CO: 50. GR: Costa Rica-Bolivia. EMG: exotroph: lotic: gastromyzophorous. LTRF: 213. OA: typid: ventral. MP: wide ventral gap: uniserial. SUP: absent. DEM: lateral. NA: nearer eye than snout. VT: medial. EP: dorsal. SP: sinistral. UJ: narrow, smooth arc. LJ: narrow, open U-shaped. DE: low, originates near or slightly distal to dorsal td-body junction, tip rounded. BS: oval to round/depressed. CP: uniformiy black, may have white blotches or bands on t d . TL: 15-20136. CI: Duellman and Lynch (1969); Gascon (1989a); Lidquist and Hetherington (1988); J. D. Lynch (1986); Starrett (1967). Bufi: CO: 217. GR: widespread. EMG: exotroph: lentic: benthic; lotic: benthic, suaorial, gastromyzophorous; endotroph. LTRF: 2(2)/3(1), 2(2)/3,2/3,2(2)/2(1). Ok. typical: anteroventral. MP: wide dorsal and ventral gaps, complete: uniserial. SUP: few lateraiiy, absent. DEM: lateral, absent. NA: large and usuaiiy not round, often with me-
DIVERSITY
diai papdla. VT: mediai, dextrai. EP: dorsal. SP: sinistral. UJ: narrow, smooth arc, angled lateraiiy. LJ: narrow, open V-shaped. DE: low, originates at dorsai td-body junction, tip rounded. BS: ovai-round/depressed. CP: typicaiiy uniformly black, tail muscle sometimes bicolored or banded. TL: 15-35/36. NO: smaii size is cornrnon; morphologicaliy conservative and species characteristics poorly docurnented; no consistently recognized morphologicai dserences among numerous species groups except in debilis group; Crump (1989b) reported facultative endotrophy in B.pm$enes. CI: Altig (1970); Berry (1972); McDiarmid and Altig (1990); Zweifel (1970). Bufoides: CO: 1. GR: hdia. Tadpole unknown; see Piüai and Yazdani (1973). Capensibufo: CO: 2. GR: southwestern South Africa. EMG: exotroph: lentic: benthic. LTRP: 2(2)/3. OA: typicai: anteroventral. MP: wide dorsai and ventral gaps: uniserial. SUP: absent. DEM: lateral. NA: large, nearer eye than snout. VT: mediai. EP: dorsai. SP: sinistrai. UJ: medium, broad mediai convexity. LJ: medium, open U-shaped. DE: low, originates at dorsai taii-body junction, tip round. BS: ovai/depressed. CP: uniformly dark. TL: 35/36. CI: Power and Rose (1929); Wager (1986). Crepzdophryne: CO: 1. GR: Costa Rica. Unknown developmentai trajectory. Dendruphryniscus: CO: 3. GR: Ecuador-Pem-Guianas-Brazil. EMG: exotroph: lentic: benthic, arboreal. LTRF: 213, 2(2)/3. OA: typicai: anteroventral. MP: wide dorsai and ventral gaps: uniserial. SUP: absent. DEM: laterai. NA: large, nearer eye than snout. VT: medial. EP: dorsai. SP: sinistrai. UJ: medium, angled at dorsolaterai points. LJ: medium, open V-shaped. DF: low, originates at dorsai td-body junction, tip rounded. BS: ovai/depressed. CP: untformly dark. TL: 10-13136. CI: Izecksohn and Da Cmz (1972). Didynamipus: CO: 1. GR: Cameroon. EMG: endotroph. Frostt'us: CO: 1. GR: Brazil. EMG: endotroph. Laurentuphyne: CO: 1. GR: Zaire. EMG: endotroph. Leptupbryne: CO: 2. GR: Maiaysia. EMG: exotroph: lentic: benthic. LTRP: 2(1-2)/3. OA: typical: anteroventrai. MP: wide dorsai gap: uniserial. SUP: absent. DEM: lateral. NA: large like Bufo and equidistant between eye and snout. VT: mediai. EP: dorsal. SP: sinistrai. UJ: narrow, smooth arc. LJ: narrow, open U-shaped. DF: low, originates at dorsai tail-body junction, tip rounded. BS: oval/depressed. CP: uniformly black. TL: 151 34. NO: lack of gap in marginai papiüae of lower labium is unusual. CI: Berry (1972); Inger (1985). Melanupbyniscus: CO: 11. GR: Brazil-Paraguay-Argentina. EMG: exotroph: lentic: benthic. LTRF: 2/3[1]. OA: typicai: anteroventral. MP: wide dorsai and ventrai gaps: uniserial. SUP: absent, few lateraiiy. DEM: laterai, absent. NA: nearer eye than snout. VT: mediai. EP: dorsal. SP: sinistrai. UJ: mediurn, smooth arc, coarsely serrate. LJ: medium, open U-shaped. DF: low, originates near dorsai td-body junction, tip round. BS: ovai/depressed. CP: umformly dark, tad muscle bicolored, fins speckled. TL: 19/36. NO: figure in Prigioni and Arrieta (1992) shows laterai gaps in marginal papiüae. CI: Prigioni and Langone (1990); Starrett (1967). Mertensuphryne: CO: 2. GR: Zaire-Tanzania. EMG: exotroph: arboreal. LTRF: 112. OA: typicai: anteroventrai. MP: wide dorsai gap: uniserial. SUP: absent. DEM: laterai. NA: nearer snout than eye, withm the fleshy, hoiiow "crown" that encircles the eyes and nares. VT: mediai. EP: dorsai. SP: sinistral. UJ: wide, almost straight edge, coarsely serrate. LJ: similar to upper sheath. DE: low, originates near dorsal td-body junaion, tip broadly rounded. BS: oblong/depressed. CP: unrformly and lightly pigmented. TL: 13/30. NO: see Stephupaedes. CCI: Grandison (1980). Metaphryniscus: CO: 1. GR: Venezuela. EMG: endotroph. Nectophryne: CO: 2. GR: Cameroon-Zaire. EMG: endotroph. Nectuphrynotdes: CO: 5. GR: Tanzania. EMG: endotroph. Nimbaphymides: CO: 2 . GR: Liberia-Ivory Coast. EMG: endotroph. Oreuphrynella: CO: 6. GR: Venezuela-Guyana-Brazil. EMG: endotroph. CI: McDiarmid and Gorzula (1989). Osmnophryne: CO: 5. GR: Colombia-Ecuador. EMG: endotroph. Pedostipes: CO: 6. GR: hdia-Borneo. EMG: exotroph: lentic: benthic. LTRF: 2(2)/ 3(1). OA: typicai: ventrai. MP: wide dorsai and ventrai gaps: blunt and uniserial. SUP: absent. DEM: lateral. NA: nearer eye than snout. VT: mediai. EP: dorsal. SP: sinistral.
úpjOPhtyne
RONALD ALTIG A N D ROY W. McDIARMID
Schismudenna
Stephopaeáes
w e m n z a
Cochranella
UJ: medium, smooth arc, coarsely serrate. LJ: medium, open V-shaped. DF: low, originates near dorsai td-body junction, tip round. BS: ovai/depressed. CP: uniformly dark. TL: 16/36. CI: Inger (1966, 1985). Pelophvyne: CO: 7. GR: Philippines-China. EMG: endotroph. PeltcIphvyne: CO: 9. GR: Greater Antiües. EMG: exotroph: lentic: benthic. LTRF: 2(2)/ 3, 212. OA: typicai: anteroventral. MP: wide dorsai and ventral gaps: uniserial. SUP: row lateral to lower tooth rows. DEM: lateral. NA: nearer eye than snout. VT: mediai. EP: dorsai. SP: sinistrai. UJ: medium, smooth arc with slight mediai indentation. LJ: medium, open U-shaped. DE: low, originates near dorsal td-body junction, tip rounded. BS: ovai/depressed. CP: uniformly dark. TL: 2 1/36. CI: Ruiz Garcia (1980). Pseuúubufo: CO: 1. GR: Borneo. Tadpole unknown. Rhamphqhvyne: CO: 9. GR: Panama-Peru. EMG: endotroph. Schismaúema: CO: 1. GR: Tanzania-Zaire-South Africa. EMG: exotroph: lentic: nektonic. LTRP: 213. OA: typicai: anteroventral. MP: wide dorsai and ventral gaps: s m d and uniseriai. SUP: absent. DEM: lateral. NA: nearer snout than eye. VT: medial. EP: dorsai. SP: sinistrai. UJ: medium, long low convexity in margin; Wager (1986): upper sheath lacks serrations. LJ: narrow, open U-shaped. DE: low, originates near dorsai t d body junction, tip rounded. BS: ovai/depressed. CP: uniformly dark. TL: 35/36. NO: unique semicircular flap across body b e h d eyes; commonly schools in midwater/surface at least during the day. CI: Wager (1986). Spinophvynoihs: CO: 1. GR: Ethiopia. EMG: exotroph: lentic: benthic. LTRF: 2(2)/3. OA: typical: anteroventral. MP: wide dorsai and ventral gaps: uniseriai. SUP: -. DEM: -. NA: -. VT: -. EP: -. SP: -. UJ: -. LJ: -. DE: -. BS: -. CP: -. TL: -. CI: Grandison (1978); M. H. Wake (1980). Stephqaehs: CO: 2. GR: Tanzania-Mozambique. EMG: exotroph: arboreal. LTRF: 2(2)/2. OA: typicai: anteroventral. MP: wide dorsai gap: uniserial, some appear branched and s m d gaps between papdiae. SUP: absent. DEM: absent. NA: nearer eye than snout. VT: mediai. EP: dorsai. SP: sinistrai. UJ: wide, edge nearly straight. LJ: absent or not keratinized. DE: low, originates near dorsai td-body junction, siight arc about midiength, tip broadiy rounded. BS: ovai/depressed. CP: uniformly paie. TL: 201 37. NO: fleshy "crown" encircles nares and eyes; see MertenscIphvym. CI: Channing (1978, 1993). Tmebella: CO: 2. GR: Peru. EMG: endotroph. CI: Graybeal and Cannatella (1995). Werneria: CO: 4. GR: Togo-Cameroon. EMG: exotroph: lotic: suaorial. LTRP: 213. OA: typicai: ventral, suaoriai. MP: wide dorsai gap: biseriai. SUP: absent. DEM: lateral. NA: s m d , nearer snout than eyes. VT: medial. EP: dorsai. SP: sinistrai. UJ: narrow. LJ: narrow, open V-shaped. DE: low, originates at dorsai td-body junction. BS: oval/ depressed. CP: uniformly dark. TL: 27/36. CI: Mertens (1938); Perret (1966). Wolterstorffina:CO: 2. GR: Cameroon-Nigeria. EMG: endotroph. CENTROLENIDAE: CO: 31103. GR: Mexico-Brazil-Boiivia. NO: generic and specific drfferences poorly known. Centrolene: CO: 33. GR: Honduras-Peni-Venezuela. EMG: exotroph: lotic: burrower. LTRF: 5 213. OA: typicai: anteroventral. MP: wide dorsai gap: uniierial. SUP: absent. DEM: lateral. NA: s m d , about equidistant between eye and snout. VT: medial, dextrai. EP: dorsal: tiny and near sagittal line. SP: sinistrai. UJ: narrow to medium, smooth arc, sometimes coarsely serrate. LJ: narrow to medium, U- or V-shaped. DE: low, originates on t d muscle to near td-body junction, tip rounded. BS: oval/strongly depressed. CP: reddish in iife because of skin vascularization, uniformly tan in preservative. TL: 40-501 36. CI: J. D. Lynch et ai. (1983); Mijares-Urrutia (1990). Cochranella: CO: 44. GR: Nicaragua-Bolivia-Brazil. EMG: exotroph: lotic: burrower. LTRF: 5 213. OA: typicai: anteroventral. MP: wide dorsai gap: uniserial. SUP: absent. DEM: lateral. NA: s m d , about equidistant between eye and snout. VT: medial, dextrai. EP: dorsai: tiny and near sagittai luie. SP: sinistral. UJ: narrow to medium, smooth arc, sometimes coarsely serrate. LJ: narrow to medium, U- or V-shaped. DE: low, originates on t d muscle to near td-body junction, tip rounded. BS: ovai/strongly depressed. CP: reddish in iife because of skin vascularization, uniformly tan in preservative. TL: 40-501 36. CI: Duellman (1978).
DIVERSITY
Hyalimbatrachzztm: CO: 26. GR: Mexico-Bolivia-Tobago-Guyana-Brazil. EMG: exotroph: lotic: burrower. LTRF: 5 213. OA: typical: anteroventral. MP: wide dorsal gap: uniserial. SUP: absent. DEM: lateral. NA: small, about equidistant between eye and snout. VT: medial, dextral. EP: dorsal: tiny and near sagittal line. SP: sinistral. UJ: narrow to medium, smooth arc, sometimes coarsely serrate. LJ: narrow to medium, U- or V-shaped. DF: low, originates on taii muscle to near taii-body junction, tip rounded. BS: oval/strongly depressed. CP: reddish in Me because of skin vascularization,uniformiy tan in preservative. TL: 40-50136. CI: Duellman (1978); Heyer (1985). DENDROBATIDAE: CO: 81164. GR: Nicaragua-Bolivia-Brazil. EMG: exotroph: lentic: benthic, arboreal; lotic: benthic, neustonic; endotroph. LTRF: number of variations from O/ O to 213. OA: typical: anteroventral, terminal, umbelliform. MP: medium to wide dorsal gap: uni- and biserial. SUP: few lateral, absent. DEM: lateral, absent. NA: nearer eye than snout or reverse. EP: dorsal. SP: sinistral. UJ: narrow to wide, smooth arc. LJ: narrow to wide, Uor V-shaped. DF: low, originates near dorsal td-body junction, tip rounded to slightly pointed. BS: oval to rounded/depressed. CP: uniform or muted variations. TL: 12-68/36. NO: generic and specific differences poorly understood. Aromobates: CO: 1. GR: Venezuela. EMG: exotroph: lotic: benthic. LTRF: 2(2)/3(1). OA: typical: anteroventral. MP: wide dorsal gap: uniserial on upper labium, biserial on lower labium. SUP: few ventrolaterally. DEM: lateral. NA: nearer eye than snout. VT: dextral. EP: dorsal. SP: sinistral. UJ: massive, finely serrated edge a uniform arc. LJ: large, moderately V-shaped. DF: low, originates near dorsal taii-body junction, tip rounded. BS: globular/depressed. CP: uniformiy dark. TL: 68/37. CI: Myers et al. (1991). Colostethus:CO: 85. GR: Costa Rica-Peru-Brazil. EMG: exotroph: lentic: benthic, arboreal, neustonic; lotic: neustonic; endotroph. LTRF: 2(2)/3[1], 212, 010. OA: typical: anteroventral,umbehform, largely absent in endotrophs. MP: medium dorsal gap: uniserial. SUP: row throughout extent of marginal papiiiae, absent, few laterally and distal to P-3. DEM: lateral. NA: nearer eye than snout. VT: medial. EP: dorsal. SP: sinistral. UJ: medium to wide, smooth arc. LJ: medium to wide, open V-shaped. DF: low, originates near dorsal td-body junction, tip rounded. BS: oval/depressed. CP: muted tones, dark line from nostril to snout common. TL: 15-30136. NO: C. nubicola group has umbelliform oral disc and jaw sheaths but no labial teeth. CI: Kaiser and Altig (1994); Lescure (1984); J. M. Savage (1968). Dendrobates: CO: 26. GR: Nicaragua-Peru-Brazil. EMG: exotroph: lentic: benthic, arboreal. LTRF: 1/1,2(2)/3[1]. OA: typical: anteroventral. MP: wide dorsal gap: uniserial, sometimes narrow ventral gap. SUP: absent. DEM: lateral. NA: nearer snout than eye. VT: medial. EP: dorsal. SP: sinistral. UJ: mediun~to very wide, smooth arc. LJ: medium to wide, open U-shaped. DF: low, originates near dorsal taii-body junction, tip rounded to slightly pointed. BS: oval/depressed. CP: uniform and muted variations. TL: 15-25/36. CI: J. M. Savage (1968); Silverstone (1975). Epipedubates: CO: 24. GR: northern South America. EMG: exotroph: lentic: benthic, arboreal. LTRF: 2(2)/3[1-21. OA: typical: anteroventral.MP: wide dorsal gap: uniserial. SUP: few laterally, absent. DEM: lateral. NA: nearer snout than eye. VT: medial. EP: dorsal. SP: sinistral. UJ: narrow to medium, smooth arc. LJ: narrow to medium, open U-shaped. D E low, originates near dorsal tail-body junction, tip rounded. BS: oval/depressed. CP: u d o r m and muted variations. TL: 15-20136. CI: J. M. Savage (1968); Silverstone (1975). Mannophryne: CO: 9. GR: Venezuela-Tobago. EMG: exotroph: lentic: benthic, arboreal. EMG: exotroph: lentic: benthic, arboreal, neustonic; lotic: neustonic; endotroph. LTRF: 2(2)/3[1], 212, 010. OA: typical: anteroventral, umbelhform, largely absent in endotrophs. MP: medium dorsal gap: uniserial. SUP: row throughout extent of marginal papillae, absent, few laterally and distal to P-3. DEM: lateral. NA: nearer eye than snout. VT: medial. EP: dorsal. SP: sinistral. UJ: medium to wide, smooth arc. LJ: medium to wide, open V-shaped. D E low, originates near dorsal td-body junction, tip rounded. BS: oval/depressed. CP: muted tones, dark h e from nostril to snout common TL: 15-30136. NO: see Colostethus. CI: J. R. Dixon and Rivero-Blanco (1985). Minyobates: CO: 9. GR: Venezuela-Ecuador. EMG: exotroph: lentic: benthic. LTRF:
tnnitatU
Colostethw; C.fitatw
Dendrobates
RONALD ALTIG AND ROY W. McDIARMID
2(2)/3. OA: typical: anteroventral. MP: wide dorsai gap: uniserial. SUP: absent. DEM: absent, lateral. NA: nearer eye than snout. VT: rnedial. EP: dorsal. SP: sinistral. UJ: wide, srnooth arc. LJ: wide, open U-shaped. DE: low, originates near dorsai td-body junction, tip rounded. BS: ovai/depressed. CP: uniformly dark. TL: 12-18/36. CI: J. M. Savage (1968); Silverstone (1975). Nephalobates: CO: 5. G R Venezuela. EMG: exotroph: lentic: benthic. LTRF: 2(2)/3. OA: typical: anteroventral. MP: wide dorsal gap: uniserial. SUP: absent. DEM: absent, lateral. NA: nearer eye than snout. VT: rnediai. EP: dorsai. SP: sinistrai. UJ: wide, srnooth arc. LJ: wide, open U-shaped. DE: low, originates near dorsal td-body junction, tip rounded. BS: ovai/depressed. CP: uniformly dark. TL: 12-18/36. NO: forrner Colostethus albogztlaris group. CI: La Marca and Mijares-U (1988). Phyllobates: CO: 5. G R Costa Rica-Colornbia. EMG: exotroph: lotic: benthic. LTRF: 2(2)/3. OA: typical: anteroventrai. MP: wide dorsal gap: uni- and biserial. SUP: absent. DEM: lateral. NA: nearer eye than snout. VT: rnediai. EP: dorsal. SP: sinistral. UJ: wide, srnooth arc. LJ: wide, open V-shaped. DE: low, originates near dorsai td-body junction, tip rounded. BS: oval/depressed. CP: uniforrnly dark. TL: 15-25/36. CI: Donnelly et ai. (1990b); Lescure (1976); J. M. Savage (1968). DISCOGLOSSIDAE: CO: 219. G R Europe. EMG: exotroph: lentic: benthic. LTRF: 2/3(1), biserial. OA: typical: anteroventrai. MP: complete: uniseriai. SUP: absent. DEM: lateral. NA: nearer snout than eye. VT: rnediai. EP: dorsai. SP: low on lefi side. UJ: narrow, srnooth arc. LJ: narrow, open U-shaped. DE: low, originates near dorsal tail-body junction, tip rounded. BS: oval/depressed. CP: chainlike melanophore pattern in skin. TL: 3555/36. Alytes: CO: 4. G R Europe. EMG: exotroph: lentic: benthic. LTRF: 2/3(1), biserial. OA: typical: anteroventral. MP: complete: uniserial. SUP: absent. DEM: lateral. NA: nearer snout than eye. VT: rnedial. EP: dorsai. SP: low on lefi side. UJ: narrow, smooth arc. LJ: narrow, open U-shaped. DE: low, originates near dorsal td-body junction, tip rounded. BS: ovai/depressed. CP: chainlike rnelanophore pattem in skin. TL: 35-55/36. CI: Bouienger (1892); Lanza (1983). Dism~lossus:CO: 5. G R Europe-Syria. EMG: exotroph: lentic: benthic. LTRF: 2/3(1), biserial. OA: typical: anteroventral. MP: córnplete: uniserial. SUP: absent. DEM: lateral. NA. nearer snout than eye. VT: rnedial. EP: dorsai. SP: low on lefi side. UJ: narrow, srnooth arc. LJ: narrow, open U-shaped. DE: low, originates near dorsal tail-body junction, tip rounded: BS: oval/depressed. CP: chadke rnelanophore pattern in skin. TL: 35-55/36. CI: Bouienger (1892); Lanza (1983). HELEOPHRYNIDAE: CO: 115. G R South Afi-ica. EMG: exotroph: lotic: suctorial. LTRF: 4114-15(1). OA: typicai: ventral, upper jaw sheath absent, sometimes lower also. MP: complete: biserial. SUP: rows below distai rnost lower row. DEM: absent. NA: equidistant between eye and snout, slightly tubuiar. VT: rnedial. EP: dorsai. SP: sinistrai. UJ: absent. LJ: when present: rnedium, open V-shaped. DE: low, originates on taii rnuscle, tip rounded. BS: oblong/depressed. CP: rock/lichenlike rnottiing, yeiiow/gold ofien in background color in life. TL: 50-85/36. NO: fewer than 14 tooth rows on lower labium common; hypertrophed, isolated jaw serrations in the position of jaw sheaths of srnd tadpoles are soon lost (Visser 1985); large subbranchial rnuscle present ventrolaterdy along anterior two-thirds of body gives ventrai silhouette a distinaive shape. Heleophyne: CO: 5. CI: Channing (1984); Channing et ai. (1988); Van Dijk (1966). HEMISOTIDAE: CO: 118. G R sub-Saharan Africa. EMG: exotroph: lentic: nektonic. LTRP: 5(3-5)/4(1), 6(3-6)/3. OA: typicai: anteroventrai. MP: wide dorsai gap: uni- and biseriai, some ventrai papiüae exceedingly long. SUP: absent, few laterally. DEM: absent. NA: srnd, doser to snout than eye. VT: dextrai. EP: lateral. SP: sinistral. UJ: rnedium to wide, strong rnedial convexity. LJ: rnedium, open U-shaped. DE: low, originates near dorsal taii-body junaion, tip pointed. BS: ovai/cornpressed. CP: stripes on taii, distal thrd dark, basai conneaive tissue sheath visible. TL: 40-60136. Hemks: CO: 8. CI: Lambiris (1988a, b); Van Dijk (1966); Wager (1986). HYLIDAE: CO: 411743. GR: Holaraic-Neotropic-Australopapua. EMG: exotroph: lentic: severai guilds; lotic: several guilds; endotroph. LTRF: rnany variations between 010 and
DIVERSITY
17/21. OA: typical: anteroventral, ventral, terminal. MP: dorsal gap, complete, dorsal and ventral gaps: variable, ofien bi- or multiserial. SUP: highly variable. DEM: absent, lateral. NA: round, variable in size, closer to snout than eye or reverse, ofien rimrned and countersunk. VT: dextrai, mediai. EP: lateral, dorsai. SP: sinistral, low on lefi side, ventral. LJ: highiy variable. DE: highiy variable. BS: oval to oblong/depressed, equidimensional and compressed. CP: highiy variable. TL: 20-60136. NO: marginal papiiiae always smder and more densely arranged than ranids, the most commonly confused taxa; few taxa with 1-3 anterior rows with medial gaps distal to nonbroken rows. Hemiphractinae: CO: 5/64. GR: Panama-South America. Cryptoba~rachus:CO: 3. GR: Colombia. EMG: endotroph. Fhctonotus: CO: 5. GR: Brazil-Venezuela-Trinidad. EMG: endotroph; exotroph: arboreal. LTRF: 010. OA: typical but lacking labial teeth; anteroventral. MP: dorsal gap: uniserial. SUP: absent. DEM: absent. NA: nearer snout than eye. VT: medial. EP: dorsal. SP: ventral. UJ: medium, wide arc. LJ: narrow, wide U-shaped. DE: low, originates near dorsal td-body junction, tip round. BS: oblong/depressed. CP: iightly pigmented. TI,: 18/31. NO: exotrophic larvae are morphologicdy similar to those of nidicolous endotrophs. CI: Dueliman and Gray (1983); Heyer et al. (1990); and Weygoldt (1989). Gastrotheca: CO: 44. GR: Panama-Brazil. EMG: exotroph: lentic: benthic; endotroph. LTRF: 2(2)/3(1). OA: typical: anteroventral. MP: medium dorsal gap: uniserial. SUP: ventrolaterdy. DEM: absent. NA: equidistant between snout and eye. VT: dextral. EP: dorsal. SP: sinistral. UJ: medium, smooth arc. LJ: wide, open V-shaped. DF: low, originates near dorsal taii-body junction, tip rounded. BS: oval/depressed. CP: uniformiy dark. TL: 40-60136. CI: Wassersug and Dueliman (1984). Hemiphractus: CO: 5. GR: Panama-Bolivia. EMG: endotroph. Stgrania: CO: 7. GR: Venezuela-Guyana. EMG: endotroph. Hylinae: CO: 26/488. GR: Eurasia and North, Central, and South America. A h s : CO: 2. GR: eastern North America. EMG: exotroph: lentic: benthic. LTRP: 2(2)/ 2. OA: typical: anteroventral. MP: wide dorsal gap: uniserial. SUP: few laterdy. DEM: absent. NA: nearer snout than eye. VT: dextral. EP: dorsal. SP: sinistral. UJ: medium, wide smooth arc. LJ: medium, U-shaped. DF: low, originates near dorsal taii-body junction, tip pointed. BS: oval/depressed. CP: dorsum of t d muscle banded; taii tip usudy black. TL: 40-50136. NO: spiracular tube long. CI: Altig (1970); Orton (1952); A. H . Wright and Wright (1949). Anotheca: CO: 1. GR: Mexico-Panama. EMG: exotroph: lentic: arboreal. LTRF: 2(2)/ 2. OA: typical: nearly terminal. MP: complete: uniserial. SUP: few laterdy. DEM: absent. NA: about equidistant between snout and eye. VT: d m a l . EP: dorsal. SP: sinistrai. UJ: wide, long shdow arc, finely serrate. LJ: wide, open V-shaped. DE: low, originates near dorsal taii-body junction, tip rounded. BS: ovalJdepressed. CP: uniformiy purpiish brown. TI,: 45/38. NO: gut not coiled. CI: Robinson (1961); E. H . Taylor (1954). Apa~mphenodon:CO: 2. GR: Brazil-Venezuela. EMG: lentic: benthic. LTRF: 2(1)/56(1). OA: typical: anteroventral. MP: wide dorsal gap: mdtiserial. SUP: s m d group ventrolaterdy. DEM: absent. NA: -. VT: mediai. EP: lateral. SP: sinistral. UJ: -. LJ: -. DF: low, originates anterior to the dorsal td-body junction, tip pointed. BS: ovoid in dorsal view. CP: dark brown with irregular dark spots; taii muscle banded dorsdy. TL: 47/36. CI: H. R. de Silva (personal communication). Aplastodiscus: CO: 1. GR: Brazil. EMG: exotroph: lentic: benthic. LTRF: 2(2)/4(1). OA: typical: anteroventral. MP: medium dorsal gap: uniserial. SUP: absent. DEM: absent. NA: nearer eye than snout. VT: dextral. EP: lateral. SP: sinistral. UJ: medium, straight medial edge. LJ:medum, U-shaped. DE: low, originates at dorsal taii-body junction, tip pointed. BS: oval/depressed. CP: distal one-third of taii darkened; anterior part of t d muscle with lateral stripe. TL: 68/38. CI: Caramaschi et al. (1980). Argenteohyíu: CO: 1. GR: Argentina-Paraguay. EMG: exotroph: lentic: benthic. LTRF: 2(2)/4(1). OA: typicai: anteroventral. MP: medium dorsal gap: biserial. SUP: absent. DEM: absent. NA: nearer eye than snout. VT: medial. EP: dorsal. SP: sinistral. UJ: medium, smooth arc. LJ: medium, open V-shaped. DF: somewhat arched, originates on body, tip pointed. BS: oval/depressed. CP: uniformiy brown. TL: 42/31. CI: De Sá (1983).
