Amphibian Biology
Amphibian Biology Edited by
Harold Heatwole
Volume 9
Status bf Decline of Amphibians: Western Hemisphere Issue Number 1 Paraguay, Chile and Argentina
Co-editon for this volume
Cesar L. Barrio-Amorbs and John W. Wilkinson
Published by
Surrey Beatty & Sons
AMPHIBIAN BIOLOGY
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The National L b r q of Austraha Cataloguing-in-Publimtion Ens)-: Amphibian Biology. I b h m e 9, Status of D e c h e of Amphibians: Western Hemisphere Includes Index Bibliography. ISBN 0 949324 53 1 (set) ISBN 0 949324 54 X (v. 1) ISBN 0 949324 60 4 (v. 2) ISBN 0 949324 72 8 (v. 3) ISBN 0 949324 87 6 (v. 4) ISBN 0 949324 94 9 (v. 5)
ISBN 0 949324 95 7 (v. 6) ISBN 978 0 98031 13 10 (v. 7) ISBN 978 0 9803113 34 (v. 8) 1 . Amphibians - Classification. I. Heatwole, Harold.
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PRELIMINARIES
V
Preface to Series
T"
ERE are several outstanding treatises of amphibian biology. Biology of Amphibians (Duellman and Trueb 1986) is an excellent general work, clearly written and well illustrated, and with a remarkable depth and breadth for a single volume. It will be the standard general reference on amphibians for many years to come and the present generation of herpetologists will consider it the "amphibian bible" much as their predecessors regarded G. K. Noble's (1931) The Biology of the Amphibia. No single volume, however, hlfils the need for a sequential, monographic treatment of specialized topics. A few individual subjects have been treated in considerable depth. These include the three volumes of Physiology of the Amphibia (Moore 1964; Lofts 1974, 1976), Frog Neurobiology, a Handbook ( ~ l i n a sand Precht 1976) and The Reproductive Biology of Amphibians (Taylor and Guttman 1977), but it has now been many years since these appeared and many topics are in need of updating. Enuironmentul Physiology ofthe Amphibians (Feder and Burggren 1992) did that for some aspects and treated other new ones, but it too is now getting out of date. Two books, Patterns of htmbutwn of Amphibzans (Duellman 1999) and Tadpoles (McDiarmid and Altig 1999) closed out the 20th century with excellent reviews of amphibian biogeography and of the biology of larval amphibians, respectively. Starting the millennium was a multi-volume treatment of reproductive biology and phylogeny: l&fmd& Biology and Phylogeny of Urodela (edited by David M. Sever) and R , c p d d w BwZogy and Phylogeny of Anura (edited by Barrie Jamieson), both in 2003, followed by RPproducfine Biolog?. and Phylogeny of Gymnophiona (edited byJean-Marie E x b ~ a t t in ) 2004. Reproduction was hrther treated by Ogielska (2009) in Reproduction of -4nphibta~u. Recent molecular techniques led to a rearrangement of amphibian taxonomy (Frost Et al. 2006). Behaviour and ecology of amphibians was given a recent, comprehensive, thoughtfd update (Wells 2007). Collectively, all the above works, excellent though they are, still leave large, unaddressed gaps in amphibian biology. Recognizing that the discipline of amphibian biology had reached sufficient maturity to warrant detailed, multi-volume review and that such a need had been filled only partly, and with no commitment to continuation, the present series, Amphibian Biology, was launched in 1994. The present volume represents the ninth in the series. Amphibian Biology does not compete with the titles mentioned above. Topics recently reviewed elsewhere are not covered in current volumes, but are reserved for such time as hrther update is required. The need for this series was evidenced by the enthusiastic response from potential authors. Of the 64 people contacted with invitations to contribute to the first few volumes, only three declined, and then because of heavy commitments otherwise. Most expressed the view that such a series was long overdue. With this initial encouragement the series was launched and it is continuing to enjoy undiminished support.
Amphibian Biology was inspired by Biology of the Reptilia (1969-2008), edited by Car1 Gans, and is intended as a companion to that series. Biology of the Reptilia is a unique, monumental contribution to herpetology and has become the most authoritative single source of information on reptiles that is available. Comprehensive treatments of all aspects of reptilian biology are presented in detail and are exhaustively documented by literature. It has been, and continues to be, invaluable. It is hoped that Amphibian Biology will serve herpetologists in the same way and that it will maintain the high standard set by its reptilian counterpart. Raleigh, North Carolina, USA
Harold Heatwole
January 1993, revised September 2009
Series Editor
REFERENCES Duellman. l\'.E., 1999. "Patterns of Distribution of Amphibians". The John Hopkins University Press, Baltimore. Duellman. It7.E-and Trueb. L., 1986. "Biology of Amphibians". McGraw-Hill Book Company, New York. Exbrayat, J.-\I. (ed.). 2004. "Reproductive Biology and Phylogeny of Gymnophiona". Science Publishers, Enfield. Feder, M. E. and Burggren, W, (ed.s) 1992. "Environmental Physiology of the Amphibians". University of Chicagopress, Chicago.
V1
AMPHIBIAN BIOLOGY
Frost, D. R., Grant, T., Faivovich, J., Bain, R., Haas, A., Haddad, C. F. B., de S-, R., Channing, A., Wilkinson, M,, Donnellan, S. C., Raxworthy, C., Campbell, J. A., Blotto, B. L., Moler, E, Drewes, R. C., Nussbaum, R. A., Lynch, J. D., Green, D. M. and Wheeler, W., 2006. The amphibian tree of life. Bulktin of the American Mweum of Natural History 297: 1-370 Gans, C. (ed.), 1969-1998. "Biology of the Reptilian. 19 vols, Academic Press, New York; Alan R. Liss, Inc., New York; The University of Chicago Press, Chicago; Society for the Study of Amphibians and Reptiles. Jamieson, B. G. M. (ed.), 2003. "Reproductive Biology and Phylogeny of Anura". Science Publishers, Enfield. Llins, R. and Precht, W., 1976. "Frog Neurobiology, a Handbook. Springer-Verlag, Berlin. Lofts, B. (ed.), 1974. "Physiology of the Amphibia", volume 2. Academic Press, New York. Lofts, B. (ed.), 1976. "Physiology of the Amphibia", volume 3. Academic Press, New York. McDiarmid, R. W. and Altig, R., 1999. "Tadpoles". The University of Chicago Press, Chicago. Moore, J. A. (ed.), 1964. "Physiology of the Amphibia". Academic Press, New York. Noble, G. K., 1931. "The Biology of the Amphibia". McGraw-Hill Book Company, New York. Ogielska, M. (ed.), 2009. "Reproduction of Amphibians". Science Publishers, Enfield. Sever, D. M. (ed.), 2003. "Reproductive Biology and Phylogeny of Urodela". Science Publishers, Enfield. Taylor, D. H. and Guttman, S. I. (eds.), 1977. "The Reproductive Biology of Amphibians". Plenum Press, New York. Wells, K. D. 2007. "The Ecology and Behavior of Amphibians". The University of Chicago Press, Chicago.
PRELIMINARIES
Preface to Volume 9
T
HE late 20th century and the early 21st century has been characterized by an unprecedented deterioration of the environment of the earth and the throes of one of the major extinction events of all time. Unmitigated deforestation, desertization, erosion and salinization of soil, pollution of water and air, and thinning of the UV-protective ozone layer constitute dire ecological threats for life on the planet. Fossil carbon is being returned to the atmosphere at an accelerated rate with a concomitant change in the earth's climate that is likely to make serious inroads into ecological stability.
The human population now exceeds the long-term carrying capacity of the earth and is able to subsist at its present levels only because it is sustained by fossil resources of energy, soil, water and even oxygen. With continuing decrease in biodiversity, progressive destruction of essential habitats, degradation of major ecosystems, and contamination of life-support systems, it is likely that the carrying capacity of the earth will decline below present levels while at the same time the human population continues to rise. The outstripping of even its fossil resources, likely to occur within the present century, presents a bleak outlook for our own species. We may well become a victim ourselves of this most recent mass extinction. While it is undisputable that many aspects of environmental degradation and loss of biodivenity is directly attributable to unwise human activities, other aspects are deemed to result h m natural cycles beyond the influence of mankind. It is important to be able to distinguish between the two, so that attention can be focused on mitigating those effects over which we do have control. It is important to ascertain the causes of particular declines and extinctions as soon as possible, so that steps can be taken to preserve what diversity we can. b
Amphibians, by virtue of their thin, moist, permeable skins, are poorly protected from harsh environments and are especially susceptible to chemical changes, desiccation and habitat alteration. Accordingly, it is not surprising that they have manifest proportionately high extinction rates and more severe declines than most other organisms. They are especially important to study as they serve as an early-warning system portending changes that may soon impinge upon more resistant species, including ourselves. Volumes eight and ten are devoted to an elucidation of the myriad of factors responsible for amphibian decline and extinction and an assessment of measures that can be taken to conserve this important taxon. The present volume (9) assesses the status of amphibian decline and extinction in the Western Hemisphere, and a future one (11) will deal with the Eastern Hemisphere. There are various websites that indicate the status of amphibians at a particular time and place. These websites change as status changes. The present volumes do not compete with those. Volumes nine and 1 1 indicate status at the time of publication, but in addition provide an historical baseline against which hture changes can be related - a sort of timecapsule. In one sense, because species of amphibians are going extinct while chapters are being written and put to press, volumes nine and 11 will already be going out of date by the time they are published. In another sense, however, they are timeless as one can return to them for information on status was at a particular time as a means of assessing subsequent extents and rates of change. Raleigh, North Carolina, USA 22 September 2009
Harold Heatwole Series Editor
AMPHIBIAN BIOLOGY
I
I
r(
PRELIMINARIES
IX
Dedication
F"
RTUNATELY for amphibians Lee Berger decided to take a year off from her veterinary studies in 1991 to travel around Australia to see what research on wildlife diseases was being conducted. On that trip she met the eclectic scientist, veterinarian and doctor Rick Speare in Townsville, Queensland, and worked for him on an anti-parasitic drug that was causing mortality in wallabies. Little did she know how that would change our lives. Several years later, in 1995, while she was working as a veterinarian in Melbourne, Victoria, I remember her excitedly putting down the telephone to tell me that Rick had offered her a PhD position to determine the spreading agent that he thought was causing frog decline and extinction in Queensland. She moved to the Australian Animal Health Laboratory in Geelong, Victoria, to study samples collected by Keith McDonald during a mass mortality of frogs at Big Tableland, Queensland. This is the premier virology laboratory in Australia and she was given the task of finding a virus in those samples. During six months of negative findings for viruses she discovered a novel organism that we now know as Batrachochytrium dendrobatidis infecting the skin of these frogs as well as others submitted to the laboratory as dead or sick. The key breakthrough came in 1996 when this pathogen appeared in winter dieoffs and Lee decided to take this organism seriously and started to investigate the disease it caused, chytridiomycosis, and its role in amphibian declines and
aainction. Since the 41980s scientists were unable to explain declines and extinctions of amphibians in protected habitats until Lee's discovery. Her work, and that of her colleagues, was published in the Proceedings of the National Academy of Sciences (Berger et al. 1998) and they were awarded the Australian Commonwealth Scientific and Industrial Research Organisation medal for ~cience.It wasn't all smooth sailing, however. There were numerous difficulties working with a novel pathogen and in the field of amphibian disease where there was little expertise. She spent many late nights at work overcoming these obstacles. There was also the pressure of solving the cause of amphibian declines as well as intense scrutiny of her work and opposition to the hypothesis that a spreading disease was the cause of amphibian decline. Since then, she has continued to make major contributions in understanding the epidemiology and pathogenesis of chytridiomycosis and has investigated other emerging diseases of amphibians. She has also devoted much of her time in assisting others in Australia and overseas in conducting research on amphibian diseases. Significant management recommendations for managing the disease have been adopted based on her work. These include (1) the Amphibian Ark Program that operates an emergency captive-breeding programme to prevent extinctions of populations and species due to outbreaks of chytridiomycosis, (2) the World Animal Health Organisation's (OIE) listing of chytridiomycosis as a notifiable disease in order to prevent its spread, and (3) the Australian Government listing it as a key threatening process in order to prevent its spread and to abate its current impact on threatened species of frogs. The spectacular informative nature of Dr. Berger's work demonstrates the risk of introducing virulent pathogens into naive host populations and ultimately will lead to better conservation of amphibians in particular and in the long term to better conservation of wildlife in general. Currently, Dr. Berger holds a Postdoctoral Research Fellowship at James Cook University, balancing work on amphibian diseases with the care of three young children. It has been my pleasure to know and work with Lee, who is not only an outstanding scientist but a lovely human being. I am extremely pleased that this volume on amphibian conservation is dedicated to her in recognition of how much she has contributed already to this field during her career. Alligator Creek, Queensland, Australia February 2009
Lee F. Skerratt
AMPHIBIAN BIOLOGY
PRELIMINARIES
Contents . . . . . . . . . . . . . . . . . . . . . . . . . .
v
Preface to Volume 9 . . . . . . . . . . . . . . . . . . . . . . . . . .
vii
. . . . . . . . . . . . . . . .
xii
Chapter 1. Status of Amphibian Conservation and Decline in Paraguay. E. 0 . Lavilla and F. A. Brusquetti . . . . . . . . . . . . . . . . . .
1
Chapter 2. Status of Conservation and Decline of the Amphibians of Chile. . . . . . . . . . . . . . . Juan Carlos Ortiz and Harold Heatwole..
20
Chapter 3. Status of Amphibian Conservation and Decline in Argentina. E. 0. Lavilla and Harold Heatwole.. . . . . . . . . . . . . . . . .
30
Preface to Series
Contributors to volume 9, issue number 1
AMPHIBIAN BIOLOGY
Contributors BARRIO-AMOROS, Char L. (Co-editor),Fundaci6n AndigenA, Apartado Postal 210, MCrida 5 101-A, Venezuela.
[email protected] BRUSQUETTI, Francisco A., Instituto de Investigaci6n Mjuiguel Lillo - CONICET, Miguel Lillo 25 1-(4000), San Miguel de Tucumhn, Argentina.
[email protected] HEATWOLE, Harold, Department of Biology, North Carolina State University, Raleigh, NC 27695-76 1'7, USA.
[email protected] LAVILLA, E. O., Instituto de Herpetologia, Fundacidn Miguel Lillo, CONICET - Miguel Lillo 251 - 4000, Tucumhn, Argentina.
[email protected] ORTIZ, Juan Carlos, Departamento de Zoologia, Universidad de Concepci6n, Casilla 160 n,
[email protected] C, ~ o n c e ~ c i oChile. WILKINSON, John, (Co-editor) Durrell Institute of Consenration and Ecology, Marlowe Building, University of Kent, Canterbury, Kent CT2 '7NR UK.
[email protected] [email protected] CHAPTER 1
Status of Amphibian Conservation and Decline in Paraguay E. 0. Lavilla and F. A. Bmsquetti
I. Introduction II. The Amphibian Fauna of Paraguay A. Amphibians Recently Added to the Paraguayan Batrachofauna B. Nomenclator~alRe-arrangements Ill. Geography of Paraguay A. Geophysical Regions of Paraguay 1. The Oriental Region 2. The Occidental Region IV. Eco-Regions of Paraguay A. Chaco Savannahs B. Humid Chaco
C. Brazilian Interior Atlantic Forest D. Cerrado E. Pantanal V. Principal Environmental Problems in Paraguay A. Agriculture and Cattle Farming B. Generation of Hydroelectric Power C. Urban Sprawl VI. Categories of Protection for the Paraguayan Batrachofauna VII. References
I. INTRODUCTION
P
ARAGUAY is the poorest known country in South America in terms of the composition and status of its batrachofauna. Up to 31 August 2009, it consisted of 83 species (plus two species inquirenda), arranged in two orders, nine families and 28 genera, with only one endemic. Except for Chile (with less than 60 species; see chapter 2, this issue), this is the lowest biodiversity of amphibians in the continent; this assessment may not represent biological reality, however, because of the dearth of herpetological studies in Paraguay. Available collections show a marked bias towards the western lowlands (Chaco Savannahs and Humid Chaco, in the sense of Dinerstein et al., [1995]), while the eastern forests and the Cerrado and Pantanal are underestimated. The importance of future studies in these areas arises from several causes, including the fact that the Brazilian Interior Atlantic Forest is one of the most diverse eco-regions in adjacent Argentina and Brazil and, along with the Cerrado, are two of the five hotspots established for South America (Myers et al. 2000). Related to the paucity of modern studies of the amphibians of Paraguay is the scarcity of information related to their conservation status. Up to the year 2009, the only available data are the results of the Global Amphibian Assessment (IUCN et al. 2004) and the ecoregional assessment of the Gran Chaco (The Nature Conservancy et al. 2005) but both were at supra-national levels. Recently, Motte et al. (2009) carried out a national evaluation of the herpetofauna of Paraguay, following the methods proposed by UICN (2001).
2
AMPHIBLAN BIOLOGY
As a supplement to the above works, the present chapter (1) lists the amphibian species recorded from Paraguay and incorporates verified additions and modifications since the last available account (Brusquetti and Lavilla 2006); (2) summarizes the principal geographic and biogeographic characteristics of the country in relation to the known distribution of the native batrachofauna; (3) assesses the principal threats to Paraguayan amphibians, and (4) presents a summary of the available information on the assignment of conservation categories to Paraguayan amphibians. 11. THE AMPHIBIAN FAUNA OF PARAGUAY The first published list of Paraguayan amphibians was by Bertoni (1914); he included 36 species, and 25 years later (Bertoni, 1939), he raised the number to 52. The next general contribution appeared almost sixty years later, and was by Aquino et al. (1996). This valuable paper, based on material housed at the Museo Nacional de Historia Natural del Paraguay (MNHNPa), included 63 species. In addition to these check-lists and some original descriptions of new species, important contributions dealing with the amphibians of Paraguay have been published by Cope (1862), Boettger (1885a, b), Boulenger (1894, 1898), Peracca (1895, 1904), Budgett (1899), MChely (1904), Bertoni (1918, 1928), Miiller and Hellmich (1936), Mertens (1937), Gallardo (1957, 1965), Scott and Lovett (1975), Heyer (1978; 1979; 1994; 1995), Aquino (1986), McDiarmid and Foster (1987), Cei (1990), Aquino and Motte (1991), Faivovich (1994), Lobo (1994), Norman (1994), hvarez et al. (1995), De la Riva (1995), Baldo (2001), CCspedez and Motte (2001), Ziegler et al. (2002), Cruz and Caramaschi (2003), Padial et al. (2003), Cacciali Sosa and Scott (2004), and Cacciali Sosa (2007). In recent times, Brusquetti and Lavilla (2006) published an extensive annotated checklist of Paraguayan amphibians, based on identified specimens from diverse museums (for identification numbers of voucher specimens see Appendix I1 of that paper), and since then, diverse taxa were recorded for the country. Table 1 summarizes information on Paraguayan amphibians at the generic level and an annotated list of the species appears in Appendix 1, following the arrangement proposed by Frost et al. (2006)eand Grant et al. (2006) and subsequent modifications (see section 11. B). Discrepancies between the present chapter and the most recent previous summary of this batrachofauna (Brusquetti and Lavilla 2006) arise from additions and deletions of one species, and from changes at the supraspecific level, as discussed below.
A. Amphibians Recently Added to the Paraguayan Batrachofauna (1) Melanophryniscus krauczuki was cited as probably present in forested areas of the southeast by Brusquetti and Lavilla (2006) and recorded by Brusquetti et al. (2007) from the neighbourhoods of Carmen del Paranh (27O14' S, 56O06' W) in the Department of Itapua (125 m elevation). (2) Melanophryniscus devincenzii was cited as probably present in forested areas of the southeast by Brusquetti and Lavilla (2006) and recorded by Airaldi et al. (2009) h m Pirapo'i stream (25"55' S, 56O09' W, 260 m), in the department of Guairh. (3) Melanophryniscus paraguayensis was cited as Melanophryiscus sp. by Brusquetti and Lavilla (2006) and later described by CCspedez and Motte (2008) from diverse localities of Central, Cordillera and Paraguari departments. This is the only endemic amphibian in Paraguay. (4) Hypsiboas curupi was cited as Hypsiboas aff. semiguttatus by Brusquetti and Lavilla (2006) and later described by Garcia et al. (2008) k m several localities of Misiones Province (Argentina). The taxon is present in the Departments of Caazaph (Arroyo Tava-y, at Caaguazfi National Park [MNHNPa 69921) and Itapfia (Arroyo Tingazu, 52 km NW from Pirap6 [MNHNPa 96591, and Arroyo Tarumh, Compafiia Heriberta Stroessner, Colonia Tarumh [MNHNPa 3672, 3619, 3618, 3682, 3683, 3687, 36911). All known localities are within the Brazilian Interior Atlantic Forest Eco-region.
LAVILLA and BRUSQETTI: AMPHIBIAN CONSERVATION AND DECLINE IN PARAGUAY
3
B. Nomenclatorial Re-arrangements (1) Phurodema fuscomaculata traditionally was considered as Physalaemus fuscomaculatus but was transferred to the genus Pleurodema by Nascimento et al. (2006).
( 2 ) Pseudis, Lysapsus and Podonectes: Garda and Cannatella (2007) proposed the resurrected name Podonectes for the species considered here as Pseudis minutus plus the Brazilian taxon Pseudis cardosoi. Later, Aguiar et al. (2007) concluded that the genus Pseudis (including Pseudis minutus and Pseudis cardosoi) is not a monophyletic group with respect to &sapsus and suggested synonymizing these genera into a single genus (Pseudis), the scheme followed here. (3) Pseudis platensis: Aguiar et al. (2007) suggested that all the subspecies previously included in Pseudis paradoxus should be considered as full species, an interpretation followed here. (4)Pseudis occzdentalis was considered a synonym of Pseudis platensis by Aguiar et al. (2007). (5) Rhinella spp. All the species traditionally included in the genus Bufo and later m s f e r r e d to Chuunus by Frost et al. (2006) are at present considered as Rhinella, following Chaparro et al. (2007).