Ami~
RONALD ALTIG AND ROY W. McDIARMID
Duellmanohyla
Hyla; H. bromeliacia
Hyia; H. picadoi
Hyia; H. sarayaçuensiJ
Hyla; H. armata
Cal'tahyh: CO: 1. GR: Jamaica. EMG: exotroph: lentic: arboreal. LTRP: 110. OA: typical: anteroventral.MP: narrow dorsal gap: uniserial. SUP: throughout lower labium. DEM: absent. NA: nearer eye than snout. VT: medial. EP: dorsal. SP: sinistral. UJ: medium, serrated edge a smooth arc. LJ: medium, open V-shaped. DF: somewhat arched, originates on body, tip pointed. BS: oval/depressed. CP: uniformly brown. TL: 42/31. CI: E. R. Dunn (1926). Cmythomantis: CO: 1. GR: Brazii. Tadpole unknown. Duellmanohyh: CO: 8. GR: Mexico-Costa Rica. EMG: exotroph: lotic: adherent. LTRF: 3(1,3)/3[1], 2(2)/3,2(2)/2. OA: typical: ventral. MP: complete: small and uniseriai. SUP: scattered throughout disc. DEM: midventral. NA: small, nearer snout than eye. VT: dextral. EP: dorsal. SP: sinistral. UJ: wide, coarsely serrate, srnooth arc to slightly indented medially. LJ: medium, coarsely serrate, V-shaped. DF: low, originates near dorsal tail-body junaion, tip rounded. BS: oval/depressed. CP: largely brown, some rnotthg on tail. TL: 33/26. NO: tooth rows much shorter than transverse diameter of oral disc. CI: J. A. CampbeU and Srnith (1992); D u e h a n (1970). Hyh: CO: 289. GR: North, Central and South America-Eurasia. EMG: exotroph: lotic: arboreal, benthic, adherent, clasping, suctorial; lentic: benthic, nektonic, arboreal. LTRF: many variations between 010 and 17/21; 2/3 most comrnon. OA: typical: terminal, anteroventral,ventral; reduced to various degrees. MP: dorsal gap, dorsal and ventral gaps: uni-, bi-, and multiserial. SUP: few to many laterally, distinct rows above upper and below lower tooth rows, absent. DEM: absent. NA: variou positions. VT: dextral, rnedial. EP: dorsal, lateral. SP: sinistral. UJ: many variations. LJ: many variations. DF: very low to very high, originates anterior to, near (most cornmon), or posterior to dorsai taii-body junaion, tip pointed to round. BS: oval to oblong/depressed, cornpressed or equidimensional. CP: variable. TL: 20-60/36. NO: a number of species groups have distinaive rnorphologies. CI: Caldweli (1974); D u e h a n (1970, 1978); Duellman and Altig (1978); Duellman and Fouquette (1968); D u e h a n and Tmeb (1989); Peixoto and Da Cmz (1983); J. M. Savage (1980b). Nyctimuntis: CO: 1. GR: Ecuador. Tadpole unknown. Osteocephalus: CO: 14. GR: Guianas-Venezuela-Amazon Basin-Argentina. EMG: exotroph: lentic: benthic, arboreal. LTRF: 2(2)/5(1), 3(2-5)/5(1). OA: typical: anteroventrai. MP: wide dorsal gap: biserial. SUP: few laterally. DEM: absent. NA: equidistant between eye and snout. VT: dextral. EP: dorsal. SP: sinistral. UJ: narrow, wide smooth arc. LJ: narrow, V-shaped. DF: low, originates near dorsal taii-body junaion, tip rounded. BS: oval/depressed. CP: uniformly dark. TL: 49/37. CI: Duellman (1978); Duellman and Lescure (1973); Tmeb and Duellman (1970). Osteopilus: CO: 3. GR: Greater Antiiies-Florida. EMG: exotroph: lentic: benthic, arboreal. LTRF: 2(2)/4(1). OA: typical: anteroventral, ventral. MP: dorsal gap: uniserial. SUP: absent. DEM: absent. NA: nearer eye than snout. VT: dextrai, rnedial. EP: lateral, dorsal. SP: sinistral. UJ: medium, edge forms smooth arc. LJ: medium, deep rnedial indentation. DF: low, originates near dorsal taii-body junaion, tip slightly pointed. BS: oval/depressed. CP: uniformly dark or pale. TL: 37/41. CI: Duellman and Schwar~ (1958); Lannoo et al. (1987). Phtynohyas: CO: 5. GR: Mexico-Argentina. EMG: exotroph: lentic: nektonic, benthic, arboreal. LTRF: 4(1-2,4)/6(1), 3(1,3)/5(1),2(2)/4[1]. OA: typical: anteroventral. MP: rnedium dorsal gap: biserial. SUP: few ventrolaterally. DEM: absent. NA: nearer eye than snout. VT: rnedial. EP: lateral. SP: sinistral. UJ: medium, edge describes a smooth arc, coarsely serrate. LJ: medium, open U-shaped. DF: rnedium, originates on body, tip pointed. BS: oval/compressed. CP: taii rnucle striped. TL: 30-38/36. NO: unusual LTRF shared with TrachcephcúzLs;Pyburn (1967) shows a rnedial constriaion in the upper jaw sheath; Zweifel (1964) shows a rnediaiiy broken upper sheath; apparently random breaks, not gaps as noted above, cornrnon in lower rows. CI: Pyburn (1967); Zweifel (1964). Phyllodytes: CO: 7. GR: Trinidad-Brazil. EMG: exotroph: lentic: benthic, arboreai. LTRF: 2(2)/3. OA: typical: anteroventral. MP: wide dorsal gap: uni- and biserial. SUP: few laterally. DEM: absent. NA: nearer snout than eye. VT: rnedial. EP: dorsal. SP: sinistral. UJ: medium, smooth arc. JJJ: rnedium, open U-shaped. DF: low, originates
DIVERSITY
near dorsal taii-bodyjunction, tip rounded. BS: oval/depressed. CP: uniformiy dark. TL: 29/36. CI: Bokermann (1966); F. M. Clarke et al. (1995); Giarretta (1996). Plectrobyla: CO: 16. GR: Mexico-Guatemala. EMG: exotroph: lotic: clasping. LTRF: 2(2)/3. OA: typicai: ventral. MP: complete: uni- and biserial. SUP: row above A-1 and below P-3, scattered laterally. DEM: absent. NA: small, nearer snout than eye. VT: dextral. EP: dorsal. SP: sinistral. UJ: wide, uniform arc, uniform graded series of serrations, hypertrophied serrations in specific sections. LJ: wide, open U-shaped. D E low, originates near dorsal tail-body junction, tip round. BS: oval/depressed. CP: uniformiy dark, some mottiing on tail. TL: 35-43/34. CI: J. A. Campbeii and Kubin (1990); Dueiiman (1970). Pseudacris: CO: 13. GR: North America. EMG: exotroph: lentic: nektonic, benthic. LTRF: 2(2)/3[1]. OA: typical: anteroventral.MP: medium dorsal gap: uni- and biserial, sometimes narrow ventral gap. SUP: few laterally. DEM: absent. NA: nearer eye than snout. VT: dextral. EP: lateral. SP: sinistrai. narrow to medium, wide arc, sometimes medial zone straight. LJ: medium, V-shaped. D E medium to high, originates near dorsal tail-body junction, on body, tip pointed. BS: oval/compressed. CP: muted mottling, stripes or bicolored on tail. TL: 25-45/36. CI: Aitig (1970); D u e h a n (1970); A. H. Wright and Wright (1949). Pternobyla: CO: 2. GR: southern Arizona-Mexico. EMG: exotroph: lentic: benthic. LTRF: 2(2)/3. OA: typical: anteroventral. MP: dorsal gap: uniserial dorsolaterally, biserial elsewhere. SUP: few laterally. DEM: absent. NA: small, equidistant between eyes and snout. VT: dextral. EP: lateral. SP: sinistral. UJ: wide, edge a smooth arc. LJ: medium, open U-shaped. DF: high, originates on body, tip somewhat pointed with slight flagellum. BS: oval/compressed. CP: pale dorsolateral stripes. TI,: 38/36. CI: R. G. Webb (1963). Ptycbobyla: CO: 10. GR: Mexico-Panama. EMG: exotroph: lotic: benthic, suctorial. LTRF: 4(1,4)/7(1), 4(4)/7(1), 4(4)/6(1). OA: typical: nearly ventral. MP: complete: biserial. SUP: many lateraüy. DEM: absent. NA: small, nearer snout than eye. VT: dextral. EP: dorsal. SP: sinistral. U J: medium, edge a smooth arc. LJ: medium, V-shaped. DF: low, originates near dorsal taii-body junction, tip pointed to rounded. BS: oval/ depressed. CP: dark, some minor mottling, especially on tail. TL: 33-39125-31. CI: J. A. Campbeii and Smith (1992); D u e h a n (1970). Scarthyla: CO: 1. GR: Peru. EMG: exotroph: lentic: nektonic. LTRF: 2(1-2)/2(1). OA: typical: nearly terminal. MP: wide dorsal and ventral gaps: uniserial. SUP: absent. DEM: absent. NA: nearer snout than eye. VT: dextral. EP: lateral. SP: sinistral. UJ: medium, prominent arch, coatsely serrate. LJ: wide, open U-shaped, coarsely serrate. DF: low, originates posterior to dorsal taii-body junction, tip pointed. BS: oval/depressed. CP: tail h s with prominent serial blotches that look like incomplete bands. TL: 28/36. NO: see Scinax. CI: D u e h a n and De Sá (1988). Scinm: CO: 81. GR: Mexico-Uruguay. EMG: exotroph: lentic: nektonic, benthic. LTRF: 2(2)/3[1.]. OA: typical: anteroventral, almost terminal. MP: narrow dorsal gap: uni- and biserial; rostrata group: ventral gap 2 extent of short P-3 that sits upon an armiike derivative of the lower labium. SUP: few laterally. DEM: absent. NA: nearer eye than snout. VT: dextral. EP: lateral. SP: sinistral. UJ: wide, smooth arc or with medial convexity, sometimes coarsely serrate. LJ: medium to wide, V- to open U-shaped. DF: low, originates near dorsal taii-body junction, tip pointed, or quite high, originates anterior to dorsal td-body junction, tip pointed, sometimes with flagellum. BS: oval/depressed or compressed. CP: iightly pigmented, eye iine common. TL: 20-30136. NO: see Scartbyla; at least rostrata and wbra groups with distinctive morphology of the oral apparatus. CI: D u e h a n (1970); Hero and Mijares-Urrutia (1995); Heyer et al. (1990); McDiarmid and Aitig (1990). Smilisca: CO: 6. GR: southern Texas-northern South America. EMG: exotroph: lentic: benthic; lotic: adherent. LTRF: 2(2)/3. OA: typical: anteroventral, ventral. MP: dorsal gap, complete: uni- and multiserial. SUP: many laterally. NA: nearer eye than snout. VT: dextral. EP: lateral, dorsal. SP: sinistral. UJ: medium to wide, edge a smooth arc or indentation medially. LJ: medium to wide, open U-shaped. D E low, slightly arched, originates near dorsal td-body junction or onto body, tip pointed. BS: oval/siightly de-
v:
Scinax; S. su~dlata
Scinm; S. staufiri
RONALD ALTIG AND ROY W. McDIARMID
Cycloma
pressed. CP: uniformly brownish; pale dorsolateral stripe on body; dorsurn of tail muscle lightiy banded. TL: 2 2 4 0 / 3 0 4 0 . CI: Dueilman (1970). Spbaenmbyncbus: CO: 11. GR: Trinidad, Orinoco and Amazon basins of northern South America. EMG: exotroph: lentic: benthic. LTRF: 2(2)/3(1).OA: typical: anteroventral. MP: wide dorsal gap: uniserial. SUP: few lateraiiy and ventrolateraiiy. DEM: absent. NA: smaii, nearer snout than eye. VT: medial. EP: lateral. SP: sinistral. UJ: wide, slight medial convexity. LJ: wide, very open U-shaped. DP: low, originates near dorsal tailbody junction, tip pointed. BS: oval/depressed. CP: stripes below eye and on mil. TL: 57/35. CI: Bokermann (1974); Da Cniz and Peixoto (1980a); Heyer et al. (1990). Tepuibyla: CO: 7. GR: eastern Venezuela. NO: no tadpoles known for the 0. rodnauezi group that was recently elevated to a genus distinct from Osteocepbalus. Tracbycepbalus: CO: 3. GR: Brazii-Ecuador. EMG: exotroph: lentic: nektonic. LTRF: 4(1-2,4)/6(1). OA: typical: anteroventral. MP: medium dorsal gap: biserial. SUP: patch ventrolateraiiy. DEM: absent. NA: small, nearer snout than eye. VT: medial. EP: lateral. SP: sinistral. UJ: medium, forms smooth arc. LJ: mediurn, open V-shaped. DF: high, originates on body, tip pointed. BS: oval/cornpressed. CP: body and tail striped. TL: 381 34. NO: shares uncommon LTRF with Pbqmbyas. CI: McDiarmid and Altig (1990). Triprion: CO: 2. GR: western and southern Mexico. EMG: exotroph: lentic: benthic. LTRF: 2(2)/3. OA: typical: anteroventral. MP: mediurn dorsal gap: biserial. SUP: few lateraiiy. DEM: absent. NA. nearer eye than snout. VT: dextral. EP: lateral. SP: sinistral. UJ: wide, smooth arc. LJ: wide, broadly U-shaped. DE: low, originates at dorsal tailbody junction, tip rounded. BS: oval/slightly depressed. CP: udormly brown. TL: 27/ 30. CI: Duellman (1970). Xenobyla: CO: 2. GR: Brazii. EMG: exotroph: lentic: nektonic. LTRF: 2(2)/3(1). OA: typical: anteroventral. MP: medium dorsal gap: uniserial. SUP: absent. DEM: absent. NA: ncarer tip of snout than eye. VT: -. EP: lateral. SP: sinistral. UJ: medium, with moderate medial convexity LJ: wide, broadly U-shaped. DF: high, originates directly behmd plane of eye, tip with prominent flageiium. BS: oval/cornpressed. CP: bold bands on tail, prominent eye stripe. TL: 32/33. CI: Izecksohn (1997). Pelodryadiae: CO: 4/143. GR: Australia-New Guinea. Cyciurana: CO: 12. GJk Australia. EMG: exotroph: lentic: benthic. LTRF: 2(2)/3(1). OA: typical: anteroventral. MP: wide dorsal gap: biserial. SUP: absent. DEM: absent. NA: nearer snout than eye. VT: dextral. EP: dorsal. SP: sinistral. UJ: wide, smooth arc. LJ: wide, V-shaped. DF: low, originates near dorsal td-body junction, tip pointed. BS: oval/depressed. CP: unicolored to faintiy mottled or blotched. TL: 40-70/42. CI: Watson and Martin (1973). Litmia: CO: 104. GR: Australia-New Guinea. EMG: exotroph: lentic: benthic; lotic: benthic, suctorial. LTRF: 213, 2(2)/3[1], 2(2)/2. OA: typical: anteroventral, ventral. MP: narrow to wide dorsal gap: uni- and biserial; complete: biserial. SUP: absent, few lateraiiy, many lateraiiy. DEM: absent. NA: nearer eye than snout and reverse. VT: dextrai. EP: lateral, dorsal. SP: sinistral. UJ: narrow to wide, smooth arc, slight medial convexity. LJ: narrow to wide, open U-shaped. DF: low, originates near dorsal tail-body junction, tip pointed to rounded. BS: oval/depressed or compressed. CP: variable. TL: 30-60/36. NO: species groups not well defined (e.g., Barker and Grigg 1977; King 1981; Tyler 1968; Tyler and Davies 1978). CI: Watson and Martin (1973). Nyctimystes: CO: 24. GR: northern Australia-New Guinea. EMG: exotroph: lotic: suctorial. LTRF: 2/3. OA: typical: ventral. MP: complete: uniserial. SUP: radiaiiy oriented, elongate papillae across lower labium distal to P-3. DEM: absent. NA: nearer snout than eye. VT: medial. EP: dorsal. SP: sinistral. UJ: wide, medial modification for suctorial existence. LJ: wide, open U-shaped. DF: low, originates posterior to dorsal tail-body junction, tip round. BS: oval/depressed. CP: muted mottiing. TL: 33/36. CI: Davies and Richards (1990); Tyler (1989). Peiudryas: CO: 3. GR: Australia. EMG: exotroph: lentic: benthic. LTRF: 2(1-2)/3. OA: typical: anteroventral. MP: medium dorsal gap: biserial. SUP: absent. DEM: absent. NA: equidistant between eye and snout. VT: dextral. EP: lateral. SP: sinistral. UJ: med i u , smooth arc, coarsely serrate. LJ: medium, open V-shaped, coarsely serrate. DF: low, originates near or slightly posterior to dorsal tail-body junction, tip pointcd. BS: oval/depressed. CP: tail striped. TL: 41/41. NO: see Litoria. CI: Tyler et al. (1983).
DIVERSITY
Phyllomedusinae: CO: 6/48. G R Mexico-Bolivia. Agalychnis: CO: 8. G R Mexico-Ecuador. EMG: exotroph: lentic: suspension-rasper, nektonic, arboreai. MP: medium dorsai gap, complete: biseriai. SUP: absent. DEM: absent. NA: nearer snout than eye. VT: dextrai. EP: lateral. SP: low on left side without mediai wall. UJ: medium to wide, smooth arc, slight mediai convexity. LJ: medium, open U-shaped. DF: low, originates near dorsai tail-body junction, tip rounded. BS: oval/ compressed. CP: lightly pigmented. TL: 30-60136. NO: ventrai fin often higher than dorsai fin. CI: Donneliy et ai. (1987); Duellman (1970); Hoogmoed and Cadle (1991). Hylomantis: CO: 2. G R Brazii. EMG: exotroph: lentic. NO: similar to tadpoles ofPhasmabyla (0.L. Peixoto, personai communication). Pachymedusa: CO: 1. G R western Mexico. EMG: exotroph: lentic: suspension-rasper. LTRE: 2(2)/3(1). OA: typicai: anteroventrd. MP: wide dorsai gap: uniserial. SUP: few bordering marginal papillae. DEM: absent. NA: nearer snout than eye. VT: dextrai. EP: laterai. SP: low on left side without mediai wall. UJ: medium, smaii serrations on smooth, broad arc. LJ: medium, open V-shaped. DF: medium, originates at dorsai taiibody junction, tip pointed. BS: ovai/compressed. CP: bluish gray in Me, tan in preservative. TL: 45/34. CI: Duellman (1970). Phasmubyla: CO: 4. G R Brazii. EMG: exotroph: lentic: neustonic. LTRP: 1/2(1). OA: typicai: umbelliform. MP: complete, absent: minute. SUP: scattered, some large and oriented radial to mouth. DEM: dorsai, dorsai and ventrai. NA: equidistant between eye and snout. VT: dextrai. EP: laterai. SP: low on left side without mediai waii. UJ: medium, prominent mediai convexity. LJ: medium, open V-shaped. BS: oval/compressed. DF: low, originates near or anterior to dorsai taii-body junction, tip pointed. CP: body uniformly paie, tail s i d a r or with distai portion darker. TL: 39/36. NO: ventrai h extends onto abdomen and higher than ventrai fin; vent tube not associated with ventrai fin. CI: Da Cruz (1980,1982); Heyer et ai. (1990). Phlynomedusa: CO: 5. G R Brazii. EMG: exotroph: lentic: suspension-rasper.LTRP: 2/ 3(1), 2(2)/3(1). OA: typicai: anteroventrd. MP: complete: bi- or multiserial. SUP: few to many lateraiiy. DEM: absent. NA: nearer snout than eye. VT: dextrai. EP: lateral. SP: low on left side without mediai waii. UJ: medium, smooth arc. LJ: medium, open Vshaped. DP: low, originates near dorsai taii-body junction, tip pointed. BS: ovai/compressed. CP: uniformiy paie. TL: 3046/28-38. NO: ventrai h often higher than dorsai h.CI: Da Cruz (1982); Heyer et ai. (1990); Izecksohn and Da Cruz (1976). Phyllomedusa: CO: 28. G R Costa Rica-Argentina. EMG: lentic: suspension-rasper. LTRE: 2(2)/3/(1). OA: typicai: anteroventrai.MP: medium dorsai gap: uni- and biseriai, sometimes with ventrai gap. SUP: few lateraiiy. DEM: absent. NA: nearer snout than eye. VT: dextrai. EP: laterai. SP: low on left side without mediai wall. UJ: medium, smooth arc with straight area medially. LJ: medium, V-shaped. BS: oval/compressed. DF: low, originates anterior of dorsai taii-body junaion, taii pointed with flagellum. CP: umformiy paie; diflüse yeliow, orange to black area common in anterior part of lower h.TL: 30-50133-37. NO: ventrai h higher than dorsai fin and extends anteriorly onto abdomen. CI: Cei (1980); Da Cruz (1982); Duellman (1970).
Phyllomedusa
HYPEROLIIDAE: CO: 191232. G R sub-Saharan Africa-Madagascar. EMG: exotroph: lentic: benthic, nektonic; lotic: benthic. LTRP: variations between 010 and 513; 113 most commoniy. OA: typicai: anteroventrai,terminal. MP: medium to wide dorsai gap, sometimes narrow ventrai gap: uni- and biseriai. SUP: absent, few laterally, throughout extent of marginal papdlae. DEM: absent. NA: often small, usually nearer snout than eye. VT: dextrai, mediai. EP: laterai, dorsai. SP: sinistrai. UJ: narrow to wide and massive, smooth arc or mediai convexity, coarse serrations in some. LJ: narrow to wide, U- or V-shaped. DF: low, originates near dorsai taii-body junction, tip pointed to rounded or very high, originates anterior to dorsai td-body junaion, tip pointed as flagellum. BS: oval/depressed and compressed. CP: variable -usuaiiy rather uniform, may have striped taii or tip black. TL: 25-85/36. Hyperoliinae: CO: 121161. G R Africa-Madagascar-Seychelie Islands. AcanthiXalus: CO: 1. G R Cameroon-Zaire. EMG: exotroph: lentic arboreai. LTRE: 4(24)/3. OA: typicai: subterminai. MP: wide dorsai and narrow ventrai gaps: biseriai. SUP: abundant centripetally around lower labium. DEM: absent. NA: nearer snout than eye. VT: mediai. EP: dorsai. SP: sinistrai. UJ: wide, large mediai convexity. LJ: wide, Amnthhalw
RONALD ALTIG AND ROY W. McDIARMID
open U-shaped. DF: low, originates near dorsal taii-body junction, tip rounded. BS: oval/ depressed. CP: udormly dark. TL: 52/33. CI: Lamotte et al. (1959a). Af7walus: CO: 28. GR: sub-Saharan Africa. EMG: exotroph: lentic: benthic. LTRE O/ 0, 011. OA: typical: nearly terminal. MP: wide dorsal gap: uni- and biserial ventraiiy, large, widely spaced. SUP: few rnidventrdy. DEM: absent. NA: very smaii, nearer snout than eye, or reverse. VT: dextral. EP: lateral. SP: sinistral. UJ: wide, smooth arc or with medial convexity, serrations often coarse. LJ: wide, smooth arc. DF: low, originates near dorsal tail-body junction, tip pointed. BS: oblongldepressed. CP: uniformly dotted. TL: 30-65136. NO: ecomorphologicalguild poorly known, may in fact be occur in midwater or near the surface. CI: Drewes et al. (1989); Pickersgiii (1984); Schgtz (1967, 1975). Aiextmoon: CO: 1. GR: Cameroon. EMG: exotroph: lotic: benthic. LTRF: 2(2)/3(1). OA: typical: anteroventral. MP: wide dorsal gap: uniserial. SUP: single row from tip of A-1. DEM: absent. NA: nearer snout than eye. VT: dextral. EP: dorsal. SP: sinistral. UJ: medium, broad arc with medial area straight, coarsely serrate. LJ: medium, open Ushaped. DF: low, originates near dorsal taii-body junction, tip slightly pointed. BS: oval/ depressed. CP: uniformly brown, margins of fins largely unpigmented. TL: 29/33. CI: Amiet (1974b). Arleguinus: CO: 1. GR: Cameroon. EMG: exotroph: lentic: benthic. LTRF: 113. OA: typical: anteroventral. MP: medium dorsal gap: uniserial. SUP: many throughout the extent of the marginal papillae. DEM: absent. NA: nearer snout then eye. VT: dextral. EP: lateral. SP: sinistral. UJ: medium, smooth arc. LJ: medium, open U-shaped. DF: low, originates near dorsal td-body junction, tip pointed. BS: oval/depressed. CP: black stripe the length of dorsal haif of taii musde and body bordered above and below with pale stripes; dorsum of taii musde white. TL: 43/36. NO: adult pattern appears before metamorphosis. CI: Amiet (1976). Callkalus: CO: 1. GR: Rwanda-Zaire. Tadpole unknown. Chlorolius: CO: 1. GR: Cameroon-Gabon. EMG: exotroph: lentic: benthic. LTRE 1/ 3(1). OA: typical: anteroventral. MP: wide dorsal gap: uniserial. SUP: single row dosely adjacent to marginal papillae laterdy and ventraiiy. DEM: absent. NA: nearer snout than eye. VT: dextral. EP: lateral. SP: sinistral. UJ: wide, slight convexity mediaiiy, coarsely serrate. LJ: medium, V-shaped. DF: low, originates near dorsal td-body junction, tip pointed. BS: oval/depressed. CP: uniform body pigmentation with pale lines from snout to eyes; distal haifof tail lightly pigmented. TL: 38/36. CI: Amiet (1976). Chrysobatrachus: CO: 1. GR: Zaire. Tadpole unknown. Cwtothylux: CO: 2. GR: Cameroon-Zaire. EMG: exotroph: lentic: benthic. LTRF: 1/ 3. OA: typical: anteroventral. MP: wide dorsal gap: uniserial. SUP: single row extending from A-1. DEM: absent. NA: nearer snout than eye. VT: -. EP: dorsal. SP: sinistral. UJ: medium, serrated edge describes a smooth arc. LJ: narrow, open U-shaped. DF: low, originates near dorsal td-body junction, tip pointed. BS: oblongldepressed. CP: body brown, td faintly striped. TL: 22/26. CI: Larnotte et ai. (1959b). Hetwixalus: CO: 7. GR: Madagascar. EMG: exotroph: lentic: benthic. LTRF: 1/3(1). OA: typical: anteroventral. MP: medium dorsal gap: uniserial. SUP: few lateraiiy and row inside marginal papiilae of lower labium. DEM: absent. NA: nearer snout than eye. VT: medial. EP: lateral. SP: sinistral. UJ: medium, wide, smooth arc, coarsely serrate. LJ: medium, open V-shaped. DF: low, originates near dorsal tail-body junction, tip rounded. BS: oval/compressed. CP: uniform body, blotched t d . TL: 35/36. CI: Arnoult and Razarihelisoa (1967); Blommers-Schlosser (1982); Blommers-Schlosser and Blanc (1991). Hyprolius: CO: 116. GR: sub-Saharan Africa. EMG: exotroph: lentic: benthic. LTRF: 1/3[1], 213. OA: typical: anteroventral. MP: wide dorsal gap: uni- and biserial, ventral papillae sometimes elongate. SUP: absent. DEM: absent. NA: aperture margin sometimes papiilate. VT: dextral. EP: lateral. SP: sinistral. UJ: wide, smooth arc or slight medial convexity, serrations coarse. LJ: wide, open U-shaped. DF: low, originates near dorsal taii-body junction, tip pointed. BS: oval/depressed. CP: variable: unicolored or striped tail, td tip black, fin margins dark. TL: 30-50136. NO: P-3 usuaiiy much shorter than P-2. CI: Amiet (1979); Channing and De Capona (1987); Lamotte and Perret (1963~);Schigtz (1967,1975).
DIVERSITY
Kassinula: CO: 1. GR: Zambia-Zaire. Tadpole unknown. Neswnixalus: CO: 2. GR: Sao Tomé. Tadpole unknown. Kassininae: CO: 5/21. GR: sub-Saharan Africa. Kasrina: CO: 13. GR: sub-Saharan Africa. EMG: exotroph: lentic: nektonic. LTRF: l/ 2(1) or 113. OA: typical: anteroventral. MP: dorsal gap: wide; ventral gap: narrow or absent. SUP: numerous lateraiiy. DEM: absent. NA: closer to snout than eye. VT: medial. EP: lateral. SP: sinistral. UJ: massive, smooth but prominent arc. LJ: massive robust, very widely V-shaped, at least medially. DF: very hgh, originates weii anterior to dorsal tail-body junction, tip pointed. BS: oval/compressed. CP: clear parts of taii fins often red or orange. TL: to 83/36. NO: keratinized area on lower disc below jaw sheath sometimes present. CI: Largen (1975); Schigtz (1975); Wager (1986). Opistbothyfw: CO: 1. GR: Cameroon-Zaire. EMG: exotroph: lotic: benthic. LTRF: O/ O. OA: typical: reduced. MP: wide dorsai gap: uniserial and large. SUP: absent. DEM: absent. NA: tiny, nearer the snout than the eye. VT: dextral. EP: dorsal. SP: sinistral. UJ: very narrow, smooth arc. LJ: wider than upper, open V-shaped. DF: low, originates near dorsal tad-body junction, tip slightly pointed. BS: ovalJdepressed. CP: body brown, fins and taii muscle mottled; throat dark. TL: 26/36. CI: Arniet (1974a). Parwssina: CO: 2. GR: Ethiopia. EMG: exotroph: lentic: nektonic. LTRF: 1/3(2). OA: typicai: anteroventral. MP: wide dorsai gap, very narrow ventral gap where P-3 positioned. SUP: many lateraiiy. DEM: absent. NA: -. VT: medial. EP: lateral. SP: sinistral. UJ: massive, serrated edge describes smooth arc. LJ: massive, open V-shaped. DE: tall, highIy arched, originates weli anterior of the dorsal tail-body junction, tip pointed. BS: oval/compressed. CP: uniformly dark on body, taii dark in distai third. TL: 54/36. NO: keratinized area posterolateral to lower jaw sheath. CI: Largen (1975). Phlyctimantis: CO: 4. GR: Ivory Coast-Tanzania. EMG: exotroph: lentic: benthic. LTRF: 1/3[1-21. OA: typical: anteroventral. MP: wide dorsal gap: biserial. SUP: numerous throughout extent of marginal papiiiae. DEM: absent. NA: nearer snout than eye. VT: medial. EP: dorsal. SP: sinistral. UJ: wide, serrated margin describes a fairly uniform arc. LJ: medium, open U-shaped. DF: low, originates near dorsal taii-body junction, tip pointed. BS: oval/depressed. CP: uniformly pale with blotches. TL: 49/34. NO: P-3 exceptionally short. CI: Guibé and Lamotte (1958); Schi~tz(1975). S e m v w ~ l u s CO: : 1. GR: South Africa. EMG: exotroph: lentic: nektonic. LTRE 1/ 3(1). OA: typical: anteroventral. MP: dorsal gap: biserial. SUP: few lateraiiy. DEM: absent. NA: nearer snout than eye. VT: dextral. EP: lateral. SP: sinistral. UJ: wide, coarsely serrate. LJ: massive, open U-shaped. DE: high, originates on body, tip pointed. BS: ovai/compressed. CP: distinct dark stripe on taii muscle. TI,:58/36. NO: P-3 exceptionally short. CI: Wager (1986). Leptopelinae: CO: 1/49. GR: sub-Saharan Africa. EMG: exotroph: lentic: benthic. LTRF: 3-5/3[1], usually 2-n rows on upper labium broken medially. OA: typical: anteroventral. MP: wide dorsal gap: uniserial dorsaiiy, biserial ventrally. SUP: absent. DEM: absent. NA: smaii, nearer snout than eye. VT: dextral. EP: dorsai. SP: sinistral. UJ: wide, medial indentation. LJ: wide, V-shaped. DP: low, originates near dorsal taii-body junction, tip pointed. BS: oval/depressed. CP: uniformly dark. TL: 49/36. Leptopelis: CO: 49. CI: Drewes et ai. (1989); Lamotte and Perret (1961b); Lamotte et ai. (1959b); Schi0tz (1967, 1975). Tachycneminae: CO: 111. GR: Seycheile Islands. EMG: exotroph: lotic: benthic. LTRF: 3(211)/3. OA: typicai: anteroventral. MP: wide dorsai gap: uniseriai midventraiiy. SUP: -. DEM: absent. NA: very smaii, nearer to snout than eye. VT: dextrai. EP: dorsai. SP: sinistral. UJ: wide, broad arch. LJ: medium, V-shaped. DP: low, originates distal to body. BS: oval/depressed. CP: uniformly paie brown, venter clear in preservative. TI,: 44/27. TachynemZr: CO: 1. GR: Seycheile Islands. CI: specimens. LEIOPELMATIDAE: CO: 113 GR: New Zeaiand. EMG: endotroph. Leiopelma: CO: 3. GR: New Zeaiand. EMG: endotroph. LEPTODACTYLIDAE: CO: 481850. GR: southern United States-South ArnericaCaribbean. EMG: exotroph: lentic: various guilds; lotic: various guilds; endotroph. LTRF: many variations between 010 and 919, 213 most common. OA: typical: anteroventrai or aii
LeptopeLis
RONALD ALTIG AND ROY W. McDIARMID
Lepiriobatracbus
keratinized mouthparts absent. MP: medium to wide dorsal gap, complete, narrow ventral gap: uni- and biserial. SUP: absent, few laterally or dorsolateraiiy. DEM: absent, lateral. NA: nearer snout than eye or reverse. VT: medial, dextral or sinistral. EP: dorsal. SP: sinistral except in Lqt'dubatrachus (dual/lateral). UJ: variable, narrow to wide, usually a smooth arc, incised or not. LJ: variable, narrow to wide, U to V-shaped. DF: low, originates near, slightiy anterior to or weii posterior to the dorsal tail-body junction, tip rounded to pointed. BS: round, oval to oblong/depressed. CP: variable but uniformly dark is cornmon. TL: 15-1301 36. Ceratophryinae: CO: 6/33. G R South America. Ceratophlys: CO: 8. G R South America. EMG: exotroph: lentic: benthic, often carnivorous and spends considerable time swimming in midwater. LTRF: 6(3-6)/7(3), 9(7-9)/ 9(1-3) but teeth often lost. OA: typical: nearly terminal. MP: complete: large and sparsely distributed. SUP: absent. DEM: absent. NA: nearer snout than eye, or reverse. VT: medial, dextral or sinistral. EP: dorsal. SP: sinistral. UJ: wide, medial notch. LJ: wide, medial convexity complimentary to upper sheath. DE: low, originates near dorsal taii-body junction, tip pointed. BS: oval/depressed. CP: mostiy uniformly dark. TL: 40-70136. NO: jaw musculature hypertrophied. CI: Cei (1980); D u e h a n (1978); Honegger et ai. (1985). Champhlys: CO: 1. G R Argentina. EMG: exotroph: lentic: benthic. LTRF: 1/2(1). OA: typical: anteroventral. MP: complete: uniserial, widely spaced. SUP: absent. DEM: lateral. NA: large, nearer snout than eye. VT: medial. EP: dorsal. SP: sinistral. UJ: wide, smooth arc. LJ: wide, open V-shaped. DF: low, originates at dorsal td-body junction, tip pointed. BS: oval/depressed. CP: uniformly gray, tail muscle bicolored. TL: 40136. NO: unique flap projects upward from tip of snout. CI: Faivovich and Carrizo (1992). Lepidubatvachus: CO: 3. G R southern South Arnerica. EMG: exotroph: lentic: carnivore. LTRF: 010. Ok. slitlike mouth exceptiondy large and terminal. MP: complete: uniserial. SUP: absent. DEM: absent. NA. nearer eye than snout. VT: medial. EP: dorsal. SP: dual and lateral, but not homologous to spiracles of pipids and rhinophrynids. UJ: few, widely spaced jaw serrations without basai sheaths on one or both jaws. LJ: see upper jaw. DF: low, originates near dorsal taii-body junction, tip broadly pointed. BS: round/strongly depressed, widest near plane of eyes. CP: unúormly gray or faintiy mottied. TL: 40-60136. NO: Cei (1980) states that L. llanensis has one upper and one lower tooth row; based on our observations of L. 1 4 , we note that these are actually isolated jaw serrations, tooth rows are absent; this condition probably occurs in aii three species. CI: Cei (1980); Ruibal and Thomas (1988). M ~ * c y ~ e ' n w ~ ~ CO: t t u s :1. GR: Brazii. EMG: exotroph: lentic: benthic. LTRF: 2(2)/ 3(1). OA: typical: anteroventral. MP: wide dorsal gap: uniserial. SUP: absent. DEM: lateral. NA: equidistant between eye and snout. VT: dextral. EP: dorsal. SP: sinistral. UJ: very narrow, wide, smooth arc, serrations lacking. LJ: very narrow, open U-shaped, serrations laterally. DF: low, originates at dorsal taii-body junction, tip pointed. BS: oblong/depressed. CP: brownish-gray, reticulated with nonpigmented areas, dorsurn of tail muscle banded, edges of fins with black areas. TL: 35/30. CI: Abravaya and Jackson (1978). Oduntophrynus: CO: 8. G R eastern and southern South America. EMG: exotroph: lentic: benthic, lotic: benthic. LTRF: 2(2)/3[1.]. OA: typical: anteroventral. MP: medium dorsal gap: uniserial. SUP: absent. DEM: absent. NA: nearer eye than snout. VT: dextrai. EP: dorsal. SP: sinistral. UJ: wide, smooth arc. LJ: wide, open U-shaped. DF: low originates near dorsal tail-body junction, tip pointed. BS: oval/depressed. CP: body dark, taii uniform to blotched. TL: 35-45/36. CI: Cararnaschi (1979); Cei (1980). Proceuatuphlys: CO: 12. G R Brazii-Paraguay. EMG: exotroph: lentic: benthic. LTRF: 2/3(1), 2(2)/3(1). OA: typical: anteroventral. MP: wide dorsal gap: uniserial. SUP: absent, few anterolateral. DEM: lateral, two ventrolateral. NA: large, not round, nearer eye than snout. VT: dextral. EP: dorsal. SP: sinistral. UJ: wide, smooth arc. LJ: wide, open V-shaped. DF: low, originates near tail-body junction, tip rounded. BS: oval/depressed. CP: tail muscle weakly banded, body and fins speckied. TL: 33/36. CI: Da Cruz and Peixoto (1980b); Izecksohn et al. (1979). Hylodinae: CO: 3/28. G R eastern and southern South America. Crosso~Lus:CO: 9. G R southern South America. EMG: exotroph: lotic: benthic.
DIVERSITY
LTRF: 3(1,3)/5,2(2)/3[1]. OA: typicai: anteroventrd. MP: medium dorsai gap: uniseriai. SUP: absent. DEM: absent. NA: nearer eye than snout. VT: dextral. EP: dorsai. SP: sinistrai. UJ: wide, uniform arc and coarsely serrate. LJ: wide, open U-shaped, coarsely serrate. DF: low, originates near dorsai taii-body junction, tip rounded. BS: oval/ depressed. CP: body uniformiy dark, taii and fins with dark specks. TL: 52/37. CI: Caramaschi and Kisteumacher (1989); Caramasch and Sazima (1985); Cei (1980). Hylodes: CO: 15. GR: eastern South America. EMG: exotroph: lotic: benthic. LTRP: 2(2)/3[1], 2(2)/4. OA: typicai: anteroventrai. MP: medium dorsai gap: uniseriai. SUP: absent, few lateraüy. DEM: lateral. NA: nearer eye than snout. VT: dextral. EP: dorsal. SP: sinistral. UJ: wide, smooth arc but coarsely serrate, mediai serration hypertrophied. LJ:wide, open U-shaped, coarsely serrate. DF: low, originates near dorsai taii-body junction, tip pointed. BS: ovai/depressed. CP: uniformiy dark. TL: 36/25. CI: Bokermann (1966); Heyer et ai. (1990); Sazima and Bokermann (1982). Mguelosia: CO: 4. GR: Brazil. EMG: exotroph: lentic: benthic. LTRF: 2(2)/3(1). OA: typicai: anteroventrd. MP: wide dorsal gap: smaü and uniserial. SUP: few lateraüy near emargination and below P-3. DEM: lateral. NA: smaü, nearer snout than eye. VT: dextrai. EP: dorsal. SP: sinistrai. UJ: wide, edge describes smooth arc. LJ: wide, V-shaped. DF: low, originates near dorsai tail-body junction, tip pointed. BS: oval/depressed. CP: uniforrnly dark. TL: 128125. CI: Giarretta et ai. (1993); Heyer et ai. (1990). Leptodactylinae: CO: 101121. GR: southem Texas-Chle-Antilies. Adenomera: CO: 6. GR: South America east of Andes. EMG: endotroph. NO: De la Riva (1995), based on observations in Bolivia, noted that aü species ofAdenomera are not entirely endotrophic; if the larvae of some forms gain access to free water, they can develop as typical lentic-inhabiting, leptodactylid tadpoles and resemble the tadpoles of some Leptodactylus spp., LTRF 2(2)/3(1). CI: De Ia Riva (1995); Heyer and Silverstone (1969). Edahhinu: CO: 2. GR: Colombia-Peru. EMG: exotroph: lentic: benthic. LTRF: 2(2)/ 3(1). OA: typicai: anteroventral. MP: dorsal gap: biseriai. SUP: few dorsolaterdy. DEM: absent. NA: equidistant between eye and snout. VT: dextrai. EP: dorsal. SP: sinistrai. UJ: narrow, wide uniform arc. LJ: medium, open U-shaped. DF: low, originates near dorsai taii-body junction, tip rounded. BS: ovai/depressed. CP: uniformly pale brown. TL: 14/25. CI: De Ia Riva (1995); Schiuter (1990). Hydroluetare: CO: 1. GR: Colombia-Peru. Tadpole unknown. Leptodaqlus: CO: 50. GR: southern Texas-Mexico-South America-West Indies. EMG: exotroph: lentic: benthic. LTRF: 213, 2(2)/3[.L]. OA: typicai: anteroventral. MP: medium to wide dorsai gap: uniserial, narrow ventral gap rarely. SUP: absent. DEM: laterai, absent. NA: nearer snout than eye. VT: medial. EP: dorsai. SP: sinistrai. UJ: narrow to medium, wide smooth arc. LJ: narrow to medium, U- or V-shaped. DF: low, originates Lept0-h~; L. melanonotw near dorsai tail-body junaion, tip rounded to pointed. BS: ovai/depressed. CP: often uniformiy dark. TL: 25-60136. NO: tadpoles of 4-5 species groups can be recognized by features more subtle than presented here. CI: Cei (1980); Heyer (1973a); Sazima ~eptoakty1w;L. pentaductyLus and Bokermann (1978). Lithodytes: CO: 1. GR: Venezuela-Ecuador-Peru. EMG: exotroph: lentic: benthic. LTRF: 2(2)/3(1). OA: typicai: anteroventrai. MP: wide dorsai gap. SUP: absent. DEM: absent. NA: nearer snout than eye. VT: mediai. EP: dorsai. SP: sinistrai. UJ: medium, smooth arc. LJ: narrow, wide, open U-shaped. DF: low, originates near dorsai taii-body junction, tip rounded. BS: oval/depressed. CP: uniformiy dark. TL:47/34. NO: large lower labium extends far beyond lower tooth row. CI: Lamar and Wild (1995); Regos and Schiuter (1984). Paratelmutobius: CO: 3. GR: Brazil. EMG: exotroph: lotic or lentic: benthic. LTRF: 2(2)/3(1). OA: typicai: anteroventrai. MP: wide dorsal gap: uniseriai midventraüy. SUP: absent. DEM: lateral, absent. NA: nearer eye than snout. VT: dextrai, mediai. EP: dorsai. SP: sinistrai. UJ: narrow, edge a smooth arc. LJ: medium, open U-shaped. DF: low, originates near dorsai tail-body junaion, tip bluntly pointed. BS: oval/depressed. CP: uniformiy paie brownish, belly lightly pigmented, fins nonpigmented to brownish, tail muscle blotched. TL: 26-32/37. CI: Cardoso and Haddad (1990); Giarretta and Castanho (1990). Physaluemus: CO: 37. GR: Mexico-South Arnerica. EMG: exotroph: lentic: benthic.
RONALD ALTIG AND ROY W. McDIARMID
LTRF: 2(2)/2,2/3(1),2(2)/3(1).OA: typical: anteroventral. MP: wide dorsal gap: uniserial, sometimes ventral gap. SUP: few laterdy. DEM: lateral. NA: equidistant between snout and eye. VT: dextral. EP: dorsal. SP: sinistral. UJ: wide, smooth arc. LJ: medium, open V-shaped. DF: low, originates near dorsal td-body junction, tip pointed. BS: oval/ depressed. CP: uniformly dark, mottied. TL: 23/38. NO: some (e.g., l?petersi) with prominent, white glands on body. CI: Barrio (1953); Heyer et al. (1990). Pieurodema: CO: 12. GR: southern South America. EMG: exotroph: lentic: benthic. LTRF: 2(2)/2, 2(2)/3[1]. OA: typical: anteroventral. MP: wide dorsal gap: uniserial, ventral gap sometimes. SUP: rare lateraiiy. DEM: lateral. NA: nearer eye than snout. VT: medial. EP: dorsal. SP: sinistral. UJ: medium, smooth arc. LJ: medium, U-shaped. DF: low, originates near dorsal tail-body junction, tip rounded. BS: oval/dcpressed. CP: uniformly dark, tail muscle mottied. TL: 25/36. CI: Cei (1980); Leon-Ochoa and Donoso-Barros (1970); Peixoto (1982). Pseudopaludicoiu: CO: 8. GR: southern South America. EMG: exotroph: lentic: benthic. LTRF: 2(2)/3. OA: typical: anteroventral. MP: wide dorsal and narrow ventral gaps: uniserial. SUP: row(s) ventrolaterdy. DEM: lateral. NA: nearer snout than eye. VT: dextral. EP: dorsal. SP: sinistral. UJ: medium, wide smooth arc. LJ: medium, wide Ushaped. DF: low, originates near or anterior to dorsal tail-body junction, tip pointed. BS: oval/depressed. CP: uniformly dark. TL: 22/36. CI: Barrio (1953); Cei (1980). Vanwlinius: CO: 1. GR: Ecuador-Peru. EMG: exotroph: lentic: benthic. LTRF: 213. OA: typical: anteroventral. MP: dorsal gap: uniserial. SUP: -. DEM: lateral. NA: nearer eye than snout. VT: medial. EP: dorsal. SP: sinistral. UJ: narrow. LJ: narrow. DF: low, originates near dorsal tail-bodyjunction, tip rounded. BS: oval/depressed. CP: uniformly tan or brown. TL: 25/30. CI: Duellman (1978). Telmatobiinae: CO: 291668. GR: central to southern South America. Adelopbqvne: CO: 2. GR: Guiana Shield. EMG: endotroph. Alsodes: CO: 11. GR: Chile-Argentina. EMG: exotroph: lotic: benthic. LTRF: 2(2)/ 3(1). OA: typical: anteroventral. MP: wide dorsal gap: uniserial. SUP: few dorsolateraiiy and row(s) distal to P-3. DEM: lateral. NA: equidistant between eye and snout, nearer eye than snout. VT: dextral. EP: dorsal. SP: sinistral. UJ: wide, smooth arc. LJ: wide, open V-shaped. DF: low, originates distal to dorsal td-body junction, tip broadly rounded to pointed. BS: oval/depressed. CP: uniformly dark, few s m d spots on t d . TL: 60-75136. CI: Diaz and Valencia (1985). Atelognathus: CO: 7. GR: Chile-Argentina. EMG: exotroph: lentic: benthic. LTRF: 2(2)/3(1).OA: typical: anteroventral. MP: medium dorsal gap: uniserial. SUP: few lateraiiy. DEM: lateral. NA: equidistant from eye and snout. VT: dextral. EP: dorsal. SP: sinistral. UJ: wide, medial zone of serrate edge straight. LJ: wide, open V-shaped. DF: low, originates near dorsal tail-body junction, tip pointed. BS: oval/depressed. CP: brown, sparsely pigmented, belly transparent. TL: 57/36. CI: Cei (1964, 1980). Atqpqphlynus: CO: 1. GR: Colombia. Tadpole unknown. Baqvcholos: CO: 2. GR: Ecuador-Brazil. EMG: endotroph. Batrachqphqvnus: CO: 2. GR: Peru-Bolivia. EMG: exotroph: lentic: benthic. LTRF: 2(2)/3(1). OA: typical: anteroventral. MP: wide dorsal gap: biserial. SUP: throughout extent of marginal papillae. DEM: absent. NA: -. VT: medial. EP: dorsal. SP: sinistral. UJ: wide, smooth arc. LJ: wide, open U-shaped. DF: low, originates at dorsal td-body junction, tip broadly rounded. BS: oval/depressed. CP: uniformly dark, smaii spots on fins. TL: 67/26. CI: Sinsch (1990). Bamachyla: CO: 3. GR: ChdeArgentina. EMG: exotroph: lentic: benthic. LTRF: 2(2)/ 3(1). OA: typical: anteroventral. MP: wide dorsal gap: uniserial. SUP: dorso- and ventrolaterdy. DEM: lateral. NA: equidistant between eye and snout. VT: dextral. EP: dorsal. SP: sinistral. UJ: medium, smooth arc. LJ: medium, open V-shaped. DF: lou; originates near dorsal tail-body junction, tip roiinded. BS: oval/depressed. CP: uniformly dark, t d speckled. TL: 27-37/33. NO: early stages develop like nidicolous endotrophs. CI: Cei (1980); Cei and Capurro (1958); Formas and Pugín (1971). Caudiverbera: CO: 1. GR: Chile. EMG: exotroph: lotic: benthic. LTRF: 2(2)/3(1).OA: typical: anteroventral. MP: medium dorsal gap: uniserial. SUP: few laterdy. DEM: lateral. NA: nearer snout than eye. VT: dextral. EP: dorsal. SP: sinistral. UJ: narrow, edge describes smooth arc. LJ: narrow, open U-shaped. DF: low, originates at dorsal tail-body
DIVERSITY
junction, tip pointed. BS: ovai/depressed. CP: paie green in life, distai third of tail dark. TL: 95/37. NO: Cei (1962) shows a LTRF of 3(2)/3(1) and p-2 and P-3 with nonrnedial gaps. CI: Diaz and Vaiencia (1985); Jorquera and Izquierdo (1964). Cromductylodes: CO: 3. GR: Brazil. EMG: exotroph: lentic: arboreai. LTRF: 2(2)/3. OA: typicai: anteroventral. MP: wide dorsai gap: uniserial. SUP: absent. DEM: laterai. NA: nearer snout than eye. VT: dextrai. EP: dorsai. SP: sinistrai. UJ: medium, small but prominent mediai convexity, basai margin aiso with convexity. LJ: medium, open Vshaped. DF: low, originates near dorsai tail-body junction, tip round. BS: oblong/depressed. CP: uniforrnly dark. TL: 19/35. CI: Peixoto (1981). Cycloramphus: CO: 25. GR: Brazil. EMG: exotroph: lotic: semiterrestriai; endotroph. LTRF: 213, 2(1-2)/3(1), 2/3(1), 2(1)/3(1). OA. typicai: anteroventral, ventrai. MP: wide dorsai gap: uniseriai. SUP: absent. DEM: absent. NA: see notes. VT: mediai. EP: dorsai. SP: sinistral. UJ: medium, strongly arched. LJ: medium, strongly arched. DF: low, originates weli posterior of dorsai tail-body junction, tip pointed. BS: oblong to oval/depressed. CP: umform to mottled, tail muscle may be slightly banded. TL: 2 0 4 0 1 36. NO: Heyer et ai. (1990) reported nares absent in C. boraceiensis but seem apparent in figure; Heyer (1983a, b) did not locate a spiracle on C. boraceiensis or C. v a h ; may have parts of abdominal w d expanded as a free flap. CI: Heyer (1983a, b). Dirchidodagylus: CO: 2. GR: Venezuela. EMG: endotroph. Eíeutherodactylus: CO: 515. GR: North, Central, and South America-Caribbean. EMG: endotroph. Euparkerella: CO: 4. GR: Brazil. EMG: endotroph. Eupsophw: CO: 8. GR: Chile-Argentina. EMG: endotroph. Geobatrachus: CO: 1. GR: Colombia. EMG: endotroph. Holoaden: CO: 2. GR: Brazil. EMG: endotroph. Hylorina: CO: 1. GR: Chile-Argentina. EMG: exotroph: lentic: benthic. LTRP: 2(2)/ 3(1). OA: typicai: anteroventral. MP: wide dorsal gap: uniserial. SUP: few centripetally arranged throughout extent of marginai papiilae. DEM: laterai. NA: equidistant between snout and eyes. VT: dextrai. EP: dorsai. SP: sinistrai. UJ: wide, serrated edge alrnost transversely straight. LJ: wide, open U-shaped. DF: somewhat arched, originates near dorsai tail-body junction, tip broadiy rounded. BS: oval/depressed. CP: uniform with dark spots throughout t d . TL: 51/38. CI: Barrio (1976); Formas and Pugín (1978). Insuetophlynw: CO: 1. GR: Chile. EMG: exotroph: lotic: benthic. LTRF: 2(2)/2(1-2) or' less. OA: typicai: ventrai, jaw sheaths and labial tooth rows reduced. MP: medium dorsai gap: uniserial, papillae very s m d . SUP: absent. DEM: absent. NA: s m d , nearer eye than snout. VT: dextrai. EP: dorsai. SP: sinistrai. UJ: s m d , weakly developed but serrate. LJ: similar and U-shaped. DF: low, originates at dorsai td-body junction, tip broadiy rounded. BS: ovai/depressed. CP: greenish brown in life, irregularly mottled. TL: 61/37. NO: lower tooth rows sometimes absent, one drawing of oral variation shows complete marginal papiiiae, laterai line visible. CI: Diaz and Vaiencia (1985); Formas et al. (1980). Ischnucnema: CO: 3. GR: Amazonia-Brazil. EMG: endotroph. Limnumedusa: CO: 1. GR: Brazil-Argentina. EMG: exotroph:. LTRF: 2(2)/3(1). OA: typicai: anteroventral. MP: medium dorsai gap: uniserial. SUP: numerous aiong d marginal papiiiae. DEM: laterai. NA: nearer eye than snout. VT: mediai. EP: dorsai. SP: sinistrai. UJ: wide, uniform arc. LJ: medium, open U-shaped. DF: low, originates near dorsai tail-body junction, tip pointed. BS: ovai/depressed. CP: body uniform, tail boldiy spotted. TL: 42/34. CI: Cei 1980; Gehrau and De Sá (1980). Phlynupus: CO: 20. GR: Andean South America. EMG: endotroph. Phyllonaster: CO: 4. GR: Pem-Ecuador. EMG: endotroph. Phyzelaphlyne: CO: 1. GR: Brazil. EMG: endotroph. Scythrophlyr: CO: 1. GR: Brazil. Tadpole unknown. Somuncuria: CO: 1. GR: Argentina. EMG: exotroph: lotic: benthic. LTRF: 2(2)/3(1). OA: typicai: anteroventral. MP: wide dorsai and smaüer ventral gaps: biseriai. SUP: absent. DEM: lateral. NA: equidistant between eye and snout. VT: dextrai. EP: dorsai. SP: sinistrai. UJ: wide, smooth arc, or perhaps a slight mediai concavity in margin. LJ: wide, open U-shaped. DF: low, originates near dorsai tail-body junction, tip rounded. BS: ovai/depressed. CP: body dark, tail blotched. TL: 46/36. CI: Cei (1980).
Insuetophvynw
RONALD ALTIG AND ROY W. McDIARMID
Thoropa
L.eptobracheUa
Lqtobrnchium
Telmatobius: CO: 35. GR: Ecuador-Argentina. EMG: exotroph: lentic: benthic; lotic: benthic. LTRF: 2(2)/3(1). OA: typical: anteroventral. MP: wide dorsal gap: uni- and biserial. SUP: few dorsolateraiiy, lateraliy and distal to P-3. DEM: lateral. NA: equidistant between eye and snout. VT: dextral. EP: dorsal. SP: sinistral. UJ: wide, edge a smooth arc. LJ: wide, open U-shaped. DF: low, originates near dorsal taii-body junction, tip rounded to pointed. BS: oval/depressed. CP: uniform to muted motthng. TL: 60100137. CI: Diaz and Valencia (1985); Lavilla (1984a, 1985,1988). Telmatobufo: CO: 3. GR: Chile. EMG: exotroph: lotic: suctorial. LTRP: 2/3(1). OA: typical: ventral. MP: complete: uniserial. SUP: muitiple rows centripetaiiyto ali marginal papillae except at lateral margins of disc. DEM: lateral. NA: nearer eye than snout. VT: dextral, vent flap underiies tube. EP: dorsal. SP: sinistral. UJ: medium, open V-shaped. LJ: medium, open V-shaped, "internal borders smooth" (Diaz et al. 1983). DF: low, originates weii posterior of dorsal td-body junction, tip broadly pointed. BS: oval/depressed, may narrow appreciably posterior to oral disc. CP: dark brown, orange protuberances over body dorsum. TL: 107140. CI: Diaz et al. (1983); Formas (1972). Thopa: CO: 5. GR: Brazil. EMG: exotroph: lotic: serniterrestrial. LTRP: 2(1-2)/3(1). OA: typical: ventral. MP: wide dorsal gap: uniserial. SUP: absent. DEM: absent. NA: nearer snout than eye. VT: medial. EP: dorsal. SP: sinistral. UJ: medium, strongly arched and coarsely serrate. LJ: wide, strongly arched. DF: low, originates on taii muscle weii posterior to dorsal taii-body junction, almost absent in some, tip rounded. BS: obIongJdepressed. CP: uniform dark to mottled; taii muscle banded. TL: 20-30136. NO: some have parts of lateral margins of abdominal wali expanded as a free flap; nidicolous endotrophs may be involved (Bokermann 1965). CI: Caramaschi and Sazirna (1984). Z1u:haenus: CO: 3. GR: Brazil-Argentina. EMG: endotroph. MEGOPHRYIDAE: CO: 9/79. GR: northern India-China-Philippines. EMG: exotroph: lotic: clasping, neustonic, benthic; endotroph. LTRF: 010 to 717. OA: typical: anteroventral, ventral; umbeliiform: oral disc bi-triangular. MP: narrow dorsal gap, complete, absent: uniserial. SUP: scattered near mouth, few lateraliy, some arranged radialiy to mouth. DEM: absent, dorsal and ventral. NA: equidistant between eye and snout, nearer eye than snout or reverse. VT: dextral, medial. EP: dorsal, lateral. SP: sinistral but weii below longitudinal axis. UJ: absent, medium to wide, smali medial convexity or not. LJ: absent, medium to wide, Uor V-shaped. DF: low, originates near or posterior to dorsal tail-bodyjunaion, tip rounded to pointed. BS: oval to elongate/depressed. CP: muted mottiing to unicolored. TL: 25-75/36. Atympanophys: CO: 1. GR: China. Tadpole unknown. Bv1u:hytamophys: CO: 1. GR: Burma-China-Thdand. Tadpole unknown. Leptubvachelía: CO: 7. GR: Borne+Natuna Islands. EMG: exotroph: lotic: benthic. LTRF: 010. OA: typical: ventral. MP: narrow dorsal gap: uniserial. SUP: scattered near mouth. DEM: dorsal and ventral. NA: nearer snout than eye, one medial projection. VT: dextral. EP: dorsal. SP: sinistral but weii below longitudinal axis. UJ: medium, smali medial convexity. LJ: medium, open U-shaped. DF: low, especialiy in proximal third, originates near dorsal tail-body junction, tip round. BS: oblong/depressed. CP: uniformly dark. TL: 3045/36. CI: Inger (1983,1985). Leptobrachium: CO: 10. GR: Indonesia-China-Philippines. EMG: exotroph: lotic: benthic. LTRP: 3(1-3)/4(1-3) to 7(2-6)/6(1-5). OA: typical: anteroventral to ventral. MP: complete: uniserial. SUP: few lateraliy. DEM: absent. NA: equidistant between eye and snout, 1-3 medial projeaions. VT: dextral. EP: dorsal. SP: sinistral but weii below longitudinal axis. UJ: wide, smooth arc. LJ: wide, wide V-shaped. DF: low, originates near dorsal tail-body junaion, tip pointed to rounded. BS: oval to oblongJdepressed. CP: uniforndy dark. TL: 30-50136. NO: LTRF very variable, integumentary glands sometimes present, submarginal papillae commonly have labial teeth. CI: Berry (1972); Inger (1983, 1985). Leptohh: CO: 7. GR: Burma-China-Borneo. EMG: exotroph: lotic: suctorial, clasping. LTRF: 5(2-5)/3(1-2). OA: typical: ventral. MP: narrow dorsal gap or complete: uniserial. SUP: scattered above and below mouth, probably rudimentary tooth ridges. DEM: dorsal and ventral. NA: nearer snout than eye. VT: dextral. EP: dorsal. SP: sinistrai but weii below longituduial axis. UJ: wide, smooth arc. LJ: wide, open U-shaped. DF: low, particuiarly in first fourth, originates distal to dorsal td-body junction, tip
DIVERSITY
rounded. BS: oblong/very depressed. CP: uniformiy brown. TL: 25-50136. NO: integumentary glands dorsolateraiiy. CI: Inger (1966). MgupInys: CO: 25. GR: Southeast Asia-China-Philippines-Greater Sundas. EMG: exotroph: lotic: neustonic; endotroph. LTRF: 010. OA: umbelliform: bi-triangular. MP: slight crenulations to none. SUP: scattered throughout oral disc, some arranged radiaiiy to mouth. DEM: absent. NA: nearer snout then eye. VT: medial. EP: lateral. SP: sinistral but well below longitudinal axis. UJ: absent, minor keratinization. LJ: minor keratinization. DF: low, originates near or posterior to dorsal td-body junction, tip pointed. BS: oblong/depressed. CP: beily striped in some. TL: 30-50136. CI: Inger (1985); C.C. Liu and Hu (1961); Ye and Fei (1996). Ophryophryne: CO: 3. GR: Vietnam-China. Tadpole unknown. Scutigev: CO: 24. GR: India-China. EMG: exotroph: lotic: benthic, clasping. LTRF: 5(2-5)/4(14), 5(2-5)/6(1-5), 6(2-6)/6(1-5), 7(2-7)/7(1-6). OA: typical: anteroventrai. MP: narrow dorsal gap: uniserial, dorsal gap absent: uniserial. SUP: few lateraüy. DEM: absent. NA: nearer snout than eye. VT: dextral. EP: dorsal. SP: sinistral but well below longitudinal axis. UJ: very wde, smooth arc, very coarsely serrate. LJ: wide, wide U-shaped, coarsely serrate. DF: low, originates near dorsal tail-body junction, tip rounded. BS: oval/depressed. CP: uniformiy dark. TL: 60-75136. NO: C.-C. Liu (1950) showed labial teeth on submarginal papdae. CI: C.-C. Liu (1950). Vibrissaphora: CO: 1. GR: southern Cima. EMG: exotroph: lotic. LTRF: 6(2-6)/4(1), 6(2-6), 6(1-5), A-1 exceptionaiiy short. OA: typical: anteroventral. MP: narrow dorsal gap: uniserial. SUP: few ventrolaterally. DEM: absent. NA: nearer snout than eye. VT: -. EP: dorsal. SP: sinistrai but weil below longitudinal axis. UJ: very wide, narrow Ushaped, very coarsely serrate. LJ: very wide, wide U-shaped, coarsely serrate. DF: low, originates near dorsai tail-bodyjunction, tip rounded. BS: oval/depressed. CP: uniformiy dark body, fins with coarse blotches. TL: -. CI: C.-C. Liu and Hu (1961). MICROHYLIDAE: CO: 651327. GR: North and South America, Mrica, India-KoreaAustropapuan region. EMG: exotroph: lentic: suspension feeder, psarnmonic; endotroph. LTRF: 010. OA: keratinized structures absent (except in Otophyne and Scaphiophlyne); any resemblance to an oral disc absent (except in umbelliformMicvohyla, Nelsonuphryne, Otophryne, and Scaphiophryne), oral apparatus usuaiiy involves semicircular to straight-edged oral flaps pendant over terminal mouth, few species with umbelliform oral disc. MP: not applicable except-in Nelsonuphyne and some endotrophs. SUP: not applicable except perhaps in Nelsonupbryne. DEM: not applicable. NA: usuaiiy absent until metamorphosis but positioned nearer snout than eye. VT: medial, dextral. EP: lateral, dorsal. SP: midventral on chest, abdomen or near vent, appears sinistrai in diflerent configurations in Otophryne and Stereocyclops. UJ: usuaiiy absent but Scaphwpbryne has unpigmented jaw sheaths, Otuphryne has hypertrophied serrations without a basal sheath. LJ: as upper jaw. DF: low, originates near dorsal tail-body junction, sometimes with flagellum. BS: round to oval/depressed. CP: dorsum uniform, sometimes with sagittal line, venter sometimes mottled or striped. TL: 15-35/36. Asterophryinae: CO: 8/49. GR: New Guinea. Asteruphrys: CO: 1. GR: New Guinea. EMG: endotroph. Barygenys: CO: 7. GR: New Guinea. EMG: endotroph. Callulops: CO: 13. GR: New Guinea. EMG: endotroph. Hylophorbus: CO: 1. GR: New Guinea. EMG: endotroph. Mantuphryne: CO: 3. GR: New Guinea. EMG: endotroph. Pherohapsis: CO: 1. GR: New Guinea. EMG: endotroph. Xenoba~acbus:CO: 17. GR: New Guinea. EMG: endotroph. Xenurhzna: CO: 6. GR: New Guinea. EMG: endotroph. Brevicipitinae: CO: 5/19. GR: eastern and southern Afiica. Balebrevimps: CO: 1. GR: Ethiopia. EMG: endotroph. Breuiceps: CO: 13. GR: southern f i c a . EMG: endotroph. Callulina: CO: 1. GR: Tanzania. EMG: endotroph. Probreuiceps: CO: 3 . GR: Tanzania-Zimbabwe. EMG: endotroph. Spelaeuphryne: CO: 1. GR: Tanzania. EMG: endotroph. Cophylinae: CO: 7/36. GR: Madagascar. Anuhnthyla: CO: 4. GR: Madagascar. EMG: endotroph.
320
RONALD ALTIG AND ROY W. McDIARMID
Cophyh: CO: 1. GR: Madagascar. EMG: endotroph. Madecmsophryne: CO: 1. GR: Madagascar. EMG: endotroph. Plittypelis: CO: 9. GR: Madagascar. EMG: endotroph. Plethhntohyla: CO: 14. GR: Madagascar. EMG: endotroph. Rhombophryne: CO: 1. GR: Madagascar. EMG: endotroph. StumpffùG: CO: 6. GR: Madagascar. EMG: endotroph. Dyscophinae: CO: 219. GR: Madagascar and Southeast Asia. Calluella: CO: 6. GR: Southeast Asia. EMG: exotroph: lentic: suspension feeder. LTRF: 010. OA: straight-edged upper lip without medial notch above terminal mouth. MP: absent SUP: absent. DEM: not applicable. NA: absent until metamorphosis VT: medial. EP: lateral. SP: midventral below gut UJ: absent LJ: absent DF: low, originates near dorsal tail-body junction, tip pointed. BS: oval/depressed. CP: pale brown, translucent, distal part of t d dark. TL: 24/31. NO: ventral fin with lobe near body, hangs in midwater at a 45" angle. CI: C.-C. Liu and Hu (1961); M. A. Smith (1917). Dyscophus: CO: 3. GR: Madagascar. EMG: exotroph: lentic: suspension feeder. LTRF: 010. OA: straight-edged upper lip without medial notch above terminal mouth. MP: absent SUP: absent. DEM: not appiicable. NA: absent until metamorphosis VT: medial. EP: lateral. SP: midventral below gut UJ: absent LJ: absent DF: low, originates near dorsal tail-body junction, tip pointed. BS: oval/depressed. CP: uniformly pale melanic pigment, sometimes more intense on distal part of t d . TL: 36/36. CI: BlomrnersSchlosser (1975); Blomrners-Schlosser and Blanc (1991); Glaw and Vences (1992); Pintar (1987). Genyophryninae: CO: 8/89. GR: Australia-New Guinea-Philippines. Albmicus: CO: 3. GR: New Guinea. EMG: endotroph. Aphantophryne: CO: 3. GR: New Guinea. EMG: endotroph. Choemphryne: CO: 1. GR: New Guinea. EMG: endotroph. Cophixalus: CO: 28. GR: New Guinea-northeastern Australia. EMG: endotroph. Copiula: CO: 5. GR: New Guinea. EMG: endotroph. Genyophryne: CO: 1. GR: New Guinea. EMG: endotroph. Oreophryne: CO: 24. GR: Philippines-Celebes-New Guinea. EMG: endotroph. Sphenuphryne: CO: 24. GR: New Guinea-northeastern Australia. EMG: endotroph. Melanobatrachinae: CO: 314. GR: India-Tanzania. Hoplophryne: CO: 2. GR: Tanzania. EMG: exotroph: lentic: arboreal, probably spends considerable time out of water. LTRF: 010. OA: absent to transversely straight upper lip above terminal mouth. h W not appiicable. SUP: not applicable. DEM: not appiicable. NA: absent. VT: medial. EP: dorsal. VT: medial. SP: midventral on belly. UJ: absent. LJ: absent. DF: low, originates near dorsal tail-body junaion, tip pointed. BS: oval/ depressed. CP: uniform pale pigmentation. TL: 30136. NO: hgerlike projeaion at anterolateral extent of abdomen. CI: Noble (1929). Melunobatrachus: CO: 1. GR: southern India. EMG: endotroph. Parhoplophryne: CO: 1. GR: Tanzania. EMG: endotroph. Microhylinae: CO: 291106. GR: North and South America and Southeast Asia. Ahhstes: CO: 1. GR: Venezuela. EMG: endotroph. A l ~ ~ i uCO: s : 1. GR: Peru. EMG: exotroph: lentic: suspension feeder. LTRF: 010. OA: immense, paired, quadrangular oral flaps pendant over terminal mouth. MP: not applicable. SUP: not appiicable. DEM: not appiicable NA: absent. VT: dextrai. EP: lateral, fully visible from below. SP: midventral, near vent. UJ: absent. LJ: absent DF: low, originates near dorsal td-body junction, tip pointed. CP: generdy dark with middorsal stripe. TL: 59/36. CI: Wild (1995). Arcovomw: CO: 1. GR: Brazil. Tadpole unknown. Chaperina: CO: 1. GR: Borneo. EMG: exotroph: lentic: suspension feeder. LTRE 010. OA: s m d semicircular oral flaps with smooth edges pendant over terminal mouth. MP: not applicable SUP: not appiicable. DEM: not appiicable. NA: absent. VT: medial. EP: lateral. SP: midventral on abdomen. UJ: absent. LJ: absent. DF: low, originates near dorsal td-body junction, tip pointed. BS: rounded/depressed. CP: uniformly black. TL: 25/42. CI: Inger (1956, 1966, 1985). Chiawwcletr: CO: 15. GR: Panama-South America. EMG: exotroph: lentic: suspension feeder. LTRF: 010. OA: s m d semicircular oral flaps with smooth edges pendant over
DIVERSITY
terminal mouth. MP: not applicable. SUP: not applicable. DEM: not applicable. NA: absent. VT: medial. EP: lateral. SP: midventral on lower abdomen. UJ: absent. LJ: absent. DF: low, originates at dorsal taii-body junaion, tip pointed with flageiium. BS: rounded/depressed. CP: unifordy pale. TL: 17/36. CI: Schiüter and Salas (1991). Cteqhryne: CO: 2. GR: Colombia-Brazii. EMG: exotroph: lentic: suspension feeder. LTRF: 010. OA: straight-edged upper lip without oral flaps above terminal mouth. MP: not applicable. SUP: not applicable. DEM: not applicable. NA: absent. VT: medial. EP: lateral. SP: midventral. UJ: absent. LJ: absent DF: low, originates at dorsal tail-body junaion, tip round. BS: rounded/depressed. CP: unifordy pale. TL: 12/25. CI: Schiüter and Salas (1991). Dmypops: CO: 1. GR: Brazii. EMG: exotroph: lentic: suspension feeder. LTRF: 010. OA: labial flaps reduced without medial notch. MP: not applicable. SUP: not applicable. DEM: not applicable. NA: absent. VT: medial. EP: lateral. SP: midventral near vent. UJ: absent. LJ: absent. DF: low, originates at dorsal taii-body junction, tip rounded without flageiium. BS: oval/depressed. CP: unifordy dark, beliy spotted and banded. TL: 52/37. CI: Da Cruz and Peixoto (1978). Demzatonotus: CO: 1. GR: Brazil-Paraguay. EMG: exotroph: lentic: suspension feeder. LTRF: 010. OA: semicircular oral flaps with smooth edges pendant over terminal mouth. MP: not applicable SUP: not applicable. DEM: not applicable. NA: absent. VT: medial. EP: lateral. SP: midventral below vent. UJ: absent. LJ: absent. DF: moderately high, originates at dorsal taii-body junction, tip rounded as flageiium. BS: rounded/depressed. CP: unifordy dark. TL: 36/35. NO: tail sheath (see text) present. CI: Cei (1980); Laviiia (1992b); Vizotto (1967). Elachistocleis: CO: 4. GR: Panama-Argentina. EMG: exotroph: lentic: suspension feeder. LTRP: 010. OA: semicircular oral flaps with smooth edges pendant over terminal mouth. MP: not applicable SUP: not applicable. DEM: not applicable. NA: absent. VT: medial. EP: lateral. SP: midventral near vent. UJ: absent. LJ: absent. DF: low, originates near dorsal taii-body junaion, tip pointed. BS: rounded/depressed. CP: unifordy pale, tail muscle striped. TL: 15-22/36. CI: J. D. Wdiams and Gudynas (1987). Gascrophryne: CO: 5. GR: United States-Costa Rica. EMG: exotroph: lentic: suspension feeder. LTRF: 010. OA: semicircular oral flaps with smooth edges pendant over terminal mouth. MP: not applicable SUP: not applicable. DEM: not applicable. NA: absent. VT: medial. EP: lateral. SP: midventral near vent. UJ: absent. LJ: absent. DF: low, originates ne'ar dorsal tail-body junaion, tip pointed. BS: rounded/depressed. CP: uniform dorsaliy, sagittal stripe, beliy mottled or blotched. TL: 35/36. CI: Donneliy et ai. (1990a); C. E. Nelson and Altig (1972); C. E. Nelson and Cueliar (1968); Orton (1952); A. H. Wright and Wright (1949). Gas~rophrynoides:CO: 1. GR: Borneo. EMG: exotroph: lentic: arboreal (probably stiü feeds as a suspension feeder). LTRP: 010. OA: greatiy reduced straight-edged oral flap above terminal mouth. MP: not applicable SUP: not applicable. DEM: not applicable. NA: absent. VT: medial. EP: lateral. SP: midventral on gut. UJ: absent. LJ: absent. DF: low, originates near dorsal taii-body junaion, tip round. BS: rounded/depressed. CP: unifordy dark. TL: -. CI: tentative identification based on Inger (1985:38). Glyphoglosus: CO: 1. GR: Burma-Thailand. EMG: exotroph: lentic: suspension feeder. LTRP: 010. OA: straight-edgedupper lip without oral flaps above terminal mouth. MP: not applicable SUP: not applicable. DEM: not applicable. NA: absent. VT: medial. EP: lateral. SP: midventral below gut. UJ: absent. LJ: absent. DF: low, originates near dorsal td-body junaion, tip pointed. BS: oval/depressed. CP: pale brown, translucent, distal part of tail dark. TL: 40136. NO: M. A. Smith (1917) reports data on the nares as if they were present, hangs in midwater at a 45" angle. CI: M. A. Smith (1917). Hamptophryne: CO: 1. GR: northern and western Arnazon Basin-Guianas-Bolivia. EMG: exotroph: lentic: suspension feeder. LTRF: 010. OA: semicircular oral flaps with smooth to slightiy crenulate edges pendant over terminal mouth. MP: not applicable SUP: not applicable. DEM: not applicable. NA: absent. VT: medial. EP: lateral. SP: midventral near vent. UJ: absent. LJ: absent. DF: low, originates near dorsal taii-body junaion, tip pointed. BS: rounded/depressed. CP: dark, taii striped. TL: 32/36. CI: Dueilman (1978); Schiüter and Salas (1991). Hyophryne: CO: 1. GR: Brazii. Tadpole unknown.
Hamptophryne
RONALD ALTIG A N D ROY W. McDIARMID
Microhyla
Nelsonoplnyne
Hypopachus: CO: 2. GR: southern United States-Costa Rica. EMG: exotroph: lentic: suspension feeder. LTRF: 010. OA: semicircular oral flaps with scalioped-papiilate edges pendant over terminal mouth. MP: not applicable SUP: not applicable. DEM: not applicable. NA: absent. VT: medial. EP: lateral. SP: midventral near vent. UJ: absent. LJ: absent. DF: low, originates near dorsal tail-body junaion, tip pointed. BS: rounded/ depressed. CP: dark reticulations, lightiy striped tail. TL: 21/36. NO: tadpoles described by E. H . Taylor (1942) as H . alboventer likely belong to a species of Gastrophyne. CI: C. E. Nelson and Cuellar (1968); Stuart (1941). Kduphynus: CO: 10. GR: southern China-Java-Phdippines. EMG: endotroph Kkloula: CO: 10. GR: Korea-Sri Lanka. EMG: exotroph: lentic: suspension feeder. LTRF: 010. OA: straight-edged upper lip without oral flaps above terminal mouth. MP: not applicable. SUP: not applicable. DEM: not applicable. NA: absent. VT: medial. EP: lateral. SP: midventral near vent. UJ: absent. LJ: absent. DF: low, originates near dorsal tail-bodyjunaion, tip pointed. BS: rounded/depressed. CP: uniform, tail striped, terminal part of tail may be unpigmented. TL: 25-30136. CI: Kirtisinghe (1958); C.-C. Liu (1950). Metaphynella: CO: 2. GR: Malaysia-Borneo. EMG: exotroph: lentic: suspension feeder. LTRF: 010. OA: dorsoterminal, no oral flaps, 2-3 papiilae at lower jaw. MP: not applicable. SUP: not applicable. DEM: not applicable. NA: absent. VT: medial. EP: dorsal. SP: midventral on chest. UJ: absent. LJ: absent. DF: low, originates slightiy posterior of dorsal tail-body junaion, tip round. BS: oval/depressed. CP: uniforrnly brown. TL: 32/36. NO: Berry (1972) reports open nares from stage 26 onward. CI: Berry (1972). Micyohyh: CO: 24. GR: Sri Lanka-Japan-China-Southeast Asia. EMG: exotroph: lentic: suspension feeder. LTRF: 010. OA: smali to large semicircular oral flaps with smooth edges pendant over terminal mouth, umbeiliform taxa have oral disc with radialiy arranged submarginal papiilae, and formed almost entirely of lower labium. MP: not applicable. SUP: not applicable. DEM: not applicable. NA: absent. VT: medial. EP: lateral. SP: midventral on belly or near vent. UJ: absent. LJ: absent. DF: low, originates near dorsal tail-body junaion, tip pointed with or without a flagellum. BS: round to oval/ depressed. CP: dark, belly sometimes mottle or banded, tail striped. TL: 20-30136. CI: Chou and Lin (1997); Heyer (1971); Inger (1985); Inger and Frogner (1979). Myersielh: CO: 1.GR: eastern Brazil. EMG: endotroph. Nelsonophyne: CO: 2. GR: Costa Rica-western Ecuador. EMG: exotroph: lentic: suspension feeder. LTRF: 010. OA: labial flaps absent, upper lip derivative forms large lateral flaps, smali lower labium. MP: absent, although some papillae midventrally resemble marginal papiilae. SUP: absent. DEM: not applicable. NA: absent. VT: medial. EP: lateral. SP: midventral on gut. UJ: absent. LJ: absent. DF: low, originates near dorsal td-body junaion, tip rounded. BS: oval/depressed. CP: uniformly dark. TL: 44/34. CI: Donneily et al. (1990a). Otophlyne: CO: 3. GR: northern South America. EMG: exotroph: lotic: psamrnonic. LTRF: 010. OA: oral disc derivatives reduced to lateral, verticaliy oriented flaps, nascent tooth ridges present below lower jaw but no teeth present. MP: not applicable. SUP: not applicable. DEM: not applicable NA: absent VT: medial. EP: lateral. SP: appears sinistral but starts development midventrally, spiracular tube very long and free from body wall. UJ: isolated, hypertrophied jaw serrations without basal sheath. LJ: similar to upper jaw. DF: low, originates near dorsal tail-body junaion, tip rounded. BS: oblong/ depressed. CP: uniformiy pale brown. TL: 36/36. CI: J. A. Campbeil and Clarke (1988); Pyburn (1980); Wassersug and Pyburn (1987). Phynelh: CO: 1. GR: Malaysia-Sumatra. EMG: endotroph. Ramanelh: CO: 8. GR: India-Sri Lanka. EMG: exotroph: lentic: suspension feeder. LTRF: 010. OA: smooth-edged, entire, smali oral flap slightiy pendant over terminal mouth. MP: not applicable SUP: not applicable. DEM: not applicable. NA: absent. VT: medial. EP: lateral. SP: midventral near vent. UJ: absent. LJ: absent. DF: low, originates near dorsal tail-body junction, tip rounded. BS: rounded/depressed. CP: uniform. TL: 27/32. NO: Kirtisinghe (1958) reports open nares. CI: Kirtisinghe (1958). Relictovomer: CO: 1. GR: Panama-Colombia. Tadpole unknown. Stereocyc&ps: CO: 1. GR: Brazil. EMG: exotroph: lentic: suspension feeder. LTRF: 010.