(6) Rhinella aurrxzi and R. m u . Nanaes and Rodriguez (2009) considered each of these pmiousb- included as subspecies of Rhinella granulosa, to be a h11 species. l- * h i b ~ c
known from Paraguay up to 31 August 2009. Family names are in boldface.
m AkmuBL* C+mmph~ona IsStegokmtaphia b B~aeciliidae:~hthonerpeton-(l),htkenotyphlus (l), Siphrmops ( 1 ) U Batrachia . U Anura BLalagobauachia
m m Soblanun . 1 I I I 1 .Acosmanura -U Neobatrach~a B ...Phthanobatrachia = B .D I. Hyloides .UIM.DDN.. Notogaeanura -MUM.&. Nobleobatrachia II.8.DM.M. Meridianura -DBB .8 .. Cladophrynia m.B..UUDBD Tinctanura -M I. B .R . B. Athesphatanura -.88DDDD. Hylidae: A~enteohyla(l), Dendropsophus (6), Hypsdboas (7), Itapotihyla ( l ) , Aeudis (Z), Scinux (7), Trachyccphalus ( l ) , Phybhmdusa (3) HHBU.U.i....W Leptodactyliformes BBIIHU-m. Leptodactylidae: LeptodactyLuc (14) . . . .W -. Chthonobatrachia ..U.DDDUUB.B... Ceratophryidae: Ceratophrys ( l ) , Chacophrys (I), Lepidobatrachw (3) ..IIDBD.B.#.IIB... Hesticobatrachia D .D .I.B .D i. D .B . Cycloramphidae: LEmnomedusa ( l ) , Odontophrynus (2), Proceratophrys ( 1 ) I.UIU.BDUB..B..B.D Calamitophrynia fln.mrU.B.W Leiuperidae: Eupemphix ( l ) , Physalaemus ( 5 ) , Pleurodema ( l ) , Aeudopaludicola ( 4 ) UIIID.D.IIBII1.8.I. Agastorophrynia W..UDI1D..R..#.88B8R Bufonidae: Melanophlyniscuc ( 6 ) , Rhinella (8) M ..B .IB ..RBUBR .. Nobleobatia I.BD.D.IUU.IE8BIII.. Hylodidae: Crossoductylus ( 1 ) D .U .B D . Ranoides II.II8D.I. Allodapanura D .......... Microhylidae: Chiasmocleis ( l ) , Dermutonotus ( l ) , Elachistocleis ( 1 )
AMPHIBIAN BIOLOGY
111. GEOGRAPHY OF PARAGUAY
The following summary was taken from various sources, including the "Direccibn General de Estadisticas, Encuestas y Censos" (DGEEC 2003), "Biodiverszdad del Paraguay" (Salas-Dueiias and Facetti 2007), the "CIA Factbook (CIA 2007), "Evaluaci6n Ecorregional del Gran Chaco AmericanolGran Chaco American0 Ecoregional Assessment" (The Nature Conservancy et al. 2005) and diverse documents from the "Estrategza Nacional y Plan de Accibn de Biodiverszdad del Paraguay" (ENPAB 2003). Paraguay is a small, landlocked country in central South America, whose extreme geopphic limits are the parallels 1S018' and 27O30' S, and the meridians 54O19' and 6Z038' W. The country's land surface area is approximately 406 752 km2, making it one of the smallest of the continent. Paraguay has a perimeter of 3,995 km that borders three other countries (Argentina, Bolivia, and Brazil). The human population (according to the National Census of 2002) was estimated to be 5 206 101 inhabitants, with an estimated growth rate of 2.4%, while inferences for July, 2007 raised this number to 6 669 086, with a doubling time of 28 years. Although the human density is about 16.4 persons/km2 (one of the lowest of South America), the population is unevenly distributed, with about 97% of the inhabitants occupying the departments east of the Paraguay River and mainly aggregated in the large cities (human density in Asunci6n is slightly greater than 5 000 persons/km2).The ratio of urban to rural population is 1.31: 1. A. Geophysical Regions of Paraguay
The Paraguay River divides the country into two geophysical regions, the Oriental, on the Brazilian Shield, and the Occidental, also known as Chuco Boreal, in the Andean Depression (Fig. 1). 1. The Oriental Region
This region occupies the eastern part of the country and has a surface area of about 159 000 km2 (39% of the country) and houses 97% of the Paraguay population (Bartrina 2007). It is bounded by the Paraguay River on the west and the Paran5 River on the east. The relief is slightly undulating, with elevations between 50 m and 700 m. The main ranges are the Amambay and Mbaracayfi (natural borders with Brazil) and the Caaguazfi and Ybytyrusud, with the highest point of the country being C e m Tres Kundu (842 m). Soils are red and highly fertile in the East, calcareous in the north and alluvial and fertile in the south. The climate is Tropical wet and dry (Aw) in the northwest and Humid subtropical (Cfa) in the remaining areas; annual precipitation is between 1,500 mm and 1,800 mm, while mean temperatures are 26.1°C in summer and 20.8"C in winter. The Oriental Region is traversed by several rivers including the Apa (380 km), Aquidadan (270 km), Jejui (350 km), Manduvira (212 km), Piribebuy (100 km), and C o h s o (290 km) in the Paraguay drainage, and the rivers Carapa (95 km), Acaray (160 km) and Tacuary (80 km), that drain into the Paran5 River. The administrative divisions of the Oriental Region includes the Departments of Alto Paranh, Amambay, Caaguazir, Caazaph, Caninde*, Central, Concepcibn, Cordillera, Guair5, Itapua, Misiones, ~ e e m b u c uParaguari, , and San Pedro. 2. The Occidental Region
The Chaco Boreal or Occidental Region occupies the western part of the country and has a surface area of about 247 752 km2 (61% of the country) and houses only 3% of the Paraguayan population (Bartrina 2007). It is bounded by the Paraguay River in the east, the Pilcomayo River in the south and Bolivia in the west. The relief is almost flat (the general gradient is about 1% west to east), with a mean elevation of about 130 m. There is
LAVILLA and BRUSQETTI: AMPHIBIAN CONSERVATION AND DECLINE IN PARAGUAY
a great variety of environments, including swamps, dry and seasonally flooded savannahs, marshes, salt flats and diverse kinds of forests and scrublands. The main elevations are isolated hills, such as Cerro Le6n, Chovoreca, Jara, Olimpo, Conhso, Galvhn, Siete Cabezas, and Desolaci6n). The soils are sedimentary sands and clays, grayish in colour and somewhat
*-
The climate is Tropical wet and dry (Aw); the annual rainfall is between 400 mm and 700 mm, while mean temperature can reach up to 3'7.g°C in certain areas of the Gran Chaco. Permanent flowing waters are represented by short rivers such as the Negro, Aguaray Guazfi, and San Carlos and longer ones like the Verde (275 km) and the Monte Lindo (400 km). The administrative divisions of the Oriental Region includes the Departments of Alto Paraguay, Boquerbn, and Presidente Hayes. IV. ECO-REGIONS OF PARAGUAY
According to the classic study of Dinerstein et al. (1995), Paraguay is divided into five eco-regions (Fig. l), including ( h m west to east) Chaco Savannahs, Humid Chaco, Brazilian Interior Atlantic Forest, Pantanal, and Cerrado, the last two almost being marginal ingressions into the country.
Paraguay
1
ZLpdn 3 Recdne Hayes 4 -
5. Amambay
6. San Pedro
7. Canindeyir 8. Central (Capital)
1
9. Cordillera
10. Caaguazti 11. Alto Parana 12. Qeembucu 13. Paraguari
I Chaco Savannas )
Occldental Region
Humid Chaco
B
P
I Pantanal
t
I
Cerrado Brazilian InteriorAtlantic Forest
Fzg. I . Map showing the political departments (1-17), eco-regions (colour-coded), and geophysical regions (Ur~ental and Occidentai) of Paraguay.
6
AMPHIBIAN BIOLOGY
A. Chaco Savannahs
In Paraguay, the Chaco Savannahs Eco-Region occupies all the surface of Department Boquerbn, a great part of Department Alto Paraguay and a narrow band in the west of Department Presidente Hayes. It coincides in general with the Paraguayan portion of the Dry Chaco biogeographic province (in the sense of Cabrera and Willink 1973) and has diverse habitats, mainly savannahs and thorny woodlands, plus transitional areas between them. The amphibian fauna contains 36 species (Rhinella granulosa azarai, Rhinella granulosa major, Rhinella schneideri, Melanophryniscus klappenbachi, Dendropsophus nanus, Hypsiboas punctatus rubrolineatus, Hypsiboas raniceps, Pseudis occzdentalis, Pseudis plahsis, Scinax muminatus, Scinax fuscovarius, Scinax nasicus, Trachycephalus venulosus, Phyllomedusa azurea, Phyllomedusa sauvagii, Ceratophrys cranwelli, Chacophrys Pierottii, Lepzdobatrachus laevis, Lepzdobatrachus Uanensk, Odontophrynus lavillai, Leptodactylus bufonius, Leptodactylus chaquensis, Leptodactylus elenae, Leptodactylus fuscus, Leptodactylus laticeps, Leptodactylus latinasus, Leptodactylus mystacinus, Leptoductylus ocellatus, hptodactylus podic$inus, Physalaemus albonotatus, Physalaemus biligonigem, Pseudopaludicola boliviana, Pseudopaludicola falcipes, Pseudopaludicola ternetzi, Dermatonotus muelleri, and Elachistocleis bicolor). Although no endemism has been reported, two species, Pseudis occzdentulis and Lepzdobatrachus llanensis, are exclusive to this eco-region in Paraguay. B. Humid Chaco
In Paraguay, the Humid Chaco Eco-Region occupies all the surface of the Departments of Central, Cordillera, ~eembucG,and Misiones, a great part of Department Presidente Hayes and smaller portions of the Departments of Concepci6n, Amambay, San Pedro, Caaguaz6, Paraguari, Guairh, Caazaph, and Itapuh. It coincides in general with the Paraguayan portion of the Humid Chaco biogeographic province (in the sense of Cabrera and Willink 1973) and is characterized by patches of xerophytic woodlands alternating with palm savannahs. The amphibian fauna has 59 species (Chthonerpeton indktinctum, Melanophryniscus atroluteus, Melanophryniscus fulvoguttatus, Melanophryniscus klappenbachi, Melanophryniscus paraguayensis, Rhinella bergi, Rhinella fernandehe, Rhinella granulosa azarai, Rhinella granulosa major, Rhinella schneideri, Argenteohyla siemersi pederseni, Dendropsophus minutus, Dendropsophus nanus, Dendropsophus sanborni, Hypsiboas caingua, Hypsibom puhhellus, Hypsiboas punctatus rubrolineatus, Hypsiboas raniceps, Pseudis limellum, Pseudis platensis, Scinax acuminatus, Scinax berthae, Scinax jkcomarginatus, Scinajc jkcovarius, Scinajc m k u s , Scinax similis, Scinax squalirostris, Trachycephalus venulosus, Phyllomedusa hj~ochondrialis azurea, Phyllomedusa sauvagii, Ceratophrys cranwelli, Chacophrys pierottii, Lepidobatrachus asper, Lepidobatrachus laevis, Odontophrynus americanus, Odontophrynus lavillai, Eupemphix nattereri, Leptodactylus bufonius, Leptodactylus chaquensis, Leptodactylus elenae, Leptodactylus fuscus, hptodactylus gracilis, Leptodactylus labyrinthicus, Leptodactylus laticeps, Leptodactylus latinasus, Leptodactylus mystucinus, L.eptodactylus ocellatus, Leptodactylus podicipinus, Leptodactylus syphax, Leptodactylus diptyx, Physalaemus albonotatus, Physalaemus biligonigerus, Physalaemus cuvieri, Physalaemus riograndensis, Pseudopaludicola boliviana, Pseudopaludicola falcipes, Pseudopaludicola ternetzi, Dermatonotus muelleri, and Ehhistocleis bicolm). In Paraguay, Chthonerpeton indZrtimtum, Rhinella fernandezae, Melanophryniscus atroluteus, Melanophryniscus sp., Leptodactylus syphax, Physalaemus riograndensis, Scinax similis and Lepidobatrachus mper are exclusive to this ecoregion. C. Brazilian Interior Atlantic Forest
In Paraguay, the Brazilian Interior Atlantic &rest Eco-Region occupies all of Department Alto Paranh, a significant portion of the Departments of Amambay, CanindeyG, CaaguazG and Guairh, and part of the Departments of Concepci6n, San Pedro, CaazapB, and Itapua. It coincides in general with the Paraguayan portion of the Paranaense biogeographic province (in the sense of Cabrera and Willink 1973) and is a humid, semi-deciduous, subtropical forest, rich in plant species but with low endemism. The amphibian fauna consists of 50 species (Luetkeno~phlusbrasiliensis, Siphonops paulensis, Melanophryniscus devincenzii,
LAVILLA and BRUSQETTI: AMPHIBIAN CONSERVATION AND DECLINE IN PARAGUAY
7
Melanophryniscus fulvoguttatus, Melanophryniscus krauczuki, Rhinella &erica, Rhinella ornata, Rhinella schneideri, Argenteohyla siemersi pederseni, Dendropsophus minutus, Dendropsophus nanus, Dendropsophus sanborni, Hypsiboas albopunctatus, Hypsiboas caingwl, Hypsiboas curupi, Hypsiboas fabq Hypsiboas pulchellus, Hypsiboas punctatus rubrolineatus, Hypsiboas raniceps, Ztapotihyla langsdorfii, Scinax berthae, Scinax fuscomarginatus, Scinax fuscovarius, Scinax nasicus, Scinax squalirostris, Trachycephalus venulosus, Phyllomedusa hypochondrialis azurea, Phyllomedusa tetraploidea, Crossodactylus schmidti, Limnomedusa macroglossa, Odontophrynus americanus, Proceratophrys avelinoi, Eupemphix nattereri, Leptodactylus chaquensis, Leptodactylus diptyx, Leptodactylus elenae, Leptodactylus fumrius, Leptodactylus jkscus, hptodactylus gracilis, L~ptodactylus labymnthicus, Leptodactylus mystacinus, Leptodactylus ocellatus, Leptodactylus podicipinus, Physalaemus albonotatus, Physalaemus centralis, Physalaemus cuvieri, Pleurodema &scomaculata, Pseudopaludicola mystacalis, Pseudopaludicola ternetzi, Elachistocleis bicolor, and Chiasmocleis albopunctata). In Paraguay, Luetkenotyphlus brasiliensis, Siphonops paulensis, Rhinella ornata, Melanophryniscus krauczuki, Hypsiboas curupi, Hypsiboas fabe? Itapotihyla langsdorfii, Phyllomedusa tetraploidea, Pseudopaludicola mystacalis, Limnomedusa macroglossa, Proceratophrys avelinoi, Physalaemus jkcomaculatu, and Crossodactylus schmidti are exclusive to this eco-region. D. Cerrado
In Paraguay, the Cerrado Eco-Region occupies areas of diverse sizes in the Departments of Concepcion, -Imamba);, and Canindeyfi. It coincides in general with the Paraguayan portion of the Cerrado biogeographic province (in the sense of Cabrera and Willink 1973) and is a vast savannah with woodlands scattered along the rivers. The amphibian fauna consist of 27 species (Melanophryniscus fulvoguttatus, Rhinella icterica, Rhinella schneideri, Rhinella scitula, Dendropsophus eliuneae, Dendropsophus jimi, Dendropsophus nanus, Hypsiboas albopunctatus, Hypsiboas panctatus rubrolineatus, Hypsiboas raniceps, Scinax fuscomarginatus, Scinax fuscovarius, Scinax nasicus, Trachycephalus venulosus, Phyllomedusa sauvagii, Eupemphix nattereri, Leptodactylus elenue, Leptodactylus furnarius, Leptodactylus fuscus, Leptodactylus hbymnthicus, Leptodmtylus ocellatus, Leptodmt~luspodicipinus, Physalaemus albonotatus, Physalaemus centralis, Ph?shrnus cuvimi, Elachktocleis bicohq and Chiasmocbis albopmctata), with Rhinella scitula, Dendropsophw eliuneae and Dendropsophus jimi being exclusive to this Eco-region in Panguay. E. Pantanal In Paraguay, the Pantanal Eco-Region occupies the eastern margin of the Department of Alto Paraguay. It coincides in general with the Paraguayan portion of the Pantanal biogeographic province (in the sense of Cabrera and Willink 1973) and is an extensive flooded plain. The amphibian fauna has 24 species (Rhinella bergi, Rhinella schneideri, Dendropsophus melanargyreus, Dendropsophus nanus, Hypsiboas punctatus rubrolineatus, Hypsiboas raniceps, Pseudis limellum, Scinax acuminatus, Scinax nasicus, Trachycephalus venulosus, Phyllomedusa hypochondrialis azurea, Ceratophrys cranwelli, Eupemphix nattereri, Leptodactylus bufonius, Leptodactylus c h a q w i s , Leptodactylus elenae, Leptodactylus fuscus, Leptodactylus ocellatus, Leptodactylus podicipinus, Leptodactylus syphax, Leptodactylus diptyx, Physalaemus albonotatus, Elachistocleis bicolor, and Chiusmocleis albopunctata). Dendropsophus melanargyreus is the only species exclusive to this Eco-region in Paraguay. V. PRINCIPAL ENVIRONMENTAL PROBLEMS IN PARAGUAY There are no available studies of the environmental problems and their impacts on amphibian populations in Paraguay. Notwithstanding, it is possible to make some inferences based on indirect evidence. The economy of Paraguay is based on two main activities, (1) the export of goods derived from agriculture and cattle farming, and ( 2 ) the production of hydroelectric energy; both actions lead to the loss of extensive surfaces of natural environments. On the other hand, unplanned urban sprawl, highly concentrated in the Oriental Region, also has impacts on amphibian populations.
8
AMPHIBIAN BIOLOGY
A. Agriculture and Cattle Faming
According to Fleytas (2007), loss of habitat started in colonial times, but had an exponential growth between 1945 and 1997, a period in which about the 76.3% of the original area of woodlands was removed, either for export of timber or to have clear agricultural fields andlor grazing lands. Data for 2001 showed that 44% of the arable land was devoted to soybeans, a figure that surpassed 50% by 2004, with an annual growth of about 8.5% (Fleytas 2007). During the period 1984-1991 the area (in hectares) of logged surface in the Departments of the Oriental Region were: Caaguazd (180477), CaazapA (129 076), Canindeyli (301 538), Central (4 056), Concepcibn (100 673), Cordillera (10 537), GuairA (22 661), Itapda (308,812), Misiones (5 179), ~eembucfi(1 063), Paraguari (5 639), and San Pedro (333 080) (Rojas de Arias, 2007). The practice of growing only one type of crop in extensive areas has several associated impacts on natural populations of amphibians (and on the biota in general), including: (1) Clear-felling of natural woodlands produces irreversible loss of habitats, diminishes biological diversity and produces indirect effects that eventually are harmful to amphibians, including aridity, erosion of soils, and edge effects, among others (Woodwell 1983; Salati and Vose 1984; Myers 1986).
(2) The implantation of genetically modified soy seeds implies the use of glifosate-based herbicides, which are known to interfere with the cutaneous respiration of adult amphibians and with the branchial respiration of larvae (Tyler 1997). (3) The use of pesticides of diverse chemical composition is lethal to amphibians; these toxic chemicals are in direct contact with amphibians both in the terrestrial and aquatic ecosystems. Even the "safest" of these (those based on pyrethroids) have been shown to be lethal for tadpoles by producing neuronal apoptosis (Izaguirre et al. 2000, 2001). (4) Current agricultural practices use a great amount of fertilizers, with high contents of nitrites, nitrates and phosphorous. Leached by rains, they accumulate in ponds and other bodies of stagnant water and accelerate the process of eutrophication. As shown by Halliday (2000) and Marco and Ortiz-Santaliestra (in press), these chemicals severely affect the development and survival of tadpoles, and algal blooms facilitate the development of trematodes that parasitize amphibians. B. Generation of Hydroelectric Power
Paraguay houses two of the greatest dams in the world, ItaipG (shared with Brazil), and YacyretA (shared with Argentina). The resultant artificial lakes flooded an estimated 1,600 km2 (YacyretA) and 1,350 km2 (Itaipd) of the biodiverse and otherwise threatened Atlantic Forest. No data on amphibians prior to the flooding exist, except for those of kvarez (1995), but damages to local populations should be considered severe, taking into consideration that Talavera Island was completely flooded, as was 80% of Yacyreth Island. C. Urban Sprawl
As previously noted, 9'7% of the Paraguayan population is concentrated in the oriental region, with slightly more than half a million of inhabitants in the Metropolitan Area of Asuncibn. Setting aside the problems related to urban expansion that are common to several cities in the world (e.g., occupation of physical space, fragmentation of habitats, contamination and imperviousness of soil, pollution of air and water, transfer of basins, draining of wetlands, generation of inorganic and organic residues, peri-urban desertification, etc; see Lavilla and Heatwole, this volume), one of the most important problems related to urban sprawl is the disposal of black waters. According to Facetti (2007), only 27% of the population of the country has sewer facilities (a figure that reaches 56% in Asuncibn); not only are superficial waters polluted, but so are subterranean ones (to 40 m depth).
LAVILLA and BRUSQETTI: AMPHIBIAN CONSERVATION AND DECLINE IN PARAGUAY
VI. CATEGORIES OF PROTECTION FOR THE PARAGUAYAN BATRACHOFAUNA Available data on the conservation status of the Paraguayan amphibians include the Global Amphibian Assessment (IUCN et al. 2004), the eco-regional assessment of the Gran Chaco (The Nature Conservancy et al. 2005), and a national evaluation, carried out by Motte et al. (2009). The Global Amphibian Assessment included 67 taxa in the least concern (LC) category, four taxa as near threatened (NT), three as data deficient (DD) and eight were not evaluated (NE). The eco-regional assessment of the Gran Chaco selected 19 taxa as Conservation Targets, nine of which are present in Paraguay. Finally, the National evaluation (Motte et al. 2009) included 82 taxa, of which 62 are in the least concern (LC) category, two taxa are vulnerable (VU), six are endangered (EN), one is critically endangered (CR), 11 are data deficient and one was not evaluated. The conservation status for each taxon appears in Appendix I. VII. REFERENCES Aguiar, O., Bacci M., Lima, k E, Rossa-Feres, D. C., Haddad C. F. B. and Recco-Pimentel. S. M.. 2007. Phylogenetic relationships of ~ c u d i c ' a n d~ ~ a p s u s ( - h u r a , H:-lidae, Hylinae) inferred from mitochondnal and nuclear gene sequences. Cladittics 23: 1-9.
Airaldi, K., Baldo, D. and Lavilla, E. O., 2009. Amphibia, Anura, Bufonidae, Melanophryniscus devincenzii: First record for Paraguay and geographic distribution map,Check List 5: 377-379. Avarez B., Lions, M,, Aguirre, R., Cespedez, J. and Hernando, A., 1995. Herpetofauna del Brea de influencia del embalse de la Represa Y a c y r e ~ (Argentina-Paraguay). Fa11: 57-73.
Boettger, O., 1885a. Liste von Reptilien und Batrachien aus Pararmav. Zeitschrii? f Naturwiss. 58: 2 14-248. U
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Boettger, O., 188513. Berichtigung der Liste von Reptilien und Amphibien aus Paraguay. L. Naturuiss. 4: 436-437. Boulenger, G. A, 1894. List of the reptiles and baaachians collected by Dr. J. Bohls near Asuncidn, Paraguay. AnnaLs and Magazine of Natural History 13: 342-348. Boulenger, G. A., 1898. A list of the reptiles, batrachians, and fishes collected by Cav. Guido Boggiani in the northern Chaco. Ann. M m . Civ. Stol: Nut. G a o v a 19: 125-127.
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Brusquetti, F. and Lavilla, E. O., 2006. Lista comentada de 10s anfibios de Paraguay. Cuadernos de Herpetologh 20: 3-79.
Aquino, A L. and Motte, M., 1991. Relacidn del indigena Chamacoco con la herpetofauna del Alto Paraguay. Boletin del Museo Nacional de Historia hTatural del Paraguay 10: 11-22.
Brnsquetti, E, Baldo, D. and Motte, M., 2007. Amphibia, Anura, Bufonidae, Melanophryniscus krauczuki: Geographic distribution map and first record for Paraguay. Check-list 3: 141-142.
Aquino, A. L., Scott, N. and Motte, M., 1996. Lista de 10s anfibios y reptiles del Museo Nacional de Historia Natural del Paraguay. Pp. 331-400 in "Colecciones de Fauna y Flora del Museo Nacional de Historia Natural del Paraguay", ed by 0 . Romero. MNHNPa, Asuncidn.
Budgett, J. S., 1899. Notes on the Batrachians of the Paraguayan Chaco, with observations upon their breeding habitats and development, especially with regard to Phyllomedusa hypochondrialis, Cope. Also a description of a New Genus. Quart. J. Microscopical Sci. 42: 305-333.
Baldo, D., 2001. Acerca de la localidad tip0 y la distribucidn geogrhfica de Melanophryniscus klappenbachi Prigioni y Langone, 2000 (Anura: Bufonidae). Cuadernos ok Herpetologia 15: 141-142.
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Bartrina, L., 2007. Contexto geogrilico general. Pp. 25-32 in "Biodiversidad del Paraguay. Una aproximacidn a sus realidades", ed by D. A. Salas-Duexias and J. F. Facetti. Fundacidu MoisCs Bertoni, Asuncidn. Bertoni, A, de W., 1914. Cattilogos sistemiticos de 10s vertebrados del Paraguay: Clase Segunda Batrachia. Descripcih fiica y Econdmica del Paraguay 59: 21-22. Bertoni, A. de W., 1918. Adiciones a 10s vertebrados del Paraguay. Anales Cient$cos del Paraguay 2 : 233-24 1. Bertoni, A. de W., 1928. Notas zooldgicas. Revista de La Sociedud Cientifica del Paraguay 2: 185-189. Benoni, A. de W., 1939. Cadlogos sistemiticos de 10s vertebrados del Paraguay: Clase Tercera Batrachia. Revista de l a Sociedad Cientijica del Paraguay 4: 42-43.
Cacciali Sosa, l?, 2007. Diversidad de anfibios y reptiles en Paraguay. Pp. 109-117 in "Biodiversidad del Paraguay. Una Aproximacidn a sus Realidades", ed. by D. A. Salas-Duefias and J. F. Facetti. Fundaci6n MoisCs Bertoni, Asuncidn. Cacciali Sosa, l? and Scott, N. J., 2004. Nuevo registro de Hyla melanargyrea Cope, 1887 (Anura, Hylidae) para Paraguay. Cuadernos de Herpetologia 18: 73-74. Cei, J. M., 1990. On a Paraguayan sample of a long time confused species: Physalaemus fmcomaculatus (Steindachner, 1864) (Anura, Leptodactylidae). Bolletino del Museo Regionale di Scienze Naturali Torino 8: 215-231. CCspedez, J. A. and Motte, M., 2001. Distribucidn de sapos del G n e r o Melanophlyniscus (Gallardo, 1961) en Argentina y Paraguay (Anura: Bufonidae). Boletin de la Asociacidn Herpetoldgzca EspalZola 12: 7 1-76.
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Cespedez, J. A. and Motte, M., 2008 (2007). Una nueva especie de Melanophryniscus Gallardo, 1961 de Paraguay (Amphibia: Anura: Bufonidae). FACENA 23: 31-42.
Garcia, F! C. A., Faivovich, J. and Haddad, C. F. B., 2007. Redescription of Hypsibocss semiguttatus, with the description of a new species of the Hypsiboas pulchellw group. Copeia 2007: 933-951.
Chaparro, J. C., Pramuk, J. B. and Gluesenkamp, A G., 2007. A new species of arboreal Rhinella (Anura: Bufonidae) from cloud forest of southeastern Peru. Herpetologica 63: 203-2 12.
Garda, A. A. and Cannatella, D. C., 2007. Phylogeny and biogeography of paradoxical frogs (Anura, Hylidae, Pseudae) inferred from 12s and 16s mitochondtial DNA. Molec. Phylog. Euol. 44: 104114.