DIVERSITY
OA: semicircular oral flaps with smooth edges pendant over terminal mouth. M E not applicable SUP: not applicable. DEM: not applicable. NA: absent. VT: medial. EP: lateral. SP: midventral but opens to lefi of the plane of the ventral fin along with vent. UJ: absent. LJ: absent. DE: low, originates near dorsal tail-body junction, tip pointed. BS: round/depressed. CP: uniform (see note). TL: -. NO: I. Grifliths and De Carvalho (1965) discuss polymorphisms of a middorsal stripe and spiracular tube length; tail sheath (see text) present. CI: I. Grifliths and De Carvalho (1965). Synapturanus: CO: 3. GR: Colombia-Guianas-Brazil. EMG: endotroph. Syncope: CO: 2. GR: eastem Ecuador-Peru. EMG: endotroph. Uperodon: CO: 2. GR: India-Sri Lanka. EMG: exotroph: lentic: suspension feeder. LTRF: 010. OA. smooth-edged entire (no medial notch) oral flap pendant over terminal mouth. MP: not applicable SUP: not applicable. DEM: not applicable. NA: absent. VT: medial. EP: lateral. SP: midventral near vent. UJ: absent. LJ: absent. DE: low, originates near dorsal tail-body junction, tip pointed. BS: oval/depressed. CP: uniform or mottled with striped tail. TI,: 28/36. NO: Bhaduri and Daniel (1956) and Mohanty-Hejrnadi et al. (1979) report open nares. CI: Kirtisinghe (1957). Phrynomerinae: CO: 115. GR: sub-Saharan Africa. EMG: exotroph: lentic: suspension feeder. LTRF: 010. OA: no keratinized mouthparts, entire (without medial notch) oral flap with smooth edges pendant over terminal mouth. MP: not applicable. SUP: not applicable. DEM: not applicable. NA: absent. VT: medial. EP: lateral. SP: rnidventral, below vent. UJ: absent. LJ: absent. DE: low, originates near dorsal tail-body junction, flagellurn present. BS: round/depressed. CP: uniformly pale, tail fins may be darker. TL: 37/36. Phryvwmantzs: CO: 5. CI: Lamotte (1964); Wager (1986). Scaphiophryninae: CO: 2/10. GR: Madagascar Paraáuxophyh: CO: 1. GR: Madagascar. EMG: exotroph: lentic: suspension feeder. LTRF: 010. OA: semicircular oral flaps with smooth edges pendant over terminal mouth. MP: absent. SUP: absent. DEM: not applicable. NA: absent. VT: medial. EP: lateral. SP: midventral, on abdomen. UJ: absent. LJ: absent. DE: low, originates near dorsal tail-body junction, tip pointed. BS: round/depressed. CP: dark dorsaily with pale spot on snout and over lungs. TL: 28/36. NO: looks like a microhyline tadpole. CI: BlommersSchlosser and Blanc (1991); Glaw and Vences (1992). Scaphiophryne: CO: 9. GR: Madagascar. EMG: exotroph: lentic: suspension feeder, may rasp some materials, sometimes carnivorous. LTRF: 010. OA: s m d oral disc with papillae and unpigmented, serrated jaw sheaths, labial teeth lacking. MP: complete. SUP: few dorsaily and ventraily. DEM: absent. NA: absent. VT: medial. EP: dorsal. SP: midventrai at center of beiiy. UJ: wide, uniform arc, unpigmented. LJ: wide, open U-shaped, unpigmented. DE: low, originates near dorsal tail-body junction, tip pointed. BS: oval/ depressed. CP: very lightly pigrnented, translucent. TL: 30136. NO: only rnicrohylid tadpole with fdiy formed jaw sheaths (see Otophryne). CI: Blornmers-Schlosser (1975); Blommers-Schlosser and Blanc (1991); Glaw and Vences (1992); Wassersug (1984). MYOBATRACHIDAE: CO: 231118. GR: Australia-New Guinea. EMG: exotroph: lentic: benthic, carnivore, nektonic; lotic: benthic, clasping; endotroph. LTRF: many variations between 010 and 813. OA: typical: anteroventral, ventral. MP: complete, mediurn to wide dorsal gap, narrow to wide ventrai gap. SUP: absent, throughout extent of marginal papiiiae, below P-3, few lateraily. DEM: absent, lateral. NA: nearer eye than snout or reverse. VT: dextral, medial. EP: dorsal. SP: sinistral. UJ: narrow to wide, smooth arc. LJ: narrow to wide, U- to V-shaped. DE: low, originates near dorsal tail-body junction, high and originates anterior to dorsal tail-body junction, tip rounded to pointed. BS: oval/depressed. CP: uniform to variou muted patterns. TL: 15-70136. Lirnnodynastinae: CO: 11151. GR: Australia-New Guinea. Adehtus: CO: 1.GR: eastern Australia. EMG: exotroph: lentic: benthic. LTRF: 3(2-3)/ 3(1). OA: typical: anteroventral. MP: mediurn dorsal gap: uniserial. SUP: throughout extend of marginal papillae. DEM: absent. NA: nearer snout than eye. VT: dextral. EP: dorsal. SP: sinistral. UJ: narrow, wide smooth arc. LJ: narrow, open V-shaped. DF: low, originates near dorsal tail-body junction, tip rounded. BS: oval/depressed. CP: uniform. TL: 33/33. CI: Watson and Martin (1973).
Adehtus
324
RONALD ALTIG AND ROY W. McDIARMID
Helezbporus: CO: 6. GR: Australia. EMG: exotroph: lentic: benthic. LTRF: 8(2-8)/3(1), 6(2-6)/3(1), 5(3-5)/3(1), 5(2-5)/3(1). OA: typical: anteroventral. MP: medium dorsal gap: uniseriai. SUP: row below P-3. DEM: lateral. NA: nearer eye than snout. VT: medial. EP: dorsal. SP: sinistral. UJ: medium, smooth arc. LJ: medium, open U-shaped. DF: low, originates near dorsal tail-body junction, tip rounded. BS: oval/depressed. CP: udormiy dark. TL: 30-45136. CI: Davies (1991); A. K. Lee (1967). Kyawanus: CO: 3. GR: eastern Australia. EMG: endotroph. Lechriodus: CO: 5. GR: eastern Australia-New Guinea. EMG: exotroph: lentic: carnivore. LTRF: 6(2-6)/3(1). OA: typical: anteroventral. MP: wide dorsal gap: biserial. SUP: throughout extent of marginal papillae. DEM: lateral. NA: nearer snout than eye. VT: medial. EP: dorsal. SP: sinistral. UJ: medium, wide smooth arc. LJ: medium, open V-shaped. DF: low, originates near dorsal taii-body junction, tip broadly rounded. BS: oval/depressed. CP: uniformly dark. TL: 33/34. CI: Watson and Martin (1973). Limmdynastes: CO: 12. GR: Australia-New Guinea. EMG: exotroph: lentic: benthic; lotic: benthic. LTRF: 6(2-6)/3(1), 5(2-5)/3(1), 4(3-4)/3(1), 4(2-4)/3(1), 2(2)/3(1). OA: typical: anteroventral. MP: medium dorsal gap: biserial. SUP: few lateraiiy. DEM: lateral. NA: nearer snout than eye or reverse. VT: medial. EP: dorsal. SP: sinistral. UJ: medium, smooth arc. LJ: medium, open U-shaped. DF: low, originates near dorsal taiibody junction, tip pointed. BS: oval/depressed. CP: uniform to muted mottling. TL: 35-70136. CI: Tyler et al. (1983). Mgiistobtis: CO: 1. GR: northwestern Australia. EMG: exotroph: lotic: clasping. LTRF: 6(3-6)/3. OA: typical: anteroventral. MP: narrow dorsai gap: uniserial ventraiiy and biserial dorsolateraiiy. SUP: few lateraiiy and below lower tooth rows. DEM: absent. NA: nearer eye than snout. VT: mediai. SP: sinistrai. EP: dorsai. UJ: medium, edge describes smooth arc. LJ: medium, open V-shaped. DF: low, originates near dorsal taiibody junction, tip rounded. BS: oval/depressed. CP: uniformiy dark. TL: 52/42. CI: Tyler et al. (1979). Mkophyes: CO: 6. GR: eastern Australia. EMG: exotroph: lotic: benthic; lentic: benthic. LTRF: 6(2-6)/3(1). OA: typical: anteroventral. MP: complete: uniserial. SUP: few lateraiiy. DEM: lateral. NA: nearer eye than snout. VT: dextral. SP: sinistral. EP: dorsal. UJ: medium, smooth arc. LJ: medium, very wide U-shaped. DF: low, originates near dorsai taii-body junction, tip rounded. BS: oval/depressed. CP: uniformiy dark. TL: 60-70137. NO: 1-5 accessory rows may be present anterior of lateral ends of lower rows. CI: Davies (1991); Watson and Martin (1973). Neobatrachus: CO: 10. GR: Australia. EMG: exotroph: lentic: benthic. LTRF: 3(2-3)/ 3(1). OA: tjpical: anteroventral. MP: dorsal gap: uniserial. SUP: absent. DEM: laterai. NA: nearer eye than snout. VT: dextrai. EP: dorsal. SP: sinistral. UJ: medium to wide, smooth arc. LJ: medium to wide, open V-shaped. DF: low, originates near dorsal taiibody junaion, tip rounded. BS: oval/depressed. CP: uniformiy dark. TL: 40-50136. CI: Davies (1991); Watson and Martin (1973). Notaden: CO: 4. GR: Australia. EMG: exotroph: lentic: benthic. LTRF: 3(2-3)/3(1), 2(2)/2(1). OA: typical: anteroventral. MP: wide dorsal and ventral gap: uniserial. SUP: absent. DEM: absent. NA: nearer eye than snout. VT: dextral. EP: dorsal. SP: sinistral. UJ: medium, smooth arc. LJ: medium, open U-shaped. DF: low, originates near dorsal tail-body junction, tip rounded. BS: oval/depressed. CP: uniform. TL: 25/24. CI: E Slater and Main (1963); Tyler et al. (1983). Philoria: CO: 1. GR: northeastern Australia. EMG: endotroph. Rhwbatrachus: CO: 2. GR: northeastern Australia. EMG: endotroph. Myobatrachinae: CO: 12/67. GR: Australia-New Guinea. Arenophlyne: CO: 1. GR: Western Australia. EMG: endotroph. Assa: CO: 1. GR: northeastern Australia. EMG: endotroph. Blyobatrachus: CO: 1. GR: Tanzania. EMG: endotroph. Crinia: CO: 14. GR: Australia-New Guinea. EMG: exotroph: lentic: benthic; lotic: benthic. LTRF: 2(2)/3(1), 2/3(1), 2(2)/2. OA: typicai: anteroventral. MP: wide dorsal gap and narrow to wide ventral gap: uniserial. SUP: absent. DEM: laterai, absent. NA: nearer snout than eye. VT: dextral. EP: dorsai. SP: sinistral. UJ: medium wide smooth arc. LJ: medium, open U-shaped. DF: low, originates near dorsai taii-body junction, tip
DIVERSITY
rounded. BS: ovai/depressed. CP: dark, minor mottling. TI,: 15-20136. CI: Littlejohn and Martin (1965); Watson and Martin (1973). Geocrinia:CO: 7. GR: southern Austraiia. EMG: exotrophic: lentic: benthic. LTRF: 010, 2(2)/3[I.]. OA: typicai: anteroventral. MP: wide dorsai and narrow ventrai gaps: biserial. SUP: absent. DEM: absent. NA: nearer eye than snout. VT: dextral. EP: dorsai. SP: sinistrai. UJ: medium, smooth arc with mediai part straight. LJ: medium, open U-shaped. DF: low, originates near dorsai taii-body junction, tip round. BS: ovai/depressed. CP: uniformiy dark. TL: 22/30. CI: Littlejohn and Martin (1964); Watson and Martin (1973). Met-nia: CO: 1. GR: southwestern Australia. Tadpole unknown. Myobacrmhus: CO: 1. GR: Western Australia. EMG: endotroph. Paracrinia: CO: 1. GR: eastern Australia. EMG: exotroph: lentic: nektonic. LTRF: 2(2)/2. OA: typicai: anteroventrai. MP: medium dorsai gap: uniserial. SUP: absent. DEM: absent. NA: nearer eye than snout. VT: dextrai. EP: dorsai. SP: sinistral. UJ: medium, smooth arc. LJ: narrow, open U-shaped. DF: high, originates anterior to dorsai tail-body junction, tip pointed. BS: oval/depressed. CP: uniformiy paie. TL: 34/34. CI: Watson and Martin (1973). Aeudophryne: CO: 10. GR: eastern Austraiia. EMG: exotroph: lentic: benthic. LTRF: 2(2)/3[:1.]. OA: typicai: anteroventral. MP: wide dorsai gap and narrow ventrai gap: uniserial. SUP: absent. DEM: lateral. NA: nearer eye than snout. VT: dextrai. EP: dorsai. SP: sinistrai. UJ: medium, smooth arc. LJ: medium, open U-shaped. DF: low, originates near dorsai tail-body junction, tip pointed. BS: ovai/depressed. CP: uniformly dark. TL: 20-25136. CI: Watson and Martin (1973). Spicospina: CO: 1. GR: southwestern Australia. Tadpole unknown. CI: J. D. Roberts et ai. (1997). Taua!&yLus:CO: 6. GR: eastern Australia. EMG: exotroph: lotic: benthic. LTRF: 010, 2(2)/3(1). OA: typical: anteroventral, ventral. MP: complete: uniserial. SUP: absent. DEM: lateral. NA: nearer eye than snout. VT: dextrai. EP: dorsai. SP: sinistral. UJ: very narrow, smooth arc, coarsely serrate. LJ:very narrow, open U-shaped, coarsely serrate. DF: low, originates near dorsai taii-body junction, tip round. BS: ovai/depressed. CP: uniformly dark. TL: 15-25/36. CI: Retaüick and Hero 1998; Watson and Martin (1973). Uperoieia: CO: 23. GR: northeastern Australia-New Guinea. EMG: exotroph: lentic: benthic. LTRF: 1/3,2(2)/3[1]. OA: typical: anteroventral. MP: wide dorsai and ventrai gaps: uniserial. SUP: absent. DEM: absent. NA: nearer eye than snout. VT: dextrai. EP: dorsai. SP: sinistral. UJ: wide, smooth arc with slight mediai convexity. LJ: medium, open U-shaped. DF: low, originates near dorsai taii-body junction, tip slightly rounded. BS: ovai/depressed. CP: uniformly dark. TL: 31/36. CI: Tyler et al. (1983). PELOBATIDAE: CO: 3111. GR: Europe-North America. EMG: exotroph: lentic: benthic, carnivore. LTRF: 414 to 616, A-1 usuaily very short. OA: typical: anteroventral, aimost terminal. MP: narrow dorsai gap: uniserial. SUP: absent, few lateraily. DEM: absent. NA: nearer snout then eye. VT: mediai. EP: dorsai. SP: low on lefi side, sometimes aimost midventral. UJ: wide, smooth arc, uniess a carnivore and then with a mediai convexity. LJ:wide, smooth arc, uniess a carnivore and then with a mediai concavity. DF: low, originates near dorsai taiibody junction, tip bluntly pointed. BS: oblong/depressed. CP: uniformiy dark or paie, depending on environmental conditions. TL: 20-80136. NO: cannibal morphotypes of Spea have highly modified keratinized mouthparts and jaw muscuiature. Pelobates: CO: 4. GR: Europe. EMG: exotroph: lentic: benthic. LTRP: 4(24)/5(1-3). OA: typical: anteroventral. MP: narrow dorsai gap: uniserial. SUP: row throughout extent of marginal papillae. DEM: absent. NA: nearer snout then eye. VT: medial. EP: dorsai. SP: low on lefi side. UJ: medium, smooth arc. LJ: wide, open U-shaped. DF: low, originates near dorsai taii-body junction, tip bluntly pointed. BS: ovai/globuiar. CP: muted mottling. TL: 40-60136. CI: Bouienger (1892); Lanza (1983). ScaphiUpus: CO: 3. GR: North America. EMG: exotroph: lentic: benthic. LTRF: 6(4-6)/6(1), 4(34)/4(1-2). OA: typical: anteroventral. MP: narrow dorsai gap: uniserial. SUP: few lateraily. DEM: absent. NA: nearer snout then eye. VT: mediai. EP: dorsai. SP: low on lefi side. UJ: narrow, smooth arc. LJ: medium, open U-shaped, basai part may appear striated. DF: low, originates near dorsai taii-body junction, tip bluntly
scaphiupw
RONALD ALTIG AND ROY W. McDIARMID
pointed. BS: ovai/depressed. CP: uniformly dark. TL: 20-35136. CI: Aitig (1970); A. H. Wright and Wright (1949). Spea: CO: 4. GR: North America. EMG: exotroph: lentic: benthic, facultative carnivore. LTRF: 4(2-4)/4(1-3), 4(3-4)/4(1-2). OA: typical: aimost terminal. MP: narrow dorsai gap: uniseriai. SUP: few lateraüy, absent. DEM: absent. NA: nearer snout then eye. VT: mediai. EP: dorsai. SP: low on lefi side. UJ: typicai: wide, smooth are; carnivore: mediai convexity. LJ: typical: wide, V-shaped; carnivore: mediai indentation, basai pan- may appear striated. DF: low, originates near dorsai tail-body junction, tip bluntiy pointed. BS: oval/globular. CP: uniformly dark or pde. TL: 40-80136. NO: usuaüy has keratinized knob on the roof of the buccai cavity, LTRF vanable. CI: Aitig (1970); A. H. Wright and Wright (1949).
Peíodytes
Hymenocbirus
PELODYTIDAE: CO: 112. GR: southwestern Europe-Caucasus. EMG: exotroph: lentic: benthic. LTRP: 4(34)/5(1-3). OA: typicai: anteroventral. MP: dorsai gap: wide. SUP: absent. DEM: lateral. NA: nearer snout than eye. VT: medial. EP: dorsai. SP: sinistral. UJ: narrow, uniform arc. LJ: narrow, wide U-shaped. DF: mediurn, onginates near dorsai tailbody junction. BS: oval/depressed. CP: uniformly dark. TL: 26/36. Pelodytes: CO: 2. CI: Boulenger (1892); Lanza (1983). PIPIDAE: CO: 5/28. GR: South America and sub-Saharan Africa. EMG: exotroph: lentic: suspension feeder, carnivore; endotroph. LTRF: 010. OA: oral disc or keratinized mouthparts absent, slitiike mouth, terminal or nearly so, sometimes with large barbels, highly derived protrusible mouthpan-s of microphagous carnivore. MP: not appiicable. SUP: not appiicable. DEM: not applicable. NA: much nearer snout than eye. VT: mediai. EP: lateral. SP: dual/laterai. UJ: not applicable. LJ: not appiicable. DF: low, originates near dorsal tail-body junction, tip pointed, often with flageiium that undulates continudy. BS: oval/ depressed. CP: uniformly iightiy pigmented, ofien translucent. TL: 30-60136. NO: low ventrai fin extends onto abdomen, ofien as a pronounced lobe, most resemble rhinophrynid tadpoles. Pipinae: CO: 117. G R South America. EMG: exotroph: lentic: suspension feeder; endotroph. LTRF: 010. OA: absent, mouth transverse and siitiike. MP: not applicable. SUP: not appiicable. DEM: not appiicable. NA: near mouth. VT: mediai. EP: lateral. SP: dual/ lateral. UJ: not appiicable. LJ: not applicable. DF: low, originates near dorsai tail-body junction, tip pointed as a flageilum. BS: ovai/depressed. TL: 40-50136. NO: barbels absent, ventral fin extends onto abdomen as a lobe. Pipa: CO: 7. G R Panama-northern South America. CI: Gines (1958); F. Schutte and Ehrl (1987); O. M. Sokol(1977a). Xenopodinae: CO: 4/21. G R sub-Saharan Africa. Hymenochims: CO: 4. G R Cameroon-Zaire. EMG: exotroph: lentic: carnivore. LTRF: 010. OA: absent, protrusible, rounded opening, opens dorsaüy when at rest. MP: not applicable. SUP: not applicable. DEM: not applicable. NA: nearer mouth than eye. VT: medial. EP: lateral. SP: dual/laterai. UJ: not applicable. LJ: not applicable. DF: low, originates near dorsai tail-body junction, tip bluntiy pointed BS: ovai/depressed. TL: 12-21/34. CI: O. M. Sokol(l959, 1962). Pseu&ymenochims: CO: 1. GR: western Africa. EMG: exotroph: lentic: carnivore. LTRF: 010. OA. protrusible, rounded opening, opens dorsaüy when at rest. MP: not appiicable. SUP: not applicable. DEM: not applicable. NA: small, nearer snout than eye. VT: medial. EP: lateral. SP: dual/laterai. UJ: not applicable. LJ: not appiicable. DF: low, originates posterior to dorsal tail-body junction, tip rounded. BS: ovai/depressed. CP: uniformly paie. TL: 19/34. NO: I. Griffiths (1963) reported fine "denticles" on the mouthparts. CI: Lamotte (1963). Szlurana: CO: 2. GR: western Africa. EMG: exotroph: lentic: suspension feeder. LTRF: 010. OA: single barbel at corners of terminal, slitiike mouth. MP: not appiicable. SUP: not applicable. DEM: not applicable. NA: near snout, transversely elliptical. VT: medial. EP: lateral. SP: dual/lateral. UJ: not applicable. LJ: not applicable. DF: very low, originates near or posterior to dorsai tail-body junction, tip pointed as a constantly undulating flagellum. BS: ovai/depressed. CP: uniformly paie. TL: 35-60136. NO: barbel with extrinsic musculature and cartilage support, ventral fin extends onto abdomen as a rounded lobe; floats head-downward in water. CI: O. M. Sokol (1977a).
DIVERSITY
Xenopus: CO: 14. GR: sub-Saharan Africa. EMG: exotroph: lentic: suspension feeder. LTRF: 010. OA: single barbel at corners of terminal, slitlike mouth. MP: not applicable. SUP: not applicable. DEM: not applicable. NA: near snout, transverseiy elliptical. VT: medial. EP: lateral. SP: dual/lateral. UJ: not applicable. LJ: not applicable. DF: very low, originates near or posterior to dorsal tail-body junction, tip pointed as a constantly undulating flagellum. BS: oval/depressed. CP: uniformly pale. TL: 35-60136. NO: barbel with extrinsic musculature and cartilage support, ventral fin extends onto abdomen as a rounded lobe; floats head-downward in water. CI: Arnoult and Lamotte (1968); Nieuwkoop and Faber (1967); Rau (1978); Vigny (1979). PSEUDIDAE: CO: 215. GR: South America. EMG: exotroph: lentic: benthic, nektonic. LTRF: 2/3[1], 2(2)/3. OA: typical: anteroventral. MP: medium dorsal gap: biserial. SUP: few lateraily, absent. DEM: absent. NA. nearer snout than eye. VT: medial, sinistral. EP: lateral. SP: sinistral. UJ: medium to wide, medial edge arced or straight. LJ: medium, open U-shaped. DF: hgh, originates well anterior of dorsal tail-body junction or low, originates weii anterior of dorsal td-body junction, tip rounded to pointed. BS: oval/compressed. CP: often brightly patterned and prominent ontogenetic change. TL: 34-230136. Lysapsus: CO: 3. GR: South America east of Andes. EMG: exotroph: lentic: benthic. LTRP: 2(2)/3. OA: typical: anteroventral. MP: medium dorsal gap: biserial. SUP: few lateraliy. DEM: absent. NA: nearer snout than eye. VT: sinistral. EP: lateral. SP: sinistral. UJ: wide, medial edge straight. LJ: medium, open U-shaped. DF: low, originates weli anterior of dorsal tail-body junction, tip pointed. BS: oval/compressed. CP: entire t d boldly banded. TL: 34/37. NO: tail tip black, black bar at base of tad muscle and h, perhaps only case reported of a sinistral vent tube being characteristic of a species. CI: Kehr and Basso (1990). Pseudis: CO: 2. GR: South America. EMG: exotroph: lentic: nektonic. LTRF: 2/3(1). OA: typical: anteroventral. MP: medium dorsal gap: biserial. SUP: absent. DEM: absent. NA: nearer snout than eye. VT: medial. EP: lateral. SP: sinistral. UJ: medium, smooth are. LJ: medium, open U-shaped. DF: high, originates near or anterior to plane of eyes, tip rounded. BS: oval/compressed. CP: young tadpole boldly banded, older ones unicolored dark. TL: 230136. NO: metamorphc atrophy of fins precedes that of tad myotomes. CI: De Sá and Lavilla (1997); Dixon et al. (1995); Kenny (1969a). RANIDAE: CO: 451635. GR: widespread. EMG: exotroph: lentic: several gudds; lotic: several gudds; endotroph. LTRF: many variations benveen 010 and 918, 213 and n/3 most common. OA: typical: anteroventral, ventral to almost terminal, oral disc reduced and LTRF absent. MP: wide dorsal gap, dorsal and ventral gaps: uni- and biserial. SUP: absent, few lateraily. DEM: lateral, absent. NA: nearer eye than snout or reverse. VT: dextral, medial. EP: dorsal, lateral. SP: sinistral. UJ: narrow to wide, smooth arc, mediai convexity. LJ: narrow to wide, U- to V-shaped. DF: low, originates near dorsal tail-body junctions, very low, originates on tail muscle, tip pointed to round. BS: oval/depressed. CP: mostly muted tones of mottling. TL: 30-100136. Petropedetinae: CO: 13/94. GR: Africa. Anhydrophiyne: CO: 1. GR: South Africa. EMG: endotroph. Archroleptella: CO: 3. GR: South Africa. EMG: endotroph. Archroleptzdes: CO: 2. GR: Tanzania-Kenya. EMG: exotroph: lotic: semiterrestrial. LTRF: 3(1-3)/3(1). OA: typical: ventral. MP: wide dorsal gap: biserial ventrally. SUP: absent. DEM: absent. NA: smail, nearer snout than eye. VT: medial. EP: dorsal. SP: sinistral. UJ: wide, strongly arched, medial convexity. LJ: similar to upper sheath. DF: very low, originates on tail muscle, tip round. BS: oval/depressed. CP: mottled. TL: 301 36. NO: eyes bulge noticeably, hind legs develop precociously relative to front legs and general development. CI: Drewes et ai. (1989). Cacostemum: CO: 7. GR: southern Africa. EMG: exotroph: lentic: benthic. LTRF: 2(2)/3(1), 3(2-3)/3,4(2-4)/3 (1).OA: typical: anteroventrai. MP: wide dorsal gap: uniserial. SUP: few in row laterally. DEM: lateral, absent. NA: equidistant or nearer eye than snout. VT: dextral. EP: dorsal. SP: sinistral. UJ: wide, medial convexity, coarsely serrate. LJ: wide, open V-shaped. DF: low, originates near dorsal tail-body junction, tip pointed to rounded. BS: oval/depressed. CP: uniformly dark. TL: 28-50136. CI: De Villiers (1929a); Power (1927a); Van Dijk (1966).
327
Xenopus
Pseudis
RONALD ALTIG AND ROY W. McDIARMID Dimorphognathus: CO: 1. GR: Cameroon-Gabon. Tadpole unknown. Ericabatracbus: CO: 1. GR: Ethopia. EMG: Tadpole unknown. Microbatracbella: CO: 1. GR: South Africa. EMG: exotroph: lentic: benthic. LTRF: 3(2-3)/3(1). OA: typical, anterovenual. MP: wide dorsal and narrow venual gaps: uniseriai. SUP: few lateraiiy in a row. DEM: absent. NA: nearer snout than eye. VT: dextral. EP: dorsal. SP: sinistral. UJ: medium, mediai convexity. LJ: medium, open U-shaped. DF: low, originates at dorsal tail-body junction, tip pointed. BS: oval/depressed. CP: brown dorsaiiy, white ventraiiy. TL: 25/36. CI: Van Dijk (1966); Wager (1986). Natalobatrachus: CO: 1. GR: South Africa. EMG: exouoph: lotic: benthic. LTRF: 5(2-5)/3. OA: typical, anteroventral. MP: wide dorsal gap: biserial. SUP: absent. DEM: lateral. NA: nearer snout than eye. VT: dextral. EP: dorsal. SP: sinisuai. UJ: wide, prominent medial convexity. LJ: medium, open V-shaped. DF: low, originates at dorsal tailbody junction, tip rounded. BS: oval/depressed. CP: pale gray. TL: 41/36. CI: Van Dijk (1966); Wager (1986). Nothqhlyne: CO: 1. GR: Malawi-Mozambique. Tadpole unknown. Petmpedetes: CO: 7. GR: Cameroon-Sierra Leone. EMG: exotroph: lotic: suctorial, semiterrestrial. LTRF: 3(1-3)/3(1), 3(3)/3(1), 415, 7(5-7)/6(1). OA: typical: venual. MP: wide dorsai gap: uniserial, large folds in lateral part of disc. SUP: two rows below distal most lower tooth row. DEM: lateral. NA: nearer eyes than snout. VT: medial. EP: lateral. SP: sinisual. UJ:wide, smooth arc, broken into two pieces connected by a narrow part. LJ: wide, open V-shaped. DF: low, originates near dorsal tail-body junction, tip pointed. BS: oval/depressed. CP: uniformly dark. TL: 35/36. NO: upper rows much longer than lower rows in R natatoz CI: Lamotte et al. (1959a); Lamotte and ZuberVogeli (1954b). Phlynobatrachus: CO: 67. GR: sub-Saharan Africa. EMG: exouoph: lentic: benthic. LTRF: 112, 113, 1/4(1), 2(2)/2. OA: typicai: anterovenual. MP: medium dorsal gap: uniserial, ventral papdlae sometimes elongate. SUP: row throughout lower labium. DEM: lateral, absent. NA: nearer snout than eye. VT: mediai. EP: dorsai. SP: sinisual. UJ: wide, prorninent medial convexity. LJ: wide, open U-shaped. DF: low, originates near dorsal tail-body junction, tip pointed. BS: oval/depressed. CP: dark. TL: 20-351 36. CI: Lamotte and Dzieduszycka (1958); Van Dijk (1966). Phlynodon: CO: 1. GR: Cameroon-Fernando P. EMG: endotroph. Poyntonia: CO: 1. GR: South Africa. EMG: exouoph: lentic: benthic. LTRF: 112 or 1(2)/2. OA: typical. MP: wide dorsal gap UP: lateral patch. DEM: absent. NA: smaii, about equidistant between eye and snout. VT: dexual. EP: dorsal. SP: sinisual. UJ: wide, forms shaiiow arch with a mediai convexity in serrated margin. LJ: V-shaped. DF: low, originates posterior of dorsal tail-body junction, tip rounded. BS: oval/depressed. CP: pale brown with dark speckles. TL: 32/26. NO: skin glands prominent throughout dorsum, margin of vent tube slightly scaiioped. CI: Channing and Boycott (1989). Raninae: CO: 321541. GR: widespread. Amolops: CO: 24. GR: northern India-China-Southeast Asia-Indonesia. EMG: exotroph: lotic: gastromyzophorous. LTRF: 4-8/34, usuaiiy with three complete distai rows on upper labium and a medial gap in first lower row. OA: typical: suctorial. MP: wide dorsal gap. SUP: absent. DEM: lateral. NA: closer to eye than snout. VT: medial. EP: dorsai. SP: sinistral. UJ: medium, wide U-shaped. LJ: medium, wide U-shaped. DF: low, originates near or posterior to dorsai tail-body junction, tip rounded. BS: oval/ depressed. CP: muted mottling. TL: 50-70136. NO: postorbital and posteroventral integumentary glands, some species with keratinized spindes in the skin. CI: Inger (1985); Inger and Gritis (1983). Aubria: CO: 2. GR: Cameroon-Zaire. EMG: exotroph: lentic: benthic. LTRF: 5(3-5)/ 3. OA: typical: anteroventral. MP: wide dorsal gap: mdtiserial lateraiiy and uniserial ventraiiy. SUP: absent. DEM: absent. NA: nearer snout than eye. VT: dextrai. EP: dorsal. SP: sinisual. UJ: medium, smooth arc. LJ: medium, V-shaped. DF: low, originates near dorsal tail-body junction, tip rounded. BS: oval/depressed. CP: totaiiy black. TL: 40136. NO: school in compact balls. CI: Schiotz (1963). Batrachylodes: CO: 8. GR: Solomon Islands. EMG: endotroph. Ceratobatrachus: CO: 1. GR: Solomon Islands. EMG: endotroph.