CIA, 2007. CIA World Factbook. Online reference, available at ttps://www.cia.gov/cia/publications/factboo~
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Cope, E. D., 1862. Catalogue of the reptiles obtained during the explorations of the Parana, Paraguay, Vermejo and Uruguay Rivers, by Capt. Thos. J. Page. Proc. Acad. Nut. Sci. Philadel. 14: 346359. Cruz, C. A. G. and Caramaschi, U., 2003. Taxonomic status of Melanophryniscus stelzneri dorsalis (Mertens, 1933) and Melanophryniscus stelzneri fulvoguttatus (Mertens, 1937) (Amphibia, Anura, Bufonidae). Boletin do Museo Nacional, Rio de Janeiro 500: 1-11. De la Riva, I., 1995. A new reproductive mode for the genus Ahomera (Amphibia: Anura: Leptodactylidae): Taxonomic implications for certain Bolivian and Paraguayan populations. Stud. Neotropical Fauna and Env. 30: 15-29. DGEEC., 2003. Direccidn General de Estadisticas, Encuestas y Censos, Paraguay. http:// www.dgeec.gov.py/F'rincipal.php Dinerstein, E., Olson, D. M., Graharn, D. J., Wbster, A L., Primm, S. A, Bookbinder, M. E? and Ledec, G., 1995. "Una Evaluacibn del Estado de Consenraci6n de las Ecorregiones T e r ~ s m e sde America Latina y el Caribe". WMF-Banco Mundial. ENPAB., 2003. Estrategia Nacional y Plan de Accibn de Biodiversidad del Paraguay. http:/ www.seam.gov.py1 enpab Facetti, J. F., 2007. Conclusiones sobre el estado de la contaminacidn ambiental del Paraguay. Pp. 223-233 in "Biodiversidad del Paraguay. Una Aproximacibn a sus Realidades", ed. by D. A. Salas-Dueiias and J. F. Facetti. Fundacidn Moises Bertoni, Asuncibn. Faivovich, J., 1994. La distribucidn del genera Lepidobatrachus (Budgett, 1899) (Leptodactylidae: Ceratophlynae). Acta Zoolo'gica Lilloana 43: 105-1 15. Fleytas, M. C., 2007. Cambios en el paisaje. Evolucidn de la cobertura vegetal en la Regidn Oriental del Paraguay. Pp77-87 in "Biodiversidad del Paraguay. Una Aproximacibn a sus Realidades", ed. by D. A. Salas-Dueiias and J. F. Facetti. Fundacidn MoisCs Bertoni, Asuncidn. Frost, D. R., Grant, T., Faivovich, J., Bain, R. H., Haas, A., Haddad, C. F. B., De SA, R. O., Channing, A., Wilkinson, M,, Donnellan, S. C., Raxworthy, C . J., Campbell, J. A., Blotto, B. L., Moler, F!, Drewes, R. C., Nussbaum, R. A., Lynch, J. D., Green, D. M. and Wheeler, W. C., 2006. The amphibian tree of Life. Bulletin of the American Museum of Natural History 297: 1-370.
Halliday, T, 2000. Nitrates and amphibians. Froglog 38: 2. Heyer, W. R., 1978. Systematic of the fuscus group of the frog genus Leptodactylus (Amphibia, Leptodactylidae). Nut. Hist. Mus. Los Angeles County, Sci. BuU. 29: 1-85. Heyer, W. R., 1979. Systematic of the pentadactylus species group of the frog genus hptodactylus (Amphibia: Leptodactylidae). Smithsonian Contributions Zool. 301: 1-43. Heyer, W. R., 1994. Variation within the Leptodactylus podicipinus-wagneri complex of frogs (Amphibia: Leptodactylidae). Smithsonian Contributions 2001. 546: 1-124. Heyer, W. R., 1995. South . b e r i c a n r o c k habltat Lcptoductplur ( h p h i b i a : h u r a : Leptodactylidae) with description of m-o new species. h. the Bwlog. Soc. Wahingtm 108: 695-716. IUCN (Conservation International and Natureserve), 2004. Global Phnphibians Assessment. http://www. globalamphibians.org. Izaguirre, M. F., Lajmanovich, R. C., Peltzer, F! M,, Peralta-Soler, A. and Casco, V H., 2001. Induction of cell death by the synthetic pyrethroid insecticide cypermethrin in the dereloping brain of Physahmuc biZigonigerus tadpoles from A-gentma. Fioglog 43: 2. Izaguirre, M. E, Lajmanovich, R. C., Peltzer, F! M., Soler, k F! and Caxo, V. H., 2000. C~permethrin-induced apoptosis in the telencephalon of Physalaemus biligonigerw tadpoles (Anura: Leptodactylidae). Bull. Environ. Contam. Toxicol. 65: 501-507.
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Gallardo, J. M,, 1957. Las subspecies argentinas de Bufo granulosus Spix. Revista del Museo Argentino de Ciencins Naturales, Cienck Zool6gicas 3: 337-374.
McDiarmid, R. W. and Foster, M. S., 1987. Additions to the reptile fauna of Paraguay with notes on a small herpetological collection from Amambay. Studies on Neotropical Fauna and Environment 22: 1-9.
Gallardo, J. M,, 1965. The species Bufo granulosus and its geographic variation. Bull. Mus. Compar: Zool. 134: 107-138.
MChely, L., 1904. Investigations on Paraguayan Batrachians. Annales Museo Nationalis Hungarici 2: 207-232
LAVILLA and BRUSQETI'I: AMPHIBIAN CONSERVATION AND DECLINE IN PARAGUAY Mertens, R., 1937. Ein neuer Frosch der Gattung Dendrophryniscus aus Paraguay. Senckenbelgiana 19: 175-177.
Motte, M., Nliiiez, K., Cacciali, E, Brusquetti, F., Scott, N. and Aquino, A. L., 2009. Categorizacidn del estado de conservaci6n de 10s anfibios y reptiles de Paraguay. Cuadernos de Herpetologia 23: 5-18 Willer, L. and Hellmich, W., 1936. Amphibian und Reptilien. I. Teil: Amphibia, Cheloni, Loricata. Wwsenschaftliche Ergebnisse der Deutschen Gran ChacoExpedition. Amphibien und Reptilien 1: 1-120. Myers, N., 1986. Tropical deforestation and megaextinction spasm. Pp. 3 9 4 4 0 9 i n "Conservation Biology. The Science of Scarcity and Diversity", ed by M. E. Soul. Sinauer Assoc., Sunderland. Myem, N., Mittermeier, R., Mittermeier, C., da Fonseca, G. and Kent, J., 2000. Biodiversity hotspots for conservation priorities. Nut. 403: 853-858.
Sarvaes, P. and Rodriguez, M. T, 2009. Taxonomic revision of Rhinella granulosa species group (Amphibia, Anura, Bufonidae), with a description of a new species. Anpivac de Zoologia 40: 1-73. Sa-ento. L B.. Pimenta, B. 1'. S., CC. A G. and Caramaschi. C . . 2006. Taxonomic status of Gomphobates marmoratus Reinhardt and Liitken, 1862 1861" and Eupemphix fuscomaculatus Steindachner, 1864 (Amphibia, Anura, Leptodactylidae). Sth Ame?: J. Herpetol. 1: 166- S 74. "
Norman, D. R., 1994. "Anfibios y Reptiles del Chaco Paraguayo". Vol. S. Private Edition, San Jose, Costa Rica. b d d , J. M., de Figueroa, J. M. T and Castroviejo, J., 2003. Notas sobre la Herpetofauna de Bahia Negra (.Alto Paraguay, Paraguay). Bobtin L In Asociacwn Herpetolo'gica EspaiioIn 14: 12-14.
Peracca, M. G., 1899. l'iaggio del dott. Alfredo Borelli nella Repubblica Argentina e nel Paraguay. Bolletino &l Museo di Zoologia ed Anatomia Comparata d e l h R . C7nii.e~sitadz Torino 10: 1-32. Peracca, M. G., 1904. Viaggio del Dr. Borelli nel matto Grosso brasiliano e nel Paraguay, 1899. Rettili e Aufibi. Bolletino del Museo di Zoologia ed Anatomia Comparata della R . Universitu di Torino 19: 1-15.
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Prigioni, C. M. and Langone, J. A., 2000. Una nueva especie de Melanophryniscus Gallardo, 1961, de Argentina y Paraguay (Amphibia, Anura, Bufonidae). Comunicaciones Zool6gicas del Museo de Histork Natural de Montevzdeo 195: 1-12. Rojas de Arias, A., 2007. Ecosistema y salud. El impact0 de las alteraciones ambientales en las enfermedades transmitidas por vectores. Pp. 57-76 in "Biodiversidad del Paraguay. Una Aproximacidn a sus Realidades", ed. by D. A. Salas-Duefias and J. F. Facetti. Fundaci6n MoisCs Bertoni, Asunci6n. Salas-Duenas, D. A. and Facetti, J. F. (eds), 2007. "Biodiversidad del Paraguay. Una Aproximaci6n a sus Realidades." Fundacidn Moisks Bertoni, Asunci6n. Salati, E. and Vose, P. B., 1984. Amazon basin: a system in equilibrium. Sci. 224: 129-138. Scott, N. J. and Lovett, J. W., 1975. A collection of reptiles and amphibians from the Chaco of Paraguay. Occasional Papers, Uni. Connecticut, Biolog. Sci. Series 2, 16: 257-266. The Nature Conservancy, Fundaci6n Vida Silvestre Argentina, Fundacidn el Desarmllo Sustentable del Chaco and Wildlife Conservation Society Bolivia, 2005. Evaluaci6n Ecorregional del Gran Chaco AmericanoIGran Chaco Arnericano Ecoregional Assessment. Fundacio'n I4da Silvestre, Buenos Aires: 1-24 + 1 map + 1 CD,
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Tyler, M. J., 1997. Herbicides kill frogs. Froglog 21: 2. UICN, 2001. Categorias y criterios de la Lista Roja de la UICN. Versidn 3.1. Comisidn de Supervivencia de Especies de UICN. UICN, Gland, Switzerland and Cambridge, UK. Woodwell, G .M., 1983. Global deforestation: contribution to atmospheric carbon dioxide. Sci. 222: 1081-1086. Ziegler, T., Unger, J., Feiler, A. and Lehr, E., 2002. The first Gran Chaco expedition of the Museum fur Tierkunde Dresden: Records of amphibians, reptiles and mammals from the Dry Chaco of Paraguay (Amphibia, Reptilia, Mammalia). Faunistiche Abhandlungen: Staatliches Museum fur Tierkunde Dresden 23: 219-238.
AMPHIBIAN BIOLOGY
APPENDIX 1 Distribution, habitat, and conservation status of the amphibians recorded from Paraguay up to 31 August 2009
KEY TO ABBREVIATIONS: DISTR: Distribution by political units (Departments) or by countries when the taxon is not endemic. ECOR: Eco-regional distribution, following the scheme of Dinerstein et al. (1995). ST: The status of the taxon according to the Global Amphibian Assessment (http://www.globalamphibians.org).An asterisk indicates the species is a Conservation Target for the Gran Chaco. ST1: The status of the taxon according to the national evaluation by Motte et al. (2009). For ST and STI the Code is: CR=Critically Endangered; EN=Endangered; VU=Vulnerable; LC=Least Concern; DD=Data Deficient; NE=Not Evaluated. Subcodes for STI, when present, follow the categories of UICN (2001) Categories and Criteria (vs. 3.1). Taxa in boldface are endemic to Paraguay
APODA CAECILIIDAE CAECILIINAE Luetkenotyphlus brasiliensis DISTR: Paraguay: Alto ParanP, Itapba. Also in Argentina, Brazil. ECOR: Brazilian Interior Atlantic Forest. ST. DD STI: DD Siphonops paulensis DISTR: Paraguay: Amambay. Also in Argentina, Bolivia, Brazil. ECOR: Brazilian Interior Atlantic Forest. S T LC STI: DD
TYPHLONECTINAE
*
Chthonerpeton indistinctum DISTR: Paraguay: Misiones. Also in Argentina, Brazil, Uruguay. ECOR: Humid Chaco S T LC STI: DD
ANURA HYLIDAE HYLINAE Argenteohyla siemersi pederseni DISTR: Paraguay: GuairP. Also in Argentina, Uruguay. ECOR: Brazilian Interior Atlantic Forest, Humid Chaco. S T NE* ST1: VU (B2b[iii]) Dendropsophus elianeae DISTR: Paraguay: Amambay, Concepci6n. Also in Brazil. ECOR: Cerrado. S T LC ST1: LC Dendropsophus jimi DISTR: Paraguay: Amambay, C a n i n d e ~Also . in Brazil. ECOR: Cerrado. S T LC ST1: LC Dendropsophus melanargyreus DISTR: Paraguay: Alto Paraguay. Also in Bolivia, Brazil, French Guayana, Surinam. ECOR: Pantanal. S T LC ST1: LC
LAVILLA and BRUSQElTI: AMPHIBIAN CONSERVATION AND DECLINE IN PARAGUAY Dendropsophus minutus DISTR: Paraguay: Alto Parani, Amambay, Caaguazb, Caazapi, Canindeyd, Central, Concepcibn, Cordillera, Itapba, Paraguari. Also in Argentina, Bolivia, Brazil, Colombia, Ecuador, French Guayana, Guyana, Perb, Surinam, Trinidad-Tobago, Uruguay, Venezuela. ECOR: Brazilian Interior Atlantic Forest, Humid Chaco. m. LC ST1: LC Dendropsophus nanus DISTR: Paraguay: Alto Paraguay, Alto Parani, Amambay, Boquerbn, Caaguazb, Caazapi, Canindeyti, Central, Concepcibn, Cordillera, Guairi, Itapda, Misiones, Neembucii, Paraguari, Presidente Hayes, San Pedro. Also in Argentina, Bolivia, Brazil, Uruguay. ECOR: Brazilian Interior Atlantic Forest, Cerrado, Humid Chaco, Chaco Savannas, Pantanal. S T LC ST1: LC Dendropsophats s a n b a i DISTR: Etiraguay: Caaguazti, Caninde~li,Guairi, Itapba, Misiones, Paraguari, San Pedro. Also in Argentina, Brazil, Umgua)-. ECOR: Brazilian Interior Atlantic Forest, Humid Chaco. ST: LC STl: LC Hypsiboas albopunctatus DISTR: Paraguay: Alto Parani, Amambay, Canindeyb, Concepci6n, ItapGa. Also in Argentina, Bolivia, Brazil, Uruguay. ECOR: Brazilian Interior Atlantic Forest, Cerrado. S T LC ST1: LC Hypsiboas caingua DISTR: Paraguay: Alto Parani, Amambay, Caaguazb, Canindeyti, Cordillera, Guairi, Itapda, Misiones, Paraguari Also in Argentina, Brazil. ECOR: Brazilian Interior Atlantic Forest, Humid Chaco. m Lc b ST1: LC Hypsiboas curupi DISIX Paraguay: Caazapi, Itapua. Also in Argentina, Brazil ECOR: Brazilian Interior Atlantic Fomst. ST. S E ST1: EX (A3c) Hypsiboas faber DISTR: Paraguay: Alto Parani, Caaguazd, Caazapi, Canindey6, Guairi, Itap6a. Also in Argentina, Brazil. ECOR: Brazilian Interior Atlantic Forest. S T LC ST1: LC Hypsiboas pulchellus DISTR: Paraguay: Itapba, Misiones. Also in Argentina, Brazil, Uruguay. ECOR: Brazilian Interior Atlantic Forest, Humid Chaco. S T LC ST1: LC Hypsiboas punctatus rubrolineatus DISTR: Paraguay: Alto Paraguay, Alto Parani, Amambay, Boquerbn, Caaguazii, Canindeyb, Central, Concepcibn, Cordillera, Guairi, Misiones, Paraguari, Presidente Hayes, San Pedro. Also in Argentina, Bolivia, Brazil. ECOR: Brazilian Interior Atlantic Forest, Cerrado, Humid Chaco, Chaco Savannas, Pantanal. S T LC STl: LC Hypsiboas raniceps DISTR: Paraguay: Alto Paraguay, Alto Parani, Amambay, Boquerbn, Caaguad, Caazapi, Caninde*, Central, Concepcibn, Cordillera, Guairi, Itapba, Misiones, Neembuni, Paraguari, Presidente Hayes, San Pedro. Also in kgentina, Bolivia, Brazil, Colombia, French Guayana. -R: Brazilian Interior Atlantic Forest, Cerrado, Humid Chaco, Chaco Savannas, Pantanal. SE LC ftapotihyla langsdorffii DISTR Paraguay: Caazapk, Itapba. Also in Argentina, Brazil ECOR: Brazilian Interior Atlantic Forest. ST: LC STl : IT (A9c)
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AMPHIBIAN BIOLOGY
Pseudis limellum DISTR: Paraguay: Alto Paraguay, Central, Concepcibn, Cordillera, ~ e e m b u c b ,Presidente Hayes, San Fkdro. Also in Argentina, Bolivia, Brazil, Uruguay. ECOR: Humid Chaco, Pantanal. S T LC ST1: LC Pseudis platensis DISTR: Paraguay: Alto Paraguay, Amambay, Boquerbn, Central, Concepcibn, Misiones, Neembucb, Presidente Hayes. Also in Argentina, Brazil. ECOR: Humid Chaco, Chaco Savannas. S T NE ST1: LC Scinax acuminatus DISTR: Paraguay: Alto Paraguay, Boquerbn, Central, Concepcibn, Cordillera, Presidente Hayes. Also in Argentina, Bolivia, Brazil. ECOR: Humid Chaco, Chaco Savannas, Pantanal. ST: LC ST1: LC Scinax berthae DISTR: Paraguay: Canindeyb, Central, Itapba, Misiones, Paraguari. Also in Argentina, Brazil, Uruguay. ECOR: Brazilian Interior Atlantic Forest, Humid Chaco. ST: LC ST1: LC Scinax fuscomarginatus DISTR: Paraguay: Alto Parani, Amambay, CanindeyG, Concepcibn, Cordillera, Itapba, h e e m b u d , Presidente Hayes, San Pedro. Also in Argentina, Bolivia, Brazil. ECOR: Brazilian Interior Atlantic Forest, Cerrado, Humid Chaco. S T LC ST1: LC Scinax fuscovarius DISTR: Paraguay: Alto Paraguay, Alto Parand, Amambay, CaaguaA, Caazapd, Canindeyi, Central, Concepci6n, Cordillera, Guairi, Itapba, Misiones, Paraguari, Presidente Hayes. Also in Argentina, Bolivia, Brazil, Uruguay. ECOR: Brazilian Interior Atlantic Forest, Cerrado, Humid Chaco, Chaco Savannas. ST: LC STl: LC 1
Scinax nasicus DISTR: Paraguay: $to Paraguay, Amambay, Boquerbn, Caaguazli, Canindeyl, Central, Concepcibn, Cordillera, Guairi, I t a p ~ a Misiones, , Neembud, Paraguari, Presidente Hayes, San Pedro. Also in Argentina, Bolivia, Brazil, Uruguay. ECOR: Brazilian Interior Atlantic Forest, Cerrado, Humid Chaco, Chaco Savannas, Pantanal. S T LC STl: LC Scinax similis DISTR. Paraguay: Itapba, Misiones. Also in Brazil. ECOR: Humid Chaco. ST: LC ST1: DD Scinax squalirostris DISTR: Paraguay: Central, Itapba, Misiones, ~ e e m b u c b Paraguari, , Presidente Hayes, San Pedro. Also in Argentina, Bolivia, Brazil, Uruguay. ECOR: Brazilian Interior Atlantic Forest, Humid Chaco. S T LC ST1: LC Trachycephalus venulosus DISTR: Paraguay: Alto Paraguay, Alto Parani, Amambay, Boquerbn, Caaguazb, Caazapi, CanindeyG, Central, Concepcibn, Cordillera, Itapba, Misiones, Paraguari, Presidente Hayes, San Fkdro. Also in Argentina, Bolivia, Brazil, Belize, Colombia, Costa Rica, Ecuador, French Guayana, Guatemala, Guyana, Honduras, MCxico, Nicaragua, Panama, Pet%, Surinam, El Salvador, Trinidad-Tobago, Venezuela. ECOR: Brazilian Interior Atlantic Forest, Cerrado, Humid Chaco, Chaco Savannas, hntanal. S T LC ST1: LC Phyllomedusa azurea DISTR: Paraguay: Alto Paraguay, Amambay, Boquerbn, Caazapi, Canindeyb, Central, Concepcibn, ~ e e m b u c b , Paraguari, Presidente Hayes, San Pedro. Also in Argentina, Bolivia, Brazil. ECOR: Brazilian Interior Atlantic Forest, Humid Chaco, Chaco Savannas, Pantanal.
LAVILLA and BRUSQETTI: AMPHIBIAN CONSERVATION AND DECLINE IN PARAGUAY
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Phyllomedusa sauvagii DISTR: Paraguay: Alto Paraguay, Boquerbn, Concepcibn, Presidente Hayes. ECOR: Cerrado, Humid Chaco, Chaco Savannas. Also in Argentina, Bolivia, Brazil. S T LC* ST1: LC Phyllomedusa tetraploidea DISTR: Paraguay: Itapua. Also in Argentina, Brazil. ECOR: Brazilian Interior Atlantic Forest. S T LC. ST1: VU (B2a)
LEPTODACTYLIDAE Leptodactylus bufonius DISTR: Paraguay: Alto Paraguay, Boquerbn, Central, Concepcibn, Presidente Hayes. ECOR: Humid Chaco, Chaco Savannas, Pantanal. Also in Argentina, Bolivia, Brazil. S T LC ST1: LC Leptodactylus chaquensis DISTR: Paraguay: Alto Paraguay, Arpambay, Boquerbn, Caaguaz6, Caazapi, Canindeyd, Central, Concepcibn, Cordillera, Guairi, ItapGa, Misiones, Neembud, Paraguari, Presidente Hayes, San Pedro. Also in Argentina, Bolivia, Brazil, Uruguay. ECOR: Brazilian Interior Atlantic Forest, Humid Chaco, Chaco Savannas, Pantanal. ST: LC ST1: LC Leptodactylus diptyx DISTR: Paraguay: Alto Paraguay, Amambay, Caaguazu, Central, Concepcibn, Cordillera, ~ e e m b u c u ,Paraguari, Presidente Hayes, San Pedro. Also in Argentina, Bolivia. ECOR: Brazilian Interior Atlantic Forest, Humid Chaco, Pantanal. m LC ST1: LC 4
Leptodact~luselenae D S I X h a g m y : Alto Paraguay, Amambay, Boquerbn, Caazapi, Canindeyti, Concepcibn, Itapua, ~ e e m b u d Paraguari, , Presi&nte Hayes, San Edm. Also in Argentina, Bolivia, Brazil. ECOE Bradian Interior Mantic krest, Cerrado, Humid Chaco, Chaco Savannas, Pantanal. 3T LC ST1: LC Leptodactylus furnarius DISTR: Paraguay: Amambay, Canindeyii. Also in Brazil, Uruguay. ECOR: Brazilian Interior Atlantic Forest, Cerrado. S T LC ST1: LC Leptodactylus fuscus DISTR: Paraguay: Alto Paraguay, Alto Parani, Amambay, Boquerbn, Caaguazb, Caazapi, Canindeyu, Central, Concepcibn, Cordillera, Guairi, Itapua, Misiones, Neembucu, Paraguari, Presidente Hayes, San Pedro. Also in Argentina, Bolivia, Brazil, Colombia, French Guayana, Guyana, Panami, Peni, Surinam, Trinidad-Tobago, Venezuela. ECOR: Brazilian Interior Atlantic Forest, Cerrado, Humid Chaco, Chaco Savannas, Pantanal.