DIVERSITY
Chaparana: CO: 6. GR: India-Chna. EMG: exotroph: lotic: clasping. LTRE 8(3-8)/ 3. OA: typicai: ventrai. MP: wide dorsai gap: uniserial. SUP: few ventrolaterdy and in a row distai to P-3. DEM: absent. NA. -. VT: dextral. EP: dorsai. SP: sinistral. UJ: medium, wide smooth arc. LJ: wide, V-shaped. DF: low, originates near dorsai taii-body junction. BS: ovai/depressed CP: uniformiy dark. TL: -. CI: C.-C. Liu and H u (1961). Conraua: CO: 6. GR: tropical sub-Saharan Africa. EMG: exotroph: lotic: clasping. LTRF: 7(5-7)/7(1), 8(5-8)/9, 14(7-14)/12(1-2). OA: typicai: ventral. MP: narrow dorsai gap: biserial at least ventrdy. SUP: abundant lateraüy and distai to posterior rows. DEM: lateral. NA: nearer eye than snout. VT: dextrai. EP: dorsal. SP: sinistrai. UJ: wide, mediai edge straight, exceptionaüy long processes laterally. LJ: medium, V-shaped. DF: low, originates near dorsai taii-body junction, tip rounded. BS: ovai/depressed. CP: body dorsum spotted, dorsum of taii muscle lightly banded. TL: 45-60134. CI: Lamotte et ai. (1959a); Lamotte and Zuber-Vogeli (1954a); Sabater-Pi (1985). Discodebs: CO: 5. GR: Solomon Islands. EMG: endotroph. Eúuhyjlossa: CO: 1. GR: Thaiiand. Tadpole unknown. Euphhctis: CO: 4. GR: Arabia-Sri Lanka-Malaysia. EMG: exotroph: lentic: benthic. LTRF: 1/2[1]. OA: typicai: anteroventral. MP: wide dorsal arid medium ventrai gaps: uniseriai. SUP: few laterdy. DEM: lateral. NA: nearer snout than eye. VT: dextral. EP: dorsai. SP: sinistral. UJ: medium, edge a smooth arc. LJ: medium, V-shaped. DF: low, originates near dorsai taii-body junction, tip pointed. BS: ovai/depressed. CP: tail and body striped. TL: 35/36. CI: Annandaie and Rao (1918); Kirtisinghe (1957). Hildebrantia: CO: 3. GR: Ethiopia-Mozambique. EMG: exotroph: lentic: benthic. LTRF: 012. OA: typicai: anteroventrd. MP: wide dorsai gap: uniserial, widely spaced. SUP: absent. DEM: absent. NA: equidistant between snout and eye. VT: mediai. EP: dorsai. SP: sinistrai. UJ: wide, massive with mediai convexity. LJ: wide, massive, open U-shaped. DF: low, originates near dorsai taii-body junction, tip pointed and attenuate. BS: ovai/depressed. CP: uniformiy dark. TL: 95/36. CI: Van Dijk (1966); Wager (1986). H~lobatrachus:CO: 5. GR: Angola-Ethiopia-southern Asia-Chia. EMG: exotroph: lentic: carnivore; lotic: carnivore. LTRF: 4(34)/4(1-2), 5(3-5)/5(1). OA: typicai: anteroventral. MP: complete: uniseriai. SUP: absent. DEM: absent. NA: nearer eye than snout. VT: dextrai. EP: dorsal. SP: sinistrai. UJ: wide, prorninently medidy incised. LJ: wide, prominently medidy incised. DF: low, originates near dorsai taii-body junction. BS: ovai/depressed. CP: uniformly brown. TL: 43/30. NO: M. A. Smith (1917) discussed variations and nonconcordance among sources that suggest other species are involved. CI: Annandaie and Rao (1918); Lamotte and Zuber-Vogeli (1954a); M. A. Smith (1917). Huia: CO: 4. GR: China-southeastern Asia-Greater Sundas. EMG: exotroph: lotic: gastromyzophorous. LTRP: several variations between 518 arid 1116. OA: typicai: suaoriai. MP: usudy wide dorsai gap. SUP: absent. DEM: absent. NA. nearer eye than snout. VT: mediai. EP: dorsai. SP: sinistrai. UJ: wide, M-shaped. LJ: wide, V-shaped. DF: low, originates on taii posterior to dorsai taii-body junction, tip pointed. BS: oval/ depressed CP: dark gray with paie spots, taii dark with paie spots at margins. TL: 681 39. NO: ventrai h originates on tail muscle, transverse keratinized patch on roof of sucker, clusters of glands on body, buccai papiiiae may be distinctive among Amo@, Huia, and Meriscogenys (Inger 1985). CI: Inger (1966); Yang (1991) Indirana: CO: 9. GR: India. EMG: exotroph: lentic: semiterrestriai. LTRP: 5(2-5)/ 3(1). OA: typicai: ventrai. MP: wide (entire upper labium) dorsai gap: uniserial. SUP: none. DEM: absent. NA: nearer eye than snout. VT: dextrai. EP: dorsai. SP: sinistrai. UJ: wide, strongly arched. LJ: strongly arched. DF: low, originates on taii muscle, tip rounded. BS: ovai/depressed. CP: taii muscle banded. TL: 31/33. CI: Annandaie (1918); Dubois (1985). Ingerana: CO: 8. GR: western China-Thaiiand-BornewPhilippines. EMG: endotroph. Lanzarana: CO: 1. GR: Somalia. Tadpole unknown. Lzmnonectes: CO: 62. GR: China-Southeast Asia-Phiiippines. EMG: exotroph: lotic: benthic; lentic: benthic. LTRF: 1/3(1), 1/4(1), 2(2)/3[1]. OA. typical: anteroventrd. MP: wide dorsai gap: papiiiae often with elongate basal areas, narrow ventral gap some-
RONALD ALTIG AND ROY W. McDIARMID
times present. SUP: few lateraiiy. DEM: absent. NA. nearer snout than eye or reverse. VT: dextral. EP: dorsal. SP: sinistral. UJ: narrow to mediurn, smooth arc or slight medial convexity. LJ: narrow to medium, open U-shaped. DF: low, originates near dorsal tail-body junction, tip rounded to pointed. BS: ovalJdepressed. CP: variable, un&orm to prorninently spotted/mottied. TL: 2540136. CI: Inger (1954, 1966, 1985). Menjtogenys: CO: 9. GR: Borneo. EMG: exotroph: lotic: gastromyzophorous. LTRF: several variations between 616 and 817. OA: typical: suctorial. MP: complete: uniserial, reduced to crenulations dorsaiiy, lateral papillae may be larger than elsewhere. SUP: few laterdy. DEM: absent, but folds for expansion of the disc present. NA: nearer eye than snout. VT: medial. EP: dorsal. SP: sinistral. UJ: broadly divided, constructed of few cellular palisades (= ribbed). LJ: ribbed and sometimes broken mediaiiy. DF: low, originates near dorsal tail-body junction, tip pointed. BS: oval/depressed. CP: mottled, íins with lide pigment. TL: 3040/36. NO: ventral íin originates on tail muscle, slun glands present (e.g., behind eye, midlaterdy, sometimes on tail); keratinized areas in roof of sucker. CI: Inger (1985); Yang (1991). MicnXalus: CO: 6. GR: India. Tadpole unknown. Nannupbrys: CO: 3. GR: Sri Lanka. EMG: exotroph: lotic: semiterrestrial. LTRF: 2(2)/ 3(1). OA: typical: ventral. MP: wide dorsal gap: uniserial, very s m d ventrdy. SUP: absent. DEM: absent. NA: nearer eye than snout. VT: dextral. EP: dorsal. SP: sinistral. UJ: wide, strongly arched, coarsely serrate. LJ: wide, strongly arched, coarsely serrate. DF: very low, originates well posterior to dorsal tail-body junction, tip rounded. BS: oval/depressed. CP: mottied. TL: 27/38. NO: ventral fin originates on tail muscle, eyes bulge noticeably, hind legs develop precociously relative to front legs and general development. CI: B. T. Clarke (1983); Kirtisinghe (1958). Nannorana: CO: 3. GR: China. EMG: exotroph: lotic: benthic. LTRF: 3(2-3)/3(1). OA: typical: anteroventral. MP: wide dorsal gap: uniserial. SUP: throughout lateral and ventrolateral areas. DEM: lateral. NA: equidistant between snout and eye. VT: sinistral. EP: dorsal. SP: sinistral. UJ: wide, edge a smooth arc. LJ: wide, U-shaped. D E low, originates near dorsal tail-body junction, tip rounded. BS: oval/depressed. CP: uniformly dark. TL: 36/36. CI: C.-C. Liu and H u (1961). Nyctibatracbus: CO: 10. GR: India. EMG: exotroph: lotic: benthic. LTRF: 010. OA: typicaí: anteroventral. MP: complete: uniserial. SUP: scattered throughout disc. DEM: dorsolateral and midventraí. NA: nearer to eye than snout. VT: dextral. EP: dorsal. SP: sinistral. UJ: narrow, smooth arc. LJ: narrow, open U-shaped. DF: low, originates posterior of dorsal tail-body junction, tip bluntly pointed. BS: oval/depressed. CP: dark mottling, tail muscle banded. TL: 52/36. NO: see Rao (1923). CI: Pillai (1978). Occiáqyga: CO: 2. GR: Southeast Asia-Java. EMG: exotroph: lentic: carnivore. LTRF: 010. OA: oral disc and papdiae reduced to fleshy rim, jaw sheaths recessed. MP: dorsal gap in fleshy, nonpapdlate rim, smaii rounded flap middorsdy. SUP: absent. DEM: absent. NA: equidistant between eyes and snout. VT: medial. EP: dorsal. SP: sinistral. UJ: -. LJ: distinctly U-shaped deeply semilunar in shape. DF: anterior portion prominently high, drops abruptly with remainder low, tip pointed. BS: oval/depressed. CP: black stripe through eye, tail variegated. TL: 30-50136. CI: Inger (1985); M. A. Smith (1916b). Paa: CO: 26. GR: India-Southeast Asia-China. EMG: exotroph: lotic: clasping. LTRF: 4(2-4)/3(1), 7(3-7)/3(1). OA: typical: anteroventral. MP: medium dorsai gap: uniserial. SUP: laterdy and below P-3. DEM: absent. NA: nearer snout than eye. VT: dextral. EP: dorsal. SP: sinistral. UJ: wide, smooth arc. LJ: wide, smooth arc, open U-shaped. DF: low, originates near dorsal tail-body junction, tip round. BS: oval/depressed. CP: body uniformly dark, tail iighter with flecking. TL: 55/36. CI: Annandaie (1912); C.-C. Liu and H u (1961). Palmatorappia: CO: 1. GR: Solomon Islands. EMG: endotroph. Pbrynoyghssus: CO: 9. GR: Southeast Asia-East Indies. EMG: exotroph: lentic: carnivore. LTRF: 010. OA: oral disc and papiiiae reduced to fleshy rim, jaw sheaths recessed. MP: dorsai gap in fleshy, nonpapillate rim. SUP: absent. DEM: absent. NA: equidistant between eyes and snout. VT: medial. EP: dorsal. SP: sinistral. UJ: -. LJ: deeply semilunar in shape. DF: low, originates posterior to dorsal tail-body junction, tip pointed. BS: oval/depressed. CP: black marks form scdoped appearance along margins of fins.
DIVERSITY
TL: 51/36. NO: snout noticeably pointed, lower lip sometimes visible from above, othenvise similar to Occzhzy~a.CI: Inger (1985); M. A. Smith (1916b). Pl~ztymantis:CO: 39. G R Fiji-New Guinea-Phiiippines-China. EMG: endotroph. Ptychdna: CO: 40. GR: sub-Saharan Africa. EMG: exotroph: lentic: benthic. LTRF: 3(2-3)/2, 3(2)/2, 2(2)/2, 112. OA: typical: anteroventral. MP: medium to wide dorsal gap: uni- and biserial. SUP: few lateraliy, row below distai most lower row. DEM: absent. NA: nearer snout than eye, or reverse. VT: medial. EP: dorsal. SP: sinistral. UJ: wide, medial convexity. LJ: wide, open U-shaped. DF: low with slight arc, originates near dorsal tail-body junction, tip pointed. BS: ovalJdepressed. CP: muted but variable. TL: 30-55136. CI: Lamotte et al. (1958); Lamotte et al. (1959b); Lamotte and Perret (1961a); Van Dijk (1966); Wager (1986). Pyxicephalus: CO: 2. GR: sub-Saharan Africa. EMG: exotroph: lentic: benthic. LTRF: 5(3-5)/3. OA: typical: anteroventral. MP: wide dorsal gap: multiserial laterally, biserial ventraliy. SUP: few laterally DEM: lateral. NA: near eye than snout. VT: medial. EP: dorsal. SP: sinistral. UJ: wide, medial convexity. LJ: medium, open U-shaped. DF: medium with slight arc, originates near dorsal tail-body junction, tip bluntly pointed. BS: ovalJdepressed. CP: uniformly dark. TL: 70136. NO: schools, sometimes in midwater and with other species. CI: Power (1927a); Van Dijk (1966). Rana: CO: 224. GR: widespread. EMG: exotroph: lentic: benthic; lotic: benthic, clasping, gastromyzophorous; endotroph. LTRF: many variations between 112 and 918,213 is common in North America, n/3 common elsewhere. OA: typical: anteroventral, ventral. MP: dorsal gap: usualiy uniserial, more rarely a narrow ventral gap, ventral papillae may be elongate. SUP: few laterally, absent. DEM: lateral, absent. NA: nearer eye than snout or reverse. VT: dextral. EP: dorsal. SP: sinistral. UJ: narrow to wide, smooth arc, medial part of edge straight. LJ: narrow to wide, narrow V-open U-shaped. DF: low, originates near dorsal tail-body junction, tip pointed to round. BS: ovalJdepressed. CP: variable. TL: 30-100136. NO: a number of species groups have distinctive morphologies. CI: Boulenger (1892); Hilhs (1982); Hillis and Frost (1985); Hdhs and De Sá (1988); Lanza (1983); Scott and Jemings (1985); A. H. Wright and Wright (1949); Zweifel (1958). Staurois: CO: 3. G R Borneo-Philippines. EMG: exotroph: lotic: burrower. LTRF: 2(2)/9(1). OA: typicai: ventral. MP: wide dorsal and narrow ventral gap: uniserial dorsolaterally, biserial ventraliy. SUP: few dorsolateraliy. DEM: lateral. NA: smali, much nearer snout than eye. VT: medial. EP: dorsal. SP: sinistral. UJ: narrow, wide arc. LJ: medium, open V-shaped. DF: low, originates near dorsal tail-bodyjunction, tip rounded. BS: ovalJdepressed. CP: very lightly pigmented, skin appears shiny. TL: 32/31. NO: convergent on the general centrolenid morphology, eyes particularly smali. CI: Inger and Tan (1990); Inger and Wassersug (1990). Taylorana: CO: 2. GR: India-Vietnam-Java. EMG: endotroph. Tomoptema: CO: 13. GR: India-sub-Saharan Africa. EMG: exotroph: lentic: benthic. LTRF: 3(2-3)/3, 4(2-4)/3. OA: typical: anteroventral. MP: wide dorsal gap: biserial, except uniserial midventraiiy. SUP: few lateraliy. DEM: lateral. NA: nearer eye than snout or reverse. VT: dextral. EP: dorsal. SP: sinistral. UJ: wide, massive with medial convexity. LJ: wide, massive, open U-shaped. DF: low, originates at dorsal tail-bodyjunction, tip pointed. BS: ovalJdepressed. CP: uniforrnly dark. TL: 3644136. CI: GriUitsch et al. (1988); Van Dijk (1966); Wager (1986). RHACOPHORIDAE: CO: 121292. G R Africa-India-southeastern Asia. EMG: exotroph: lentic: benthic, arboreal, nektonic; lotic: benthic, clasping, suaorial; endotroph. LTRF: many variations between 110 and 813; n/3 most common. OA: typical: anteroventral or terminal. MP: wide dorsal gap, sometimes narrow ventral gap or complete: uni-, bi-, and multiserial. SUP: absent, lateraliy or below P-3, row(s) centripetal to marginal papiiiae. DEM: lateral, absent. NA: nearer snout than eye or reverse. VT: dextral, medial. EP: dorsal, lateral. SP: sinistral. UJ: variable including wide, medial margin straight or smooth arc coarsely serrate or not, absent. LJ: medium to wide, U- to V-shaped, coarsely serrate or not, sometimes smali medial convexity. DF: low to moderately high, originates near dorsal tail-body junction, tip rounded to pointed. BS: round, oblong or ovalJdepressed. CP: variable. TL: 25-90136. Buergeriinae: CO: 114. G R China-Japan. EMG: exotroph: lentic: benthic; lotic: benthic.
Wchadena
RONALD ALTIG A N D ROY W. McDIARMID
Mantidaqlus; Mantidaqlus sp.
Mantidaqlus; M. 0pqat-m
LTRF: 5(2-5)/34(1), 6(3-6)/4(1). OA: typicai: anteroventrai.MP: wide dorsai gap: uniseriai. SUP: row(s) centripetal to most marginal papillae. DEM: lateral. NA. nearer snout than eye or reverse. VT: dextrai. EP: dorsai. SP: sinistrai. U J:wide, mediai margin straight, coarsely serrate. LJ: medium, V-shaped, coarsely serrate. DF: low, originates near dorsai taii-body junction, tip pointed. BS: oblong/depressed. CP: iightly pigmented with flecks and spots on tad. TL: 30-44136. Buegeria: CO: 4. GR: China-Japan. CI: Maeda and Matsui (1989); Okada (1931); Utsunomiya and Utsunomiya (1983). Mantellinae: CO: 2/68. GR: Madagascar. Mantella: CO: 10. GR: Madagascar. EMG: exotroph: lentic: benthic, arboreai. LTRF: 3(2-3)/3,5(2-5)/3[1]. OA: typicai: anteroventrai.MP: wide dorsai gap: uniseriai dorsolaterdy, biseriai ventrolaterdy. SUP: absent. DEM: lateral. NA: nearer snout than eye. VT: dextrai. EP: dorsai. SP: sinistrai. UJ: medium, smooth arc. LJ: medium, open Vshaped. DF: low, tip rounded. BS: ovai/depressed. CP: uniforrnly dark. TL: 20-30136. CI: Arnoult (1965); Blommers-Schlosser and Blanc (1991); Glaw and Vences (1992). Mantidactylus: CO: 58. GR: Madagascar. EMG: exotroph: lentic: benthic, arboreai; lotic: benthic, psarnmonic, umbeiiiform; endotroph. LTRF: a number of variations between 010 and 613. OA: typicai: anteroventrai, terminal, ventrai. MP: wide dorsai gap: uniseriai, s m d ventrai gap less common, complete. SUP: few laterdy, row below P-3. DEM: lateral, absent. NA: dose to snout then eye and reverse. UJ: absent, narrow to wide, smooth arc, sometimes with mediai convexity, serrations fine to coarse, one species with no basai sheath and serrations elongated into series of spikelike projections. LJ: narrow to wide, V-shaped, spikelike projections. DF: tip pointed, sometimes proximai part low with a prominent increase in height more posteriorly. BS: ovai/depressed. CP: quite variable, often uniformiy dark. TL: 25-70136. NO: M. lugubrzs without labiai teeth but pigmented stniaures in rows on lower labium look iike labiai teeth. CI: Arnoult and Razarihelisoa (1967); Blommers-Schlosser and Blanc (1991); Glaw and Vences (1992). Rhacophorinae: CO: 91220. GR: Africa-Madagascar-Seycheiie Islands-India-southeastern Asia. Aglrptodactylus: CO: 1. GR: Madagascar. EMG: exotroph: lentic: benthic. LTRF: 6(2-6)/3(1). OA: typical: anteroventrai. MP: wide dorsai gap: uniseriai. SUP: absent. DEM: lateral. NA: nearer eye than snout. VT: dextrai. EP: dorsai. SP: sinistral. UJ: wide, mediai edge straight. LJ: wide, U-shaped. DF: low, originates near dorsai taii-body junction, tip round. BS: ovai/slightly depressed. CP: paie with reticulations on taii. TL: 25/36. CI: Blommers-Schlosser and Blanc (1991); Glaw and Vences (1992). Boophis: CO: 37. GR: Madagascar. EMG: exotroph: lotic: benthic, clasping, suctoriai; lentic: benthic. LTRF: 3(2-3)/3, 5(2-5)/3(1), 6(2-6)/3[1], 6(3-6)/3(1), 7(2-7)/3(1), 75-7)/3, 8(3-8)/3,8(5-8)/3. OA: typicai: anteroventrai, ventrai. MP: wide dorsai gap, sometimes narrow ventrai gap, uncommonly complete: uni- and biseriai. SUP: common laterdy and below P-3. DEM: lateral, absent. NA: various sites. VT: dextrai. EP: dorsai. SP: sinistrai. UJ: medium to wide and various shapes, absent. LJ: medium to wide, various shapes. DF: low, originates near dorsai taii-body junction, tip pointed to rounded. BS: ovai/depressed. CP: variable mottled. TL: 30-90136. CI: BlommersSchiosser (1979b); Blommers-Schiosser and Blanc (1991); Glaw and Vences (1992). Chimiafus: CO: 8. GR: Southeast Asia. EMG: exotroph: lentic: arboreai. LTRF: 5(2-5)/3, 4(24)/3(1), 212. OA: typicai: terminal or anteroventrai. MP: wide dorsai gap: multi- or uniseriai midventrdy, narrow ventral gap. SUP: absent. DEM: lateral, absent. NA: nearer snout than eye. VT: dextrai. EP: dorsai. SP: sinistrai. UJ: medium, massive construction, smooth arc. LJ: medium, V-shaped. DF: low, originates at dorsai tail-bodyjunction, tip slightly rounded. BS: ovai/depressed. CP: siightly speckled on taii, uniformiy dark, distal part of tail dark. TL: 30141. NO: C. ezjinderi oophagous. CI: Bourret (1942); Heyer (1971); Kam et ai. (1996); Kurarnoto and Wang (1987); Utsunomiya and Utsunomiya (1983). Chiromantis: CO: 3. GR: sub-Saharan Africa. EMG: exotroph: lentic: benthic. LTRF: 3(2-3)/3, 5(2-5)/3. OA: typicai: anteroventrai. MP: wide dorsai gap, narrow ventrai gap: uniseriai dorsolaterdy and biseriai ventrdy. SUP: absent. DEM: lateral. NA. s m d , nearer snout than eye. VT: mediai. EP: dorsai. SP: sinistrai. UJ: medium, smooth arc. LJ: narrow, V-shaped. DF: low, originates near dorsai taii-body junction, tip pointed.
DIVERSITY
BS: oval/depressed. CP: u d o r d y paie with blotches on taii. TL: 45-55/34. CI: Lamotte and Perret (1963a); Van Dijk (1966). NyctkaLus: CO: 5. GR: Greater Sundas-Philippines. EMG: exotroph: lentic: arboreai. LTRE 5(2-5)/3, 5(3-5)/3. OA: typicai: anteroventrai. MP: wide dorsai gap: biseriai. SUP: absent. DEM: lateral. NA: equidistant between eye and snout, smaii medial projection. VT: medial. EP: dorsal. SP: sinistral. UJ: medial convexity, coarsely serrate. LJ: medlurn, V-shaped, coarsely serrate. DF: low, originates near dorsal mil-body junction, tip rounded. BS: oval/depressed. TL: 43/26. CP: unifordy purplish brown. CI: Alcala and Brown (1982); Inger (1966, 1985). Philautus: CO: 87. GR: India-China-Philippines. EMG: exotroph: lentic: arboreal; endotroph. LTRP: 110. OA: typical: terminal. MP: complete: biserial. SUP: -. DEM: lateral. NA: tiny, nearer snout than eye. VT: medial. EP: dorsal. SP: sinistrai. UJ: wide, without serrations. LJ: wide, coarsely serrate. DF: low, originates near dorsal tail-body junction, tip rounded. BS: oval/depressed, widest near plane of eyes, snout truncate. CP: unifordy paie brown. TL: 29/37. CI: Wassersug et ai. (1981a). Polpedutes: CO: 19. GR: India-China-Japan-southeastern Asia-Phhppines. EMG: exotroph: lentic: benthic. LTRF: 4(24)/3[1.], 5(2-5)/3[:1]. OA: typical: anteroventral. MP: wide dorsal gap: biserial, narrow ventral gap. SUP: few lateraiiy, throughout extent of marginal papillae, absent. DEM: lateral. NA: nearer snout than eye. VT: dextral. EP: dorsai, lateral. SP: sinistral. UJ: medium, high smooth arc, medial convexity. LJ: medium, open V-shaped. DF: moderately high, originates near dorsal td-body junaion, tip pointed. BS: oval/depressed. CP: variable. TL: 2545136. NO: Inger (1966) shows tail sheath (see text chap. 3) in l?macrotis and l? otiiuphus. CI: Inger (1985). Rhacuphoms: CO: 51. GR: India-China-Celebes Islands. EMG: exotroph: lentic: benthc, nektonic. LTRF: 4(2-3)/3(1), 5(2-5)/3[1]. OA: typicai: anteroventral. MP: wide dorsal gap: biserial, sometimes s m d ventral gap. SUP: absent, few laterally. DEM: lateral. NA: nearer snout than eye. VT: dextral. EP: dorsal. SP: sinistral. UJ: medium to wide, smooth arc or smaii medial convexity. LJ: medium to wide, V-shaped. DF: low to medium, originates near dorsal taii-body junction, tip pointed. BS: oval/depressed. CP: usudy unicolored, often pale. TL: 3545136. CI: Inger (1966, 1985). Tbelodema: CO: 9. GR: Burma-Malaysia. EMG: exotroph: lentic: arboreal. LTRF: 4(24)/4(1). OA: typical: nearly terminal. MP: wide dorsal gap: biserial. SUP: absent. DEM: lateral. NA: s m d , nearer snout than eye. VT: medial. EP: dorsal. SP: sinistral. UJ: medium, medial convexity, coarsely serrate. LJ: wide, more finely serrate, open Ushaped. DF: medium, erupts abruptly from near dorsal td-body junction, tip broadly rounded. BS: round/depressed. CP: unifordy dark. TL: 28/28. CI: Wassersug et ai. (1981a).
Polrpedates
RHINODERMATIDAE: CO: 112. GR: southwestern South America. Rhinoakma: CO: 2. GR: southwestern South America. EMG: endotroph. RHINOPHRYNIDAE: CO: 111. GR: Texas-Costa Rica. EMG: exotroph: lentic: suspension feeder. LTRP: 010. OA: terminal, wide, slitlike mouth with multiple barbels. MP: not appiicable. SUP: not applicable. DEM: not applicable. NA: smaii, nearer eye than snout. VT: medial. EP: lateral. SP: dual/lateral. UJ: not applicable. LJ: not appiicable. DF: low, originates near dorsal tail-body junction, tip bluntly pointed. BS: oval/depressed. CP: unifordy pale or dark. TL: 50136. NO: papilla-like structure at syrnphysis of infrarostral cartilages; looks grossly like a %nopus tadpole. Rhin@hrvnus: CO: 1. GR: Texas-Costa Rica. CI: Orton (1943): E. H. Tavlor (1942). SOOGLOSSIDAE: CO: 213. GR: Seycheiie Islands. Nesomantis: CO: 1. GR: Seycheiie Islands. EMG: endotroph. Sooglosus: CO: 2. GR: Seycheiie Islands. EMG: endotroph.
fiivwpbrynus
334
RONALD ALTIG A N D ROY W. McDIARMID
Alphabetical List of Representative Morphotypes Presented in the Text: Genus, Guild, Species Drawn, and Source (s) Acanthkai~(Arboreal Type 2); A. spznosus; after Larnotte et al. (1959a) Acris (Benthic);A.~lyllus;USNM 332799 Adelotus (Benthic);A. b r h ; after Watson and Martin (1973) Afnxalus (Nektonic); Afnxalus sp.; composite of USNM 308801-03 Ansonia (Clasping);A. lon&&ita; USNM 306204 Ascaphus (Suctorial);A. wei; USNM 297184 Astylosteemus (Adherent);Astylosteemw sp.; USNM 306967 Atelupus (Gastromyzophorous); A. pachydemzus; USNM 286455 Bombina (Benthic); B. bombina; composite of cultured B. orientalis and after Angel (1946), Boulenger (1892), and Lanza (1983) Boophis (Suctorial); Boophis sp.; USNM field number 107433A B u . (Benthic);B. woodhousiz; USNM 320297 Cardw~lossa(Benthic); C. ~racilis;composite of USNM 306968 and C. sp. USNM 306969 Ceratophlys (Carnivorous Type 1); C. comuta; USNM 299936 Chawphlys (Benthic); C. pierottiz; after Faivovich and Carrizo (1992) Cochranella (Fossorial); C. jranulosa; composite of USNM 29 1045 and after C. uranoscopa of Heyer (1985) Colostethus (Benthic);C. hinztatis; USNM 167515 Colostethus (Neustonic); C. flotatur; composite of USNM 203704-07 Cyclorana (Benthic); C. cultripes; after Watson and Martin (1973) Dendrobates (Arboreal Type 2); D. guinguivittatus; USNM 269075 Discglossus (Benthic);D. pictus; after Boulenger (1892) Duellmanohyla (Adherent);D. salvavida; USNM 304979 Hamptophlyne (Suspension-feeder Type 1); H. boliviana; composite of USNM 298826,299953, and 299957 Hehioporus (Benthic); H. australiacus; after Watson and Martin (1973) Hehophlyne (Suctorial);H. regir; USNM 300543 Hemzsus (Benthic); H. Juttatum; composite of USNM 308795 and308798 Hyla (Suctorial);H. amutta; USNM 346278 Hyla (Arboreal Type 1); H. bromeliacia; USNM 304997 Hyla (Arboreal Type 2) ;H. picadoi; USNM 331374 Hyla (Macrophagous);H. sarayacuensis; USNM 313525 Hymnochirus (Carnivorous Type 2); H. curttpes; USNM 140275 Insuetophrynus (Benthic); I. acarpicus; composite after Diaz and Valencia (1985) and Formas et al. (1980) Kassina (Nektonic); K. senegalensis; composite of USNM 308809 and Wager (1986) Lepzdobatrachus (Carnivorous Type 2); L. Ilanensis; composite of USNM 307185 and Cei (1980) Leptobrachella (Benthic);L.~raczlis;after Inger (1966) Leptobrachium (Benthic);Leptobrachium sp.; composite of L. hasselti and L. ngrops after Inger (1966) and Berry (1972)
Leptodactylodon (Neustonic); Leptodactylodon sp.; USNM 306971 Leptodactylus (Benthic);L. melanonutus; USNM 304941 Leptodactylus (Benthic, sometimes carnivorous);L. pentadactylus; USNM 203730 Leptopelis (Benthic); L. natahnsis; composite of USNM 308812 and Wager (1986) Leptophlyne (Benthic);L. borbonica; after Berry (1972) Mdntidaclylus (Benthic); Mantidactylus sp.; USNM field number 107426A Mdntidactylus (Fossorial); M. femoralzs; USNM field nurnber 107404 Mantidactylus (Fossorial); M. lugubmr; USNM field number 107405 Mantidactylus (Neustonic);M. opiparus; USNM field number 11828 Megophlys (Neustonic);Megophlys sp.; USNM 292051 Microhyla (Neustonic); M. heymonsi; composite of USNM 206402-05 NelsonUphlyne (Suspension-feeder Type 1); N. atewimus; after Donneiiy et al. (1990) Otupblyne (Psamrnonic); 0.pyburnz; composite of USNM 304280 and after Wassersug and Pyburn (1987) Pelodpes (Benthic); E punctatus; composite after E. N. Arnold and Burton (1978), Boulenger (1892), Lanza (1983), and Noiiert and Noiiert (1992) Phasmahyla (Neustonic);E ~uttata;USNM 241258 Phyllomedusa (Suspension-rasper); E vazllanti; USNM 321149 Polfiedates (Nektonic); E mgmphala; USNM 3 13968 Pseudis (Nektonic); Eparadoxa; USNM 302522 Ptychadena (Benthic);Ptychadena sp.; composite of USNM 308829 and Wager (1986) RhinUphlynus (Suspension-feederType 2); R. dorsalis; composite of USNM 306925,307148, and 307157 Scaphwphryne (Suspension-feeder but may rasp or feed as a carnivore); Scaphiophlyne sp.; USNM field number 11691 Scaphwps (Benthic); S. couchii; USNM 320302 Scarthyla (Nektonic); S. ostinudactyla; USNM 266112 Schismademza (Benthic);S. carens; USNM 308793 Scinax (Nektonic); S. sugillata; composite of USNM 285280-88 Scinax (Nektonic); S. eimochroa; USNM 330834 Scinm (Nektonic);S. stauffm>composite of USNM 306917 and 306921 Stephopaedes (Arboreal Type 3); S. anotis; after Channing (1978) Thorupa (Semiterrestrial); ?: miliaris; USNM 209372 Trichobatrachus (Suctorial);?: robustus; composite of USNM 306974 and 306976 Werneria (Suctorial); Iilpeussi; reconstructed after dorsal and ventral views in Mertens (1938) Xen~pus (Suspension-feeder Type 2); X. l m s ; USNM 308822
DIVERSITY
335
Table 12.4 World ranges of anuran families with aotrophc tadpoles in mogeographical realms. Families are listed in approximate order of increasing number of species in each realm, and endemic families are in boldface
Summary
Severai interesting things came out of our attempt to characterize the morphologicai variation represented among ali genera and families of anuran tadpoles. The use of a standard African: Sooglossidae, Heleophrynidae, Hemisotidae, Microhylidae, Arthroleptidae, Pipidae, Rhacophoridae, Bufonidae, Ranidae, format and terminology gave us a much better appreciation and ~ ~ ~ e r o l i i d a e of the distribution of Iamal traits among living frogs. This Austropapuan: Ranidae, Hylidae, and Myobatrachidae summation also uncovered the types of gaps in our knowl- Nearctic: Ascaphidae, Rhinophqmdae, Leptodactylidae, Microhyliedge. By our count, no information is available on the reprodae, Pelobatidae, Bufonidae, Ranidae, and Hylidae duaive mode for 29 genera ( 8%) of frogs, and only four Neotropical: Rhinophrynidae, Pseudidae, Pipidae, Ranidae, Microhylidae, Bufonidae, Centrolenidae, Dendrobatidae, Leptodactylidae, of these are reasonable candidates for endotrophy. Most and Hylidae (86%)of these 43 species are in monotypic genera, and a- Oriental: Bombinatoridae, Hylidae, Megophryidae, Microhylidae,Buing this gap has a high probability of uncovering different fonidae, Rhacophoridae, and Ranidae tadpole morphotypes. Although we currently do not know Palearaic: Pelodytidae, Pelobatidae, Hylidae, Bombinatoridae, Discoglossidae, Bufonidae, and Ranidae the total number of different tadpoles that have been described, we know that those of many species in genera from which some tadpoles are known remain to be discovered. Given past findings, we are confident that some of these undiscovered forms also will provide new insights into tadpole if there are unworked larvai coiiections in some European morphology. Whde this summation confirms that we know museums similar to the extensive holduigs of reptiles that something about the reproduaive mode of most frog spe- were amassed during periods of European colonial occucies, the inclusion of data for a given taxon does not imply pancy of tropical Africa. If not, efforts should be made to that comparable data are available for ali species in that genus overcome the logisticai and politico-economic problems that nor that the recorded data necessarily are representative of too often make field work in these areas so difficult and astadpoles of ali included species. Less than a third of ali tad- semble new colleaions that are direaed specificaliy at the poles have been described reasonably well, and the number tadpole fauna. To facilitate tadpole work there and in other of entries that have no data, including endotrophs and exo- regions of the world, we have summarized (table 12.4) the trophs, shows that much work remains. We have a reason- general distributions of anuran families as an aide to their ably good foundation in certain aspects of tadpole morpho- identification and an adjuna to the comparative study of logicai diversity, but there is much to learn. tadpole morphology. The foiiowing key ais0 grew out of the Another spin-off from t h s compilation was a better ap- summation and is intended not so much as an help to identipreciation of the geographical gaps in our knowledge. It fication (which it may be) but more as an iüustration of the seems clear to us that of the tropical regions of the world distribution, including notable cases of convergence, of a where frog diversity is high, the tadpole fama of equatorial few major larvai traits among anuran families and subfamilAfrica stands out as one in need of much more study. ies. Aü taxa are not accounted for in every case, and the key Whether a broader sampling of lamal morphology would could have been compiled in several ways (i.e., the same or shed new light on ranoid phylogeny is debatable, but the different charaaers in different sequences). Even so, the confew glimpses we have had of morphologicai diversity and veyed message in each case would have been the same -taddevelopmental patterns characteristic of some arthroleptid poles in a few families can be keyed easily and those in antadpoles cry out for attention. We are not aware of much other large group of families cannot be separated based on current interest in tadpoles from tropical Africa and wonder these few charaaers.