Leptodactylus gracilis DISTR: Paraguay: Amambay, Caazapi, Central, Itapfia, Misiones, Presidente Hayes. Also in Argentina, Bolivia, Brazil, Uruguay. ECOR: Brazilian Interior Atlantic Forest, Humid Chaco. S T LC ST1: LC Leptodactylus labyrinthicus DISTR: Paraguay: Alto Parani, Amambay, Caaguazu, Canindeyu, Concepcibn, Misiones, Paraguari. Also in Argentina, Bolivia, Brazil, Venezuela. ECOR: Brazilian Interior Atlantic Forest, Cerrado, Humid Chaco. S T LC ST1: LC Leptodactylus laticeps DISTR: Paraguay: Alto Paraguay, Boquerbn, Presidente Hayes. Also in Argentina, Bolivia ECOR: Humid Chaco, Chaco Savannas. S T NT* ST1: LC
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AMPHIBIAN BIOLOGY
Leptodactylus latinasus DISTR: Paraguay: Boquerbn, Central, fieembucfi, Presidente Hayes. Also in Argentina, Bolivia, Brazil, Uruguay. ECOR: Humid Chaco, Chaco Savannas. S T LC ST1: LC Leptodactylus mystacinus DISTR: Paraguay: Alto Paraguay, Alto ParanA, Boquerbn, Caazapi, Canindeyti, Central, Codillera, Itapba, Presidente Hayes. Also in Argentina, Bolivia, Brazil, Uruguay. ECOR: Brazilian Interior Atlantic Forest, Humid Chaco, Chaco Savannas. S T LC ST1: LC Leptodactylus ocellatus DISTR: Pacaguay: Alto Paraguay, Alto Parani, Caaguazu, CaazapA, CanindeyCi, Central, Concepcibn, Cordillera, Itaplia, Misiones, Neembucfi, Paraguari, Presidente Hayes, San Pedro. Also in Argentina, Bolivia, Brazil, Colombia, French Guayana, Guyana, Surinam, Trinidad-Tobago, Uruguay, Venezuela. ECOR: Brazilian Interior Atlantic Forest, Cerrado, Humid Chaco, Chaco Savannas, Pantanal. S T LC ST1: LC Leptodactylus podicipinus DISTR: Paraguay: Alto Paraguay, Alto Parani, Amambay, Boquerbn, Caaguazb, Caazapi, Canindeyu, Central, Concepcibn, Cordillera, GuairA, Itapfia, Misiones, Paraguari, Presidente Hayes, San Pedro. Also in Argentina, Bolivia, Brazil, Uruguay. ECOR: Brazilian Interior Atlantic Forest, Cerrado, Humid Chaco, Chaco Savannas, Pantanal. S T LC ST1: LC Leptodactylus syphax DISTR: Paraguay: Cordillera. Also in Bolivia, Brazil. ECOR: Humid Chaco. S T LC ST1: DD
CERATOPHRYIDAE Ceratophys cranwelli DISTR: Paraguay: Alto Paraguay, Boquerbn, Presidente Hayes. Also in Argentha, Bolivia, Brazil. ECOR: Humid Chaco, Chaco Savannas, Pantanal. ST: LC ST1: LC Chacophrys pierottii DISTR: Paraguay: Alto Paraguay, Boquerbn, Presidente Hayes. Also in Argentina, Bolivia ECOR: Humid Chaco, Chaco Savannas. S T LC* ST1: LC Lepidobatrachus asper DISTR: Paraguay: Alto Paraguay, Central, Presidente Hayes. Also in Argentina. ECOR: Humid Chaco. ST: NT* ST1: LC Lepidobatrachus laevis DISTR: Paraguay: Alto Paraguay, Boquerbn, Presidente Hayes. Also in Argentina, Bolivia. ECOR: Humid Chaco, Chaco Savannas. ST: LC* ST1: LC Lepidobatrachus llanensis DISTR: Paraguay: Alto Paraguay. Also in Argentina. ECOR: Chaco Savannas. ST: LC* ST1: LC
CYCLORAMPHIDAE Limnomedusa macroglossa DISTR: Paraguay: Alto Parani. Also in Argentina, Brazil, Uruguay. ECOR: Brazilian Interior Atlantic Forest. ST: LC ST1: EN (A3c)
LAVILLA and BRUSQETTI: AMPHIBIAN CONSERVATION AND DECLINE IN PARAGUAY
17
Odontophrynus americanus DISTR: Paraguay: Amambay, Caaguazii, Canindepi, Central, Concepcibn, Cordillera, Itapiia, Misiones, Paraguari, Presidente Hayes. Also in Argentina, Brazil, Uruguay. ECOR: Brazilian Interior Atlantic Forest, Humid Chaco. S T LC ST1: LC Odontophrynus lavillai DISTR: Paraguay: Alto Paraguay, Boquerbn, Presidente Hayes. Also in Argentina. ECOR: Humid Chaco, Chaco Savannas. S T LC* ST1: LC Proceratophrys avelinoi DISTR: Paraguay: Itapiia. Also in Argentina, Brazil ECOR: Brazilian Interior Atlantic Forest. S T LC ST1: VU (B2)
LEIUPERIDAE Eupemphkc nattereri DISTR: Paraguay: Alto Paraguay, Amambay, Canindeyii, Concepcibn. Also in Bolivia, Brazil. ECOR: Brazilian Interior Atlantic Forest, Cerrado, Humid Chaco, Pantanal. S T LC ST1: LC Physalaemus albonotatus DISTR: Paraguay: Alto Paraguay, Alto Paranb, Amambay, Boquerbn, Caaguazii, Canindeyu, Central, Concepcibn, Guairi, Itapua, Misiones, Neembucu, Paraguari, Presidente Hayes, San Pedro. Also in Argentina, Bolivia, Brazil. ECOR: Brazilian Interior Atlantic Forest, Cerrado, Humid Chaco, Chaco Savannas, Pantanal. S T LC ST1: LC Physalnemus biligonigerus D E I R hraguay: Alto Paraguay, Amambay, Boquerbn, Central, Concepcibn, ~ e e m b u d Paraguari, , Presidente Hayes. ALXI in Argentina, Bolivia, Brazil, Uruguay. ECORr Humid Chaco. Chaco Savannahs. 3 : LC STl: LC Physalaemus centralis DISTR: Paraguay: Amambay, Canindeyii. Also in Bolivia, Brazil. ECOR: Brazilian Interior Atlantic Forest, Cerrado. S T LC ST1: VU (BPb[iii]) Physalaemus cuvieri DISTR: Paraguay: Alto Paraguay, Alto Parani, Amambay, Caaguazii, Caazapi, Canindeyii, Central, Concepcibn, Cordillera, ItapGa, Misiones, Paraguari, San Pedro. ECOR: Brazilian Interior Atlantic Forest, Cerrado, Humid Chaco. Also in Argentina, Brazil. ST. LC ST1: LC Physalaemus ~iograndensisMilstead, 1960 Also in Argentina, Brazil, Uruguay. DISTR: Paraguay: Itapiia, Presidente Hayes. ECOR: Humid Chaco. S T LC ST1: DD Pleurodema fuscomaculata DISTR: Paraguay: Amambay, Canindeyii, Concepci6n. Also in Brazil. ECOR: Brazilian Interior Atlantic Forest. S T LC ST1: LC Pseudopaludicola boliviana DISTR: Paraguay: Alto Paraguay, Amambay, Caaguazii, Central, Concepcibn, Cordillera, Paraguari, Presidente Hayes, San Pedro. Also in Argentina, Bolivia, Brazil, Colombia, Guyana, Surinam, Venezuela. ECOR: Humid Chaco, Chaco Savannas. S T LC ST1: LC
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AMPHIBIAN BIOLOGY
Pseudopaludicola falcipes DISTR: Paraguay: Alto Paraguay, Boquerbn, Concepcibn, Central, Itapda, Misiones, ~ e e m b u c d Paraguari, , Presidente Hayes. Also in Argentina, Brazil, Uruguay. ECOR: Brazilian Interior Atlantic Forest, Humid Chaco, Chaco Savannas. S T LC ST1: LC Pseudopaludicola mystacalis DISTR: Paraguay: Itapba. Also in Argentina, Bolivia, Brazil. ECOR: Brazilian Interior Atlantic Forest. S T LC ST1: LC Pseudopaludicola t m e t z i DISTR: Paraguay: Amambay, Boquerbn, Concepcibn, Misiones, Presidente Hayes. ECOR: Brazilian Interior Atlantic Forest, Humid Chaco, Chaco Savannas. Also in Brazil. ST. LC
UFONIDAE Melanoph yniscus atroluteus DISTR: Paraguay: Itapda. Also in Argentina, Brazil, Uruguay. ECOR: Humid Chaco. ST: LC ST1: CR (BBb[iii]) Melanophyniscus darincenzii DISTR: Paraguay: Guairi. Also in Argentina, Uruguay. ECOR: Brazilian Interior Atlantic Forest. S T EN ST1: NE Melanophyniscus fulvoguttatus DISTR: Paraguay: Amambay, Caaguani, Canindeju, Concepci6n, Guaid, Paraguari, San Pedro. Also in Argentina, Brazil. ECOR: Brazilian Interior Atlantic Forest, Cerrado, Humid Chaco. S T LC ST1: LC Melanophryniscus klappenbachi DISTR: Paraguay: Alto Paraguay, ~ e e m b u c b Presidente , Hayes. Also in Argentina. ECOR: Humid Chaco, Chaco Savannas. S T LC* ST1: LC Melanophryniscus krauczuki DISTR: Paraguay: Itapda. Also in Argentina, . ECOR: Brazilian Interior Atlantic Forest - Humid Chaco transition S T DD ST1: DD Melanophyniscus paraguayensis DISTR: Paraguay: Central, Cordillera, Paraguari. ECOR: Humid Chaco. S T NE ST1: DD Rhinella bergi DISTR: Paraguay: Alto Paraguay, Central, Concepci6n, Itapiia, Presidente Hayes. Also in Argentina, Brazil. ECOR: Humid Chaco, Pantanal. ST: LC ST1: LC Rhinella fernandezae DISTR: Paraguay: Alto Paraguay, Central, Concepci6n, Cordillera, Presidente Hayes, San Pedro. Also in Argentina, Brazil, Uruguay. ECOR: Humid Chaco. S T LC ST1: LC RhineZla azarai DISTR: Paraguay: Alto Paraguay, Central, Itapba, San Pedro. Also in Argentina, Brazil. ECOR: Humid Chaco, Chaco Savannas. ST: NE ST1: LC
LAVILLA and BRUSQETTI: AMPHIBIAN CONSERVATION AND DECLINE IN PARAGUAY Rhinella major DISTR: Paraguay: Alto Paraguay, Boquer6n, Central, Concepcibn, Presidente Hayes ECOR: Humid Chaco, Chaco Savannas. Also in Argentina, Bolivia, Brazil. S T NE ST1: LC Rhinella icterica DISTR: Paraguay: Amambay, Canindeyfi. Also in Argentina, Brazil. ECOR: Brazilian Interior Atlantic Forest, Cerrado. S T LC STl : VU (B2a) Rhinella ornata DISTR: Paraguay: Caaguazb, Caazapi, Caninde+, Itapiia. Also in Argentina, Brazil. ECOR: Brazilian Interior Atlantic Forest. S T LC ST1: LC
IUineUa schneidwi DISTR: Paraguay: Alto Paraguay, Alto Paran&,-Amambay, Boquerbn, Caaguazd, Caazapi, Caninde*, Central, Concepcibn, Cordillera, Guairi, Itapiia, Misiones, Neembud, Paraguari Presidente Hayes, San Pedro. Also in Argentina, Bolivia, Brazil, Uruguay. ECOR: Brazilian Interior Atlantic Forest, Cerrado, Humid Chaco, Chaco Savannas, Pantanal. ST: LC ST1: LC Rhinella scitula DISTR: Paraguay: Amambay, Concepci6n. Also in Brazil. ECOR: Cerrado. S T DD ST1: DD
HYLODIDAE Crossodactylus schmidti 4 DISTR: Paraguay: Itapiia. Also in Argentina, Brazil. ECOR: Brazilian Interior Atlantic Forest.
ST:m STl: DD
MICROHYLIDAE Chiasmocleis albopunctata Boettger, 1883 Also in Bolivia, Brazil. DISTR: Paraguay: Alto Paraguay, Amambay, Caninde@, Concepcibn. ECOR: Brazilian Interior Atlantic Forest, Cerrado, Pantanal. S T LC ST1: LC
GASTROPHRYNINAE D m a t o n o t u s muelleri DISTR: Paraguay: Alto Paraguay, Boquerbn, Central, Presidente Hayes. Also in Argentina, Bolivia, Brazil. ECOR: Humid Chaco, Chaco Savannas. S T LC STl: LC Elachistocleis bicolor DISTR: Paraguay: Alto Paraguay, Alto Parani, Amambay, Boquerbn, Caaguazli, Caninde$, Central, Concepcibn, Corddera, Itapda, Misiones, Neembuc6, Paraguan', Presidente Hayes, San Pedro. Also in N e n t i n a , Bolivia, Brazil, Uruguay. ECOR: Brazilian Interior Atlantic Forest, Cerrado, Humid Chaco, Chaco Savannas, Pantanal. ST: LC ST1: LC
SPECIES INQUIRENDAE The concept "species inpuirenda" applies to those taxa doubtfully identified and in need of further research (ICZN 2000). Two species reported for Paraguay are considered as such: Rhinelh diptycha (Cope, 1862) Described as Bufo diptychw based on one individual collected during the expedition of Captain Page (1859), without mdication of type locality. The name-bearing type, USNM 5841, is lost, and the characters provided in the original description precludes its attribution to any adult toad inhabiting Paraguay. Rhinella levicristata (Boettger, 1885a) Described as Bufo levicristatw based on three individuals not identified (probably housed at SMF, but reported as lost by Baldissera et al. [2004]); the species was considered as a junior synonym of Rhinelh crucfera by Boettger (1885 b) and as species inquirenda by Baldissera et al. (2004).
CHAPTER 2
Status of Conservation and Decline of the Amphibians of Chile Juan Carlos Ortiz and Harold Heatwole
I. Introduction II. Geography and Biogeography A. Biogeography Applied to the Amphibians of Chile
IV. Threats to Chilean Amphibians A. Destruction and Modification of Habitats V. References Appendix I.
Ill. Threatened Species Abbreviations and acronyms used in the text and references: CONAF= Corporaaon Nacional Forestal (National Forestry Corporation); CORFO=Corporacion de Fomento de la Produccion (Chile); IUCN=lnternational Union for the Conservation of Nature; SUMIN= Suqatoria indice; UICN=Unibn lnternacional para la Conservacibn de la Naturaleza
I. INTRODUCTION
T
HE amphibian fauna of Chile is numerically poor and of low diversity in comparison with other neotropical countries. Its fundamental significance stems from its important endemics and monotypic genera. The great majority of Chilean species are native to the Nothofagus temperate rainforest. Recent accounts by Formas (1995), Diaz-PAez and Ortiz (2003) and Ortiz and DiazPAez (2006) indicate that the Chilean amphibian fauna consists of 57 species distributed among four families, one of which is introduced (Pipidae: Xenopus laevis) (Appendix 1). The other five families are: ( 1 ) Bufonidae with the genus Rhiwlla, in which there are five species, (2) Cycloramphidae the largest family with five genera, Rhinoderma, containing two species, Alsodes with 14 species, Eupsophus with nine and two Hylorina and Insuetophrynus each with one species, (3) Ceratoph~yidae,with three genera: A&lognathus with three species, Batrachyla with four and Telmatobius with ten, (4) Calyptocephalellidae with two genera, Telmatobufo with three species, and Calyptocephalella with one, and ( 5 ) Leiuperidae with a single genus, Pleurodema with three species. Of the 13 native genera, three are monotypic (Calyptocephalella, Hylorina and Znsuetophynus) of which two are endemic to Chile (Calyptocephalella, Insuetophrynus) and the third (Hylorina) has its major distribution in Chile but is found marginally in Argentina in the Nothofagus forests of the eastern foothills of the Andes. Thirty-three (58%) of the native species are endemic to Chile.
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11. GEOGRAPHY AND BIOGEOGRAPHY
Geographically, continental Chile is located on the western edge of southern South America between latitudes 17" S and 56" S (excluding the Chilean Antarctic Territory). It extends as a narrow strip of land over 4,000 km long and 9 0 4 0 0 km wide (Fuenzalida 1965). It is limited on the north by Peru, with which it shares a desert region, on the west and south by the Pacific Ocean, and on the east by the Andes mountain range that separates it from Bolivia and Argentina. In this region three important geographic features converge: (1) a moderate depression closed by the ranges that run parallel to the length of the territory, (2) the coastal range, and (3) the Andes. A. Biogeography Applied to the Amphibians of Chile
There have been various proposals for delimiting biogeographic regions (Reiche 1907; Schmithiisen 1956; Mann 1960; Pisano 1965; di Castri 1968; O'Brien 1971: Artigas 19'75; Quintanilla 1981; Gajardo 1994; Grau 1995 ). Schemes on the South American model have been devised by Cabrera and Willink (1973) and Dinerstein et al. (1995). For Chilean amphibians, it would seem instructive to recognize five regions: (1) The Andes, (2) Desert, (3) Central Chile, (4) Subantarctica and (5) Patagonia. The Andean Region extends from the north of the country to approximately 34" S. It is characterized in general by being dry and cold with great contrasts in temperature between day and night. Rains are mainly in summer and are variable, with a decreasing gradient h m north to south. The species of amphibian living between approximately 2,200 and 4,000 m thus are adapted to such climatic conditions. They live in the high wetlands ("bofedales") along the moist borders of streams and near riverbeds with poor drainage. Characteristic of these environments are Rhinella spinulosus, Pleurodema marmorata and the genus Telmatobius. The last tontains ten species in Chile, of which eight are endemic.
The Desert extends from the border with Peru to approximately latitude 30" S. Except for the Loa River there are no streams that reach the sea. There is scant rainfall but the coastal areas receive moisture in the form of fog, called "camanchaca" that permits the development of vegetation on hills with slopes facing the ocean. Amphibians are scarce and are represented fundamentally by the endemic species Rhinella atacamensis, and by northern populations of Pleurodema thaul. The Central Chilean Region covers the centre of the country with the exception of the high ranges approximately between latitudes 32" and 39" S. The climate is strictly Mediterranean with four marked seasons and is characterized by winter rainfall. A sclerophyllic woodland of shrubs occurs in parts of the coastal foothills and there are still small remnants of temperate rain forest that originated from migration of vegetation during the most recent glacial cycle (Villagran and Armesto 2005). This part of Chile is the area most disturbed and modified by humans. It does, however, contain two endemic species, Alsodes nodosus and Rhinoderma rufum, both of which are scarce. The Subantarctic Region is characerized by Nothofagus woodland that occupies almost all the territory between latitudes 33O S and 56OS, where the Andes descend toward the sea. Because of the proximity to the sea the dry period is reduced, the moist period is extended and precipitation can reach 3,000 mm annually. It is in this region that one finds the greatest species richness, and the greatest endemism, of amphibians in Chile. In sectors of the coastal ranges in the northern part of this region one encounters monotypic genera (Insuetophrynus, Hylorina) and high endemism (Alsodes vanzolini, Eupsophus contulmoensis, E. mzgueli, E. nahuelbutenszs, Telmatobufo australis and T. bullocki). Development of intensive silvicultural activity has begun in this region. Finally, the Patagonian Region occurs in the extreme southern part of the country, of which the most important areas for amphibians are located in Magallanes, Aysh and Chilot. Toward the north are introgressions of the Patagonian environment in the vicinities of Lake El Maule and Lake El Laja. The characteristic amphibian is Pleurodema bufonina.
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AMPHIBIAN BIOLOGY
Table 1 . Categories and approaches of conservation of the Chilean amphibians. CR = Critically endangered; EN = Endangered; VU = Vulnerable; N T = Near threatened; LC = Least concern; DD = Data deficient; I = Insufficiently known; R = Rare; F = Out of danger; NE = Not defined, (modified from Diaz-P5ez and Ortiz 2003).
Panel of experts
Expert
Species
Glade (1988)
Formas (1995) Nfiriez (1997)
Alsodes australis Alsodes barrioi Alsodes coppingeri Alsodes hugoi Alsodes igneus Alsodes kaweshkari Alsodes montanw Alsodes monticola Alsodes nodosus Alsodes tumultuosw Alsodes valdiviensis Alsodes vanzolinii Alsodes verrucosus Alsodes vittatus Atelognuthus ceii Atelognathus grandisonae Atelognathw jeinimenensis Batrachyla antartandica Batrachyla kptopw Batrachyla nibaldoi Batrachyla taeniata Calyptocephalella gayi Eupsophus calcaratw Eupsophw contulmoensis Eupsophus emiliopugini Eupsophus insularis Eupsophus migueli Eupsophus nahuelbutensis Eupsophw rosew Eupsophus septentrionalis Eupsophus vertebralis Hylorina sylvatica Znsuetophrynus acarpicus Nanophryne variega,ta Pleurodema bufonina Pleurodema rnarmorata Pleurodema thaul Rhinella arunco Rhinella atacamensis Rhinella papillosw Rhinella mbropunctatus Rhinella spinulosus Rhinoderma darwinii Rhinodermn rufum Telmatobiw dankoi Telmatobius chusrnisensis Telnzatobiw fionterkensis Telmatobius halli Telmatobius marmoratw Telmatobius pefauri Telmatobiw peruvianus Telmatobiw philippi Telmatobius vilamensis Telmatobius zapahuirensis Telmatobufo australis Telmatobufo bzlllocki Telmatobufo v e n w t w
NE R R NE NE NE I NE EN EN NE VU I NE NE I NE NE NE NE VU VU NE NE NE R EN NE NE NE NE I EN I NE NE I VU VU R VU VU VU EN NE NE NE R NE R VU NE NE R R R R
NE R NE NE NE NE EN NE EN EN NE VU I R NE R NE NE NE NE \L 'T
* In this chapter
\TT NE \TT NE \'U EN
I NE NE NE I EN I I NE I VU VU R VU VU VU EN NE NE NE R I R VU NE NE R R R VU
Panel of experts
NE R I NE NE NE EN F ENWU ENII NE EN I R NE R NE F F NE VU
EX F \T F R R I F NE \W/F I R I I R FIENWU VU VU VU R VU EN EN NE NE NE EN R R R NE NE R I R VU
SUMIN
IUCN (200 1)
Diaz and Ortiz (2003)
Diaz and Ortiz (2003)
I R R I NE I EN I I VU NE EN I R NE R NE F F I F \T F
DD NT DD DD DD* DD CR NT NT EN DD* CR NT DD DD DD DD* LC LC DD LC EN LC EN LC EN NT EN LC DD* LC LC CR LC LC DD LC LC LC LC VU LC EN CR DD NE DD DD LC DD LC DD DD DD VU VU EN
\'U
F R 'R VU F NE F F EN F F R F F F F I F VU EN I NE I R F R F I NE R R R VU
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111. THREATENED SPECIES
The problem with decline in populations of amphibian species in Chile is that it has not received the attention it should. Thus, the existence in Chile of Rhinoderma rufum, a
species described by Philippi in 1902, was in doubt until the reports by Formas et al. (1975), Jorquera et al. (1981) and Jorquera (1986) demonstrated its presence as well as the precarious state of its populations. For a long time Calyptocephalella gayi was collected for food and many specimens of Rhinella arunco were used for physiological and biochemical experimentation in the laboratory and for Gilli Mainini pregnancy tests without considering the effects of these activities on the conservation of either species (Cei 1962). The first attempt to analyse the status of conservation of the Chilean fauna originated in an initiative coordinated by the National Forestry Corporation (Corporaci6n Nacional Forestal or CONAF), with a symposium in 198'7 on "The State of Conservation of the Terrestrial Vertebrate Fauna of Chile" ("Estado de Conservaci6n de la Fauna de Vertebrados Terrestres de Chile"). The state of conservation was analysed and the results formed part of the "Red Book of the Terrestrial Vertebrates of Chile" ("Libro Rojo de 10s Vertebrados Terrestres de Chile") (Glade 1988). Determination of the conservation status of the different species of amphibians was based on the expertise of participants and according to the categories established by the International Union for the Conservation of Nature (IUCN) (Thornback and Jenkins 1982). The status of conservation of the amphibian species was later revised on the regional level by Ortiz et al. (1990, 1994) and on the national level by Formas (1995) and Nufiez et al. (1997), the last resulting from a panel of experts meeting at the Fourth Latin American Congress of Herpetology (IV Congreso Latinoamericano de Herpetologia). The methodologies employed in these endeavours were qualitative; the criteria used for estimating status were either not always defined or were not quantifiable. Thus, the methods were subjective and fundamentally based on the "best criteria" of the experts, who assigned categories accordingly and adjusted them to the definitions given by the IUCN in 1982 (Thornback and Jenkins 1982). F'revious information on populations or their densities was scant or lacking, making it difficult to identifi- the causes of decline (Glade 1988; Ortiz 1988; Ibarra-Vidal 1989). Nevertheless, Diaz-Paez and Ortiz (2003) compiled all existing bibliographic information and used their experience of the area to apply the qualitative indices SUMIN, according to the methodology proposed by Reca et al. (1994) and modified by Lavilla et al. (2000). Moreover, they applied the proposed IUCN categories (2001) that considered quantitative criteria. The results are presented in Table 1. It can be observed that 30% of the Chilean amphibians occur in category DD (insufficient data on abundance and distribution) of the IUCN (2001). This situation exists because more than 63% of the species were described within the past nine years (Alsodes australis Formas, ~ b e d a Cuevas , and Nufiez, 1997; Alsodes hugoi Cuevas and Formas, 2001; Alsodes igneus Cuevas and Formas, 2005; Alsodes kaweshkari Formas, Cuevas and Nufiez, 1998; Alsodes valdiiensis Formas, Cuevas and Brieva, 2002; Atelognathus ceii Basso, 1998; Atelognathus jeinimenensis Meriggio, Veloso Yound and Nufiez, 2004; Batrachyla nibaldoi Formas, 1997; Eupsophus septentrionulii Ibarra, Ortiz and Torres, 2004; Telmatobius dankoi Formas, Northland, Capetillo, Nufiez, Cuevas and Brieva, 1999; Telmatobius Ji-onteriensis Benavides, Ortiz and Ebrmas, 2002; Telmatobius philippii Cuevas and Formas, 2002; Telmatobius vilamensis Formas, Benavides and Cuevas, 2003) with few data available on their ecology; for most only the type locality is known. Application of the methodology of SUMIN showed most species to be either rare (R) or insufficiently known (I). (Table 1). In the categorizations of critically endangered (CR), endangered (EN) or vulnerable (TV), at least four species were critically endangered (Alsodes montanus, AEodes vanzolini, i ~ t o p h r y n u sacarpicus and Rhinoderma rufum). Of these, A. montanus, that lives in the foothills of Santiago, has populations that are drastically diminished, possibly because of contamination of watercourses stemming from the urban development and tourism that has ocrurred in this area.