-
336
RONALD ALTIG AND ROY W. McDIARMID
An Illustrative Key to Families of Anuran Tadpoles Based on a Few Major Characters SECTION 1. SPIRACLE A. Dual and lateral, centripetal waii absent B. Single, midventral on chest, abdomen, or near vent, centripetal waii absent except in cases where spiracle is near vent C. Single, low on left side, sometimes alrnost medial, centripetal waii often absent D. Single, sinistral, centripetal waü usuaüy present, at least as a ridge SECTION 2. BARBELS AND ORAL APPARATUS A. Single, long, motiie, at corners of mouth; oral disc, jaw sheaths, and labial teeth absent B. Multiple, short, nonrnotile, around mouth margin; oral disc, jaw sheaths, and labial teeth absent C. Barbels absent; oral disc and labial teeth absent; jaw sheaths present as few, spikelike projeaions
Seaion 2
Section 3 Seaion 4 Section 5
Pipidae: Pipinae and Xenopodinae Rhinophrymdae Leptodactylidae: Ceratophrymae (part)
SECTION 3. ORAL APPARATUS, NARES, AND SPIRACLE A. Oral apparatus consists of large suctorial disc, large platelike upper jaw sheath, smaii lower sheath, and some rows of biserial labial teeth; nares present; spiracle on chest Ascaphidae B. Oral apparatus consists of semicircular oral flaps overhanging mouth and no jaw sheaths or labial teeth; Microhylidae: Dyscophinae, Microhyiinae (part), nares absent; spiracle on abdomen or near vent Phyrnomerinae, and Scaphiophryninae (part) C. Oral appararus consists of large umbelliform oral disc derived mostly from the lower labium and no jaw sheaths or labial teeth; nares absent; spiracle on abdomen Microhylidae: Microhylinae (also see section 5) SECTION 4. MARGINAL PAPILLAE, TOOTH ROWS, A-1, AND LTRF A. Marginal papiüae complete or nearly so; tooth rows biserial; A-1 aimost the same length as A-2; LTRF 213 Bombinatoridae and Discoglossidae B. Marginal papiüae complete or with dorsal gap; tooth rows uniserial; A-1 almost the same length as A-2; LTRF 213 Hylidae: Phyiiomedusinae (part) C. Marginal papiüae complete or nearly so (i.e., narrow dorsal gap); tooth rows uniserial; A-1 much shorter than A-2; LTRF > 213 Megophryidae (part), Pelobatidae D. Marginal papiiiae complete or with dorsal gap; tooth rows uniserial; A-1 aimost the same length as A-2; LTRF 5 613 Myobatrachidae: Myobatrachmae (part) SECTION 5. ORAL DISC, JAW SHEATHS, LABIAL TEETH, AND BELLY A. Oral disc reduced to rim around mouth, usuaüy with dorsal gap; jaw sheaths present; labial teeth present or not; Hylidae Hemiphractinae (part), Hylinae (part) and body wall unrnodiíied Ranidae: Raninae (part) B. Oral disc present, typical size or larger than normal but Arthroleptidae: Astylosterninae (part), Dendrobatidae umbeliiform (upturned); jaw sheaths present or not; labial (part), Megophryidae (part), and Rhacophoridae: teeth present (uniserial) or not; body waü not modified Mantellmae (part; also see seaion 3) C. Oral disc normal; one or both jaw sheaths absent; labial teeth present; body waü unrnodified Section 6
D IVE RS ITY
D. Oral disc normal; both jaw sheaths present; labial teeth present; body w d unmodhed E. Oral disc normal; both jaw sheaths present; labial teeth present; body w d variously modified
Section 8
SECTION 6. LTRF BALANCE VALUE A. LTRF imbalanced negatively (3114 = - 11) B. LTRF imbalanced positively (913 = +6)
Heleophrynidae Rhacophoridae: Mantellinae (part)
SECTION 7. ORAL DISC AND LTRP A. Oral disc enlarged, often with many marginal papiiiae smaii and closely spaced (i.e., rheophilous), may be complete or not; number of tooth rows 213-17121; lotic habitats B. Oral disc typical with larger, more widely spaced marginal papdiae, usudy with at least a dorsal gap (i.e., not rheophilous); number of tooth rows 2 113; leutic or lotic habitats
SECTION 8. BODY WALL MODIFICATION A. Beiiy modified into aaively operating sucker (i.e., center can be manipulated to form negative pressure between beiiy and substrate = gastromyzophorous) B. Lateral and posterior body waii developed into free flap that cannot be manipulated to form negative pressure C. Lateral body waii with various forms and degrees of lateral sac development D. Fleshy, hoiiow crown surrounding eyes and nares E. Transverse, fleshy flap behind eyes F. Fingerlike projection ventrolaterdy at junction of opercular and abdominal cavities
ACKNOWLEDGMENTS Several persons helped with the preparation of this chapter in different ways. K. Spencer's sketches of many of the distinctive tadpole morphotypes enhanced the diversity presentation immeasurably. The sketch of Leptobrachella was redrawn frorn Inger (1966) and is reprinted by permission of Inger; the sketch of Nelsonophryne was redrawn from Donneiiy et ai. (1990a) and is reprinted courtesy of The Arneri-
Section 7
Bufonidae (part), Hylidae: Hylinae and Pelodryadinae, Leptodactylidae: Teimatobiinae (part), Megopwdae (part), Myobatrachidae: Myobatrachinae, Ranidae: Raninae and Petropedetinae Bufonidae (part), Centrolenidae, Dendrobatidae (part), Hemisotidae, Hylidae: Hyhae, Pelodryadinae (part), and Phyiiomedusinae (part), Hyperoliidae, Leptodactylidae: Teimatobiinae (part), Myobatrachidae: Lirnnodynastinae and Myobatrachinae, Pelodyidae, Pseudidae, and Ranidae: Raninae and Petropedetinae (part)
Bufonidae (part) and Ranidae: Raninae (part) Leptodactylidae: Teimatobiinae (part) Arthroleptidae: Astylosterninae (part) Bufonidae (part) Bufonidae (part) Microhyiidae: Melanobatrachinae can Museum of Natural History and De Sá. R. J. Richards suppiied a number of pertinent papers on the Austraiian fama at a moment's notice. Over the past thirty years the curators and staífat several museums have loaned specimens, permitted dissections and other speciai preparations, and coiiected or c d e d to our attention material that has noticeably advanced our research. Without the cooperation of these and others our understanding and awareness of tadpole morphology would have been noticeably lessened.
The glossary includes terms that may have been deíined or restriaed by the terminology suggested in this book or are not commonly found in other sources. Refer to chapters 2 and 3 for further discussion of many morphological terms. Pertinent citations are often presented. Terms within a definition that are defined elsewhere in the glossary are in boldface. Synonymous terms that are accepted in this book are presented in parentheses, and unaccepted ones are presented in brackets. Uniess noted othenvise, d staging notations pertain to Gosner (1960).
GLOSSARY
A-2 gap (Altig 1970) [medial i n t e ~ dor space]. Medial gap in second upper row in species with 2 upper rows; can be expanded to denote any row on either labium (e.g., A-4 gap, P-3 gap); see A-2 gap ratio and labial tooth row formula. A-2 gap ratio (Altig 1970). Length of either section of the actual row of teeth in row A-2 divided by the length of the medial gap between the two parts of the row; number > 1 indicates a gap smalier than the length of a row section and vice versa; can be calculated for any row that is broken medid y on either labium; see A-2 gap and gap. abdominal length (Carr and Altig 1991). Medial, straight line distance from base of vent tube to the spiracular w d ; this measurement is sometimes usem but has a large measurement error because neither landmark is consistentiy de&able. abdominal sucker (beily sudrer) [belly or sucker disc]. See beily sucker, also adhesive giand, belly flap, and gastromyzophorous. accessory labial tooth rows (R. G. Webb and Korky 1977). Short tooth rows oriented verticdy or transversely and often positioned near the lateral ends of tooth rows; occur norm d y in some ranids and pelobatids, infrequentiy in other taxa; this modified LTRF shows four accessory rows between solidi: 3(2)/4/3(1). acosmanura (Starrett 1973). Word synonym for Orton's (1953) Type 4 tadpole; ranoid of O. M. Sokol(1975). adaptive peak. Combination of dele frequencies or morphologies that leads to the locdy maximal fimess of a population. additive genetic variance. That fraction of total phenotypic variation caused by deles that are statisticdy additive in effea; can be aaed upon by natural selection; see nonadditive genetic variance. adherent. An ecomorphological guild that includes those lotic tadpoles that live in flowing water and have s m d , complete marginal papillae, LTRF commoniy 213, and inhabit faster water than tadpoles in the clasping guild, position maintenance via oral disc common to continuously; see table 2.2, figures in chap. 12, adherent, benthic, clasping, fossorial, gastromyzophorous, nektonic, neustonic, psammonic, rheophilous, semiterrestrial, and suctorial. adhesive gland [cement gland, oral or ventral sucker]. Transitory sticky gland of various shapes on the ventral surface of the head of an embryo or hatchling immediately posterior to the stomodeum or mouth; used to stabilize hatchlings before swimming abilities develop; comotations of "sucker" should not be used in this case. afferent nerve o r axon. Neuron that carries nerve im~ulsesto the brain (= sensory) or into a brain nucleus; see efferent nerve or axon. aggregation [school]. A general term that describes a group of tadpoles that are congregated in response to some other faaor(s) than social interactions; qualities of a school (e.g., polarized orientation and coordu-iated movements) and the
340
GLOSSARY
reason for the congregation are not implied; see biosocial aggregation, school, and taxic aggregation. alar plate. Sensory portion of the brain stem, oriented vertically and located dorsal to the sulcus limitans along the lateral ventricular wail; see basal plate. allelopathy. Produaion of chemicals into the environment by one individual that results in a reduction in the fitness of other organisrns. aiiochthonous. Originating outside the systern; usually in reference to food rnaterials. amphigyrinid. Describes the condition of having dual, lateral spiracles as in pipids, rhinophrynids, and Lepidobatrachus (leptodactylid), although latter case not hornologous with former two (Ruibal and Thornas 1988); see laevogyrinid, mediogyrinid, paragyrinid, and sinistral. anamniote. Describes the condition of lacking an amnion; characteristic of fishes and amphibians. anlage (n). An ernbryological precursor. antagonistic pleiotropy. Negative genetic correlation between two traits caused by the fixation of pleiotropic genes that d e a both traits in the adaptive direction, leaving those pleiotropic genes that d e c t one trait in the adaptive direction and the other in the rnaladaptive direction to contribute the genetic variation and covariation. anus. See vent and vent tube. aortic arches. Aortic vessels parallel with the posterior visceral arches and connecting the heart with the dorsal aorta; the major vessels c q i n g oxygenated blood. AR-1 (Thibaudeau and Altig 1988). Expansion of the tooth row notation of Altig (1970) to designate the tooth ridge prior to tooth developrnent in developrnental studies; can be expanded to denote any tooth ridge. arboreal. An ecomorphological guild that includes those lentic tadpoles that are rnodified in one of several rnorphological patterns for living and feeding in water-filled phytotelmata or similar arboreal sites; see table 2.2, figures in chap. 12, benthic, carnivorous, macrophagous, nektonic, neustonic, suspension feeder, and suspension rasper. barbel [papiüa]. Fleshy, filiforrn projection(s) at the corners of the rnouth of pipid (long with internal support and rnusculature) and rhinophrynid (short, no internal support or rnusculature) tadpoles, although structures are not hornologous between the two families (Cannateila and Trueb 1988a); barbel at the syrnphysis of the lower jaw ofRhinophrynus tadpoles is probably not homologous with either of the others. basal plate. Motor portion of the brain stem oriented h o r i i n tally and located ventral to the sulcus limitans; see alar plate. behavioral fever. Elevation of the preferred body temperature of an ectotherm in response to infection or inoculation with pathogenic bacteria, vimes, or products of these organisms. behavioral thermoregulation. Regulation of body temperature (usually by an ectotherm) by rnovernent or changes of posture or position within or between therrnal regimes. belly flap. Out-folding of lateral, posterior, or both parts of the body wall to forrn a flap; probably used in attachment by semiterrestrial tadpoles but only by increasing surface area for cohesion; see table 2.2, figures in chap. 12, belly sucker, and gastromyzmphorous. beily sucker (abdominal sucker) [beily or sucker disc]. The rnodified belly of a gastromyzophorous tadpole, includes a raised rim, rnusculature to raise the roof of the sucker to actuaily forrn a negative pressure, and papillate and sometimes keratinized areas on the roof; see table 2.2, figures in chap. 12, belly flap, rheophilous, and suctorial.
benthic [benthonic]. An ecomorphological guild that includes those lentic or lotic tadpoles that rasp food from submerged surfaces with keratinized mouthparts; mostiy at or near the bottom, pools and backwaters in lotic sites, body depressed, eyes dorsal, fins low with rounded or slightiy pointed tip, dorsal fin originates at or near the dorsal tailbody junction; see table 2.2, figures in chap. 12, adherent, arboreal, carnivorous, clasping, fossorial, gastromyzmphorous, macrophagous, nektonic, neustonic, psammonic, rheophilous, semiterrestrial, suctorial, suspension feeder, and suspension rasper. bicolored. Two colored, usually in reference to a lateral view of a tail rnuscle that is dark dorsaily and pale ventrally. biosocial aggregation. A general term that describes a group of tadpoles that are congregated because of some social interaction, although qualities of a school (i.e., polarized orientation and coordinated movernents) are not implied; see aggregation, school, and taxic aggregation. birth. (1) Release of some forrn of an immature individual fiom the reproductive traa of its mother, including viviparous and ovoviviparous arnphibians. (2) By extension, used for the analogous release of a froglet frorn nonoviducal sites (e.g.,Assa, Gdctrotheca, Rheobatrachus, and Rhivwdemza) in a parent's body; see hatch. biserial. Describes structures occurring in two series at a site, as two rows of labial teeth per tooth ridge (e.g., some tooth rows in Ascaphw and ail tooth rows in bornbinatorids and discoglossids); see multiserial and uniserial. blotch. Contrasting, usuaily dark, irregular marks of various sizes and shapes with indistinct margins; larger and more irregular than a dot or spot; see mottled, punctate, and steilate. body. (1) [head-body] That part of a tadpole minus the ta*, defined for rneasurernent as the straight iine distance frorn the tip of the snout posteriorly to the body terminus; see body length. (2) Poorly distinguishable part of a labial tooth (Gosner 1959) between the head (working surface) and sheath (embedded in tooth ridge). body axis. Irnaginary iine in lateral view that extends from the tip of the snout to the body terminus; used as a reference for describing the relative locations of stmctures; see tail axis. body length [head-bodylength]. Straight iine, lateral measurernent frorn the tip of snout to the body terminus; see fig. 3.1 and tail length. body ratio (Altig 1970). Total length divided by body length; see tail length and tail ratio. body terminus. Intersection of the posterior body wail and the axis of the tail myotornes; most accurately describes body length and tail length arnong diverse taxa in contrast to any rneasurernent involving the vent tube; see chap. 3. branchial arch(es). The three gill-supportingvisceral arches. branchial food trap (Wassersug 1976a, b). Glandular region between the ventral velurn and Mter plates of larval Types 3 and 4; see chap. 5. buccal apparatus [oral apparatus]. AU structuresin the buccopharyngeal cavity taken as a unit; does not refer to any stmctures of the mouthparts. buccal papiüa(e). Collective terrn for ail papillae in the buccal cavity; see buccai apparatus. buccopharynx, anterior and posterior. Collective term for the buccal cavity (anterior) + pharynx (posterior). carnivorous. An ecomorphologicai guild that includes those lentic tadpoles that feed on rnacroinvertebratesand conspe-
GLOSSARY cific and heterospecific tadpoles, either rasping the prey apart or e n g u h g thern intact; keratinized mouthparts present and usuaiiy rnodified; does not include opportunistic scavenging of dead organisrns; see tables 2.2 and 10.2, figures in chap. 12, arboreai, benthic, macrophagous, nektonic, neustonic, suspension feeder, and suspension rasDer. cauda equina. The spinal nerves that exit the spinal cord near the sacrum and then continue posteriorly as a series of fibers. choana(e) (internal nares). Opening of the narial canal in the roof of the buccopharynx. chromatophore. Pigrnent-containing celis derived frorn neuroectoderm; pigrnents contained in specific organelies; see blotch, dot, melanin, melanophore, mottied, punctate, spot, and steiiate. Eiliary cushion (Wassersug 1976a, b; chap. 5). In larval Types 3 and 4, at the dorsolateral pharynx, structures hanging between the íilter plates and consisting of ciiiary celis and goblet cells originating frorn the esophagus; structuraiiy like the ciliary grooves and in close contact with thern; produces and transports rnucus with entrapped food particles to the esophagus. ciliary groove (Wassersug 1976a, b; chap. 5). A horizontal groove at the rnargin of the pharyngeal roof frorn the anterolateral corner of the ventral velum and eventuaiiy into the esophagus; positioned laterdy in pipids and more posteriorly in larval Types 3 and 4; histology and function resembles the ciliary cushions. dasping. h ecomorphological guiid that includes those lotic tadpoles that iive in flowing water and have marginal papiilae with an anterior gap, LTRs comrnonly 5 but as numerous as 818 and usuaiiy with anterior rows more numerou than lower rows (e.g., 913); inhabit rnedium to slow currents, position rnaintenance via the oral disc minor; see table 2.2 and figures in chap. 12, adherent, benthic, fossoriai, gastromyzophorous, nektonic, neustonic, psammonic, rheophilous, semiterrestriai, and suctorial. dearance time. Period of time between ingestion of food and elimination of feces derived frorn that food. cold hardening. Accomrnodation to a brief exposure of low ternperature near the lethal limit such that the individual is more resistant to subsequent exposures to such ternperatures; see heat hardening. complex life cycle. A life cycle in amphibians characterized by two forrns separated by an abrupt shifi (= metamorphosis) in behavior, ecology, rnorphology, and physiology. compressed [laterdy cornpressed, depressed, or flattened]. Describes an imaginary cross-sectional view of a structure that is higher than wide; usuaiiy used in reference to body shape; see cyiindrical, depressed, fusiform, and globular. concentration refuge. That concentration or density of food below which a tadpole ceases to feed and thus the rernaining prey survive and reproduce. wntraiaterai. Occurring on the opposite side of the body; see ipsilateral. wnversion efficiency. Ratio of rnass of food ingested to body rnass increase. craniai nerve. One of about 14 nerves connected to the telencephalon (CNs O-I), midbrain (CNs 11-IV), and hindbrain (CNs V-XII); absolute nurnber of cranial nerves is controversial; see spinai nerve. crenulate. Describes an edge with a wavy margin as would be produced by a series of weakly differentiated papiüae; see emarginate and incised.
34 1
critical oxygen tension (P,). PO, below which the rate of O, consurnption of a rnetaboiic 0, regulator becornes dependent upon ambient PO,. critical thermal maximum (CT,,). Upper lirnit of the ternperature tolerance range at which locornotor activity becornes disorganized and the animal loses its abiiity to escape frorn conditions that wiü prornptly lead to its death; see critical thermai minimum. critical thermai minimum ( a - ) . Lower limit of the ternperature tolerance range at which locornotor activity becornes disorganized and the animal loses its abiiity to escape frorn conditions that wiü prornptly lead to its death; see critical thermai maximum. cusp. Projection(s) of various size, shape, number, and onentation that occur on the working end (= head) of a labiai tooth; does not refer to serrations on jaw sheaths; see incised. .-.-. cuspate. A terrn that has been used to describe jaw sheaths but should be abandoned (see incised) because of confusion with cusps of labiai teeth. cyiindricai. Describes an imaginary cross-sectional view of a structure that approaches equidirnensionality, therefore quasi-circular, neither depressed nor cornpressed; usudy used in reference to body shape; see compressed, depressed, fusiform, and globular. degree-day. Measure of cumulative potential biological activity, usudy a surn of daily rnean ternperatures. denticle. Unacceptable terrn that should be discarded in referente to the labiai teeth of tadpoles. depressed [dorsoventrdy cornpressed or dorsoventrdy flattened]. Describes an irnaginary cross-sectional view of a structure that is wider than high; usudy used in reference to body shape; see compressed, cyiindrical, fusiform, and globular. detritus. Dead organic rnatter. developmentai rate (DR). Change in forrn or stage through time. dextrai. To the right. Refers to a vent tube that opens to the right of the plane of the ventral h or tail rnuscle; ernergence frorn abdornen rnay be sagittal or not; see mediai and sinistrai. diaphragm (peribranchiai w d ) . The waii or septum separating the viscera frorn the buccopharynx of a tadpole. dserentiation rate. Generaiiy, the inverse of time to develop between two given stages. direct development. (1)Developmental rnode of a frog that results in a froglet that developed without a tadpole rnorphotype frorn an egg not intimately associated with a parent's body. (2) h ecomorphological guild that includes species that have direct development; see table 2.2 and figures in chap. 12; see endotrophy, exotrophy, exoviviparous, nidicolous, ovoviviparous, paraviviparous, and viviparous. dorsal. (1)Describes a category of eye position in which no part of the eye is induded in a dorsal silhouette of the tadpole (i.e., the entire eye is positioned medial to the lateral surface of the body). (2) h anatomical descriptor rneaning "toward top or dorsum" relative to a stated landrnark; see lateral. dorsai body terminus: See body terminus and tail-body junction. dot. Smaii, rounded, dark rnarking with discrete edges; see blotch, mottied, and spot. ecological species. A population of a species that is ewlogicaliy
342
GLOSSARY
Merent from the rest of the population; occupies a separate niche. ecomorphological guild. A categorization of a group of tadpoles from several taxa that share common morphological features that collectively suggest some sort of commonality in ecology; tadpoles with similar ecologies have similar morphologies regardless of their taxonomic relationships. ectodermal-endodermal transition zone. Zone where the epiderm from the gills transition zone overlays the pharyngeal endoderm of the anlagen of filter plates. ectotherm [cold-blooded, poikilotherm]. An organism that cannot retain and regulate metabolic heat, therefore, barring behavioral thennoregulation, the body temperature varies with the ambient temperature; see behavioral fever and behavioral thernioregulation. efferent nerve or axon. Neuron that projects away from (= motor) the brain or a brain nucleus; see afferent nerve or axon. elygium (Van Dijk 1966). A pigmented zone at the basal margin of the iris (= ocular elygium) or at the skin-cornea margin (= epidermal elygium); presumably shield the eye from excessive light; see u m b r a c u l u . emarginate [indented, Solded, folded]. Describes a margin of the oral disc (most commonly lateral) with a real indentation(~),not one caused by folor bending; distinction should be noted between emarginations, folds (= overlapping areas) and tucks (= marginal retractions caused by tensions of connective tissue and labial musculature). embryo. An individual in any stage of development from fertilization until hatching; see froglet, hatchling, immature, juvenile, larva, metamorph, and tadpole. endotroph, endotrophy (Altig and Johnston 1989). General developmental mode that results in an embryo or larva which derives its developmental energy either entirely from vitellogenic yolk or other parentally produced material, sometimes is a nonfeeding tadpole; see table 2.2, direct development, exotrophy, exoviviparous, nidicolous, oviviparous, paraviviparous, and viviparous. exotroph, exotrophy (Altig and Johnston 1989). General developmental mode which results in a larva (tadpole) that feeds on various materials not derived from a parent or trophic eggs provided by subsequent ovulations of the parent, a feeding tadpole; see table 2.2, direct development, endotrophy, exoviviparous, nidicolous, ovoviviparous, paraviviparous, ar~dviviparous. exoviviparous (Altig and Johnston 1989). (1) Developnlental mode of some frogs in which a hatched individual moves from where the eggs were oviposited to another site (often associated with male parent) from which it is eventually "birthed." (2) An ecomorphological guild that includes species that have some form of exoviviparous development; see table 2.2 and figures in chap. 12; see direct development, endotmphy, exotrophy, nidicolous, ovoviviparous, paraviviparous, and viviparous. explosive breeding. All animals in a local population reproduce within a few days. fictive swimming. Involuntary swimming induced in laboratory animals in order to study kinematic interactions (e.g., coordination of muscle groups or the cycle of firing of motor neurons). Miform. Describes a long, narrow object (i.e., filament-like in form). (1) Often a projection that usually has uniform surfaces (e.g., shape of many buccal papillae). (2) Describes the shape of some melanophores.
fin [caudal or tail crest]. Unsupported flaps of epidermiscovered, loose connective tissue usually extending the length of the dorsal and ventral edge of the tail muscle. final thermal preferendum (FIT).Temperature ultimately selected by an individual regardless of prior thermal experience; usually measured within 24-96 hr after placement in a thermal gradient. flagellum (Altig and Johnston 1989) [filament]. Elongate posterior part of the tail that is often nonpigmented and ma!. move independently of the remainder of the tail. fluctuating selection. Adaptive value of a trait varies as a h c tion of varying abiotic and biotic conditions. froglet. A small, sexually immature frog produced by either metamorphosis of an exotrophic tadpole or by direct development. Metamorph is not applicable in the case of direct developing forms; see embryo, hatchling, immature, juvenile, larva, metamorphic, metamorphic climax, premetamorphosis, and prometamorphosis. fossorial. An ecomorphologicai guild that includes those lotic, fusiform tadpoles that have marginal papillae with an anterior gap, LTKF 2/3 or less, and inhabit leaf mats in slow water areas; position maintenance via oral disc absent; see table 2.2, figures in chap. 12, adherent, benthic, datping, semiterrestrial, g~stromyzophorous, nektomk, neustonic, psamrnonic, rheophilous, and suctorial. foliose. ~ o l i a i e or - moss-like or $hape of individual or groups of chromatophores. fracture plane. Suture-Zike area in the body of a labial tooth where the head can break off of the sheath. The next replacement tooth (see tooth series) protrudes through the sheath of the old tooth. friction surface. Area that may be Gnely papillate, keratinized, or both on the roof of the befly sucker of some gastromyzophorous tadpoles. functional constraint. Limit to evolution by natural selection caused by physical or mechanical laws. funnel mouth. Has been used in reference to the upturned oral disc of some surface feeders (= umbelliform) tadpoles and the large, pendant (most easily visible in preserved specimens) oral discs of some lotic species; these usages should be abandoned to enhance clarification among the mouthparts, oral disc, and mouth, also see suctorial. fusiform [vermiform]. Describes the body shape of fossorial tadpoles, extremely depressed with dorsal eyes, long tail, and low furs; see compressed, cylindrical, depressed, and globular. ganglion. Enlargement in a nerve outside the central nervous system where pre- and postganglionic axons synapse or cell bodies of sensory nerves are located; see nucleus. gap. Literally a break or discontinuityin a linear structure; used in reference to breaks, usually medial, in a tooth row; see A-2 gap and A-2 gap ratio. gap ratio. See A-2 gap ratio. gape limited. Describes a predator that cannot eat prey above a maximum size set by the size of ~ t mouth; s see size refuge. gas exchange partitioning. Partitioning of 0, uptake and CO, elimination among available external gas exchange surfaces (e.g., lungs, gills, skin, etc.) or between media (air and water). gastromyzophorous. (1) Describes a tadpole that has the belly modified into an actual sucker (= forms negative pressure), like tadpoles of Amlops and Atelopus but not Tboropa and Cyclor~bus,for position maintenance in fast and perhaps turbulent water. An ecomorphological guild that includes those lotic tadpoles that have such a modified belly; see table
GLOSSARY
2.2, figures in chap. 12, adherent, beiiy flap, beiiy sucker, benthic, clasping, fossorial, nektonic, neustonic, psammonic, rheophiious, semiterrestrial, and suctorial. genetic correlation. Degree to which a gene(s) sirnultaneously influentes two or more traits. germ plasm. Hereditary material transmitted to the offspring through the germ ceils (as opposed to the inheritance of acquired characteristics); in anuran germ h e usually refers to a conspicuous juxtanuclear organeile aggregate consisting mostiv of mitochondria. giia. Supportiveceils of the nervous system, some ofwhich may provide nutrition to neurons or guide migrating neurons during development; may be 10-50 times more giial ceils than neurites in the brain, astrocytes, oligodendrocytes (form m y e h sheaths), and ependymal ceils (line central canal of brain). giobular. The body shape common to many tadpoles, rounded and more or less spherical or eiliptical; see table 2.2, figures in chap. 12, compressed, cylindrical, depressed, and fusiform. giomus. A number of glomeruli grouped together. growth rate (GR). Change in some measure of size over time. hatch. In amphibians, to escape from the jeily membranes that surround an amphibian embryo; in most cases, a hatchling subsequentiy develops into a tadpole, but in some endotrophs, a hatchling actively moves to another site in or on a parent either temporarily or until released (e.g., Asa; see birth) after further development, or the parent actively relocates the hatchling (e.g., Rhinoakma). In viviparous and ovoviviparous forms, hatching occurs in the oviduct. hatchling. Individual within a series of stages between hatching and a tadpole (stage 25); usually used in a generic sense to distinguish individuals in these ecologically unique developmental stages from an embryo or a tadpole; does not refer to a metamorph; see juveniie, hatch, and larva. head. (1) Cranial part of tadpole body from the snout to the pehbranchial wall or diaphragm. (2) The working surface of a labial tooth (Gosner 1959) that often bears cusps; see body and sheath. heat hardening. Accommodation to a brief exposure of high temperature near the lethal limit such that the organism is more resistant to subsequent exposures to such temperatura; see cold hardening. immature. A free-livingindividual prior to attainment of sexual maturity regardless of size or developmental stage; see embryo, froglet, hatchling, juveniie, larva, metamorph, and tadpole. incised [cuspate]. A descriptor of the shape of the cutting edge of jaw sheaths; with one or more pronounced convexities in the upper sheath and sometimes matched by a concavity in the lower sheath, not forming a uniform arc; see cusp, labial teeth, and serration. inclusive fimess. Genes contributed to the next generation by an individual indirectly by helping nondescendent kin, in effect creating relatives that would not have existed without the help of the individual. infralabial prominence (Thibaudeau and Aitig 1988). The Uor V-shaped medial protrusion of the lower jaw typical of many microhylid tadpoles. internarial distance. Transverse distance between centers of the external narial openings; see chap. 3. interorbital distance [interpupiüary or interocular distance]. Transverse distance between the centers of the pupiis of the eyes; see chap. 3.
343
ipsilateral. Occurring on the same side of the body; see contralateral. jaws. Loose but inclusive term for both jaw sheaths and their supportive infrarostral and suprarostal milages; see chaps. 3 and 4. jaw sheath (Altig 1970) [beak, maxilla (for upper jaw sheath), horny beak or jaws, labial mandible (for either lower or both jaw sheaths), mandible (for lower jaw sheath), suprarostradont (on suprarostral cartilage), infrarostradont (on infrarostral cartiiage)]. Usually serrate, keratinized sheaths that overlie the infrarostral (lower; articulates posteriorly with Meckel's cartiiage) and suprarostral (upper, articulates or attached to chondrocranium) cartiiages that serve as cutting or abrasive feeding surfaces. Used as a separate term from "beak" because it is unlikely these struaures are homologs of other structures termed beaks in birds and turtles; these structures overiie entirely different supportive elements (i.e., not dermal bones); see chap. 3. juvenile. Postmetamorphic frog up to the time of attainment of sexual maturity; see embryo, froglet, hatchling, immature, larva, metamorph, ahd tadpole. juxtagiomerular apparatus. A unit within the kidney composed of the macula densa (= part of the dista1 tubule segment), the lacis ceils (= extraglomeruiar mesangium), and the epithelioid ceils (= granular ceils around the vas afferem). Kugelzelle. "ball cell" or "uniceilular gland" (chap. 5). Kupffer ceiis (Sternzellen). Phagocytic ceiis of the reticuloendothelial system between the hepatocytes. labia. see labium. labial flap (Altig 1970; oral flap) [oral apron]. Fleshy flaps of various shapes and sizes that overhang the mouth in microhyiid tadpoles; all keratinized structures absent; derivatives of upper labium (Thibaudeauand Altig 1988) of typical tadpoles; edges may be uniform or scalloped. labial papilla (oral papilla). Coilective term for reference to any marginal or submarginal papillae (but not buccal papillae) of the oral disc. labial teeth (Altig 1970) [denticle, dermal, or labial denticle, keratodont, labial odontoid]. Keratinized tooth derived from ceiis produced in a mitotic zone in the base of the tooth ridge; composed of a head of various shapes and usually with cusps, body, and sheath, see chap. 3. labial tooth row (LTR).Transverse h e a r array of labial teeth embedded in a tooth ridge; the erupted tooth usually has several replacement teeth, number, lengths, and distribution of rows vary on both labia; see labial tooth row formula. labial tooth row formula (LTRF)(Aitig1970). Fractional notation for designating the number of tooth rows on the upper (numerator) and lower (denominator) labia and the disposition of rows with medial gaps; rows on the upper (anterior, superior) labium are numbered from the lip margin toward the mouth (distal-to-proximal) and rows on the lower (posterior, inferior) labium are numbered from the mouth posteriorly (proximal-to-distal).Numbers in parentheses indicate rows with medial gaps, and numbers in brackets indicate variation in the presence of a medial gap. A formula of 5(2-5)/3[:1.] denotes 5 anterior rows (rows 2 through 5 have medial gaps) and 3 posterior rows [row 1 may or may not have a medial gap]; see accessory rows, labial tooth, and labial tooth row. labium [lip]. Fleshy, disc-shaped structures that more or less surround the mouth; usually with labial teeth arranged in
344
GLOSSARY
transverse rows; margins mostly free and papiilate; upper and lower labia together form the oral disc; see labial teeth, labial tooth row, oral apparatus, and oral disc. laevogyrinid (sinistral). Describes a tadpole having a single spiracle on the left side; see amphigyrinid, mediogyrinid, and paragyrinid. larva. Postembryonic, hatched, immature form of a normaiiy metamorphoSing (obligate process in most anurans) species-; a larva of an anuran is specificaiiya tadpole; lawiform adults (at least partial larviform morphology but sexually mature) occur in salamanders but not in anurans; see embryo, hatchling, juvenile, and metamorph. larval transport. Parental transport over various periods of time that re-locates exotrophic larvae from the site of oviposition of terrestrial eggs to some aquatic site; larvae usuaiiy on the back of the parent; does not include endotrophs. lateral. (1) Describes a category of eye position in which some part of the eye is included in a dorsal sihouette of the tadpole (i.e., the eyes protrude further lateraliy than the surrounding body surface). (2) An anatomical descriptor meaning "toward the side" relative to a stated landmark; ser dorsal. lateral line organ (neuromast). See neuromast. lateral l h e system. Ali the pressure-sensitive neuromasts distributed over the body in specific patterns, usuaiiy in lines; see lateral line organ and receptor unit. lateral process (Aitig 1970). Poorly defined lateral portion of the upper jaw sheath beyond which serrations are small to absent; probably not a working surface for feeding. lemmanura (Starrett 1973). Word synonym of Orton's (1953) Type 3 tadpole; discoglossoid of O. M. Sokol (1975). lentic. Limnological description of any nonflowing water system; see lotic. iimbic system. Portion of forebrain, including the amygdala, habenda, hippocampus, and preoptic areas, that may form the highest correlative center in the brain. limiting resource. Resource which is in criticaiiy short supply; an increase in the availability of a limiting resource shodd increase the size of a popdation. lingual papilia (Wassersug 1980). Specifically those buccai papiilae of various numbers, shapes, and sizes that rest on the lingual anlage. lotic. Limnological description of any flowing water system; see lentic. LTR. Abbreviation for labial tooth row. LTRF.Abbreviation for labial tooth row formula. lymphatic system. Lyrnph glands and vessels that function in imrnune responses. macrophagous. An ecomorphologicai guiid that includes those lentic tadpoles that presumably feed by taking larger bites (compared with smaiier particles generated by rasping tadpoles) of attached materiais on submerged substrates, sometimes at least facultatively oophagous; oral disc nearly terminal, jaw sheaths present, LTRF 010-011, marginal papiliae greatly reduced to absent; see table 2.2, figures in chap. 12, arboreal, benthic, carnivorous, nektonic, neustonic, suspension feeder, and suspension rasper. Magenhauptzelle. "stomach main cells" (chap. 5). Malthner ceiis. Paired ceiis in the basal plate of anamniotes that mediate fast start and stade responses, especially in aquatic animais; largest ceiis in the brain stem and persist after metamorphosis in terrestrial forms of amphibians. manicotto glandulare. Sleevelike glandular larval stomach of larval Types 3 and 4.
marginal papiila(e) (Aitig 1970) [labial, oral, lower, or upper festoon or fringe; buccal, dermal, or peribuccal papiilae; papillary border]. Describes any papiiia(e) anywhere on the margin of the oral disc; cornmonly appear as a complete series [circumoral], around margin or with dorsal [rostral gap], ventral [mental gap], or dorsal and ventral gaps. mature. Describes an individual that attained sexual maturity regardless of morphology; does not apply to a tadpole in latter stages of development; see froglet, hatchling, larva, and metamorph. medial. (1) Refers to or toward the sagittal line relative to a referente. (2) Describes a vent tube that opens parailel with the plane of the ventral fin or tail muscle; see dextral and sinistral, G. F. Johnston and Aitig (1986) discuss other variations of the vent tube. median ridge (Wassersug 1980). Transverse flaplike ridge of various shapes suspended from the roof of the buccal cavity; see buccal papiliae. mediogyrinid (midventral spiracle). Having a single spiracle anywhere on the midventd, sagittal line (e.g., ascaphids and microhylids); may be on the chest, abdomen, or ventral to the vent; see amphigyrinid, laevogyrinid, paragyrinid, and sinistral. melanin. Black or brown pigment that is a complex tyrosineprotein polymer; see chromatophore, melanophore, and melanosome. melanophore. Dermal or epidermal chromatophores of various shapes that produce brown to black pigments that give colorations by the presence of melanin; see blotch, dot, chromatophore, melanophore, melanosome, mottled, melanosome, spot, punctate, and stellate. melanosome (J. D. Taylor and Bagnara 1972). Pigrnentcontaining organeiie in a melanophore; see melanin. mesangium. Tissue between the glomerular/glomdar capillaries composed of mesangial cells and mesangial matrix. metabolic depression. A normaily large decrease in the standard metabolic rate that is usuaiiy triggered by some major change in physiological status, such as estivation or hibernation; caused by biochemical regulatory mechanisms that make this a controlled response. metabolic oxygen conformer. Animal whose rate of 0, consumption is independent of ambient PO, over some specified range of ambient PO,; see metabolic oxygen regulator. metabolic oxygen regulator. Animal whose rate of 0, consumption is dependent on ambient PO, over some specified range of ambient PO,; see metabolic oxygen conformer. metabolic scope. The degree that a baseline metabolic rate, either the standard metabolic rate (SMR) or resting metabolic rate (RMR), can be increased by strenuous activity; may be expressed in relative (factorial increase) or absolute (incremental increase) terms. metamorph. An immature frog that resdts from the metamorphosis-of an exotrophic tãdpole; see embryo, hatchling, metamorphic immature,. iuveniie, larva, metamorphic, , ciimax, p.remetamo*hosis', and prometamorphosis. metamorphic. General term that describes either the process or an individual in the process of metamorphosis; see larva, hatchling, metamorph, metamorphic ciimax, premetamorphosis, prometamorphosis, and tadpole. metamorphic ciimax. That period when metamorphic changes are the most profound and most rapid; Gosner 42-46; see embryo, immature, juvenile, larva, metamorph, metamorphic, metamorphosis, premetarnorphosis, prometamorphosis, and tadpole.
213 to a maximum of 17/21; inhabits faster water than adherent and clasping tadpoles, position maintenance via oral disc continuous; see table 2.2, figures in chap. 12, beily flap, benthic, fossorial, gastromyzophorous, nektonic, neustonic, psammonic, and semiterrestrial. suspension feeder, suspension feediig (= fiiter feeding). (1) Harvesting of naturdy suspended particles by pumping water in through the mouth, over the buccopharyngeal filtering system and out the spiracle(s); tadpoles that specialize in this mode of feeding usudy lack aü keratinized and most soft mouthparts. (2) An ecomorphologicai guiid that includes those lentic tadpoles that are behaviorally and morphologicdy (e.g., lateral eyes and depressed bodies) modified to feed in this manner; see table 2.2, figures in chap. 12, arboreal, benthic, carnivorous, macrophagous, nektonic, neustonic, and suspension rasper. suspension rasper. An ecomorphologicai guiid that includes those lentic tadpoles that seemingly feed by fiitering suspended particles from within the water column and rasping submerged surfaces; jaw sheaths and labial teeth (usudy 2/ 3) present, marginal papiüae with anterior gap; eyes lateral; flagellum common t d ; see table 2.2, figures in chap. 12, arboreal, benthic, carnivorous, macrophagous, nektonic, neustonic, and suspension feeder. tadpole. Nomeproductive exotrophic or a nidicolous endotrophic larva of a frog between stages 25-41; does not refer to immatures of other amphibians; see froglet, hatchiing, juvenile, larva, mature, and metamorph. taii. That part of a tadpole minus the body; with a segmented musculaturc and dorsal and ventral fins; defined for measurement as the straight-line distance from the tail tip anteriorly to the body t e r k u s . taü axis (Van Dijk 1966). An imaginary line connecting the body terminus and the tip of the straightened tail; see body axis tail-body junction. Literaüy the junaion of the body and taii of a tadpole, but for different purposes, this junaion can be defined three ways. For most purposes of description and measurement, the site of the body terminus should be med. In some cases the ventral body tcrminus (where the ventral extent of the curvame of the posterior margin of the body contaas the plane of the ventral margin of the tail musde) and the dorsal body termùius (where the dorsal extent of the curvature of the posterior margin of the body contacts the plane of the dorsal margin of the tail musde) can be used. taii flipping. A surprisingly effiuent and accurate means of locomotion by tadpoles and particularly hatchlings, espec i d y those that hatch from arboreal egg masses; move by frantic flips of the tail and not tail undulations. taü height [tail depth]. Greatest vertical distance (i.e., height) of the tail muscle plus both fins; this site may not be the maxirnum dimension of both fins. taii length. Straight line, longitudinal distance from the body terminus to the absolute tail tip, not just to the end of the musculame; see body length. tail ratio. Total length divided by tail length; see body ratio. tail sheath. Dense layer(s) of probable conneaive tissue in the
.
348
GLOSSARY
proximal third of the taii of some tadpoles, sometimes visible in living specimens but more commonly seen in preserved specimens. taxic aggregation (aggregation) [asocial aggregation]. A general term that describes a group of tadpoles that are congregated because of each individual responding to some soa (e.g., light or temperature) of taxis and not because of social interaction; qualities of a school (i.e., polarized orientation and coordinated movements) are not implied; see biosocial aggregation and school. temperature acclimation. Accommodation by an organism in a laboratory setting by physiologically adjusting to the new temperatures; under natural conditions, it is called temperature acclimatization. temperature acclimatization. See temperature acclimation. tooth ridge [dental plate, labial ridge]. Serial, transverse fleshy ridges on the face of the oral disc surmounted by a row(s) of labial teeth generated in a mitotic wnes in the base of the ridges; present in some tadpoles that never have labial teeth see tooth row and tooth seria. tooth row [fringed fold, tooth series, supralabial row on upper or anterior labium, infralabial row on lower or posterior labium]. Transverse, u u d y close-spaced row of labial teeth each embedded within a tooth ridge. Rows on either labium face the mouth; see A-2 gap, gap, labial tooth row formula, and tooth series. tooth seria. Coiiective term for the erupted labial tooth at a given site in a tooth row and each replacement tooth interdigitated sequentially below it; see A-2 gap, gap, tooth ridge, tooth series, labial tooth row formula. total length [standard length]. Straight line distance measured from the tip of the snout to the tip of the t d ; see body length, body terminus, and tail length. transient epidermal gill (Vieael 1991). External giiis of other authors, develop along the ventrolateral paas of branchial arches I-IV and atrophy by stage 25; see chap. 5 and persistent epidermal gill. typhlosolis. Muscular invagination of the foregut. umbelliform [funnel mouth]. Describes an upward-facing oral disc, a convergent trait in several families, used for harvesting particulate matter from the surface film regardless of actual mouth position or orientation; oral disc may be formed from parts of either labium and keratinized mouthparts often lacking see neustonic and suctorial. umbraculum (Van Dijk 1966). Fleshy projection of the iris into or over part of the pupil in some ranids; assumed to protea eye from excessive light; see elygium. uniserial. Describes structures occurring in one series or row -
-
-
per site, as one row of labial teeth per tooth ridge (e.g., most tadpoles); see biserial and multiserial. Urwirbelfortsatz. Primordial vertebral process; see chap. 4. velum (Wassersug 1976a, b; chap. 5). Glandular organ between the buccal cavity and the pharynx that regulates water flow into the Ioharvnx. vent [mal opening, anus]. Posterior intestinal opening of a tadpole. Because arnphibians have a doaca, this opening is not an anus, and ali referentes as such should be omitted; see vent flap and vent tube. vent flap [mal flap]. Fleshy flap of various shapes that extends from the body w d posteriorly and ventral to the vent tube. Sometimes encloses the hind limb buds and occurs most commonly in rheophiious tadpoles. vent tube [anal or cloacal tube, mal tube piece, cloacal taii piece, proctodaeal tube]. A tube for voiding of feces with many variations in morphology; projeas from the body wall distally to an opening that may lie parallel with the plane of the ventral h (medial) or to the left (sinistrai) or right (dextral) of that plane. In a few cases, the tube does not exit the body on the sagittai lhe; see vent and vent flap. ventral body terminus. See body terminus and taii-body junction. visceral arch. Cartilaginous or bony bars of the visceral skeleton, including the mandibular arch (= mandibulare and palatoquadratum), hyoid arch, and three branchial arches. visceral pouch. Pharyngeal (endodermal) evaginations between the visceral arches from which the Eustachian,tubeis derived; pouches 2-4 open as gill slits; the íilter plate anlagen and the branchiogene endocrines are derived from this endoderm. viviparous (Altig and Johnston 1989). (1) Developmental mode of a frog which results in a larva (= fetus) that develops by consurning maternally derived, oviducal materiais after the exhaustion of viteiiogenic yolk. (2) An ecomorphological guild that includes species that have viviparou development; see table 2.2, figures in chap. 12, direct development, endotrophy, exotrophy, exoviviparous, nidicolous, ovoviviparous, and paraviviparous. VO,. A measure of the volume of 0, consumed per unit time; see PO,. whole-body 0, conductance. Change in the rate at which 0, can be consumed by a metabolic 0, regulator per unit +ange in ambient PO,; equivalent to the slope of a plot of VOZagainst ambient PO, in the range of metabolic 0, conformity. xenoanura (Starrett 1973). Word synonym of Oaon's (1953) Type 1tadpole; pipoid of O. M. Sokol(1975). i
LITERATURE CITED
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418
LITERATURE CITED
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AUTHOR INDEX
Abe, A. S., 204 Abelson, A,, 48 Abraham, M. H., 18 Abravaya, J. P., 314 Accordi, i?., 145, 147 Adams, M. J., 20 Adamson, L., 174 Adamson, M. L., 248 Adema, E. O., 250 Adler, K., 6, 168,230,233,235, 237,238 Adolph, E. F., 21,22, 254 Affa'a, F. M., 248 Aganvai, S. K., 45 Agganvai, S. J., 190, 191 Ahl, E., 297 Ahlgren, M. O., 246,247 Aho, J. M., 248 Aho, T., 266 Aichinger, M., 265 Akin, G. C., 255,272,273 AI Adhami, M. A,, 145 Aiberch, P., 28, 88, 171, 184, 188,279, 288, 289,290, 294 Aibuquerque, R. M., 296 Alcala, A. C., 172, 173, 174, 175, 178, 179, 180, 183, 186.333 Aicocer, I., 181 Alexander, R. D., 232,236 Alford, R. A., 26,48,206,218, 232, 242, 243,246, 248, 250,258, 264,268, 272, ,
,
,
.
294' Alford, S. T., 155 Ai Johari, G. M., 24 Aiiey, K. E., 159 Allison, J. D., 161 Ai-Mukthar, K. A. K., 140, 144 Altig, R., 3, 5, 9, 12, 13-14, 16, 17, 18, 19,25,26, 27, 30, 31, 34, 35,36, 37, 38,40, 42, 44,45,46,47,48,49, 50, 63,67, 79, 82,85, 87, 170, 173,178, 184,186, 201,216, 219, 221,227, 228, 229, 231,237, 238, 244,245,248,263,267, 268,280,290,292,296, 297,298,299, 300,302, 303, 305, 307, 308, 309, 310, 321, 326, 339, 340, 342,343,344,345,346, 347 Altman, J. S., 158, 164 Aivarado, R. H., 104, 106, 136, 210,211,212,213 Amboroso, E. C., 171 Amer, F. I., 142, 144 Amiet, J.-L., 5,27,248, 301, 312,313,348 Amos, W., 217 Anderson, J. D., 237 Andrén, C., 21,260,266 Andres, G., 105 Andres, K. H., 165 Andrews, R. M., 171 Angel, F., 296, 334
Anholt, B., 18 Anholt, B. R., 223, 238,253 Annandaie, N., 19,27,41,44, 228,297,298,329,330 Anstis, M., 37; 41 Antal, M., 154, 155 Archey, G., 173 Am~strong,J. B., 21 Arnauld, E., 138 Arnold, E. hT.,184, 296,334 Arnold, S. J., 79, 206,219,232, 260 Arnoult, J., 297,312,327,332 Arrayago, M.-J., 171 Arthur, W., 171 Aschoff, L., 97 Ashby, K R., 229 Ashley, H., 132 Atkinson, B. G., 106, 132, 190, 191,197 Atoda, K., 178, 180, 181 Attas, E. M., 18 Atweii, W. J, 145 Auburn, J. S., 238 Audo, M. C., 282,283 Augert, D., 235,251 Axelsson, E., 200 Azevedo-Ramos, C., 238 Babalian, A. L., 155 Babbitt, K. J., 226, 263 Baccari, G. C., 29 Bachmann, K., 202 Bacon, J. P., Jr., 200 Baculi, B. S., 101 Bagenal, T. B., 18 Bagnara, J. T., 30, 104, 105, 168,344 Bailey, C. H., 167 Baker, C. L, 197 Baker, G. C., 253 Baiasubramanian, S., 216, 247 Baidwin, G. P., 106 Balinsky, B. I., 24, 28, 104, 105, 106,121,131,140,189 Baiinsky, J. B., 132, 142 Banks, B., 242 Bantle, J. A., 16, 18 Barandun, J., 252 Barbault, R., 182 Barch, S. H., 138 Bard, K. M., 219 Bardsley, L., 271 Bargmann, W., 135, 140 Barker, J., 310 Barker, S. B., 212 Birlócher, E, 241 Bames, M. D., 159 Barreto, L., 200 Barrington, E. J. W., 123, 127, 129,269 Barrio, A., 316 Barry, T. H., 56,60 Basoglu, M., 296 Basso, N. G., 34, 327 Basu, S. L., 142, 144, 145 Bateson, P., 237 Battaglini, P., 248 Baaen, T. F. C., 145 Bauer, A. M., 296 Bavay, A., 171
420 Beach, D. H., 168 Beachy, C. K., 251, 282 Beaumont, A., 42, 106, 132, 146 Beazley, L. D., 168 Beck, C. W., 171, 250,251,282, 284 Beckenbach, A. T., 192 Beckvar, N., 223, 244,292 Beddard, F. E., 79 Beebee, T. J. C., 21, 213,242, 248,253,255,261,271 Beigl, I., 142, 144 Beiswenger, R E., 203, 207, 208,216,229,230, 232, 236,260 Bell, B. D., 173, 180 Belloy Espinosa, D., 171 Belova, Z. A., 247 Bemelmans, S. E., 155 Benbassat, J., 97 Bennett, A. F., 194, 195 Benninghoff, A., 93 Benson, D. G., Jr., 20 Benson, W. W., 236 Bentley, P. J., 106, 132, 136, 198 Bernardini, G., 144 Bernasconi, A. E, 77 Berninghausen, F., 296 Bems, M. W, 21 Berry, P. Y., 31,41, 174, 296, 303,318,334 Berton, J.-P., 140 Bertram, B. C. R., 232 Berven, K. A,, 204, 205, 208, 209, 229,243,251,252, 257, 280, 281,283, 285, 286,288,293 Bhaduri, J. L., 142, 144, 145, 323 Bhalla, S. C., 237 Bider, J. R., 260 Bigaj, J., 135, 136 Binckiey, C. A., 18 Birks, R., 149 Bishop, J. E., 269 Bixby, J. L., 154 Black, D., 150 Black, I. H., 41,203,205,213, 260 Black, J. H., 221 Blackburn, D. G., 170 Blackier, A. W., 143, 144 Blair, W. F., 267 Blanc, C. P., 296, 312, 320, 323, 332 Blaustein, A. R., 209,229, 230, 231,232,233,234,235, 236,237,238, 253,259, 261 Blaustein, L., 242,243,252, 273,275 Bleakney, S., 247 Blight, A. R., 158,226 Blommers, I,. H. M., 228,267 Blommers-Schlosser,R. M., 34, 174, 175, 180,228,267, 296,312,320,323, 332 Blouin, M. S., 243,258,286, 288,292,293,294 Boas, J. E. V, 107 Boatright-Horowia, S. S., 162
AUTHOR INDEX Bobka, M. S., 243,263 Bogart, J. P., 170,290,297 Bogett, C. M., 202 Bokermann, W. C. A., 5,8, 309, 310,315 Bolt, J. R., 288, 290, 292 Boni, P., 248 Boonkoom, V, 106,212 Boord, R. L., 163, 164 Booth, D. T., 196,223 Boothby, K. M., 225 Bork, T., 168 Borkhvardt, V G., 25 Borland, J. R., 22 Bossard, H. J., 132 Boulenger, G. A., 4, 35, 50, 179, 180, 296, 298, 302, 306, 325,326,331,334 Bourne, G. R., 171 Bournoure, L., 143 Bourquin, O., 187 Bourret, R., 5,296, 332 Boutilier, R. G., 197,201 Bowen, S. H., 246,247,268 Boycott, R. C., 328 Bradford, D. F., 21, 181, 192, 194, 195, 203,207, 211, 212,229, 240, 249,260, 263,264 Bradley, L., 34 Bragg, A. N., 12, 21,27,40,41, 218,229,230 Bragg, W. N., 40,41 Braitenburg, V, 161 Branch, L. C., 232 Brandon, R. A,, 5,296 Brandt, F. H., 248 Brattstrom, B. H., 204, 205, 206.207.208,224,225, 229,237' Brauer. A.. 229. 296 Braus,'~.:25 ' Breden, F., 232,258 Breed, W. J., 22 1 Bregman, B. S., 155 Bresler, J., 21,40, 41 Bricout-Berthout,A., 163 Bridges, C. M., 253 Briggs, R., 21 Brink, H. E., 182 Britson, C. A., 200, 246 Brock, G. T., 24, 80 Brockelman, W. Y., 252 Brodie, E. D., 111, 236,237 Brodie, E. D., Jr., 30,49, 85, 211,227,229,232, 236, 243, 251, 260,261,262, 346 Bronmark, C., 226,273,302 Brook, A. J., 267 Browder, L. W., 189 Brown, C. A., 123, 152 Brown, D., 104 Brown, D. R., 154 Brown, F. A., Jr., 209 Brown, H. A., 202,203,206, 208,209,302 Brown, L. E., 245,246 Brown, R. M., 239 Brown, S. C., 210,211,212 Brown, T. E., 213
Brown, W. C., 172, 173, 174, 175,178, 179,180,333 Broyles, R H., 95,96, 97, 100, 190 Brust, D. G., 219,247 Buchan, A. M. J., 146 Buehr, M. L., 143 Bull, C. M., 243,258,261,262, 263,270 Bullock, T. H., 163,209 Burch, A. B., 16 Burd, C;. D., 160 Burggren, W. W., 93, 181, 190, 192, 193, 194, 195, 196, 197, 198, 199,200, 201, 209,214,224 Burns, R. K., 132, 144 Burton, J. A., 296, 334 Burton, l? R., 165 Bus; R. B., 202,203,206,207, 229 Bush, F. E., 145 Busk, M., 201 Byrd, C. A,, 160 Bytinski-Salz,H., 30 Cadle, J. E., 18, 27, 311 Caetano, M. H., 245 Caidwell, J. l?,30,41,217,226, 227, 230, 231, 232,240, 243,250,255,256,261, 262,297,308 Calef, G. W., 223,236,251 Callery, E. M., 181 Cambar, R., 92,133, 137,138 Carnerano, L., 34 Campbell, F. R., 103 Cam~beii.G.. 140 ~ambbell;J. Á., 297, 308,309, 322 Campeny, R., 224 Candelas, G. C., 132,252 Cannatella, D. C., 6, 38, 52, 53, 54, 58, 59,61,63, 76, 77, 88,90,304,340 Capranica, R. R, 159, 160, 162, 163 Capurro, L., 174, 179, 316 Caraco, T., 232 Caramaschi, U., 307, 314, 315, 318 Cardoso, A. J., 3 15 Carlson, B. M., 189 Carmona-Osaide,C., 245 Carpenter, C. C., 229,236 Carpenter, K. L., 97, 135 Carr, K. E., 132 Carr, K. M., 16,25,38,49,67, 79,339 Carrizo, G. R., 27,314,334 Carroll, E. J., Jr., 34, 125 Carver, V H., 129 Casinos, A., 224 Castanet, J., 245 Castanho, L. K., 315 CasteU, L. L., 18 Casterh, M. E., 203, 204,205, 206,207 Castle, W. E., 203 Caston, J., 163 Catton, W. T., 168
Cecil, S. C., 251 Cei, J.M.,5,34,35,44, 174, 179, 181, 195, 296, 311, 314, 315, 316, 317, 321, 334 Chacko, T., 56 Chadra, B. G., 243,257 Chang, C.-T., 144 Chang, J. P., 135 Channing, A., 5, 28, 29, 30, 37, 51, 112, 304, 306, 312, 328,334 Chen, A,, 152 Cherdantsev, V G., 38 Cherdantseva, E. M., 38 Chernov, S. A., 296 Chester, M., 153 Chester-Jones,I., 147 Chibon, P., 180, 181 Chieffi, G., 143 Chopra, D. P., 137 Chou, W.-H., 5,296, 322 Chovanec, A., 225,238,243, 263 Christensen, M. S.,201,231, 236,263 Christman, S. P., 213 Cianfoni, P., 147 Ciantar,D., 132, 134, 135, 137, 138 Cioni, C., 158 Claas, B., 158, 164 Clark, A. G., 293 Clarke, B. T., 34,297, 322, 330 Clarke, F. M., 309 Clarke, J. D. W., 152, 155 Claussen, D. L., 202,203, 204, 205,206 Clemens, D. T., 196 Cline, M. J., 95 Cocroft, R. B., 228 Coggeshall, R. E., 153 Coggins, L. W., 140, 142 Cohen, l?P., 131,132 Collins, J. P., 5, 194, 204, 208, 215, 229,243,249,250, 257, 279, 280, 281,285, 291,296 Comer, C., 158, 160 Conneil, J., 229,232,235,249 Constantine-Paton, M., 149, 153,160 Cooke, A. S., 242 Cooper,A. K., 132, 181, 183, 185 Cooper, E. L., 97, 101, 103 Cooper, K. W., 34 Cooper, R. S., 24, 58 Capenhaver, W. M., 93 Cordier, R., 135, 136, 138 Corkran, C. C., 296 Corless, J. M., 166 Cornell, T J., 233,234,237 Cortwright, S. A., 200, 274 Corvaja, N., 155 Costa, H. H., 198,216,247 Cowden, R. R., 102 Cowles, R. B., 202 Cox, T C., 212 Crawshaw, L. I., 203, 205,206, 207,224,260
42 1
A U T H O R INDEX Crespo, E., 295 Cronin, J. T., 262 Crossland, M. R., 218,246,247 Crowder, W. C., 21, 193, 194, 197,198,199,200 Cmce, W L. R., 155, 160 Crump, M. L., 23, 172, 184, 206,208,211,217,218, 219,232,242,244,246, 247,249,251,262,265, 266,268,303 Cuellar, H. S., 321,322 Cuiien, M. J., 168 Cuüey, D. D., Jr., 245,247 Cummins, C. I?, 21,249,260 Cupp, P. V, Jr., 203,204,205, 206,207,224 Curtis, S. K., 103 Cusimano-Carollo,T., 35,45 Czechura, G. V, 297 Czéh, G., 154 Czolowska, R., 143 Da Cniz, C. A. G., 303,308, 310,311,314,321 Dainton, B. H., 205 Daniel, J. C., 323 Daniel, J. E, 16 Danos, S. O., 221 DarneU, R. M., Jr., 197 Das, I., 107 Das, S. K., 77 d'hcanio, E, 155 Dash, M. C., 245,246, 256, 258 Dauça, M., 131, 138 Davenpoa, C. B., 203 Davidson, E. H., 24 Davidson, M., 21 Davies, M., 34, 55, 175, 297, 310,324 Davis, M. R, 153 Davis, W. M., 151 Dawes, E. A., 158, 164 Dawson, J. T., 232,233,235 Dawson, W. R., 194 De Albuja, C. M., 175 De Araújo, M. C., 217 De Bavay, J. M., 174 De Beer, G. R., 55, 56, 59,61, 63,88 DeBenedictis, P. A., 235, 236, 273 De Boer-Van Huizen, R, 155 Debski, E. A,, 160 De Capona, M.-D. C., 312 De Carvalho, A. L., 5, 9,28,31, 33, 37,41,50,296,323 De Carvalho e Silva, S. P., 171 De Cerasuolo,A. M., 181 Decker, R. S., 154 Degani, G., 210,223,269 De Gueldre, G., 168 DeHaan, R L., 93 De Jongh, H. J., 24, 53, 56,58, 61,66,67,68,69, 70, 75, 81,82, 84,216 De Lahunta, A,, 153 De Ia Riva, I., 56, 315 Delbos, M., 135, 137, 140, 143 Deffino, G., 105 Deiidow, B. C., 249
De1 Pino, E. M., 22, 171, 172, 173, 175, 177, 178, 180, 181,186 Delsol, M., 93 Dempster, W T., 180 Denis, H., 58 Denton, J., 231,261 Denver, R. J., 225 De Pérez, G. R., 187,229 De Quiroga, B. G., 197 De Sá, R. O., 36, 55, 56, 57,63, 64, 78,91,298, 307, 309, 317,327,331 De Saint-Aubain, M. L., 104, 106,196,197,198 Desser, S. J., 248 Deuchar, E. M., 142 D e d ; J., 42 Deutsch, M. J., 97 De Villiers, C. G. S., 174, 175, 179,181,186,327 Devis, R. J., 140, 142 De Vlaming, V L., 202,203, 205,206,207,229 De Waal, S. W. P., 136, 138 De Witte, G. F., 296 Deyrup, I. J., 132, 133 Diamond, J. M., 186,209 Diaz, N. F., 296, 316, 317, 318, 334 Diaz-Paniagua, C., 216,243, 248,267,269 Di Bemardino, M. A,, 143 DiBona, D. R., 136 Dickman, M., 223,248 Diener, E., 97 Dieringer, N., 159 Diesel, R., 171 Diea, T. H., 212,213 Di Grande, F., 142, 144 Dionne, J.-C., 221 DiStefano, R. J., 12 Ditrich, H., 138 Dittrich, S., 135 Dixon, J. R., 140, 142, 143, 267,297,305,327 Dodd, J. M., 125,137 Dodd, M. H. I., 137 Donnelly, M. A., 9, 34, 38,263, 265,296,306,311, 321, 322,334 Donner, K. O., 166, 167 Donoso-Barros, R., 316 Dornfeld, E. J., 17 Doughty, I?, 171 Douglas, R. M., 26 Dowling, J. E., 167 Downie, J. R., 183,218, 219, 230,246,255 Doyle, M., 199 Dressler, G. R., 171 Drewes, R. C., 28,48, 50, 228, 312,313,327 Dreyer, T. F., 55 Drysdale, T. A., 34 Dubois, A., 40,298, 329 Dudley, R., 225 D u e h a n , W. E., 5 , 6 , 8 , 9 , 1011,28,29,34, 36,50, 54, 107, 112, 113, 123, 172, 173, 179, 180, 182, 184,
185, 190,206,207,215, 216,220,229, 230,265, 267,290,291,296,299, 300, 304, 305, 307, 308, 309, 310, 311, 314, 316, 321 Dugès, A., 4, 53, 55, 107 Duke, J. T., 192, 193, 196, 198 Duke, K L., 144 Dumas, P. C., 270 Duncan, J. T., 93 Dunham, A. E., 243 Dunlap, D. G., 29,237 Dunlop, S. A., 168 Dunn, E. R, 41,187,308 Dunn, R. F., 163 Dunson, W. A,, 202,203,211, 212,213,214,229,241, 249,267 Du Pasquier, L., 104 Dupré, R. K., 199,203,205, 206,224,238,260 Dutta, S. K., 50 Dziadek, M., 143 Dzieduszycka, S., 328 Eakin, R. M., 34, 145 Eaton, R. C., 158 Eaton, T. H., 288, 290 Ebbesson, S. O. E., 152, 154, 155, 156, 157, 158, 159, 160 Ebenman, B., 243 Eberhard, M. L., 248 Echeverría, D. D., 5, 25,40,45, 50,107,109,144 Eddy, E. M., 140,143 Edelman, A., 255 Edenhamm, E, 226 Edgeworth, F. H., 53, 55,67, 68,69, 70, 72, 74, 75, 76, 77 ..