24
AMPHIBIAN BIOLOGY
In practice, Alsodes vanzolini has been collected twice, initially from its type locality (Ramadillas, Arauco Province) on the occasion of its original description (Donoso-Barros 1974a) and later by Formas (1981) from the same locality. Since then it has not been encountered despite multiple efforts to find it (Ortiz and Ibarra-Vidal 2004). Insuetophrynus acarpicus, a monotypic species with a distribution restricted to the vicinity of its type locality (Mehuin, Valdivia Province) is being affected by deterioration of its habitat: burning of woodlands, extraction of firewood and the planting of exotic vegetation U. R. Formas, personal communication). Finally, Rhinoderma rufum, after its validation as a species by Formas et al. (1975), has not been found despite repeated searches. In relation to this situation, there are two projects, one to search for sites where populations may still remain, and another to raise this species ex situ so as to be able in the future to reintroduce it into a locality where it previously occurred. (K. Busse and C. Cuevas, personal communication). There are 1'7 species, almost a third of the total of those present in Chile, that are considered to be in the category of Least Concern (LC). This is because they are still encountered frequently, despite the great certainty that there are populations that have been locally extinguished, but without significantly affecting the extent of their geographic range. In the case of the genus Rhinella, four of the five species are in this situation and only B. rubropunctatus is considered as vulnerable because only a few sparse populations are known and its biology is unknown. The species of the genus Batrachyla are in a similar situation. These are still readily encountered in abundance in the southern parts of their ranges, but not in the northern parts where modification or destruction of habitat has caused decline or loss of some populations. Some species of Eupsophus, Pleuroderna and Telmatobius are also found in this category, but in general those species occupy wider distributional ranges (including neighbouring countries) than do their congeners. Telmatobius is also found in Bolivia and Peru and Eupsophus and Pleurodema occur in Argentina. The monotypic species Hylorim sylvatica merits special attention owing to the broad geographic range it formerly occupied: from Ramadillas (37O18"S) (Donoso-Barros 1974b) to the Lake San Rafael National Park (Parque Nacional Laguna San Rafael) (46O44'S) (DiazPAez et al. 2002). It is not possible to find it nowadays except south of the region of Los Lagos (40°S). IV. THREATS TO CHILEAN AMPHIBIANS Studies explicitly outlining the factors that are affecting the conservation of amphibians in Chile, and, of course, of the decline in their populations, are scarce. Among those, however, can be named the studies of Ortiz (1988) and Ibarra-Vidal (1989). In addition, there have been assessments of the conservation status of various species (Glade 1988; Ortiz et al. 1990, 1994; Formas 1995; Nufiez et al. 1997; Diaz-PAez and Ortiz 2003). Among the effects that can be identified as having caused decline of amphibian populations in Chile are destruction and modification of habitat, drainage and drying of wetlands, sedimentation as a result of deforestation, contamination of rivers, use for food, indiscriminate capture for pets and the introduction of exotic species. A. Destruction and Modification of Habitats
From colonial times onward, the elimination of native woodland resulting from clearing of land for agriculture and animal husbandry and later for forestry and urban and industrial use brought with it a lowering of population densities and loss of populations in many species of amphibians. Among the amphibians that have been most affected by this action are those requiring moist, shady environments and which are accordingly associated with the subcanopy of the Nothofagus temperate rainforest and of the evergreen valdiviano forest of Olivillo, Ulmo, and Tepa. Included among these is the genus Eupsophus, especially the species E.
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25
contulmoensis, E. insularis, E. nahuelbutensis and to a lesser extent E. calcaratus, E. migueli, E. roseus and E. vertebralis. It should also be noted that modification of habitat has affected the two species of Rhinoderrna, R. darwini and R. rufum, as well as Insuetophrynus acarpicus, Batrachyla taeniata (especially its northern populations) and B. leptopus. Perhaps one should also include Hylorina sylvatica in this category but the precise information on its previous distribution, needed for confirmation, is lacking. Another important modification of habitat is the draining or drying of wetlands, of which those of the south-central zone of Chile have been the most affected. The species that has suffered the greatest impact there is Calyptocephalella gayi, a species that carries out its entire life cycle in the water. A similar situation appertains to the species of the genus Telmutobius that live in the Andean and pre-Andean sectors in the north of Chile, where waters have been diverted for mining and agricultural reasons, with a concomitant decline of rivers and streams and a lowering of the water table (Ibarra-Vidal 1989). Erosion occurring as a result of loss of native forests brings with it sedimentation of the rocky bottoms of rivers and streams, the preferred habitat of tadpoles of species of the genus Telmatobufo. This situation prevents the tadpoles from grazing on the bottom and moreover deprives them of refuges and of substrate to which they can adhere. Chemical contamination of rivers and streams Erom the dumping of domestic, industrial, mining, forestry and agricultural wastes cause changes of various kinds in the larval and adult states (Gavilfin et al. 1988; Hermosilla and Ortega 1989). These contaminants seem to be generally affecting all the species distributed in the vicinity of these human disturbances and they have been seen to specifically affect species of the genus Alsodes (A. rnontanus, A. nodosus, A. tumultuosus and A vanzolini). Culinary activity affecis a single edible species in Chile (Calyptocephalella gayi) despite the fact that its capture is prohibited. Attempts to raise this species in captivity led to unclear results, and it seems that most, if not all, rearing facilities merely serve as a repository for illiat specimens captured in the wild. (Ortiz 1988, 1989) One of the non-traditional activities that occurred in Chile between 1985 and 1992 was the exportation of native fauna. The regulations existing at that time permitted, by omission, the capture of all those species that were not specifically prohibited, but fortunately from 1993 onward, new laws on fishing and hunting prohibited all hunting, possession, transport or sale without a permit in advance. The exportation of amphibians during those eight years reached a total of 212,475 individuals, sent legally to the United States and Europe, of which 37,235 were C. Gayi and the other 175 240 were of undetermined species (Servicio Agricola y Ganadero 1993). Since for the latter group it was not known which species were included, it is not possible to gauge the impact of this activitiy with certainty. In fact, with the new legislation this has ceased to be an actual threat to the amphibian fauna of Chile. Illegal international commerce in these species now seems to be nonexistent in the country. Finally, the introduction of exotic species, predominately the clawed frog (Xenopus laevis), the rainbow trout (Oncorhynchus mykiss), the carp (Cyprinus carpio) and a cichlid fish (Cuhhomu facetum) may have affected the country's amphibians. Up to the present moment, adsting data on the diet of X. laevis in Chile do not show that it preys on either larvae or W t s of native amphibians (Lobos et al. 1999). Nevertheless, it could be a potential armpetitor with C. gayi, despite the fact that X. laevis has a preference for artificial bodies d w a t e r (canals and irrigation channels) more than for natural Chilean environments. In d ~laboratory C. facetum has been observed to ingest eggs and larvae of Pleurodemu thaul (Ruiz and Marchant 1989) but there are no field studies that corroborate this occurring under natural conditons. Available data for 0 . mykiss and C. carpio do not indicate that h r a e or adult amphibians are included in the diet. Thus, it is uncertain whether these 6sh prey on local amphibians; the possibility remains that they may have a negative impact thmugh interference competition (Prochelle and Campos 1985; Taniguchi et al. 2002).
AMPHIBIAN BIOLOGY
V. REFERENCES Artigas, J., 1975. Introduccidn a1 estudio por computacidn de las ireas zoogeogrificas de Chile continental basado en la distribucidn de 903 especies de animales terrestres. Guyana (Miscekinea) 4: 1-25.
Formas, J. R., Cuevas, C. C. and Nufiez, J., 1998. A new species of Alsodes (Amphibia: Anura: Leptodactylidae) from southern Chile. Proc. Biolog. Soc. Washington 111: 521-530.
Basso, N., 1998. A new telmatobiine teptodactylid frog of the genus Atelognathus from Patagonia. Herpetologica 54: 44-52.
Formas, J. R., Pugin, E. and Jorquera, B., 1975. La identidad del batracio chileno Heminectes rufus Philippi, 1902. Physis Seccidn C. Buenos Aires 34: 147-157.
Benavides, E., Ortiz, J. C. and Formas, J. R., 2002. A new species of Telmatobius (Anura: Leptodactylidae) from northern Chile. Herpetologica 58: 210-220. Cabrera, A. and Willink, A., 1973. "Biogeografia de AmCrica Latina". Programa Regional de Desarrollo Cientifico y Tecnoldgico". Organizacidn de Estados Americanos, Washington D C. Cei, J. M., 1962. "Batracios de Chile". Ediciones Universidad de Chile, Santiago. Cuevas, C. C. and Formas, J. R., 2001. A new species of Alsodes (Amphibia, Anura, Leptodactylidae) from Central Chile. Amphibia-Reptilia 22: 187-198. Cuevas, C. C. and Formas, J, R., 2002. Telmatobius philippii, una nueva especie de rana acuitica de Ollagiie, norte de Chile (Leptodactylidae). Revista Chilena de Historia Natural 75: 245-258. Diaz-Paez, H. and Ortiz. J. C., 2003. Evaluacidn del estado de conservacidn de 10s anfibios en Chile. Reuista Chilena de Historia Natural 76: 509-525. Diaz-PBez, H., Williams, C. and Griffths, R. A., 2002. Diversidad y abundancia de anfibios en el Parque Nacional Laguna San Rafael (XI Regidn, Chile). Boletin del Museo Nacional de Historia Natural (Chile) 51: 135-146. Di Castri, F., 1968. Esquisse kcologique du Chili. Pp. 752 in "Biologie de 1'AmCrique Australe, vol. 4, ed by C. Delamare Deboutteville and T. Rapoport. Editions C. N. R. S., Paris. Dimestein E., Olson, D. M., Graham, D. J., Webster, A. L., Primm, S. A. Bookbinder, M. P: and Ledec, G., 1995. 'X Conservation Assessment of the Terrestrial Ecoregions of Latin America and the Caribbean". World Wildlife Foundation and The World Bank, Washington D C. Donoso-Barros, R., 1974a. Nuevos reptiles y anfibios de Chile. Boletin de la Sociedud de Biologia de Concepcidn 48: 217-229. Donoso-Barros, R, 197413. Distribucidn nortefia de Hylorina syluatica Bell. P R-19 in "Resumenes de Comunicaciones de la XVII Reunidn Anual de la Sociedad de Biologia de Chile". Concepcidn. Formas, J. R., 1981. The identity of the frog Eupsophus uanzolinii from Ramadillas, Nahuelbuta Range, Southern Chile. Proc. Soc. Biolog. Washington 93: 920-927. Formas, J. R., 1995. Anfibios. Pp. 314-325 i n "Diversidad Bioldgica de Chile", ed by J. A. Simonetti, M. T K. Arroyo, A. E. Spotorno and E. Lozada. C O N I m , Santiago. Formas, J. R., 1997. A new species of Batrachyla (Anura, Lepdactylidae) from Southern Chile. Herpetologzca 55: 6-13. Formas, J. R., Benavidesj, E. and Cuevas, C., 2003. A new species of Telmatobius (Anura: Leptodactylidae) from rio Vilama northern Chile, and the redescription of T halli Noble. Herpetologica 59: 253-270.
Formas, J. R., ~ b e d a ,Cuevas, C. C. and Nufiez, J., 1997. Alsodes awtralis, a new species leptodactylid frog from the temperate Nothofagus forest of southern Chile and Argentina. Stud. Neotropical Fauna €? Enu. 32: 200-2 11. Formas, J. R., Northland, I., Capetillo, J., Nufiez, J. J., Cuevas, C. C. and Brieva, L. M,, 1999. Telmatobiw dankoi, una nueva especie de rana acuitica del norte de Chile (Leptodactylidae). Reuista Chilena de Historia Natural 72: 427-445. Fuenzalida, H., 1965. Los factores naturales. Pp. 1-5 in "Geografia Econdmica de Chile". CORFO (Corporaci6n de Fomento de la Produccidn), Santiago. Gajardo, R., 1994. "La Vegetacidn Natural de Chile. Clasificacidn y Distribucidn Geogrifica". Editorial Universitaria, Santiago. Gavilin, J. F., Hermosilla, I., Alay, F. and Venegas, W., 1988. Accidn teratogenica del DDT en el desarrollo embrionario de Caudiverbera caudiverbera (LinnC, 1758) (Anura, Leptodactylidae). Boletin de la Sociedad de Biologia de Concepcidn (ChiW 59: 47-56. Glade, A. (ed.) 1988. "Libro Rojo de 10s Vertebrados Terrestres Chilenq". Corporacidn Nacional Forestal, Ministerio de Agricultura, Santiago. Grau, J., 1995. Aspectos geogrPficos de la flora de Chile. Pp. 63-83 i n "Flora de Chile", ed by C. Marticorena and R. Rodriguez. Universidad de Concepcidn, Concepcidn. Hermosilla, I. and Ortega, J. C., 1989. Efecto del fluor en el desarrollo embrionario del anuro chileno Caudiverbera caudiverbera: crecimiento y capacidad de natacidn. Boletin de la Sociedad de Biologia de Concepcidn (Chile) 60: 129-1 37. Ibarra-Vidal, H., 1989. Impacto de las actividades humanas sobre la herpetofauna en Chile. Comunicaciones del Museo Regional de Concepcidn (Chile) 3: 33-39. Jorquera, B., 1986. Biologia de la reproduccidn del gknero Rhinoderma. Anales del Museo de Historia Natural de lralparairo 17: 53-62. Jorquera, B., Pugin, E., Garrido, 0 . Goicoechea, 0 . and Formas, R., 1981. Procedimiento de desarrollo en dos especies del gknero Rhinodermu. Medio Ambiente 5: 58-71. Lavilla, E. O., Ponsa, M. L., Baldo, D., Basso, N., Bosso, A., CCspedes, J., Chebez, J. C., Faivovich, J., Ferrari, L., Lajmanovich, R., Langone, J. A., Peltzer, P, ~ b e d a , M,, Vaira, C. and Vera, F., 2000. Categorizacidn de 10s anfibios de Argentina. Chapter 2, pp. 11-34 in "Categorizacibn de 10s Anfibios y Reptiles de la Republics Argentina", ed by E. Lavilla, E. Richard and G. Scrocchi. Asociacidn Herpetoldgica Argentina, San Miguel de Tucumin.
ORTIZ and HEATWOLE: CONSERVATION AN D DECLINE OF THE AMPHIBIANS OF CHILE
27
Lobos, G., Cattan, F! and L6pez, M., 1999. Antecedentes de la ecologia tr6fica del sapo Africano Xenopus laevis en la zona central de Chile. Boletin del Museo Nacional de Historia Natural (Chile) 48: 7-18.
Pisano, E., 1965. Biogeogafia. Pp. 228-267 i n "Geografia Econ6mica de Chile." CORFO (Corporaci6n de Fomento de la Producci6n), Santiago.
Mann, G., 1960. Regiones biogeogrlficas de Chile. Znvestigaciones Zool~5gicasChilenas 6: 15-49.
Pmchelle, 0 . and Campos, H., 1985. The biology of the introduced carp Cyprinus carpio L., in the River Cayumapu, Valdivia, Chile. Stud. Neotropical Fauna €9Env. 20: 65-82.
N ~ e H., z Maldonado, V. and Pkrez, R., 1997. Reuni6n de trabajo con especialistas de herpetologia para categorizaci6n e especies segGn estados de conservaci6n. Noticiario Mensual Museo Nacional de Historia Natural (Chile) 329: 12-19. O'Brien, C., 1971. The biogeography of Chile through entomofaunal regions. Ent. News 82: 197-207 + 2 maps.
Quintanilla, V., 1981. Carta de las formaciones vegetales de Chile. Contribuciones Cientifcas. Universidad de Santiago 47: 1-32. , and Grigera, D., 1994. Conservaci6n Reca A., ~ b e d a C. de la fauna de tetrlpodos. I. Un indice para su evaluaci6n. Mastotoologia Neotropical 1: 17-28.
Ortiz, J. C., 1988. Situacidn de la exportacidn de 10s vertebrados terrestres chilenos. Comunicaciones del Museo Regzonal de Concepcidn (Chile) 2: 37-41.
Reiche, K., 1907. Grundziige der Pflanzenverbreitung in Chile. Vol. 8 in "Die Vegetation der Erde", ed by A. Engler and 0. Drude. Verlag von Wilhelm Engelmann, Leipzig.
Ortiz, J . C., 1989. El recurso fauna en la VIII Regi6n. Pp. 29-38 i n *Una Vision Caleidosc6pica de 10s Recursos Naturales., ed by J. C. Ortiz. Universidad de Concepci6n, Concepcibn.
Ruiz, V. H. and Marchant, M., 1989. Sobre Cichhoma facetum (Jennyns, 1842) (Perciformes, Cichlidae) de las lagunas Grande y Chica de San Pedro, VIII Regibn, Chile. Boletin de la Sociedad de Biologia de Concepcidn 60: 227-229.
Ortiz, J. C. and Diaz-Piez, H., 2006. Estado actual de la biodiversidad de Anfibios en Chile. Guyana 70: 114-121. Oniz, J. C. and Ibarra, H., 2004. Anfibios y reptiles de la Cordillera de Nahuelbuta (Chile). Pp. 427440 in "Biodiversidad y Ecologia de 10s Bosques Costeros de Chile", ed by C. Smith, J. Armesto and C. Valdovinos. Edirorial Universitaria, Santiago. Ortiz J. C., Quintana, V and Ibarra-Vidal, H., 1994. "Vertebrados Terrestres con Problemas de Conservaci6n en la Cuenca del Biobio y Mar Adyacente". Ediciones Universidad de Concepci6n, Concepci6n. Oniz J. C, Tmncoso, F., Ibarra-Vidal, H. and NGCez, H., 1990. Lista sistemitica, distribuci6n, estado de conservaci6n y clave para 10s herpetozoos de la VIII Regibn, Chile. Comunicaciones del Museo Regional de Concepcibn (Chile) 4: 3 1 4 3 .
?&lippi, R. A., 1902. "Suplemento a 10s Batraquios chilenos descritos en la Historia Fisica y Politica de Chile de don Claudio Gay". Libreria Alemana, Santiago.
Schmithiisen, J., 1956. Die raunmiliche Ordenung der chilenischen Vegetalis. Bonner Geographische Abhandlungen 17: 1-86. Servicio Agricola y Ganadero, 1984 -1993. "Estadisticas de Comercio Exterior de Productos Silvoagroagropecuarios de Chile". Servicio Agricola y Ganadero, Santiago. Taniguchi, Y., Fausch, K. and Nakano, S., 2002. Size structured interactions native and introduced species: can intraguild predation facilitate invasion by stream salmonids? Biological Invasion 4: 223-233. Thornback, J. and Jenkins, M., 1982. "The IUCN Mammal Red Data B o o k . Part 1. International Union for Conservation of Nature and Natural Resources, Gland. UICN, 2001. "Categorias y Criterio de la Lista Roja de la UICN". Versi6n 3.1. Comisi6n de Supervivencia de Especies de la UICN. UICN, Gland. Villagrln, C and Armesto, J. J., 2005. Fitogeografia histdrica de la Cordillera de la Costa de Chile. Pp. 99-1 16 in "Biodiversidad y Ecologia de 10s Bosques Costeros de Chile", ed By C. Smith, J. Armesto and C. Valdovinos. Editorial Universitaria, Santiago.
AMPHIBIAN BIOLOGY
APPENDIX 1 Checklist of the species of amphibians of Chile SPECIES
DISTRIBUTION
Alsodes australis Formas, ~ b e d a Cuevas , and Ndfiez, 1997
Argentina and Chile
Alsodes barrioi Veloso, Diaz, Iturra and Penna, 1981
Chile
Alsodes copperingeri Gunther, 1881
Chile
Alsodes hugoi Cuevas, Formas, 2001
Chile
Alsodes ignew Cuevas and Formas, 2005
Chile
Alsodes kaweshkari Formas, Cuevas and Nhiiez, 1998
Chile
Alj-odes montanus (Lataste, 1902)
Chile
Alsodes monticola Bell, 1843
Argentina and Chile
Alsodes nodosw (DumCril and Bibron, 1841)
Chile
Alsodes tumultuosw Veloso, Iturra and Galleguillos, I979
Chile
Alsodes valdiviensis Formas, Cuevas and Brieva, 2002
Chile
Alsodes vantolinii (Donoso-Barros, 1974)
Chile
Alsodes verrucosus (Philippi, 1902)
Argentina and Chile
Alsodes vittatw (Philippi, 1902)
Argentina and Chile
Atelognathus ceii Basso, 1998
Argentina and Chile
Atelognathus grandisonae (Lynch, 1974)
Chile
Atelognathw jeinimenensis Meriggio, Veloso, Young and NGiiez, 2204
Chile
Batrachyla antartandica Barrio, 1967
Afgentina and Chile
Batrachyla leptopw Bell, 1843
Argentina and Chile
Batrachyla nibaldoi Formas, 1997
Chile
Batrachyla taeniata (Girard, 1854)
Argentina and Chile
Cal@tocephalella gayi (DumCril and Bibron, 1841)
Chile
Eupsophw cakaratw (Gunther, 1881)
Argentina and Chile
Eupsophw contulmomis Ortiz, Ibarra-Vidal and Formas, 1989
Chile
Eupsophw emiliopugani Formas, 1989
Argentina and Chile
Eupsophw insularis (Philippi, 1902)
Chile
Eupsophus migueli Formas, 1978
Chile
Eupsophus nahuelbutensis Ortiz and Ibarra-Vidal, 1992
Chile
Eupsophus rosew (DumCril and Bibron, 1841)
Argentina and Chile
Eupsophw septentrionalis Ibarra-Vidal, Ortiz and Torres, 2004
Chile
Eupsophw vertebralis Grandison, 1961
Chile
Hylorina sylvatica Bell, 1843
Argentina and Chile
Znsuetophrynus acarpicw Barrio, 1970
Chile
Nanophryne variegata Bell, 1843
Argentina and Chile
Pleurodema bufonina Bell, 1843
Argentina and Chile
Pleurodema marmorata (DumCril and Bibron, 1841)
Argentina, Bolivia, Chile and Pen3
Pleurodema thaul (Molina, 1782)
Argentina and Chile
Rhinella arunco (Molina, 1782)
Chile continued overleaf
ORTIZ and HEATWOLE: CONSERVATION AND DECLINE OF THE AMPHIBIANS OF CHILE
29
Appendix l continued Rhinella atacamensis Cei, 1961
Chile
Rhinella papillosw Philippi, 1902
Argentina and Chile
Rhinella rubropunctatus Guichenot, 1848
Argentina and Chile
Rhinella spinulosus Wiegmann, 1843
Argentina, Bolivia, Chile and Penl
Rhinoderma danvinii Dum6ril and Bibron, 1841
Argentina and Chile
Rhinoderma rufum (Philippi, 1902)
Chile
Telmatobius chumisensis Formas, Cuevas and Nufiez, 2006
Chile
Telmatobius dankoi Formas, Northland, Capetillo, Nbfiez, Cuevas and Brieva, 1999
Chile
Telmatobius fionteriensis Benavides, Ortiz and Formas, 2002
Chile
Elmatobius halli Noble, 1938
Chile
Telmatobius marmoratw (Dumkril and Bibron, 1841)
Bolivia, Chile and Peril
Telmatobius pefauri Veloso and Trueb, 1976
Chile
Telmatobiw peruuianus Wiegmann, 1834
Chile and Pen3
Telmatobiw philippi Cuevas and Formas, 2002
Chile
Telmatobiw uilamensis Formas, Benavides and Cuevas, 2003
Chile
Telmatobius rapahuirensic Veloso, Salaberry, Navarro, Iturra, Valencia, Penna and Diaz, 1982
Chile
Telmatobufo awtralis Formas, 1972
Chile
Telmatobufo bullocki Schmidt, 1952
b
Chile
Tclmtobufo uenustus Philippi, 1899
Chile
Xenopus lacLis
Southern Africa (widely introduced, including into Chile)
CHAPTER 3
Status of Amphibian Conservation and Decline in Argentina E. 0. Lavillal and Harold Heatwole2
I. Introduction II. The Amphibian Fauna of Argentina A. Amphibians Recently Added to the Argentine Batrachofauna B. Amphibians Excluded from the Argentine Batrachofauna C. Amphibians Doubtfully Retained in the Argentine Batrachofauna D. Synonymies E. Changes in Supraspecific Categories Ill. Geography of Argentina A. The Geophysical Regions of Argentina 1. Llanura Platense 2. Subtropical Plateau 3. The Northwest 4. Cuyo 5. Pampean Sierras 6. Patagonia IV. Biogeography of Argentina A. Neotropical Region 1. Amazonian Domain 2. Chacoan Domain 3. Andean-Patagonian Domain B. Antarctic Region 1. Subantarctic Domain V. The Eco-Regions of Argentina A. High Andean Eco-Region B. Puna Eco-Region C. Monte of Sierras and Bolsones Eco-Region D. Yungas Forest Eco-Region E. Dry Chaco Eco-Region F. Humid Cham Eco-Region G. Paranaen Forest Eco-Region
'Author Translator: from Spanish to English
H. I. J. K. L. M.
Esteros of Ibera Eco-Region Campos and Malezales Eco-Region Delta and Islands of the Parana River Espinal Eco-Region Pampan Eco-Region Monte of Llanuras and Mesetas Eco-Region N. Patagonian Steppe 0.Patagonian Woodlands Em-Region VI. Batrachofaunal Regions of Argentina VII. Principal Environmental Problems in " Argentina A. Loss of Habitat 1. Alteration of Woodland Environments 2. Converting of Natural Non-Forested Areas into Agricultural Fields and Grazing Lands 3. Alteration of Wetlands and Bodies of Water 4. Urban Expansion 5. Chemical and Organic Contamination 6. Introduction of Exotic Species 7. Diseases 8. Increase in Ultraviolet Radiation 9. Global Climatic Change 10. Commercial Trade in Amphibians VIII. Regionalization of the Herpetofauna and Principal Threats IX. Categories of Protection for the Argentine Batrachofauna X. References Appendices
LAVILLA and HEATWOLE: AMPHIBIAN CONSERVATION AND DECLINE IN ARGENTINA
31
I. INTRODUCTION
A
S of 31 July 2006, the known amphibian fauna of the Reptiblic of Argentina consisted of 1'76 species in two orders, 13 families and 40 genera. Although this fauna is proportionally poor compared to those of Brazil, Colombia, Ecuador, P e h and Venezuela, it has a great number of interesting taxa (including some from hot, xeric, semi-xeric and salty habitats), and about a third of the species are endemic to Argentina.
The conservation status of Argentine amphibians was assessed by diverse methodologies, both at regional (Lavilla et al. 2000, 2002) and global levels (UICN et al. 2004) and the two levels are, in general, coincident (but see point IX, below). As a further contribution to the subject, the present chapter (1) makes the list of amphibian species recorded from Argentina current by incorporating verified changes since the last available account (Lavilla and Cei 2001); (2) summarizes the principal geographic and biogeographic characteristics of the country in relation to the known distribution of the native batrachofauna; (3) assesses the principal threats to Argentine amphibians; (4) analyses population declines and (5) presents a summary of the available informatipn on the assignment of conservation categories to Argentine amphibians. 11. THE AMPHIBIAN FAUNA OF ARGENTINA
Table 1 summarizes information on Argentine amphibians at the generic level and an annotated list of the species appears in Appendix 1, following the arrangement proposed b?- Fmst et al. (2006) and Grant et al. (2006). Discrepancies between the present chapter and the most recent previous summary of this batrachofauna (Lavilla and Cei, 2001) arise from additions and exclusions of certain species, and from changesCat the supraspecific level, as discussed below. A. Amphibians Recently Added to the Argentine Batrachofauna Scinax aromothyella: This species was described by Faivovich (2005) and at present is known only from three localities in Misiones Province. Scinax curupi: This species was described by Garcia et al. (2008) and at present is known from diverse localities in Misiones Province and Paraguay. Scinax fuscomarginatus: The presence of this species, doubtfully cited for the provinces of Corrientes and Formosa by Alvarez et al. (1996), was confirmed by Faivovich and Baldo (in Lavilla et al. 2002). who reported it also for the province of Chaco. Scinax aff. uruguayus: Reported as Hyla uruguaya by Giraudo et al. (2005) from Gobernador Virasoro, Corrientes Province. It seems to be a new species, according to Diego Baldo (personal communication). Trachycephalus dibernardo: This species was described by Kwet and Sol6 (2008) from Rio Grande do Sul and Santa Catarina (Brazil) and El Soberio, Misiones Province in Argentina. Leptoductylus firnarius: Reported by Baldo et al. (2008) from the Department Candelaria, Misiones Province. Odontophrynus cordobae: This species was described by Martino and Sinsch (2002) to include diploid forms from the province of Cordoba, previously considered as Odontophrynus americanus. Pleurodema cordobae: This species was described by Valetti et al. (2009) to include octoploid forms from the Sierra de Comechingones province of Cordoba, previously confused with Pleurodema kreigi. Oreobates barituensis: This species was described by Vaira and Ferrari (2008) from Baritu, in Salta Province; later, its range was extended by Akmentins and Vaira (2009) to a couple of localities in Valle Grande (Jujay).
32
AMPHIBIAN BIOLOGY
Table 1. Amphibians known from Argentina up to 31 August 2009. Family names are in boldface. IAmphibia E.
Gymnophiona
1.e
Stegokrotaphia
Caeciliidae: Chthonerpeton (l), LuetRenotyphlus ( l ) ,Siphom$s (2).
.B .. Bi.
Batrachia
IIPillM Lalagobatrachia I B m I B Sokolanura USU.8.
Acosmanura
Bm.81.B
Neobatrachia
......................
U .......
@PIIIB.Bl.MM
.....y.
Nobleobatrachia
I B I N U 1 I I I I 1 1 Meridianura UUUEll.B.l.l.
Terrarana
Brachycephalidae:
.IlB..R.U.llB
...........
Strabomantidae: Ombates
IlliUli..I..
U B ..I.DU I.
..
............
~ILIIIIII88lRllWS Amphignathodontidae: Gashothem ( 3 )
*
Hylidae: Aphtodiscus (l), Argenteohyla (2), Dendropsophtls ( 3 ) , Hypsibom (13), Itapotihyla ( l ) , Pseudis (S), Scinax (10), Trachycephalus (3), Phyhmedusa ( 4 )
Iff.IIB1.81IUI.1..
Centrolenidae: Hyalinab.tr.ch.~rn(1).
. . . . . . . . . . . . . . . . tI MBIBUB~8..~8R..
Leptodactylidae: LeptodacQlus (14).
B.8I11WRIIUU1IIII
Chthonobatrachia . .Ceratophryidae: . . . . . . . . . . . . . . . . . . . .g. . . Lepidobatrachus (3), Telmatobius (15).
.................a
Ceratophtys (2.. Chacophrys (1..
IIIllNmMlmE..l.8.ltEI.
Cycloramphidae:Alsodac ( 5 ) , Eupsophus ( 3 ) , Hylo7ina (l), Limnomedusa ( l ) , Odontophrynus (6), Proce~atophlys(2), Rhinod(1).
.IUIN.I11..l1B..BE~
Bufonidae: Chuunus (17), Melanophryniscus (IO), Nannoplrryt~(1).
B.liRl.l.U.88R..BHI.
Nobleobatia
RIIUl.UN.ll.8URUm.I.I IlimBPIIBI.. BImS.IU8.Im .I.lr.D.iD.D
Hylodidae: Cmssodacfylus (2).
Ranoides Allodapanura
Microhylidae: D-tonotus
( l ) , Elnchistockir (2).
LAVILLA and HEATWOLE: AMPHIBIAN CONSERVATION AND DECLINE IN ARGENTINA
33
Telmatobius rubigo: This species was described by Barrionuevo and Baldo (2009) from Laguna de 10s Pozuelos, in Jujay Province. Rhinella amrai: This species, originally described by Gallardo (1965) as Bufo granulosus azarai, was incorporated into the Argentine batrachofauna by Narvaes and Rodriguez (2009). Melanophryniscus krauckzuki: This species was described by Baldo and Basso (2004) and at present is known from only five localities in the southern part of Misiones Province, and its presence in Paraguay is highly probable (Brusquetti and Lavilla, 2006). Elachistocleis skotogaster: This species was described by Lavilla et al. (2003) and at present is known only from 1 100 m at the type locality Los Toldos in the Department of Santa Victoria, Salta, although its presence in montane forest of southern Bolivia is probable. B. Amphibians Excluded from the Argentine Batrachofauna Melanophyniscus stelzneri dorsalis: As established by Lavilla et al. (2002), the individuals considered under this name correspond to an entity close to Melanophryniscus atroluteus. Melanophyniscus rubriventris subconcolor and M. K toldosensis: According to Vaira (2002), these subspecies seem to be invalid and are included in the synonymy of the nominal taxon, Melanophryniscus rubriventris. Alsodes muntlcolu: The Argentine populations attributed to this species ought to be considered as Alsodes aemcosus (Carmen ~ b e d a personal , communication). Ezrpsophus roseus: The individuals attributed to this species have been demonstrated to belong to Eupsophus calcaratus (Lavilla et al. 2002). Eupemphix nattereri: The presence of this species in Argentina is not supported by reference specimens. The citation for the locality of La Reserva Ecol6gica El Bagual (Formosa) (as Physalaemus, Yanosky et al. 1993), based on specimen REB A-20600, corresponds to Physalaemus bilzgonigerus (Lavilla et al. 2002). Zachaenus roseus: This species was never considered as belonging to the Argentine frog fauna in summaries for the country, e.g., Berg (1896-97), Freiberg (1942), Cei (1956, 1980, 1987), Gallardo (1987a, b, 1988), Gallardo and Olmedo (1992), Lavilla (1994 "1992"), Lavilla et al. (2000), and Lavilla and Cei (2001). Nevertheless, in his original description, Cope (1890) established the type locality as "Port Otway, Patagonia" in the "Confederaci6n Argentina", and this attribution still persists today (e.g., Cochran 1961; Frost 1985, 2004). Port Otway, an old name for present-day Puerto Barroso, is located on the Chilean coast (46'49's; 75"21w). Lynch (1971) considered it as a species inquirenda given that the namebearing type was damaged, its characters rendered difficult to discern, and the observable attributes and those used in the original description clearly do not belong to the genus Zachaenus. Scinax castroviejoi: The presence of this taxon has not been reliably recorded for Argentina (Lavilla et al. 2002); the Argentine paratypes of this species overlap with the variability of Scinax fuscovarius (De la Riva et al. 2000). Pseudis paradoxus occzdentalis: Included in the synonynly of Pseudis platensis by Aguiar et al. (2007). Elachistocleis ovalis: According to Lavilla et al. (2003) the distribution of this species is restricted to northern South America; in this genus, the Argentine forms with a pure yellow venter should be referred to Elachistocleis bicolor. C. Amphibians Doubtfully Retained in the Argentine Batrachofauna
Alsodes vemcosus: This name doubtfully encompasses the populations of ALodes from the provinces of Neuquen and Rio Negro (Carmen ~ b e d a personal , communication).
AMPHIBIAN BIOLOGY
34
Crossoductylus dispar: This species is included in the Argentine batrachofauna on the basis of specimen IBA-0700, reported by Cei and Roig (1961). Since that date this taxon has not been recorded from Argentina, its identification raises doubts, and the reference specimen is apparently lost. Melanophryniscus tumifrons: This name doubtfully encompasses one population of Melanophyniscus from Misiones (probably a new species) characterized by the presence of a nasal protrusion. Physalaemus gracilis: According to Kwet and Di Bernardo (1999), the taxon considered under this name in Misiones is a new, but undescribed, cryptic species. Telmatobius cf. marmoratus: This species was included in the Argentine batrachofauna by Gallardo (1962a), based on individuals from Jujuy Province. Argentine populations of this polytypic species, widely distributed in Bolivia and southern Peh, are currently under revision (SebastiBn Barrionuevo, personal communication). D. Synonymies
Ischnocnema henselii: Kwet and Sol6 (2005) established that the populations previously considered as Eleutherodactylus guentheri occurring in the subtropical Atlantic rainforest and the Araucarza forest of Rio Grande do Sul and Santa Catarina (Brazil), and Misiones (Argentina) belong to Eleutherodactylus henselii. Later, Hedges et al. (2008) transferred the species to the genus Ischnocnema. Oreobates discoidalis: Hedges et al. (2008) transferred the taxon previously known as Eleutherodactylus discoidalis to the genus Oreobates. Leptoductylus plaumanni: Kwet et al. (2001) definitively established the priority of the name Leptodactylus plaumanni over Leptodactylus geminus. Scinax granulatus: Kwet (2001) established priority of the name Scinax granulatus over Scinax eringiophilus. Oreobates discoidalis: Hedges et al. (2008) transferred the taxon previously known as Eleutherodactylus discozdalis to the genus Oreobates. Pseudis, Lysapsus and Podonectes: Garda and Cannatella (2007) proposed the resurrected name Podonectes for the species considered here as Pseudis minutus plus the Brazilian taxon l? cardosoi. Later, Aguiar et al. (2007) concluded that the genus Pseudis (including Pseudis minutus and l? cardosoi) is not a monophyletic group with respect to Lysapsus and suggested the need to synonymize these genera in a single genus (Pseudis), the scheme followed here. Pseudis limellum: See previous comment. Pseudis platensis: Aguiar et al. (2007) suggested that all the subspecies previously included in Pseudis paradoxus must be considered as full species, the scheme adopted here. Phyllomedusa azurea: Caramaschi (2006) considered the taxon previously known as Phyllomedusa hypochondrialis azurea to be a full species. Rhinella major: Narvaes and Rodriguez (2009) considered the taxon previously known as Rhinella granulosa major to be full species. Rhinella o m t u : Argentine populations previously considered under the name Bufo crucijiu belong to this species, according to Baldissera et al. (2004). Rhinella schneideri: Gallardo (1962 b) considered, tentatively, that the name Bufo schnezderi has priority over Bufo paracnemis. The synonymy was definitively established in the Global Amphibian Assessment (IUCN et al. 2004)
E. Changes in Generic Names and Categories Recent papers (e.g., Duellman 2001; Haas 2003; Faivovich et al. 2005, Frost et al., 2006; Grant et al. 2006; Aguiar et al., 2007; Chaparro et al., 2007; Hedges et al., 2008) have
LAVILLA and HEATWOLE: AMPHIBIAN CONSERVATION AND DECLINE IN ARGENTINA
35
considerably altered the traditional taxonomic arrangement for amphibians. The newer schemes are followed here and their equivalencies with that presented by Lavilla and Cei (2001) are presented in Appendix 2 for the Argentine batrachofauna. 111. GEOGRAPHY OF ARGENTINA
The following summary was taken from various sources, including Chiozza and Figueira (1981), Clarin (1996) and CIA (2006). Argentina occupies the majority of the surface of southern South America. The extreme geographic limits of the country are the confluence of the Rio Grande de San Juan and the Rio Mojinete (Jujuy Province) in the north (21°46'S; 66"13'W), Horn Island (Tierra del Fuego Province) in the south (55'58's; 6'7"16W), a point to the northeast of Bernardo de Irigoyen (Misiones Province) in the east (21'15's; 53'38'W) and the Mariano Moreno Mountains (Santa Cruz Province) in the west (49'33's; 73'35'W). The country's land surface area is approximately 2 791 810 km2 (excluding the southern islands and Antarctic claims, with a collective area of 965 597 km2), making it the eighth largest country of the world. It has a perimeter of 14 493 km, of which 9 3'76 km constitutes borders with five other countries (Chile, Bolivia, Paraguay, Brazil and Uruguay), with the remaining 5 11'7 km being the coastlines of the Rio de La Plata and Mar Argentino (southern Atlantic Ocean immediately adjacent to Argentina). The human population (as of June 2002) was estimated to be 37 820 000 inhabitants, with a growth rate of 1.13%. The population is unevenly distributed and mainly aggregated in the large cities (e.g., Buenos Aires and its suburbs houses 42.6% of the country's inhabitants) and the ratio of urban to rural population is 8'7:13. A. Geophysical Regions h Argentina Eight geophysical regions, characterized on the basis of relief, climate and resources, are recognized for Argentina (Fig. 1). Of these, six are of interest from the standpoint of amphibian biology; two, Mar Argentino and Antarctica, lack amphibians. 1 . Llanura Platense
This region occupies the northeastern part of the country and has a surface area of about 1200 000 km2. It is bounded on the north by the Pilcomayo, Paraguay and Alto Parani rivers, on the south by the Colorado River, on the east by the Uruguay and de la Plata rivers and Mar Argentino, and in the west it grades into the piedmont of the mountains of neighbouring regions. Five subregions are included: Chaco, Esteros Correntinos, Pampa, Lomadas Entrerrianas and Planicie Deltaica. It occupies parts of the provinces of Salta, TucumBn, Santiago del Estero, Cbrdoba, San Juan, La Pampa, Buenos Aires and Corrientes, and all the area of Formosa, Chaco, Santa Fe, and Entre Rios. The relief is a general plain (with some areas flat and others undulating), with a landscape of emergent lands alternating with swamps, ponds and salt flats. 2. Subtropical Plateau
Located in the extreme northeastern part of Argentina, the Subtropical Plateau is wedged between Paraguay and Brazil, and its limits coincide with the political boundaries of those countries; the Aguapey River separates it from the Esteros Correntinos of the former region. It occupies all of Misiones Province and part of Corrientes and has an undulating r e k E with maximum elevations slightly below 1 000 m.
This region occupies the northwestern angle of Argentina and comprises three subregions: Puna, the Cordillera Oriental and the Sierras Subandinas. It occupies part of J+, Salta, Tucumh and Catamarca, and its relief consists of high plateaus (3 000-3 500 m), mountain chains, ravines and valleys.
AMPHIBIAN BIOLOGY
GEOPHYSICAL REGIONS Llanun Piatense = P k h = suebopicsl Mcdlwe&t
C u p PsmprnSirmr
P&qmia
Fig. l . Geophysical Regions of Argentina. Modified from ClarIn (1996).
LAVILLA and HEATWOLE: AMPHIBIAN CONSERVATION AND DECLINE IN ARGENTINA
37
4. CU?O
In western Argentina, this region extends from the extreme southern part of Puna to the 37th southern parallel. It occupies parts of the provinces of San Juan, Mendoza, and San Luis. Mountain chains, culminating in the peak of Aconcagua (6 959 m), dominate the region.
In the centre of the country, this region occupies parts of the provinces of TucumBn, Catamarca, La Rioja, Santiago del Estero, Cbrdoba, San Luis and San Juan. Mountain chains separated by fields or small basins ("bolsones") predominate. The highest peaks are General Belgrano (6 250 m) in La Rioja, and Nevado del Aconquija (5 550 m) in TucumBn. 6. Patagonia
Patagonia occupies the territory to the south of the Colorado River, including the provinces of Neuquen, Rio Negro, Chubut, Santa Cruz and Tierra del Fuego. Two structurally different areas are recognized: Andean Patagonia, consisting of mountain chains separated by valleys and Extra-Andean Patagonia with a complex morphology of terraced plateaus, ridges, depressions and fluvial valleys. IV. BIOGEOGRAPHY OF ARGENTINA
According to the classic studies of Cabrera (1971, 19'76)and Cabrera and Willink (1973), five biogeographic domains are recognized for Argentina, of which three (excluding Subantarctica and Antarctica) are important for amphibians (Fig. 2). A. Neotropical Region
'
The Neotropical region extends from the Sonoran Desert at the border between the United States and Mexico to the southern limit of continental South America, but excluding a narrow band on each side of the Andes in the southern part of Argentina and Chile, as well as the large island of Tierra del Fuego and its associated southern islands. It has been divided into five Domains: Caribe, Guayano, Amazonian, Chaquefio and Andino-Patag6nico. Only the last three occur in Argentina. l . Amazonian Domain
Extending over a wide area in South America, the Amazonian Domain is divided into nine biogeographic provinces (not to be conksed with the political provinces); two of these biogeographic provinces are present in Argentina. It is marginally represented in the country with ingressions in the northwest along the pre-cordilleran mountains (Yungas province) and in the northeast, extending over Misiones and Northeastern Corrientes (Paranaense Province). h YUNGAS PROVINCE
In Argentina the Yungas biogeographic province extends as a narrow band with a northsouth orientation along the eastern slopes of the mountain chains of the political provinces of Jujuy, Salta, Tucumhn, and Catamarca. It is limited in the east by Chaco Province and in the west by Prepuna andlor Puna provinces. The climate is hot and humid, with predominantly summer rains that can reach 2 500 mm annually (up to 3 000 mm in some regions). It can snow in winter. The landscape consists of mountain slopes and the undulating plains of the piedmont. Soils typically have three horizons and are predominantly acidic-The vegetation has, in general, the appearance of cloud forest.
Three large districts are recognized: (1) A district of transitional forests (Selvas de T-n) occupies the undulating plains of the piedmont and the low hills between 350 m and 300 m, (2) the montane forest district (Selvas Montanas) occurs on the slopes, between 300 m and 1 200 m-, and (3) the montane woodland district (Bosques Montanos) is found on the higher slopes between l 000 m and 2 300 m.