Edwards, M. L. O., 21 Egami, N., 140,143 Ehmann, H., 175 Ehrl, A., 175, 326 Eichler, V B., 154 Eiger, S. M., 205,214,224 Eiselt, J., 60 Eisworth, L. M., 164 Ekblom, P., 138 Ekman, G., 93, 115 Eldred, W. D., 168 Elepfandt, A., 160,164 Elias, H., 30,104 Elinson, E. E, 29,34, 172, 175, 177, 178, 179, 181, 182, 184,186,188 Emerson, S. B., 67,292,293, 294 Emlet, R. R., 171 Engel, W., 144 Engels, H. G., 136, 138 Engermann, W.-E., 296 Epple, A., 145 Erasmus, B. de W, 201 Erdmann, R., 93 Escher, K., 163 Escobar, B., 171, 172, 175, 178, 180 Estes, R., 3
Estrada, A. R, 172 Etkin, W., 9, 145, 180, 191, 208,346 Exbrayat, J. M., 182 Faber, J., 8, 33, 53, 70, 77,92, 93, 131, 136, 137, 145, 146,147,327 Fabrezi, M., 55, 56 Faier, J. M., 35,49 Faivovich, J., 27, 247, 297, 314, 334 Falconer, D. S., 284,286,287, 289,291,293 Fang, H., 182 Fanning, S. A., 296 Faragher, S. G., 240 Farel, P. B., 153, 155,226 Farlowe, V, 223, 247 Farrar, E. S., 146 Farrell, A. P., 93 Farris, J. S., 5, 9, 50, 296 Fauth; J. E., 254,274,275 Fawcett, D. W., 142 Feder, M. E., 88, 191, 192, 193, 194, 195, 196, 197, 199, 200,209,223,224,225, 226,243,261 Fei, L., 319 Feinsinger, P., 248 Felsenstein, J., 87 Feminella, J. W., 261 Feng, A. S., 159, 160, 161, 163 Fenster, D., 255 Ferguson, D. E., 168 Fennin, E, 171 Fernández, K., 5 Fernández, M., 5 Fernández-Marcinowski, K., 5 Ferns, M. J., 155 Ferrari, L., 210 Fetter, R. D., 166 Figge, F. H. J., 197 Figiel, C. R, Jr., 261 Filipello, A. M., 40 Filipski, G. T., 18 Fink, W. L., 171, 188 ~ i o n t ode Lopez, L. E., 45, 50, 107 Fisher, K C., 203,205 Fisher, M. D., 160 Fisher, R A,, 236 Fishwild, T. G., 233, 234, 235, 236 Fite, K. V, 160, 161, 162, 166 Flatin, J., 93 Fletcher, K., 191 Flock, A., 163, 164 Flores-Nava, A,, 21, 22 Flower, S. S., 297 Floyd, R B., 202,203,204, 205,206,207,260 Ford, L. S., 6, 52, 53, 54,61, 63,77,90 Ford, T. D., 221 Forehaiid, C. J., 153 Forge, P., 182 Forman, L. J., 97 Formanowicz, D. R., Jr., 30, 171, 211, 232, 236,243, 251,260,261,262,263
422 Formas, J. R, 5, 174, 179,227, 316,317,318,334 Forunan, J. R., 50 Foster, M. S., 201, 230, 231 Foster, R. G., 162, 168 Foster, S. A,, 191 Fouquette, M. J., Jr., 308 Fox, H., 72, 104, 105, 107, 119, 121, 123, 125, 129, 131, 132, 133, 135, 136, 137, 146,238,288,346 Foxon, G. E. H., 97, 135 Franchi, L. L., 144 Francis, M. G.. 200,260 Frank, B. D., 167 Frank, E., 155 Frank, G., 96, 103, 104, 135, 136 Frankino, W. A., 247 Fraser, E. A., 132 Freda, J., 211,212,213,214 Freeman, J. A,, 159 Frieden, E., 97, 129 Friedman, B.. 158 Fnedman, R. T., 104 Friet, S. C., 195 Fritsche, R., 93, 214 Fritzsch, B., 158, 162, 163, 164 Frogner, K. J., 31,322 Frohiich, J., 104 Frost, D. R., 27, 172,298 Frost, J. S., 331 Frost, S. K., 30 Frye, B. E., 146 Fujisawa, H., 160 Fder, P. M., 158 Funkhouser, A., 191,210 Gale, E. A,, 28, 184 G d , J. G., 142, 175 Gdardo, J. M., 29 Gdien, L., 92, 132 Gans, C., 168 García, G., 55, 56 Gardener, L. W., 137 Gardiner, J., 6 Gam, R, 104 Gascon, C., 20, 260, 262, 265, 266,275,302 Gates, W. R., 50 Gatherer, D., 177 Gatten, R. E., Jr., 191,192, 193, 194,195,209 Gaupp, E., 53,56 Gavasso, S., 238,263 Gavrila, L., 247 Gaze, R M., 160, 167 Gee, J. H., 224 Gegenbaur, K., 115 Gehrau, A., 317 Gérard, P., 135, 136, 138 Gerhardt, E., 104, 115 Gerschenfeld, H. M., 162 Gesner, C. von, 3 Geyer, G., 140 Ghate, H. V, 260,263 Giarretta, A. A,, 309, 315 Gibbons, J. W., 262,264 Gibley, C. W., Jr., 135 Giesel, J. T., 171 Giies, M. A., 18
A U T H O R INDEX Giü, D. E., 180,208,209, 272, 280,291 Giliiam, J. F., 243, 269 Gines, H., 326 Giorgi, P. i?,137, 143 Gipouloux, J.-D., 92, 132, 137, 138,143 Girard, C., 137, 143 Gitlin, D., 174, 175 Glaw, R., 174, 296, 320,323, 332 Gluecksohn-Waelsch, S., 171 Goater, C. P., 243, 248 Godinho, H. P., 204 Goette,A., 55,93,107,112,115 Goicoechea, O., 184 Goin, C. J., 3, 175, 178 Goin, O. B., 3 Goldacre, R. J., 221 Golden, D. W., 95 Goiichenkov, V A., 104 Gollman, B., 2, 34, 181, 229, 259,295 Goiiman, G., 2,34, 181,229, 259,295 Gomez, M., 132, 252 Gona, A. G., 159 Goniakowska-Witalínska, L., 106,107 Gonzaiez, A., 154,159 Goodyear, C. P., 238 Gordon, F. J., 12 Gordon, J., 167 Gordon, M. S., 132,210,213 Gorham, E., 213 Gorlick, D. L., 150 Gorner, P., 164 G o r d a , S., 173, 303 Gosner, K. L., 8, 10-11, 12,28, 41,42,49, 50, 53,92, 131, 142, 143,144,145,171, 178, 189,202,203,205, 213,215, 240, 260, 281, 339,340,343,345,347 Gotte, S. W., 23 Gouras, P., 167 Gradweli, N., 38,40,48, 49, 53, 55,56,57, 58,63,64,65, 68, 69, 70, 71,72, 73, 74, 75,80, 81,82,83,84,85, 86, 87, 88,90, 109, 112, 113,119,121, 198,216 Grafen, A,, 235 Graham, J. B., 201 Grandison, A. G. C., 28,50, 173,182,240,303,304 Grant, P., 167, 168 Grant, S., 168 Grassé, P.-P., 142 Grassi Milano, E., 145, 147 Gray, E. G., 168 Gray, J., 226 Gray, P., 138, 172, 173, 180, 184,307 Graybeai, A., 90, 304 Graziadei, P. P. C., 165 Green, N. B., 297 Greenwald, D. J., 136 Greenwood, P. J., 236 Greii, A., 115 Greven, H., 121
Griffin, J. R., 213 Griffiths, I., 5,9,27, 28, 31, 33, 37, 41, 50, 53, 89, 123. 125, 127, 129; 130,296, 323,326 Grifíiths, R. h, 200,223,231, 238,243,253,255,271 Grigg, G. C., 209, 260, 310 Griiiitsch, B., 40,42, 51, 109, 331 Grillitsch, H., 42, 296 Grillner, S., 226 Gritis, P. A., 298, 328 Grobstein, P., 155, 158, 160, 238 Gromko, M. H., 255 Grover, B. G., 159 Grubb, J. C., 260 Gruberg, E. R., 160 Gmse, P., 171 GNsser, O.-J., 168 GNsser-Cornehis, U., 159, 168 Gudynas, E., 321 Gugiielmotti, V, 160, 161, 165 Guibé, J., 173,297, 313 Guilford, T., 232 Guiüette, L. J., Jr., 171 Guraya, S. S., 144 Gutzeit, E., 4 Gutzke, W. H. N., 253 Guyer, C., 263,265 Guyer, M. F., 18 Guyetant, R., 21,254 Haas, A., 53, 54, 55, 56,57, 58, 59,61,62,63,65, 68,69, 70, 71, 72, 73, 74, 75, 77, 80,81,90,91, 181 Haddad, C. F. B., 315 Haertel, J. D., 50 Hah, J. H., 135 Hailman, J. P., 167, 237 Hairston, N. G., 254 Hakim, J., 132, 138 H d , B. K., 58 Hall, J. A., 24,230, 231, 234, 235 Haii, J. C., 161 H d , R. W., 132 Hamburger, V, 149 Hamilton, L., 135 Hamilton, W. D., 232,236,291 Hammerman, D. L., 107, 112 Hammerschlag, R., 224 Hampton, S. H., 41 Hanke, W., 145, 146 Hanken, J., 16, 17, 24, 55, 58, 59,62,63,66, 77,78,88, 171, 178, 181, 185, 188, 194 Hardy, J. D., Jr., 179 Harkey, G. A,, 21, 22, 205, 208, 260 Harpur, R. P., 252 Harris, R. N., 247, 248,250, 277,281,282,283,284, 288,292 Harrison, J. D., 216 Harrison, P. H., 216 Harrison, R. G., 164 Hart, M. W., 171
H a d , D. L., 293 Harvey, I. F., 261 Harvey, J. M., 210,260 Harvey, P. H., 88, 236 Hassinger, D. D., 235,236 Hastings, D., 209 Hathaway, E. S., 204 Hausen, P., 165 Hauser, K. F., 149, 159 Havenhand, J. N., 171 Hawkins, C. P., 261 Hay, J. M., 54,90 Hayes, B. P., 238 Hayes, L., 262 Hayes, S., 41 Hayes, T. B., 105, 146,249 Hazard, E. S., 111, 190 Hearnden, M. N., 242,247,276 Heasman, J., 143, 144 Heathcote, R. D., 152 Heatwole, H., 174, 203,204 Hedrick, J. L., 34 Hegner, R. W., 21,248 Heisler, N., 201 Heiff, O. M., 107, 110,112, 194,201 EIenderson, R. W., 173, 174 Hendricks, F. S., 223,247 Hendrickson, A. E., 168 Hendrickson, J. R., 221 Hennen, S., 143 Henrickson, B.-I., 260, 261,262 Hensley, F. R., 250,281,282, 283,284 Hero, J.-M., 246, 247,262,265, 267,291,296,309,325 Héron-Royer, 3 , 4 , 4 9 Herreid, C. F., 11,229, 251,260 Herrick, C. J., 158, 159, 160, 161 Hessler, C. M., 230, 231 Hetherington, T. E., 59, 60, 302 Heusser, H., 27,218,246, 247 Hewitt, J., 298 Hews, D. K., 236,238,243, 253,261,262 Heyer, W. R., 5,27,44,48,49, 107, 109, 111, 112, 113, 121, 173, 182, 196,200, 216, 223,227, 228,240, 247, 262,265,267,268, 296, 305, 307,309,310, 311, 315, 316, 317, 322, 332 Hibiya, T., 121 Higgins, G. M., 58 Hildrew, A. G., 48 Hill, C. G., 203,205,206,260 Hill, S., 57 Hdis, D. M., 34, 297, 331 Hlllman, D. E., 166 Hinckley, M. H., 4 Hirakow, R., 93 Hird, D. W., 248 Hirsch, G. C., 138 Hisaoka, K. K., 21 Hlastala, M. P., 196 Hochachka, P. W., 192 Hoegh-Guldberg, O., 171 Hoff, K., 5,48, 55, 56, 57, 87, 88,91, 109, 119,216,219,
A U T H O R INDEX 224,225,226,239, 243, 288 Hohann, M. H., 160 Hokit, D. G., 229,231,237, 253,259 Holder, N. J., 153 Holley, A., 160 Hoiiyfxld, J. G., 97, 135, 167 Holomuzki, J. R., 248 Honda, E., 110 Honegger, R. E., 314 Hood, D. C., 167 Hoogmoed, M. S., 179,311 Hoppe, D. M., 202,203,204, 205 Hora, S. L., 27 Horat, E, 243 Honuchi, T., 245 Horseman, N. D., 247 Hoaon, J. D., 97, 100, 101, 103,135,136 Hoaon, P., 142 Hoskins, S. G., 167 Hosoi, M., 49 Hota, A. K., 246,256,258 Houillon, C., 92, 132 H o u r h J., 21, 104, 131, 182, 188,254 Honrer, R. O., 17 Hoyer, M. H., 101 Hoyer, W. J., 239 Hoyt, J. A., 58 Hraouibloquet, S., 182 Hrbiçek, J., 236 Hsu, C.-Y., 144 Hu. S. Q., 319,320, 330 Huber, I., 237 Huey, R. B., 204,205,209,261 Hughes, A., 29, 154,155,168, 180,181,182,227 Hulsebus, J., 146 Humphries, A. A,, Jr., 175 Hurley, M. B., 135, 137 Huxhke, E., 107 Hutchinson, T.. 3, 6, 203,204 Hutchison, V H., 190, 205, 206,209,260 Hudey, T. H., 62 I a d o , J. M., 93 I&y-Oka, A., 127, 130 Ideker, J., 261 Ij.K. L., 140, 143 ikenishi, K., 143 In,w,R F., 5,6,9, 20,25,27, 29, 30, 33, 35, 41, 45,46, 48,49,50, 109, 123, 175, 182, 184, 190,216,223, 227,229, 240,269,279, 295,296,297, 298, 302, 303, 304, 318, 319,320, 321, 322, 328, 329, 330, 331,333,334 wennan, R. L., 171 hgie, D., 168,237,239 iqieron, P. M., 145 hpm,G . J., 187 lngram, V. M., 96,97,190,191 Iwhchi, T., 125 Iranova, N. L., 21, 247 Lshizuya-Oka, A., 127
Ison, R. E., 94 Istock, C. A,, 292, 293,294 Ito, S., 140 Iwasawa, H., 138,140,142, 143,144,145 Izecksohn, E., 5, 30, 174, 303, 310,311,314 Izquierdo, L., 317 Jablonski, D., 294 Jackson, D. C., 201 Jackson, G. D., 26,248 Jackson, J. F., 254, 3 14 Jacobson, A. G., 93 Jacobson, C. M., 55 Jacobson, M., 168 Jacoby, J., 158, 164 Jaeger, C. B., 166 Jaeger, R. G., 167, 237,240, 254 JaEee, O. C., 133, 135 Bgersten, G., 290 James, V G., 22 Jameson, D. L., 173, 180 Jande, S. S., 163 Janes, R. G., 129 Janies, D. A,, 9 Jasienski, M., 237,259 Jaslow, A. P.. 162 Jayatilaka, A. D. P., 146 Jennings, D. H., 182 Jennings, R. D., 28,29, 295, 297,331 Jensen, F. B., 216 Jenssen, T. A,, 223,247 Jia, X. X., 196 Jiang, T., 160 Johansen, K., 190 Jolui, K. R., 255 John-Alder,H. B., 243 Jolmson, D. S., 213 Jolmson, E. A,, 271,275 Johnson, S. R., 136 Johnston, G. F., 5,9, 12, 13-14, 19, 27, 31, 34,40,42,44, 48,49, 50,63,82, 87, 170, 173, 184, 186, 216,227, 228,244,280,290,297, 298,299,300,342,344, 345,346,348 Johnston, L. M., 223,247 Jolivet-Jaudet, G., 147 Joliie, M., 72, 74 Joly, E, 235,251 Jonas, L., 135 Jones, R. E., 172 Jones, R. M., 132 Jargensen, C. B., 140 Jordan, F., 226,263 Jordan, H. E., 97 Jorquera, B., 131, 175, 181, 317 Joseph, B. S., 154, 159 Juncá, F. A., 173, 178, 184 Jungfer, K.-H., 217, 219, 220, 247 Junqueira, L. C. U., 104 Jurgens, J. D., 58 Just, J. J., 97, 106, 136, 190, 191, 197, 201, 208,210, 25 1 Justis, C. S., 168, 238
Kahn, T., 5 1 Kaiser, H., 173, 178, 184, 305 Kalt, M. R., 140, 142, 143 Kam, Y.-C., 217,219, 332 Kamat, N. D., 223 Kamel, S., 243,251 Kamimura, M., 143 Kamprneier, O. F., 101 Kanamadi, R D., 143 Kaplan, M., 41 Kaplan, R. H., 225,246,253, 258,261 Karlson, P., 132 Karlstrom, E. L., 203,204 Karnovsky, M. J., 16 Kartçn, I., 237 Kashin, S., 226 Kasinathan, S., 143 Katagiri, C., 34 Kats, L. B., 240, 260, 263, 264 Katz, L. C., 230,231 Katz, M. J., 280 Kaufn~ann,T. C., 188 Kaung, H. C., 42, 46, 48, 146 Kawada, J., 212 Kdwai, A., 104 Kawamura, T., 50 Keating, M. J., 160, 168 Kehr, A. I., 34,250,257,262, 269,296,327 Keiffer, H., 4 Keiier, R., 24 Kelley, D. B., 150 Keiiy, C. H., 258 Kelly, D. E., 168 Kelly, J. P., 244 Kernali, M., 160, 161, 165 Kemp, A., 16 Kemp, N. E., 58,130 Kermy, J. S., 49, 56, 80, 81, 84, 109, 112, 113, 216,243, 244,327 Kenward, R. E., 232 Kerr, J. B., 142, 143 Kerr, J. G., 115, 129 Kessel, R. G., 24, 34, 143 Kesteven, H. L., 55 Kett, N. A., 155 Khan, M. S., 12, 15, 21, 41,44, 109,296 Khare, M. K., 223 Kiditer, E., 156, 160, 162 Kiesecker, J., 260 Kilham, P., 213 Kindahl, M., 135, 138 Kindred, J. E., 119 King, M., 310 Kingsbury, B. F., 163 Kinney, E. C., 213 Kinney, S., 229, 260 Kinoshita, T., 92 Kirtisinghe, P., 31. 44, 322, 323, 330 Kiseleva, E. I., 238 Kisseii, R. E., Jr., 200, 246 Kisteumacher, G., 315 Kiein, S. L., 165 Kiimek, M., 247 Kiuge, A. G., 5,9, 50,90,205, 296
423 Kluger, M. J., 209 Kiymkowsky, M. W., 17 Knudson, C. M., 95, 135 Kobayashi, M., 50, 140, 142, 144 Kok, D., 219,231 Koilros, J. J., 8,9,42,46,48, 92,94, 151, 159, 160, 166, 168, 189, 194, 198, 224, 229,281,288 Kopsch, F., 53, 64, 127 Korky, J. K., 40,41,49,295, 297,339 Koshida, Y., 245 Koskela, P., 240 Kotani, M., 143 Kothbauer, H., 229 Kotler, B. P., 242 Kotthaus, A., 55 Kraemer, M., 55, 59,61 Kramer, D. L., 201 Kramer, H., 20 Kratochwill, K., 56, 81, 84, 107, 112,113 Kress, A., 140 f i g e l , P., 21, 174 Krujitzer, E. M., 55 Kruse, K. C., 200,260 Ku, S. H., 137 Kubin, T. M., 309 Kunst, J., 136, 138 Kunte, K., 228 Kuna, A., 125 Kümle, H., 154 Kupferberg, S. J., 238,243, 244, 245, 248,253, 263,270, 273 Kuramoto, M., 332 Kuthe, K. S. M., 216 Kuzmin, S. L., 243 Lainson, R., 248 Laird, A. K., 280 Lajmanovich, R C., 216,247 Lamar, W. W., 315 La Marca, E., 297, 306 Lamb, A. H., 155 Lambem, G. A., 248 Lambiris,A. J.L.,28, 179, 181, 296,306 Lamborghni, J. E., 154 Lametschwandtner,A., 28,93, 138,140 Larnotte, M., 5, 9, 35, 140, 142, 144, 173, 179, 181, 183, 254,297, 301, 312, 313, 323, 326, 327, 328, 329, 331,333,334 Lancaster, J., 48 Lande, R, 285 Langone, J. A., 31,34,303 Lannoo,M. J., 5, 18,27, 88, 107, 112, 113, 121, 163, 164. 198, 217. 227.. 237,. 238; 240; 308' Lanza, B., 296,302,306, 325, 326,331,334 Largen, M. J., 313 Larseii, O., 158, 159, 163 Larson, P., 91 Larson-Prior,L. J., 160
424 Lataste, F., 4 Latsis, R. V., 135 Lauder, G. V., 90,288 Laurens, H., 237 Laurila, A,, 253,266 Laviiia,E. 0.,5,9,27,31,34, 37,41, 55, 56, 57,91,295, 298,318,321,327,346 Lawler, K. L., 262 Lawler, S. P., 243,263,275, 276 Lawson, D. P., 28,228,301 Lázár,G. Y., 160 Leaf, A., 136 Lebedinskaya, I. I., 28 Lee, A. K., 324 Lee, J. C., 12, 298 Lee, R. K. K., 158 Lefcoa, H. G., 205,209,214, 224,238,253 Leibovitz, H. E., 21,247 Leimberger, J. D., 264 Leips, J., 250,281,282,283, 284 Leloup-Hatey, J., 147 Lemckea, F., 207 Lenfant, C., 190 Leon-Ochoa,J., 316 Le Quang Trong, Y., 104 Lescure, J., 5,9,35, 183,215, 230,306,308 Leucht, T., 238 Levine, R. L., 160 Lewinson, D., 121 Lewis, E. R., 162, 163 Lewis, M. A., 194 Lewis, S., 159,208 Lewis, T. L., 145 Lewis, W. M., Jr., 201 Lewontin, R. C., 237 Leydig, E, 4, 104 Li, J. C., 245 Licht, L. E., 252,256,260,272 Licht, P., 105, 195 Lieberkund, I., 24,34 Liern, K. F., 29, 30, 149 Ligname, A. H., 15 L i e , R. D., 20 Liiiywhite, H. B., 202,204,205, 207 Lima, A. P., 265 Limbaugh, B. A., 50 Lin, C. S., 245 Lin, J.-Y., 5, 296, 322 Lin, W., 159,160 Lindquist, E. D., 302 Ling, R. w., 210 Linsenmair, K. E., 238,261 Linss, W., 140 Lips, K. R., 21,296 List, J. C., 21, 58, 78 Little, G. H., 132 Littlejohn, M. J., 5, 174, 179, 325 Liu, C.-C., 5,9,296,297,298, 319,320,322,330 . . Liu, H., 27 Lofts. B.. 140. 142. 144 Lombard, R É., 162,163 Loor-Vela, S., 177 Lopez, K., 140, 142, 143, 144, 145
AUTHOR I N D E X Lopez, P. T., 227 Loschenkohl, A., 223,269 b m p , S., 34, 105, 191, 197 Lowe, D. A., 151,160,164 Lucas, E. A., 203,205,206, 207,260 Luckenbiil, L. M., 42,46,48,49 Ludwig, D., 251,282 Lugand, A., 181, 184 Lum, A. M., 164,238 Luna, L. G., 20 Luther, A., 55,68 Lua, B., 170, 174, 179,180, 229,290,291 Lyapkov, S. M., 215 Lynch, J. D., 41, 50,90,302 Lynch, K., 25 Lynn, W. G., 55, 172, 174, 178, 180,181,182,188,255 Macgregor, H. C., 172 Mackay, W. C., 211 Maeda, N., 5,296,332 Maetz, J., 104 Maglia, A. M., 55 Magnin, E., 55 Magnusson, W. E., 246,247, 265,291 Mahapatro, B. K., 246,258 Maher, S. W., 221 Main, A. R., 202,324 Majecka, K., 267 Majecki, J., 267 Malacinski, G. M., 21 Maiashichev, Y. B., 25 Maiik, S. A., 109 Maione, B. S., 183 Malvin, G. M., 196,197 Manahan, D. T., 184 Maness, J. D., 173,204,206, 209 Maness, S. J., 172 Mangia, F., 96 Mangold, O., 115 Maniatis, G. M., 96,97 Manis, M. L., 203, 204 Mann, R., 18 Mannen. H.. 153 ~ a n n i n gM , . J., 24,97, 100, 101,103,136 Manteifel. Y. B.. 238., 253., 263 ~ a n t e k lG., , 237 Marcus, E., 104, 115 Marcus, H., 115 Marescakhi, O., 142, 144 Margalit, J., 242,243,252,273, 275 Marian, M. P., 199,208, 209, 224,251,283 Marie, Sister Aüred De, 182 Marinelli, M., 45 Maritz, M. F., 26 Marks, J. C., 294 Marlier, G., 213 Marrot, B., 92 Marshall, E., 209,260 Marshall, G. A., 21,247 Martin, A. A., 5, 132, 181, 183, 185,296,310,323,324, 325,334 Martin, M. S., 92
Martin, W., 267 Martinez, I., 21,22,28 Matesz, C., 163, 164 Mathies, T., 171 Mathis, U., 237,263 Matsui, M., 5, 296, 332 Matsurka, Y., 135 Matthews, L. H., 171 M a m a , H. R., 168 Matz, G., 22 Maurer, F., 107, 115 May, R. M., 278 Mayhew, W. W., 202 Maynard Smith, J., 232 McCann, R. G., 246 McCarrison, R., 249 McClanahan, L. L., 132, 181, 252 McClendon, J. F., 189 McCoiium, S. A,, 30,264 McCormick, C. A,, 158,162, 163 McCranie, J. R., 296, 302 McCutcheon, F. H., 97, 190, 191 McDearman, W., 245,248,292 McDiarmid, R W., 1, 16, 18, 36,38, 173, 179, 184, 187, 201,217,230, 231, 232, 266,291,303,309,310 McDonaid, D. G., 211,212, 213,214 McEdward, L. R., 9 McIndoe, R., 105, 106, 196, 197 McLachlan, A. J., 200,241,242, 243,248,251,291 McLennan, I. S., 155 McMurray, V. M., 159 McPeek, M. A., 240 Mecham, J. S., 171, 172 Medewar, P. B., 171 Méhely, E. G., 5 Meiiicker, M. C., 107, 110, 112 Meltzer, K. H., 192 Mendeii, L. M., 155 Mendelson, J. R., 111,297 Menke, M. E., 202,203,205, 206 Menzies, J. I., 44, 50, 71 Merchant-Larios, H., 140, 144 Merriil, E. G., 167 Mertens, R., 49,296, 301, 304, 334 Meseguer, J., 97, 136, 181 Metter, D. E., 182, 302 Meyer, D. L., 160 Meyer, M., 104 Michael, M. I., 55, 56,60, 70, 72, 73, 74, 75, 77,92, 106, 133, 135,137,145,163 Michaiowski, J., 50 Mijares-Urrutia, A., 304, 306, 309 Millamena, O. M., 22 Miiiard, N., 97,98,99, 136 Mills, K. S., 191 Miranda, L. A., 21,205 Mishra, P. K., 245,258 Mitcheii, S. L., 48, 186 Moaiii, R., 196
Mobbs, I. G., 249 Mocquard, F., 298 Moffat, A. J. M., 163 Moger, W. H., 187 Mohanty, S. N., 246 Mohanty-Hejmadi,P., 30, 50, 323 Mohawald, A. P., 143 Monayong Ako'o, M., 131 Montgomery, N., 159,160 Moody, A., 104,210,211,212 Mookerjee, H. K., 77 Moore, J. A., 177, 186, 189, 202,205,209 Moore, M. K., 261 Moran, N. A,, 279 Moreira, G., 200,265 Morgan, B. E., 182 Morgan, M. J., 161 Morin, P. J., 230,243,248, 254, 260,261,263,269,271, 273,274,275,276 Morris, J. L., 140 Moss, B., 190, 191 Moulton, J. M., 158 Moursi, A. A,, 77 Mous; J. D., 16,178 Mudry, K. M., 163 Mufii, S. A., 41,44 Mdally, D. l?,229 Mder, F., 106 Mumme, R. L., 266 Munn, N. L., 168,239 Munro, A. F., 132,212 Muntz, L., 29,226 Muntz, W. R. A,, 167 Murphy, A. M., 224 Murray, D. L., 258 Muto, Y., 21 Mwaiukorna, A,, 190,196,197 Myant, N. B., 191 Myers, C. A., 217, 246, 247 Myers, C. W., 305 Nachtigall, W., 34,49 Nadal, E., 172 Nadkarni, V. B., 142 Nagai, Y., 245,247 Naito, I., 136, 137, 140 Naitoh, T., 123,293 Nakata, K., 255 Nanba, H., 146 Nathan, J. M., 22 Nation, J. L., 16 Naue, H., 115 Neary, T. J., 159, 161, 162, 163 Nelson, C. E., 200, 274, 321, 322 Nelson, G., 90 Netsky, M. G., 161 Nevo, E., 210 Newrnan, R. A., 243,252,258, 281,282,284,285,286, 288,293 Nguenga, D., 217 Niazi, I. A,, 45 Nichoiis, T. J., 142 Nichols, H. W., 22 Nichols, R. J., 3, 5,49, 50 Nicholson, C., 153 Nicoii, C. S., 283
A U T H O R INDEX
Xr Jí., 190,198,200 S i i e n h u y s , R., 156, 157, 158,159,160 X ~ ~ ~ - k o o p , P . D . , 8 ,34,53, 33, 70, 77,92,93, 106, 131, 136, 137, 145, 146, 147, 296,327 Siiq-asova, E. N., 104 S i i d i w e , A. M., 157,158, 139,160 \-in, G., 266 S i m H. L., 175 Siiiukawa, A,, 25 S s h h w a , K . C.,79, 150, 153, 134,226 S d m a r a , M., 246 Soble, G. K, 5,27,29, 34, 38, 42,50,62,68,71, 74,75, 85. 89, 179, 180,228, 229, 288,290,296,320 Soden. D. M., 153, 164 S&nski, E., 25,45,46,48, 50,135,144,182,196,245 Sdan4 R, 192,193,194, 197, 199,200,203,205,207, 209,260 S d e r t , A., 296,334 S d e r t , C., 296, 334 S o m q S., 107,110 Sordlander, R. H., 150, 153, 155,158 Sorthcutt, R. G., 121, 158, 160, 161,162,165 sassai, G. J. v, 97 S o a ogrodzka-Zagórska, M., 166 Sunnemacher, R. F., 151, 153 S ~ m a nS., , 248 Odendaal, F. J., 269, 270 Ogjeiska, M., 140,142,144, 145 OXara, R. K., 229,230,231, 232,233,234,235,236, 237 Ohler. &I., 40 Ohrani, O., 140 Ohzu. E., 34 Ok Y., 152, 154, 157 Olrada, Y., 5,296,332 O ~ V., L 248 Ohitomi, K., 57 OLughlin, B. E., 282 Okiharn, R S., 227,228 O k a G. J., 70 O h n , D. H., 20,232 Omerza, F. F., 159 Opatm!; E., 221 Opdam, P., 156, 157, 158, 159 Orlando, K., 197 Orr. P. R, 204 Orron.G.L.,5,6,9,38,41,52, 55,63, 88, 89, 121, 168, 173,179,180,240,244, 280, 288,290,295,296, 298, 307, 321, 333, 339, 344,347,348 Osbome, P. L., 241, 248,291 On.M.E., 193 O m n , D., 168 OI-de, W. K., 104
Ovaska, K., 174 Overton, J., 137 Oxner, W M., 225 Ozeti, N., 296 Pace, W. L., 49 Padhye, A. D., 260,263 Pagel, M. D., 88 Paicheler, J.-C., 3 Pancharatna, M., 143 Pandian, T. J., 208,209,224, 251,283 Papernal, I., 248 Parenti, L. R., 17 Parichy, D. M., 225, 258,261 Parker, G. E., 192,209 Parker, H. W., 297 Parker, W. K., 55, 56, 76, 107 Partridge, B. L., 231 Pasztor, V. M., 53, 80 Paterson, N. F., 24, 55 Patterson, J. W., 199-200,242, 243,251 Patton, D. T., 153 Pavignano, I., 244,248 Peacor, S. D., 275 Peadon, A. M., 137, 178, 181, 182 Pearniati, P. B., 266, 267 Pearse, A. G., 20 Pehek, E. L., 211 Peixoto, O. L., 5,28, 308, 310, 311,314,316,317,321 Pelaz, M. P., 109, 255 Pérez-Rivera, R A., 172, 187 Perret, J.-L., 5, 173, 304, 312, 313,331,333 Persson, L., 261 Petersen, H., 45 Peterson, J. A., 261 Petranka, J. W., 183, 199,203, 205,206,219,224, 229, 238,242,243,246, 251, 253,255,260,262,266, 2 72 Petrini, S., 145 Pettigrew, A. G., 160 Pfeiffer, W., 104,235,263 Pfenning, D. W., 27,91,230, 237,246,247,250 Pflugfelder, O., 104 Phiiiips, C., 200,260, 263 Piavaux, A., 131 Pick, J., 151 Picker, M. D., 213,249 Pickersgili, M., 312 Pierce, B. A., 210, 211, 213, 260 Pigón, A., 34, 105, 197 Piiper, J., 192 Pdiai, R. S., 24, 297, 303, 330 Pinder, A. W., 190, 192, 194, 195,196,197,199 Pintar, T., 320 Pisanó, A., 21, 140, 144 Pitcher, T. J., 231,232 Pivorun, E. B., 21 Plasota, K., 55, 56 Plassman, W., 159 PS.tycz, B., 136,247, 286,293 Poinar, G. O., Jr., 248
Polis, G. A., 217,242,246,247, 261,269 Pollack, E. D., 155 Poole, T. J., 135 Pope, C. H., 6, 7,297 Porges, R., 2 13 Porter, R A., 154 Poska-Teiss, L., 104 Postek, M. T., 16 Potel, M. J., 230 Potter, H. D., 159 Potth08, T I,., 41 Pough, F. H., 243,251 Pouyet, J. C., 146 Poweii, G. V. N., 232 Poweii, T. L., 136 Power, J. H., 297, 303,327, 331 Prakash, R, 93 Prasadmutthy, Y. S., 143 Precht, W., 163 Prestige, M. C., 29, 155,227 Preston, F. W., 26 Pretty, R., 92 Price, G. C., 132 Prigioni, C. M., 303 Pronych, S., 224 Prosser, C. L., 104,209 Púgener, L. A., 55 Pugín, E., 5,179,316 PuiLiam, H. R., 232 Punzo, F., 168,230,239 Pusey, H. K., 53,55,56,58,60, 62,63,70, 71, 72, 73, 74, 75,76 Pyastolova, O. A., 237,259 Pyburn, W. F.,9,31,44,45,57, 121, 123, 174, 196,219, 297,298,308,322,334 Pyles, R. A., 62, 63 Qualls, C. P., 171 Quinn, D., 194, 195,201 Rabb, G. B., 187 Rabb, M. S., 187 Race, J., Jr., 132 Rada de Martinez, D., 297 Radakov, D. V., 232 R&, R. A,, 170, 182, 188,289 Rafols, C., 18 Rahwan, R. G., 22 Raies, D. E., 18 Ramaswami, L. S., 55, 56, 57, 63,64 Rao, C. R. N., 19,44,329,330 Rappaport, R., Jr., 133 Rastogi, R. K, 142 Rathke, H., 107 Ratiba, R, 143 Rau, R. E., 327 Rauthner, M., 121 Rautio, S. A., 233 Razarihelisoa, M., 297, 312, 332 Read, A. W., 21 Reading, C. J., 200 Redshaw, M. R, 140,142 Reed, S. C., 142 Regos, J., 3 15 Reh, T. A., 149, 160 Reiliy, S. M., 288
425 Reinbach, W., 55 Reiss, J. O., 55,62, 63 Rengel, D., 140, 144 Reques, R., 208,242,243,250, 251,284 Resetarits, W. J., Jr., 266, 275 Retallick, R. W., 296, 325 Reuter, T., 166, 167 Reyer, H.-U., 243,252 Reynolds, R P., 12,23 Reynolds, W. A., 203, 205,206, 207,260 Reynolds, W. W., 203,204,205, 206,207 Rhodin, J. A. G., 28,93 Rice, T. M., 18 Richards, C. M., 255 Richards, S. J., 29, 34, 37,243, 261,262,263,297,310 Richmond, J. E., 210 Richmond, N. D., 201 Richter, S., 132, 133, 135, 136, 137,138,140,144,174 Ridewood, W. G., 53,55,56, 57,71,75,76-77 Riedel, C., 196 Rieger, R. M., 279 Riggs, A,, 190, 191 Xis, N., 251 Rist, L., 240 Ritke, M. E., 266 Rivero, J. A., 297 Rivero-Blanco, C., 305 Roberts,A., 152, 153, 155,162, 168,225,226,238 Roberts, J.D., 174, 175, 181, 325 Robinson, D.C., 307 Robinson, S. J., 30 Rotek, Z., 55, 58, 61, 71 Rodel, M.-O., 220,238,261, 296 Rohlich, P., 135 Roig, V. G., 297 Roos, T. B., 143 Root, R. B., 249 Rosati, R. R, 245,246 Rose, B. R., 171 Rose, M. J., 187,286,289,293 Rose, S. M., 255 Rose, W., 303 Rosel von Rosenhof, A. J., 3 Rosen, D. E., 121 Rosenberg, E. A., 213, 260 Rosenberg, K., 107, 112, 113 Rosenthal, B. M., 155 Rossi, A,, 92 Rostand, J., 179 Roth, A. H., 254 Roth, G., 53,55,56, 72,73, 74, 75,91,151,160,181 Rouf, M. A., 102 Rougier, C., 109 Rovainen, C. M., 199 Rovira, J., 130 Rowe, C. L., 21,40,242, 267 Rowe, L., 251, 282 Rowedder, W., 58 Royce, G. J., 165 Rubin, D. I., 155 Rubinson, R, 158, 160, 164
426 Ruby, J. R, 140 Rugh, R., 93,95,106,255 Ruibal, R., 31, 35,44, 55. 113, 213,296,314,340 Rui. Garcia, F. N., 304 Rusconi, M., 107 Russeli, A. P., 296 Russeli, I. J., 158, 163, 164 Ruthven, A. G., 173 Ryan, M. J., 162 Ryke, P. A. J., 77, 78, 79 Sabater-Pi, J., 329 Sabbadin, A,, 138 Saber, P. A,, 249 Sabnis, J. H., 216 Sahu, A. K., 223 Saidapur, S. K., 142, 143 Saint-Ange,M., 4 Salas, A. W., 321 Salibián, A,, 212 Salthe, S. N., 171,172,185 Salvador, A., 296 Sampson, L. V, 27, 175, 180 Saraeva, N. Y.,135 Sarikas, S. N., 20 Sarnat, H. B., 161 Saruwatari, T., 17 Sasaki, F., 92 Sasaki, H., 153 Satel, S. L., 88,90 Sater, A. K., 93 Sato, K., 104 Satterfield, C.K., 237 Saunders, R., 22 Savage, J. M., 41,295,296, 305, 306,308 Savage,RM.,6,49,51,80, 81, 107, 112, 123, 181, 196, 240,243,244,254,268 Saxén, L., 138 Sazima, I., 315, 318 Scadding, S. R., 17 Scalia, F., 160, 165 Schechtman, A. M., 16 Scheel, J. J., 173, 231 Scheid, P., 192 Schenkel-Brunner,H., 229 Schiesari, L. C.,217,219 Schjfsrna, K.,296 Schiatz, A,, 231,296, 312,313, 328 Schlaepfer, M. A., 18 Schley, L., 224 Schlosser, G., 53, 55, 56, 72, 73, 74, 75,91, 151, 181 Schluga, A,, 135,136,138 Schluter, A., 315, 321 Schmalhausen, I. I., 29 Schmid, M., 144 Sdimidt, B. R., 272 Schmidt-Nielsen, B., 211 Schmidt-Nielsen, K., 197,206, 209 Schmiedehausen, S., 259 Schmuck, R., 211,252 Schmutzer, W., 248 Schnack, J. A., 262 Schneider, L., 104 Schoonbee, H. J., 221 Schorr, M. S., 248
A U T H O R INDEX Schubert, G., 104 Schulze, F. E., 4, 38,55,63,68, 74, 75, 80, 81, 84, 107 Schutte, F., 175, 326 Schutte, M., 167 Schwartz, A,, 173, 174,308 Schwartz, J. J., 162 Scott, N.J., Jr., 28,29, 295, 297, 331 Scott-Birabén,M. T., 5 Seale, D. B., 88, 107, 189,216, 217,221,223, 240,243, 244,248,263,292 Sedra, S. N., 55,56,60,63,66, 68,69, 70, 72, 73, 74, 75, 77,84,92, 106, 163 Seibert, E. A,, 200,201,217, 223,224,260 Seigel, R. A,, 252 Sekar, A. G., 216,247 Selenka, E., 181 Semiitsch, R. D., 21,22, 185, 205,208,226,238,243, 247,250,256,259,260, 261,262,263, 264,266, 267,272 Senn, D. G., 158 Serra, J. A., 296 Sesarna, P., 130 Sever, D.M., 20 Severtsov, A. S., 55,56, 84,216 Sexton, O. J., 200, 260,263 Seyrnour, R S., 21, 181, 192, 194,229 Shder, H. B., 20,279,295 ShafFer, L. R., 171 Shapovalov, A. I., 155 Shaw, E., 231 Shaw, J. P., 42 Shelton, P. M. J., 163, 164 Sheratt, T. N., 261 Sherman, E., 199,203,204, 205,208,224 Shield, J. W., 198 Shirnozawa, A., 127, 130 Shine, R, 171 Shrane, T., 140, 144 Shiriaev, B. I., 150 Shoemaker, V H., 132, 181,252 Shofner, W. i?,163 Shurnway, W., 8,92,93 Shupliakov, O. V, 150 Shvarts, S. S., 237, 259 Siegfried, W. R., 232 Siekrnann, J. M., 296 Sih, A., 273 Siiver, M. L., 152 Siiverstone, P. A., 173, 305, 306, 315 Simnett, J. D., 137 Simon, M. P., 174 Sirnons, B. P., 162 Sirnpson, H. B., 158 Sin, G., 247 Singer, J. F., 153 Sinsch, U., 240, 316 Sive, H., 34 Skeliy, D. K., 229,238,243, 253,263,291 Skiles, M. P., 158, 160 Slade, N. A., 88, 123,240
Slater, D. W., 17 Slater, P., 324 Srnirnov, S. V, 21 Srnith, C.L., 155 Smith, D.C., 200,208,232, 237,243,252, 259, 263, 264,280,282 Srnith. D. G., 105,106,196, 197 Srnith, E. N., 308,309 Smith, L. D.,143,144 Srnith, M.A., 28,41,229,296, 298,320,321,329,330 Smith, R J. F., 263 Srnith, S. C.,164,165 Smithberg, M.,24,25 Srnith-Gill, S. J., 204,205,208, 209,229,251,272,281, 283,285 Snetkova, E., 224 Sobotka, J. M., 22 Sokol, A., 256 Sokol, O. M., 5, 6,9, 33, 50, 53, 54, 55,56,57,58, 59,60, 61,62,63,64,68,70,71, 72, 73, 74, 75, 76, 84, 88, 90, 107, 109, 113, 123, 237,296,326, 339, 344, 347,348 Somero, G. N., 192 Song, J., 17 Sotairidis, P. K., 245, 247 Sotelo, C.,159 Souza, K. A., 61 Spallanzam, L., 171 Spannhof, I., 180 Spannhof, L., 135,180 Spemann, H., 56 Spencer, K., 10-11,23, 51, 337 Sperry, D. C., 155 Sperry, D. G., 25,79,206,219, 260 Sperry, R. W., 149 Spinar, Z. V, 3 Spitzer, J. L., 154 Spiker, N. C.,154 Splechma, H.,137, 138 Spornitz, U. M., 140 Spray, D. C.,168 Sprumont, l?, 106 Stanley, H. P., 142 Starr, R. C.,22 Starrett, P. H., 5,9, 31,33, 38, 42, 53, 56,57,62,67,68, 70, 71,82, 89,90, 121, 240, 244,296, 302, 303, 339,344,347,348 Stauffer, H. P., 226 Stebbins, R. C., 221, 302 Steele, C.W., 239 Stefanelh, A,, 158 Stehouwer, D. J., 160,226, 238 Stein, J. R., 22 Steinberg, M. S., 135 Steinke, J. H., 20 Steinman, R. M., 34 Steinwascher, K., 216, 223,239, 243,244,245,246,248, 255,256 Steneck, R. S., 49 Stensaas, L. J., 155
Stensaas, S. S., 155 Stephenson, E. M. T., 63 Stephenson, N. G., 55, 173,290 Sterba, G., 101, 103 Stevrnson, H. M., 296 Stevenson, R. D.,204,209 Stewart, M.M., 16, 171, 172, 174, 177, 178, 179, 180, 181 Stiffler, D. E, 213 Stilling, H., 147 Stirling, R. V, 167 Stohr, P., 56, 57 Stokely, l? S., 58, 78 Stone, L. S., 18, 164 Storm, R. M., 50,230 Straka, H., 159 Strathmann, R. R , 171,182 Strauss, R. E., 26,296 Straw, R. M., 203,204 Strawinski, S., 104, 106 Straznich C.,159,160 Streb, M.,254 Strickler-Shaw, S., 168,239 Strijbosch, H., 265 Strong, D. R., Jr., 278 tua