AMPHIBIAN BIOLOGY
BIWEWRAPHY OF ARGENTINA AMAZONIAN DOMAIN Yungas Prov~nce Paranaenso Pronnca CHACOAN M)yAm Chrcorn Prevmw E~plnalProvincr Propuna Provlntx Monk Provinw Pampan Prownce ANDEAN-PATAOMJIAN DOMAIN H~ghAndean Provlntx Punr Provlnce Patagonirn Provlnce
Fig. 2. Biogeography of Argentina. From Cabrera and Willink (1973)
SUBANCTARTIC BC3MAlN Suknctarbc Prov~ner Insular Pronntw
LAVILLA and HEATWOLE: AMPHIBIAN CONSERVATION AND DECLINE IN ARGENTINA
39
B. PARANAENSE PROVINCE
In Argentina, the Paranaense biogeographic province occupies all the area of the political province of Misiones and the northeastern part of Corrientes. The climate is hot and humid, with rains throughout the year. In some places annual precipitation reaches 2 000 mm. Mean temperatures oscillate between 20" and 21°C. The landscape is of low mountain ridges and plains; red, acidic soils are characteristic. The dominant vegetation types are forests and savannahs. Two districts with different climax communities are recognized: (1) a district of mixed forest that occupies almost all of the political province of Misiones, and (2) a district of open fields ("campos") that occur in southeastern Misiones and northeastern Corrientes. 2. Chacoan Domain
This Domain corresponds, in general, with the lowlands of South America between the Amazonian and Andean-Patagonian domains. It has been divided into six provinces, five of which are represented in Argentina, where they occupy the greatest part of the country. A. PREPUNA PROVINCE
In Argentina, this biogeographic province occurs in the political provinces of Jujuy, Salta, Tucumhn, Catamarca, and La Rioja. The landscape is of mountain slopes and ravines, with very loose, immature stony or sandy soils, between 2 000 m and 3 400 m, although it can occur notably lower in some regions, with its elevational limits varying according to latitude. From north to south it is bordered in the east successively by Yungas, Chaco, and Monte provinces. The climate is hot and dry. Precipitation, not exceeding 200 mm annually, falls exclusively in summer. The vegetation in general is shrubby, low and sparse, but there are also cardonales (formationsrof arborescent cacti) and cushions of bromeliads. Four principal communities are recognized: (1) A shrubby steppe, dominated by legumes, grasses and cacti, is established on gentle slopes, (2) "cardonales", dominated by arborescent cacti as well as by bromeliads and shrubs, (3) dwarf woodlands, located on ravines or following river courses, and (4) cushions of bromeliads, typically on rocky, steep slopes. B. CHACOAN PROVINCE
In Argentina, the Chacoan biogeographic province occupies all of the political provinces of Formosa, Chaco and Santiago del Estero, the east of Salta, Jujuy, Tucumhn and Catamarca, the west of Corrientes, and the north of C6rdoba and Santa Fe, and smaller areas extending into La Rioja and San Luis. The climate is hot and dry, with precipitation almost exclusively in summer, sparse in the western part of the region and abundant in the east. The landscape in general is of plains with some depressions; in the west are low ridges. The soils are sedimentary. The vegetation varies from formations with trees of large stature (commonly deciduous xerophytes) and grasslands, palm groves, savannahs, "cardonales" and halophytic steppes. Four different climax communities are recognized: (1) The Eastern Chaco District, in the east of Formosa and Chaco, the west of Corrientes and the north of Santa Fe, is the most humid of all; (2) the Western Chaco District occupies the west of Formosa and Chaco, the northwest of Santa Fe, the east of Salta, Jujuy, Tucumhn and Catamarca and includes almost all of Santiago del Estero; (3) the Chacoan Serrano District, with a north-south orientation, runs through the most eastern slopes and ridges of Jujuy, Salta, Tucumhn and Catamarca, and extends toward La Rioja, C6rdoba and San Luis; (4) finally, there is a district of savannahs in the north of Santa Fe. C. MONTE PROVINCE
In Argentina, the Monte follows a wide curve that goes from Yocavil Valley in the political provinces of Salta and Tucumhn and continues through Catamarca, La Rioja, San Juan, Mendoza, NeuquCn, La Pampa, Rio Negro and Chubut. The climate is dry with annual precipitation not exceeding 200 mm. The northern part is hot with summer rains, whereas the southern portion is cool with rains in the winter and spring. The landscape is of plains,
40
AMPHIBIAN BIOLOGY
small basins ("bolsones"), mountain slopes and plateaus. The soils are generally sandy but there are also salt flats and rocky areas. The predominant vegetation is a xerophilic, shrubby steppe, but annual plants, succulents and perennials also form climax communities, among which the jarillal (formations where the jarillas [Larrea spp.] are dominant) and thorny steppe can be distinguished. D. ESPINAL PROVINCE
In Argentina, the Espinal Province forms an arc that goes from the centre of Corrientes and north of Entre Rios through Santa Fe, C6rdoba San Luis, La Pampa and Buenos Aires. It is located between the Chacoan and Monte provinces. The climate varies from hot and humid to temperate and dry, with most of the rain in summer. It is a landscape of plains, with some low, scattered mountains; the soils are sandy or of loess. The vegetation varies from large trees (xerophilic and deciduous woodlands) to shrubby steppes, palm groves and grasses. Three districts with different climax communities are recognized: (1) The ~ a n d u b a ~ District in Corrientes, Entre Rios and Santa Fe, with various woodlands, palm groves, grassy steppes and scrubland, (2) the Algarrobo District in the centre of Santa Fe and Cordoba to the northern part of San Luis, characterized by forests and in some regions by grassy meadows, and (3) the CaldCn District that occupies the centre of San Luis, La Pampa and the south of Buenos Aires, characterized by a caldCn forest (Prosopk caldenia, now reduced to critical levels), together with grassy steppes and scrubland. E. PAMPAN PROVINCE
In Argentina the Pampan biogeographic province occupies a large part of the political province of Buenos Aires and the southern portions of Entre Rios, Santa Fe and Cordoba, eastern La Pampa and a small part of San Luis. It is located between the province of Espinal and the Atlantic Ocean. The climate is warm-temperate. There is a north-south gradient in precipitation with rainfall occurring all year long. The landscape is of plains with some low ridges. The soil varies from black and very fertile to rocky or sandy. Grassy steppes dominate the vegetation. Four different districts with different climax communities are recognized: (1) The Uruguayan District in the north of Buenos Aires, south of Santa Fe and southeast of Entre Rios, dominated by grasslands; (2) the Eastern Pampan District in the northeast of Buenos Aires to the ridges of Olavarria, where grasslands and beds of rushes, and reeds are frequent; (3) the Western Pampan District in the northwest of Buenos Aires, the northeast of La Pampa and the south of Cordoba, dominated by grasslands; and (4) the Southern Pampan District in the province of Buenos Aires, from the ridges that define the limit of the Eastern Pampan District to the vicinity of Bahia Blanca in the south; vegetation consists mainly of tall grasses, that leave spaces of bare soil between them. 3. Andean-Patagonian Domain
The Andean-Patagonian Domain occupies the intermediate and high regions of mountains in northern and western South America from Venezuela to Tierra del Fuego, and descends to include the Patagonian steppe from the west of the Argentine provinces of NeuquCn and Rio Negro to Santa Cruz. It has been divided into five biogeographic provinces, three of which are represented in Argentina. A. PUNA PROVINCE
In Argentina the Puna biogeographic province goes through parts of the political Provinces of Jujuy, Salta, Tucumhn, Catamarca, La Rioja, San Juan and Mendoza. It occupies the high mountains and plateaus of the west up to 4 500 m; its lowest elevation varies from 2 000 m in the south to 3 400 m in the north. Its upper border is with the High Andean Province whereas its lower one is variable, being either with the Yungas, Prepuna or Monte Provinces. The climate is cold and dry with precipitation almost exclusively in summer; rainfall diminishes along a north-to-south gradient to areas that practically never receive
LAVILLA and HEATWOLE: AMPHIBIAN CONSERVATION AND DECLINE IN ARGENTINA
41
rain. The landscape is of mountains, plateaus and creeks. The soils are rocky or sandy and are very poor in terms of organic content. The vegetation is characteristically shrubby steppe, although herbaceous formations and very swampy areas also exist. The height of the dominant plants varies between 20 and 100 cm. There are several climax communities, of which bogs and marshes, formed by small plants that develop in water-logged soils, are fundamental in their relations to amphibians. B. HIGH ANDEAN PROVINCE
The High Andean biogeographic province occupies the high mountains in the west of Argentina from Jujuy to Tierra del Fuego. Its upper limit is defined by the end of continuous vegetation; its lower limit varies from 4 400 m in the north of the country to 500 m in Tierra del Fuego. The climate is cold and dry, with precipitation in the form of snow or sleet at any time of year. The typical landscape is of mountain peaks. The soils are rocky, stony or sandy, and are loose and very poor in organic matter except in the bogs that act as reserves of water. The characteristic vegetation is a steppe of grasses and other plants in plates and cushions. Three biogeographic districts, each with different climax communities, are recognized; (1) The High-Andean Quichua District from Jujuy to La Rioja, between 4 300 and 5 600 m, (2) the High-Andean Cuyano District from San Juan to the northern part of NeuquCn, between 2 200 and 4 500 m and (3) the High-Andean Austral District from the centre of NeuquCn to Tierra del Fuego, between 500 and 2 000 m. C. PATAGONIAN PROVINCE
The northern limit of the Patagonian Province follows an oblique line from the precordillera in the centre of Mendoza to the outflow of the Chubut River into the Atlantic Ocean. To the south thisrprovince reaches the northeastern part of Tierra del Fuego. In the east it is limited by the Atlantic Ocean and in the west by the High-Andean Province (from Mendoza to the centre of NeuquCn) and Subantarctic Province (from the centre of NeuquCn to Tierra del Fuego). The climate is dry and cold and during winter there are frequent snowfalls. The landscape is of plains, plateaus, gorges, and low mountains. The soils are generally poor and stony or sandy. The dominant vegetation is shrubby and herbaceous, but nevertheless there are halophilic steppes and bogs. Six districts with different climax communities have been recognized: (1) Payunia District, in southwestern Mendoza and northwestern NeuquCn, (2) Occidental District, that in the west extends discontinuously from NeuquCn to the north of Santa Cruz, (3) Central District, that occupies the centre of Rio Negro and Chubut and almost all of Santa Cruz, (4) Golfo San Jorge District, an herbaceous and shrubby steppe that surrounds the gulf that gives it its name, (5) the Subandean district, a narrow band that runs between the Subantarctic Province and the Occidental and Central districts, and (6) the Fueguian District in the north of Tierra del Fuego.
B. Antarctic Region The Antarctic Region includes the extreme southern part of South America, plus New Zealand and Antarctica, three land masses that are remnants of the southern part of Gondwana. Two dominions, Subantarctic and Antarctic, are recognized of which only the former is important in relation to amphibians. 1 . Subantarctic Domain
The Subantarctic Domain extends as a narrow band on each side of the Andes, from approximately 35" to 38" S; between those parallels it occupies all of the Chilean territory and the Atlantic slopes of the Cordillera de 10s Andes to the Strait of Magellan, Tierra del Fuego and the neighbouring Atlantic and Pacific islands. This domain has been divided into three provinces, two of which are represented in Argentina; only one of these is important in relation to amphibians.
AMPHIBIAN BIOLOGY
ECO-REGIONS OF ARGENTINA
=HighMOan Imaanelrn =Y#%rafUrrrvnrnd-
Campor md M.kpks D Pategarkn Fonrt
-p-
Fig. 3 . Eco-regions of Argentina. From Burhrt
et
al. (1999).
LAVILLA and HEATWOLE: AMPHIBIAN CONSERVATION AND DECLINE IN ARGENTINA
43
A. SUBANTARCTIC PROVINCE
In Argentina the Subantarctic Province occupies a thin slender band in the west, between NeuquCn and Tierra del Fuego. The climate is humid temperate in the north and cold in the south; there is frost throughout the year and it snows in winter. The landscape is mountainous with valleys and lakes. The soils are rocky with a very fertile superficial layer. There are deciduous as well as evergreen woodlands. Four districts with different climax communities are recognized: (1) PehuCn District to the west of NeuquCn, (2) Bosque Caducifolio District from the south of NeuquCn to Tierra del Fuego, (3) Valdiviano District, represented in Argentina by a small, discontinuous area in NeuquCn, Rio Negro and Chubut, and (4) Magellanic District composed of disjunct areas in Santa Cruz and Tierra del Fuego.
V THE ECO-REGIONS OF ARGENTINA There are at least three proposals for subdividing Argentina into eco-regions. Two of these (Dinerstein et al. 1995 and Olson et al. 1998) were created to cover all of Latin America and the Caribbean, but the third (Burkart et al. 1999) focussed exclusively on Argentina. These three schemes differ in some cases, especially regarding the divisions proposed for the northeastern and central parts of Argentina. Using as a base the eco-regions of Burkart et al. (1999) (Fig. 3), selected because of their more comprehensive characterizations and for having been used in analyses of other taxa in Argentina (e.g., mammals; Parera [2002]). Table 2 compares different available models. The table excludes three eco-regions (South
Table 2. Equivalency of the eco-regions proposed for Argentina by different investigators. Burkart et al. (1999)
Dinerstein et al. (1995)
High Andean
Central Andean Puna (part) Central Andean Puna (p) + Southern Andean Steppe
Puna
Central Andean Puna (p) Central Andean Dry Puna (p)
Monte de Sierras and Bolsones
Cordoba Montane Savannahs (p) +Argentine Monte (p)
Argentine Monte (p)
Yungas Forest
Andean Yungas
Andean Yungas
Dry Chaco
Chaco Savannahs + Cordoba Montane Savannahs (p)
Chaco + Arid Chaco Montane Savannahs
Humid Chaco
Humid Chaco (p)
Humid Chaco (p)
Paranaen Forest
Brazilian Interior Atlantic Forest (p) + Brazilian Araucaria Forest
Parana-Paraba Interior Forest + BraziIian Araucaria Moist Forest
Esteros of IberP
Humid Chaco (p)
Humid Chaco (p)
Olson et al. (1998)
+
+
+
Central Andean Dry Puna (p) + Central Andean Dry Puna (p) + Southern Andean Steppe Central Andean Puna (p) Central Andean Dry Puna (p)
+ Cordoba
Campos and Malezales
Brazilian Interior Atlantic Forest (p)
Mesopotamian Savannahs (p)
Delta and Islands of the Paranh River
Parana Flooded Savannahs
Parana Flooded Savannahs
Espinal
Argentine Espinal + Pampas (p) Pampas (p) + Mesopotamian
Argentine Espinal (p) + Semi-Arid Savannahs (p) Argentine Espinal (p) + Humid Pampas Semi-Arid Pampas (p)
Pampan
+
Monte de Llanuras and Mesetas
Argentine Monte (p) Pampas (P)
Argentine Monte (p) + Semi-Arid
Patagonian Steppe
Patagonian Grasslands Patagonian Steppe + Southern Andean Steppe (p)
Patagonian Steppe + Southern Andean Steppe (p) + Argentine Monte (p)
Patagonian Woodlands
Subpolar Nothofagus Forest + Valdivian Temperate Forest
Subpolar Nothofap Forest Temperate Forest
+ Valdivian
44
AMPHIBIAN BIOLOGY
Atlantic Islands, Argentine Sea, and Antarctica) because no amphibians have been recorded from them. For an exhaustive account see Burkart et al. (1999), Bertonatti and Corcuera (2000), Parera (2002) and Brown et al. (2005). A recent review by Brown and Pacheco (2006) does not significantly alter the original scheme, at least in relation to amphibians.
A. High Andean Eco-Region In Argentina, the High Andean Eco-Region extends throughout the western parts of the political provinces of Jujuy, Salta, Catamarca, La Rioja, San Juan, Mendoza and the extreme northwestern part of NeuquCn. It coincides in general with the High-Andean Quichua and High-Andean Cuyano districts of the High-Andean biogeographic provinces (see above). The amphibian fauna is relatively scant, only Rhinella spinulosa spinulosa, Pleurodema cinereum, l? marmoratum, Telmatobius contrerasi, and 7: hau.thali having been recorded. The two species of Telmutobius are highly localized endemics (known only from their type localities) whereas the rest have wider distributions along the Cordillera de 10s Andes and associated mountain chains. B. Puna Eco-Region
In Argentina, the Puna Eco-Region extends through the high plateaux and mountain slopes in the western parts of Jujuy, Salta, Tucumfin, Catamarca, La Rioja and the northern part of San Juan, from 3,000 m upward. It coincides in general with the Puna and the more elevated parts of the Prepuna biogeographic provinces (see above). The batrachofauna includes a relatively high number of endemics (Rhinella gnustae, Telmatobius atacamensis, 7: hypselocephalus, 7: laticeps, 7: pinguiculus, T pisanoi, 7: platycephalus, 7: rubigo, 7: scrocchii, 7: schreiteri) as well as species with wider distributions, such as Rhinella spinulosa spinulosa, Telmatobius aff. marmoratus, Hypsiboas andinus, Pleurodema cinereum, and P marmoratum. C. Monte of Sierras and Bolsones Eco-Region
In Argentina, this eco-region is present from the southern part of Salta, through Catamarca, La Rioja and San Juan, to northern Mendoza. It coincides with the northern part of Monte and with the lower regions of the Prepuna biogeographic provinces (see above). The batrachofauna shows a great similarity with that of the other semi-arid regions of Argentina (Hypsiboas andinus, Chacophrys pierottii, Lepidobatrachus llanensis, Leptodactylus bufonius, L. chaquensis, Odontophrynus occidentalis, Pleurodema guayapae, l? nebulosum, I? tucumunum), but is set apart by two endemics (Hypsiboas riojanus and Odontophrynus barrioi). D. Yungas Forest Eco-Region
In Argentina, the Yungas Forest Eco-Region is located on the eastern slopes of the extraAndean mountainous region of the political provinces of Salta, Jujuy, Tucumfin and Catamarca, and coincides with the Yungas biogeographic province. The batrachofauna is rich, sharing some taxa with the Chaco that borders it to the east (Rhinella arenarum arenarum, R. schneideri, Hypsiboas andinus, H. raniceps, Scinax fuscovarius, S. nasicus, Trachycephalus venulosus, Phyllomedusa sauvagii, Leptodactylus bufonius, L. chaquensis, L. elenae, L. fuscus, L. gracilis, L. latinasus, L. mystacinus, Odontophrynus americanus, Physalaemus biligonigerus, l? cuquz, Pleurodema borelli, P tucumanum), with upper regions (Rhinella spinulosa spinulosa), and with other forested regions of Argentina or neighbouring countries (Phyllomedusa boliviana, Dendropsophus minutus, D. nanus), as well as a relatively high number of strictly endemic species (Rhinella gallardoi, R. rumbolli, Melanophryniscus rubriventris, M. stelzneri spegazzinii, Gastrotheca christiani, G. chrysosticta, G. gracilis, Hypsiboas marianitae, Oreobates baritmnsis, 0. discozdalis, Telrnatobius ceimm, 7:oxycephalus, i? stephani, and Elachistocleis skotogaster). E. Dry Chaco Eco-Region
The Dry Chaco is an immense plain that covers almost all of the province of Santiago del Estero, eastern Salta, Jujuy, TucumAn and La Rioja, extreme southwestern San Juan,
LAVILLA and HEATWOLE: AMPHIBIAN CONSERVATION AND DECLINE IN ARGENTINA
45
northern San Luis, northwestern C6rdoba and western Chaco, Formosa and Santa Fe. It largely coincides with Western Chaco and Chacoan Serrano districts of the Chaco biogeographic province (see above). The batrachofauna is rich (Rhinella arenarum arenarum, R . bergi, R . fernandezae, R . major, R. schneideri, Melanophryniscus klappenbachi, Dendropsophus minutus, D. nanus, Hypsiboas andinus, H. raniceps, Pseudis limellum, Pseudis platens&, Scinax acuminatus, S. fuscovarius, S. nasicus, S. squalirostris, Trachycephalus uenulosus, Phyllomedusa azurea, P boliviana, I? sauvagii, Ceratophrys cranwelli, Chacophrys pierottii, Lepzdobatrachus asper, L. laevis, L. llanensis, Leptodactylus bufonius, L. chaquensis, L.elenae, L. fuscus, L. gracilis, L. laticeps, L. latinasus, L. mystacinus, L. ocellatus, L. podicipinus, Odontophrynus americanus, 0. lavillai, 0. occidentalis, Physalaemus biligonigerus, P cuqui, Pleurodema borelli, l? guayapae, P nebulosum, I? tucumanum, Pseudopaludicola boliviana, Dermatonotus muelleri, and Elachistocleis bicolor) although the number of endemics (Rhinella achalensis, Melanophryniscus stelzneri stelzneri, Hypsiboas cordobae, Odontophrynus achalensis, 0 . cordobae, Pleurodema cordobae, P kriegi) is relatively low. E Humid Chaco Eco-Region
The Humid Chaco Eco-Region is found in eastern Formosa and Chaco, northern Santa Fe, northwestern Corrientes, and a small part of east-central Santiago del Estero. It is mainly located to the west of the Paraguay-Paran5 river system in the Eastern Chaco District. The batrachofauna is rich and has a number of species in common with neighbouring eco-regions (Chthonerpeton indistinctum, Rhinella arenarum arenarum, R. bergi, R . fernandezae, R . major, R. schnezderi, Melanophryniscus atroluteus, M. cupreuscapularis, Dendropsophus nanus, D. sanborni, Hypsiboas albopunctatus, H. caingua, H. pulchellus, H. punctaus rubrolineatus, H. raniceps, Pseudis limellum, Pseudis minutus, I? platensis, Scinax acuminatus, S. fuscomarginatus, S. fuscovarius, S. nasicus, S. squalirostris, Traghycephalus venulosus, Phyllomedusa azurea, P sauvagii, Ceratophrys cranwelli, Lepzdobatrachus asper, L. laeuis, L. llanensis, Leptodactylus bufonius, L. chaquensis, L. diptyx,, L. elenae, L. ficus, L. gracilis, L. laticeps, L. latinasus, L. mystacinus, L. ocellatus, L. podicipinus, Odontophrynus americanus, 0. lavillai, Physalaemus albonotatus, I? biligonigerus, l? riograndensis, l? santafecinus, Pseudopaludicola boliviana, I? falcipes, I? mystacalis, Dermatonotus muelleri, Elachistocleis bicolor,), other species with relatively restricted distribution but present in similar formations in Paraguay (Melanophryn&cusklappenbachi, M. jkZuoguttatus), and one endemic (Hypsiboas varelae). G. Paranaen Forest Eco-Region
In Misiones, the Paranaen Forest Eco-Region concides to a large extent with the Paranaense biogeographic province. It is one of the areas with major biological diversity in Argentina, as confirmed by its batrachofauna (Luetkenotyphlus brasiliensis, Siphonops annulatus, S. paulensis, Rhinella azarai, R. icterica, R . ornata, R. schneideri, Melanophryniscus atroluteus, M. deuincenzii, M. krauczuki, M. aff. tumifrons, Aplastodiscus perviridis, Dendropsophus minutus, D. nanus, D. sanborni, Hypsiboas albopunctatus, H. caingua, H. curupi, H. faber, H. pulchellus, H. raniceps, H. aff. semiguttatus, Itupotihyla langsdor-i, Scinax aromothyella, S. berthae, S. fuscovarius, S. granulatus, S. nasicus, S. perereca, S. squalirostris, S. aff. uruguayus, Trachycephalus dibemrdo, T imitatrix, T venulosus, Phyllomedusa tetmplozdea, Crossodactylus dispar, C. schmidti, Ischnocnema henselii, hptodactylus bufonius, L. diptyx, L. elenae, L. fumrius, L. fuscus, L. gracilis, L. labyrinthicus, L. mystacinus, L. ocellatus, L. plaumanni, L. podicipinus, Limnomedusa macroglossa, Odontophrynus aff. americanus, Physalaemus albonotatus, P biligonigerus, P cuuieri, l? aff. gracilis, l? riograndensis, Pseudopaludicola falcipes, P mystacalis, Proceratophrys avelinoi, I? bigtbbosa, Hyalinobatrachium uranoscopum, Elachistocleis bicolor). All of its species have also been recorded from similar formations in neighbouring countries and/or in nearby eco-regions.
H. Esteros of Ibera Eco-Region The Esteros of Iberh Eco-Region occurs in northwestern Corrientes and coincides in large part with the portion of the East Chaco District of the Chaco biogeographic province that is located to the east of the Paranh River. Its amphibian fauna contains numerous
46
AMPHIBIAN BIOLOGY
species shared with other eco-regions (Chthonerpeton indistinctum, Ceratophrys cranwelli, Lepidobatrachus asper; Rhinella bergi, R . fernandezae, R. major; R . schneideri, Melanophryniscus cupreuscapularis, M. klappenbachi, Dendropsophus nanus, D. sanborni, Hypsiboas pulchellus, H. raniceps, Pseudis limellum, Pseudis platensis, Scinax acuminatus, S. berthae, S. fuscomarginatus, S. fuscovarius, S. nasicus, S. squalirostris, Trachycephalus venulosus, Phyllomedusa azurea, I? sauvagii, Lepidobatrachus asper, Leptoductylus bufonius, L. chaquensis, L. diptyx, L. elenae, L. JiLscus, L. gracilis, L. latinasus, L. mystacinus, L. ocellatus, L. podicipinus, Odontophrynus americanus, Physalaemus albonotatus, I? biligonigemts, I? riograndensis, I? santafecinus, Pseudopaludicola boliviana, I? falcipes, E! mystacalis, Dermatonotus muelleri, and Elachistocleis bicolor) but is set apart by two taxa (Argenteohyla siemersi pederseni and Pseudopaludicola mirandae). I. Campos and Malezales Eco-Region This eco-region coincides with the ~ a n d u b aDistrict ~ of the Espinal and the Campos District of the Paranaense biogeographic provinces in Corrientes. The batrachofauna (Chthonerpeton indistinctum, Siphonops paulensis, Rhinella azarai, Rhinella bergi, R. fernandezae, R. icterica, R . major; R. ornata, R. schneideri, Melanophryniscus atroluteus, Dendropsophus nanus, D. sanborni, Hypsiboas albopunctatus, H. caingua, H. pulchellus, H. raniceps, Pseudis limellum, Scinax acuminatus, S. berthae, S, fuscomarginatus, S. fuscovarius, S. nasicus, S. squalirostris, S. uruguayus, Trachycephalus venulosus, Leptodactylus chaquensis, L. elenae, L. JiLscus, L. gracilis, L. labyrinthicus, L. latinasus, L. mystacinus, L. ocellatus, L. podicipinus, Odontophrynus americanus, Physalaemus albonotatus, I? biligonigerus, I? cuvieri, I? riograndensis, Pseudopaludicola falcipes, I? mystacalis, and Elachistocleis bicolor) lacks endemics.
J. Delta and Islands of the Parana River This eco-region extends as a narrow band from north to south along the axis formed by the Paraguay, Paranh and La Plata rivers and their islands and flood-plains, along the coasts of the political provinces of Formosa, Chaco, Santa Fe, Buenos Aires, Corrientes and Entre Rios. It corresponds with the margins of several biogeographic provinces, including ~ of Espinal the West Chacoan District of the Chacoan Province, the ~ a n a d u b aDistrict Province and the Uruguayan District of Pampan Province. The amphibian fauna is rich (Chthonerpeton indistinctum, Rhinella arenarum arenarum, R. bergi, R. fernandezae, R. major, R . schnezderi, Dendropsophus nanus, D. sanborni, Hypsiboas pulchellus, H. punctatus rubrolineatus, H. raniceps, Pseudis limellum, Pseudis minutus, E! platensis, Scinax acuminatus, S.berthae, S. fuscomarginatus, S. fuscovarius, S. granulatus, S. nasicus, S. squalirostris, Trachycephalus venulosus, Phyllomedzlsa azurea, Leptodactylus bufonius, L. chaquensis, L. diptyx, L. elenae, L. fuscus, L. gracilis, L. latinasus, L. mystacinus, L. ocellatus, L. podicipinus, Odontophrynus americanus, Physalaemus albonotatus, I? biligonigerus, I? riograndensis, I? santafecinus, Pseudopaludicola boliviana, I? falcipes, E! mystacalis, Dermatonotus muelleri, and Elachistocleis bicolor) and lacks endemics. K. Espinal Eco-Region
The Espinal Eco-Region forms an arc that covers part of Corrientes, Entre Rios, Santa Fe, Cbrdoba, San Luis, La Pampa, Rio Negro and Buenos Aires political provinces and coincides, to a large extent, with the Espinal biogeographic province. The amphibian fauna of this eco-region consists of Chthonerpeton indistinctum, Rhinella arenarum arenarum, R . bergi, R. femndezae, R . majo?; R. schneideri, Melanophryniscus atroluteus, Dendropsophus nanus, D. sanborni, Hypsiboas pulchellus, Pseudis limellum, Pseudis platensis, Scinax acuminatus, S. berthae, S. jkcomarginatus, S. JiLscovarius, S. nasicus, S. squalirostris, Phyllomedusa azurea, Ceratophrys cranwelli, C. ornata, Leptodactylus bufonius, L. chaquensis, L. fuscus, L. elenae, L. gracilis, L. latinasus, L. mystacinus, L. ocellatus, Odontophrynus americanus, 0. cordobae, 0 . occidentalis, Physalaemus albonotatus, I? biligonigerus, I? fernandezae, E! riograndensis, Pleurodema nebulosum, I? tucumanum, Pseudopaludicola falcipes, I? mystacalis, and Elachistocleis bicolor; none is endemic. L. Pampan Eco-Region
The Pampan Eco-Region occurs in southern Entre Nos and Santa FC, southeastern Cbrdoba, northeastern La Pampa and in most of Buenos Aires, coinciding in large part
LAVILLA and HEATWOLE: AMPHIBLAN CONSERVATION AND DECLINE IN ARGENTINA
47
with the Pampan biogeographic province. Its batrachofauna (Rhinella arenarum arenarum, R. dorbignyi, R . fernaderne, Argenteohyla siemersi siemersi, Dedropsophus nanus, D. sanborni, Hypsiboas pulchellus, Scinax berthae, S. granulatus, S. nasicus, Pseudis limellum, Pseudis minutus, Ceratophrys ornata, Leptodactylus gracilis, L. latinasus, L. mystacinus, L. ocellatus, Odontophynus americanus, 0. occidentalis, Physalaemus biligonigerus, l? fernanderne, l? henselii, l?riograndensis, Pseudopaludicola falc$es, and Elachistocleis bicolor) lacks endemics. M. Monte of Llanuras and Mesetas Eco-Region
This eco-region occupies parts of Mendoza, San Luis, La Pampa, NeuquCn, Rio Negro and Chubut political provinces and coincides with the most southern part of the Monte biogeographic province. Its batrachofauna is poor (Rhinella arenarum arenarum, Ceratophrys cranwelli, Ltptodactylus bufonius, L. latinasus, L. ocellatus, Odontophrynus occzdentalis, Pleurodema nebulosum, and P tucumanum) and is set apart by only one endemic (Somuncuria somuncurensis) . N. Patagonian Steppe Eco-Region
The Patagonian Steppe Eco-Region occupies parts of Mendoza, NeuquCn, Rio Negro, Chubut and Tierra del Fuego, and almost all of Santa Cruz. It coincides in large part with the Patagonian biogeographic province. Its batrachofauna contains numerous endemics (Rhinella arenarum mendocinus, ALodes pehuenche, Atelognuthus patagonicus, A. praebasalticus praebasalticus, A. p. agilis, A. P. dobeslawi, A. p. luisi, A. reverberii, A. solitarius), and has only four taxa shared with other eco-regions or with Chile (Rhinella spinulosa papillosa, Pleurodema bufoninum, Alsodes gargola gargola, A. verrucosus).
0. Patagonian Woodland8 Eco-Region This eco-region extends as a narrow, discontinuous band through northwestern NeuquCn, Rio Negro, Chubut, Santa Cruz and Tierra del Fuego, and coincides with the Subantarctic biogeographic province. The batrachofauna shows species in common with that of similar environments in Chile (Rhinella rubropunctuta, Nannophyne variegata, Pleurodema thaul, Alsodes australis, Batrachyla antartandica, B. leptopus, B. taeniata, Eupsophus calcaratus, E. emiliopug-zni, E. vertebralis, Hylorina sylvatica, Rhinoderma durwinii) but shares few species with the Patagonian steppe (Rhinella spinulosa papillosa, Pleurodema bufoninum, ALsodes gargola gargola, A. verrucosus); five species are endemic to the Argentine portion of this eco-regi6n (Alsodesgargola neuquensis, Atelognuthus aff grandisonae, A. nitoi, A. salai, and Batrachyla fitzroya). VI. BATRACHOFAUNAL REGIONS OF ARGENTINA
Cei (1980), in a summary of what was known up to the mid-1970s, recognized seven fauna1 assemblages for the amphibians of Argentina (Southern Brazilian or Eastern Subtropical Forest; Chacoan; Andean; Patagonian; Andean-Antartican; Subandean and Litoral-Mesopotamian; Fig. 4), that correspond, in general, with the biogeographic and the physical geographic regions described above. Moreover, there have been different attempts to characterize particular faunas, such as those of the Andean Yungas (Lavilla et al. 2000 b), Chaco (Gallardo 1966, 1979), southern woodlands ( ~ b e d a1999) and central Argentina (~ridarolliand Di Tada 1994). There is, however, still no satisfactory, exhaustive biogeographic analysis of the Argentine batrachofauna. An all-embracing classification, carried out on a continental scale by Duellman (1999), divided South America into 12 regions, five of which (Cerrado-Caatinga-Chaco; PampasMonte; Patagonia; Southern Temperate Forest and Southern Andes) are present in Argentina. These divisions are not completely satisfactory when analyzing the batrachofauna at a regional level. This is not the place to conduct an exhaustive critique of this classification and it is sufficient merely to indicate that, as already established, the scheme under consideration:
AMPHIBIAN BIOLOGY
BATRACHOFAUNAL REGIONS
-
Southorn Brazilian
I Lilioral-Mesopotamian
slam
Pabganian Subdun 1Andwl l Andrrn-Andwticln
Fig. 4. Batrachofaunal regions of Argentina. Modified from Cei (1980)
LAVILLA and HEATWOLE: AMPHIBIAN CONSERVATION AND DECLINE IN ARGENTINA
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(1) Leaves aside the forests of the mountains of northwestern Argentina (Yungas Province) and the forests of Misiones Province in the northeast (Paranaense Province), in the sense of Cabrera (1971, 1976) and Cabrera and Willink (1973). These two biogeographic provinces have the highest species diversity, in relation to area, in the country. (2) The highlands of southern C6rdoba and northern San Luis, an area of notable endemism, are not defined with clarity. (3) The peculiarities in the amphibian fauna of the Chaco (with three divisions from the biogeographic standpoint) are diluted when considered together with the Caatinga and the Brazilian Cerrado. (4) The mountainous region of western Argentina, considered by Duellman (1999) as "Southern Andes", also presents problems when analysed on a regional scale. The faunistic similarity between its most southern portion (in Argentina and Chile) with the most southern parts of Bolivia and Peru is limited to a few species with broad ranges (Rhinella spinulosa spinulosa, Pleurodema cinereum, l? marmoratum and Hypsiboas andinus) and the differences not only take place along a latitudinal gradient but also the Pacific and Atlantic slopes of the Cordillera share extremely few taxa. Given the unsatisfactory nature of the models that have been proposed, it is preferrable to relate the distributions of amphibians to (1) eco-regions (see section V) as a biogeographic summary, as well as to (2) physical geographic regions (see section 111-A) in order to understand the threats that confront them. VII. PRINCIPAL ENVIRONMENTAL PROBLEMS I N ARGENTINA
Lavilla (2001, 2004) analysed the principal environmental problems detected in Argentina that can have an immediate effect on the batrachofauna. They can be grouped into seven categories, including (1) fragmentation andlor irreversible loss of habitat, (2) alteration of habitats through chemical or organic contamination, (3) introduction of exotic species, (4) diseases, ( 5 ) increase in ultraviolet radiation, (6) changes in global climate and (7) commercial exploitation. Although these categories can define the threats that confront any amphibian fauna in the World, they show regional peculiarities when analysed more exhaustively. A. Loss of Habitat
In this category are included (1) alteration of woodland environments, (2) converting of natural non-forested areas into agricultural fields or grazing lands, (3) alteration of wetlands and bodies of water, and (4) urban sprawl. 1 . Alteration of Woodland Environments
More110 and Mateucci (1999) indicated that from colonization to 1992 Argentina lost approximately 7'00 000 k m b f space occupied by native woody vegetation; this process has continued up to the present time at a sustained rate estimated to be 500 000 hectares per year (Bertonatti and Corcuera 2000). At present at least two types of disturbance to native woodlands are taking place: selective tree-felling and clear-felling A. SELECTIVE TREE-FELLING
The tree species that are exploited vary regionally, the most important being quebrachos (Schinopsis balansae, S. lorentzii, S. quebracho-colorado, Aspidosperma quebracho-blanco) and algarrobos (Prosopis alba, l? chilensis, P nigra, l? Jlexuosa) in the Chaco; caldkn (Prosopis caldenia), iiandubay (Prosopk algarrobilla) and tala (Celtk tala) in Espinal; retamos (Bulnesia retamo) in Monte; rauli (Nothofagus nervosa), lengas (Nothofagus pumilio) in the southern forests, an area were the alerces (Fitzroya cupressoides) and robles (Amburana cearensis) were also exploited until recent times; cedros (Cedrela lilloi), nogales ~uglansaustralis), palo blanco
50
AMPHIBIAN BIOLOGY
(Calycophyllum multzjlorum) and pal0 amarillo (Phyllostilon rhamnozdes) in the montane and transitional forests of the northwest; and araucarias (Araucaria angustijolia) and pal0 rosa (Aspzdosperma polineurum) in the Paranaen Forest. B. CLEAR-FELLING
Only citing the best-known examples, (1) large areas of the Chaco have been and are being transformed into areas cultivated for cotton and soybeans; (2) the lower storey of the montane forests in northwestern Argentina (Yungas), especially pal0 blanco forests, have been converted for cultivation of citrus, sugar cane, tobacco and vegetables (Vervoorst 1982; Prado 1995); (3) part of the forest in Misiones has been converted to cultivation of pine trees (Pinus elliotii); (4) in the Monte, some formations of hardwoods have been replaced by vinyards; (5) extensive areas of southern forest have been felled or burned to increase the area for grazing, and (6) the inundated forests of the delta of the Paran5 River have been destroyed locally for the development of agricultural and grazing activities (fruits, pulpwood for paper, horticulture, cattle). In addition to its direct action, tree-felling brings about indirect effects that eventually are harmful to amphibians, including aridity, erosion of soils, and edge effects, among others (Woodwell 1983; Salati and Vose 1984; Myers 1986). 2. Converting of Natural Non-Forested Areas into Agricultural Fields and Grazing Lands
According to information from the Nacional Institute of Statistics and Censuses (Instituto Nacional de Estadisticas y Censos; INDEC), in 2000 Argentina had 40.4 million hectares dedicated to agriculture, as well as 40 million cattle, 13.7 million sheep and 3.4 million goats. The greatest impact by agricultural activities is on the Pampan grasslands (the region that produces about 90% of the country's income from cereals and 53% of the income from other crops), Yungas (1l%), Paranaen Forest of Misiones (6%) and the Chaco (5%) (Di Pace et al. 1992, cited by Bertonatti and Corcuera 2000). The latter source also indicated that the Pampan and Espinal regions concentrate 80% of the cattle, followed by the Chaco (15%); fifty percent of the sheep are in the Patagonian Steppe, 30% in Pampas and Espinal, and 15% in Monte, whereas 35% of the goats are concentrated in the Chaco. Agriculture and grazing exert deleterious effects on the batrachofauna because of greater exploitation of soils and the concomitant loss of organic matter, increase in compaction, decrease in the water-holding capacity, and increase in contamination by agrochemicals, including pesticides and fertilizers (Solbrig 1999). 3. Alteration of Wetlands and Other Bodies of Water
The concept of "wetland" used here is restricted to the environments accessible to amphibians, and is based on the three characteristics distinguished by Mitsch and Gosselink (1986, cited by B6 and Quintana [1999]): (1) the presence of water, (2) soils with characteristics different from those of adjacaent areas and (3) plant species adapted to inundation. Environments that encompass these descriptions are distributed throughout the country and have received attention in recent times (Calcagno 1995; Olson et al. 1998a; Canevari et al. 1999). Six wetland regions are recognized (Canevari et al., 1999). Five of these (excluding the Patagonian Coastal Zone that comprises salty or brackish waters from which no amphibians are recorded) are analysed below, following the categories of Scout (1989) and Dugan (1992). A. MOUNTAINOUS REGIONS OF THE NORTHWEST
The most conspicuous habitats are the Andean bogs, comprised of a rich and highly diverse community of phanerogams. They constitute one of the rare high-altitude regions with water throughout the year, have isolated, presumably small, populations of amphibians,
LAVILLA and HEATWOLE: AMPHIBIAN CONSERVATION AND DECLINE IN ARGENTINA
51
and doubtless played an historically important role as areas of faunistic diversification (Lavilla 1988). The impact observed in this type of environment is due to overgrazing (sheep, goats, donkeys; occasionally cows), crops (potatoes, maize, exotic pastures), drainage, mass removal andlor contamination as a result of past and present mining operations, and extraction of blocks ("champas"), used as bricks in rudimentary houses and enclosures. One phenomenon of recent, very serious, alteration is the "traversing" by all-terrain vehicles (Lavilla, 2000) that destroys the thin vegetative cover and promotes local erosion. Although extremely important for the life of high-mountain amphibians, these fresh water bogs were not taken into consideration when considering the wetlands of Northwestern Argentina (exceptions are those on the brackish margins of some Andean lakes) (Sarmiento et al. 1999). Other bodies of water of the region include rivers, streams, lakes and ponds of freshwater or brackish water (both permanent and temporary) and thermal springs. Amphibians have not been recorded from the brackish water and there are few records from ponds, lakes and thermal springs. The impact in this type of environment is attributable to trampling by cattle, and the provision (actual and potential) of water for satisfying the needs of the increasingly numerous mining projects in the region. B. LA PLATA BASIN
La Plata basin encompasses the Argentine portion of the Paran5 River basin and its delta, the Uruguay River and La Plata River, and the Esteros of IberA and Aguapey-Mirifiay. There are different kinds of bodies of water, including rivers and streams, artificial reservoirs, (e.g., Yacireta, Salto), flood-plains and swamps. The principal problems that have been detected include alteration and channelling of watercourses, the advance of agricultural and grazing lands, fragmentation of various habitats, inadequate management and overexploitation of resourws, destruction of vegetation of the basin, introduction of exotic species (principally fish and mollusks), hydraulic works, the petroleum industry, contamination by the paper industry, urban expansion (the largest cities of South America are located in this basin), and uncontrolled tourism (Bonetto and Hurtado 1999). C. CHACO REGION
The aquatic environments identified in the Chaco region include rivers and streams, permanent and temporary ponds, continental hypersaline environments, marshes, interior deltas, dams and artificial drainage canals. The principal problems detected include the filling in of rivers, the drying up of swamps, contamination by heavy metals from mining developments (see section 5. A., below), agricultural and pastoral influences (use of agrochemicals, erosion through overgrazing, compaction by trampling), contamination by urban residues and industrial organic chemicals, deforestation of marginal areas, construction of dikes and dams, the extraction of water for urban use, and the transfer of basins (Bucher and Chani 1999; Lavilla, in press). Although most species of amphibians in the Chaco are not in any category of risk (Lavilla et al. 2000), some merit special attention because of their peculiarities. Of these one can distinguish the reduced taxocenosis of frogs that occur in saline environments in northern Cdrdoba (Di Tada, 1999). These should be conserved because of their unique value for physiological, ecological and behavioural studies. D. PAMPAN REGION
The Pampan Region has permanent and temporary ponds, continental hypersaline environments, marshes, rivers and streams in the mountains and on the plains, artificial drainage canals, and dams, among the environments suitable for amphibian life, as well as estuarine and coastal marine habitats in which amphibians are not found. The principal problems detected include the expansion of agriculture and grazing, urban growth (this region is the most heavily populated part of Argentina), and organic and inorganic contamination, habitat fragmentation, inadequate management and overexploitation of resources, transfer of basins, and the development of nuclear projects (Gdmez and Toresani 1999).
52
AMPHIBIAN BIOLOGY
E. PATAGONIA
In Patagonia there are lakes, ponds and marshes in different locations (steppe, forests, high mountains), streams and rivers and their overflow margins, permanent pools and temporary environments fed by rainwater in the steppes, forests, bogs and "rnallines" at various elevations. The term "bog" is restricted to the formation dominated by Sphagnum magellanicus, whereas the "mallines" (functionally similar to the wetlands of the high mountains) resemble the high-Andean phanerogamic bogs. The main problems detected include the destruction of vegetation, mining and petroleum activities, habitat fragmentation, introduction of exotic species, urban expansion, grazing, and confined nuclear activities (e.g. washing of uranium at Sierra Pintada) (Iglesias and PCrez 1999). 4. Urban Expansion
The progressive expansion of cities generates local extinctions through multiple effects that have been little studied in relation to amphibians. Urban growth exerts a direct impact on natural environments by its occupation of physical space, fragmenting habitats, contaminating soils and making them impervious, contaminating air and both surface water and subterranean water, transfer of basins, draining of wetlands, generating inorganic and organic residues (liquids and solids), peri-urban desertification, and serving as a centre of dispersal of exotic species. The effect on biota goes from small scales (the "peladares" of the Chaco reported around each human settlement, because of the harvesting of firewood, overgrazing, and soil compaction) to very large ones (e.g., the growth of Buenos Aires city has caused the fragmentation or disappearance of at least three kinds of forests and the cina-cina (Parkinsoniu aculeata) savannah, according to More110 and Mateucci 1999). The few available studies of the relation of Argentine amphibians to urban areas are that by Stetson (1994 a,b) for the city of Posadas (Misiones) and by Acosta et al. (2005), for the city of Salta. These studies demonstrated the fragility of the majority of species in terms of survival in cities. Many of the topics treated below are indirect effects of urban growth or of its proximate cause, the increase in the human population. 5. Chemical and Organic Contamination
This section deals with the kinds of contamination reported for Argentina and includes (1) heavy metals, (2) agrochemicals, and (3) organic wastes. A. CONTAMINATION BY HEAVY METALS
There are many examples of heavy metal contamination in Argentina, and it has been verified both in sparsely populated areas as well as in areas of high industrial development. An example that can serve as a paradigm of the latter scenario is the basin of the MatanzaRiachuelo Rivers in Buenos Aires Province. An example of long-distance effects is the concentrations of heavy metals (frequently above the levels given in Table 2 in the guidelines of water quality for the protection of aquatic life in surface freshwater [Law 2405 1 - Decree 8311931) in the Pilcomayo River at Mision La Paz, Salta, due to the material dumped by the several mines located in the upper part of the basin (mostly around Potosi, Bolivia, 500 km to the northwest in a straight line from Misi6n La Paz) (Lavilla and Buti 1999). The effect on amphibians has received very little attention in Argentina (e.g. Rengel and Pisan6 1991; Rengel et al. 1994). B. CONTAMINATION BY AGROCHEMICALS
Agrochemical contaminants include toxic substances (pesticides and herbicides) and nitrogenous materials (fertilizers). Pesticzdes and herbiczdes: Bertonatti and Corcuera (2000) indicated that 60 millon litres of herbicides are used each year in Argentina (data from 1997), including 2,4,5-T (Agent
LAVILLA and HEATWOLE: AMPHIBIAN CONSERVATION AND DECLINE IN ARGENTINA
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Orange), which was employed as a defoliant in the Campaign of the Impenetrable Chaquefio in the 1970s and 1980s, and various pesticides, including compounds of chlorine and phosphorus that usually are prohibited in industrialized countries. Although there is very little direct information on the impact of agrochemicals on Argentine amphibians, it is possible to make some inferences. Application of insecticide against locusts in the summer of 1995-1996 killed 20,000 hawks (Buteo swainsoni) in the centre of the country (Krapovickas 1997; Bertonatti and Corcuera 2000). Extrapolation of the effect on amphibians - which are presumed (1) to be in direct contact with the fumigated substrate, (2) to reproduce in bodies of water that receive the insecticide, directly or after washing in by rain, and (3) to feed on insects containing the toxin - provides an extremely dark picture. It should be remembered that pesticides can be absorbed by amphibians from the aquatic medium as well as from the terrestrial environment and that in many cases these substances inhibit the action of cholinesterase, thereby bringing about malfunctioning of the central nervous system and causing death by blocking respiration (USGS 2000). Sublethal effects of agrochemicals on Canadian amphibians were analyzed by Pauli (1996), Bonin et al. (1996) and Harris et al. (1996). Recent studies in Argentina on the effect of synthetic pyrethroid insecticides (considered to be innocuous for birds and mammals) on the tadpoles of Physalaemus biligonigerus demonstrated cellular death (apoptosis) in brain neurones, although there was no alteration of integumentary cells (Izaguirre et al. 2000, 2001). Izaguirre et al. also indicated a capacity of bodies of water to concentrate insecticides, thereby becoming dangerous environments for reproduction. Salibiiin (1992) and Salibiiin and Marazzo (1995) demonstrated a neurotoxic effect of deltamethrin on the tadpoles and adults of Rhinella arenarum. Herbicides that contain glyphosphates as active ingredients (in widespread use in Argentina) are considered'to have low environmental toxicity, but it has been shown that the additive used as a dispersant and as a wetting agent interferes with the cutaneous respiration of adult amphibians and with the branchial respiration of larvae (Tyler 1997). For this reason, application of this herbicide in areas close to aquatic habitats has been prohibited in the United Kingdom, the United States, and Australia. Fertilizers: Data from 1994 indicate average use of fertilizers in Argentina to be 5 kg/ halyear, and it was presumed that those values would increase as a consequence of greater and more intense land-use for agriculture and grazing (Bertonatti and Corcuera 2000). Halliday (2000, and see contained bibliography) demonstrated that levels of nitrites and nitrates considered "safe" for human health, severely affect the development and survival of amphibian larvae by retarding growth, increasing incidence of deformities, and causing paralysis and death. There are indications (Bertonatti and Corcuera 2000) that the leaching of fertilizers by rainwater accelerates eutrophication in lentic environments. Halliday (2000) indicated that algae can harbour trematodes that parasitize amphibians and cause deformities. Organic Wastes: Examples of the contamination of surface and subterranean waters by organic material has reached alarming levels in Argentina. The most contaminating wastes in this sense stem from the production and processing of sugar, alcohol, olives, paper, cotton, meat, leather, wool, and rubber, and from the distillation of hydrocarbons (Brailovsky and Fogelmann 1992, cited by Bertonatti and Corcuera 2000), to which ought to be added the untreated black waters that are discharged into other bodies of water. Thus, numerous lakes and ponds (many of them key components of some of the oldest national parks of the country) are the sinks and sewer drains of the neighbouring cities, and the Paranii, Paraguay, Salado Norte, Salado Sur, Carcarafih, de la Plata, Suquia, Sali, and Colorado rivers are among the most severely contaminated of the country (Bertonatti and Corcuera 2000). Contamination by organic residues accelerates eutrophication of bodies of water that in consequence have an increase in primary productivity, loss of diversity of consumers, reduction (or in some cases total loss) of dissolved oxygen, increase in salinity and an increase in dissolved toxins (generated by cyanobacteria) (McNeely et al. 1995), to which
54
AMPHIBIAN BIOLOGY
one needs to add the increase in concentration of coliform bacteria and other pathogens (especially in the case of contarninaton by black water). From the point of view of amphibians this is translated into anoxic, toxic reproductive sites. Although no specific information exists for amphibians, studies on fish in the basin of the Sali River (Buti and Cancino 1999; Buti, personal communication) showed a notable diminution in the number of species recorded between San Miguel de Tucumfin and the Frontal Dam at Termas de Rio Hondo (Santiago del Estero), and one of the causes could be attributed to organic industrial waste and urban discharges. 6. Introduction of Exotic Species
The introduction of exotic species of animals and plants was considered by Elton (1958, cited by McNeely et al. 1995) as one of the great historic convulsions in the global fauna and flora, and it has a long history in Argentina, starting with the beginning of colonization.
Bufonidae Ceratobatrachidae Discoglossidae
Hylidae: Phyllomedusinae Hylidae: Pelodqadinae Megophryidae Microhylidae: Dyscophinae Microhylidae: Microhylinae Pipidae: Pipinae Pipidae: Xenopodinae Pyxicephalidae: Pyxicephalinae Ranidae Scaphiopodidae
Pseudepidalea viridis Ceratobratachus guentheri Bombina bombina Bombina orientalis Bombina variegata Agalychnis callidryas Phyllornedusa bicolor Litoria caerulea Megophrys montana Megophrys nasuta Dyscophus guineti Dyscophus insularis Kaloula pulchra Pipa pipa Xenopus muelleri Pyxicephalus adspersus Lithobates catesbeianus Scaphiopus couchii
Eurasia Bougainville, Solomon Islands Eurasia Asia Eurasia Central America South America Australia Southeastern Asia Southeastern Asia Madagascar Madagascar Southeastern Asia South America Africa Africa North America North America
CAUDATA
Ambystomatidae Amphiumidae Plethodontidae: Plethodontinae Plethodontidae: Spelerpinae Salamandridae: Pleurodelinae
Salamandridae: Salamandrinae
Ambystoma maculatum Ambystoma tigrinum Amphiuma means Plethodon glutinosus Eurycea longicauda Cynops orientalis Cynops pyrrhogaster Lissotriton vulgaris Mesotriton alpestris Notophthalmus viridescens Ornrnatotriton vittatus Pachytriton brevipes Pleurodeles waltl Triturus cristatus Tylototriton verrucosus Salamandra salamandra
North America North America North America North America North America Asia Asia Eurasia Europe North America Asia Asia Europe Eurasia Asia Eurasia; Afkica
LAVILLA and HEATWOLE: AMPHIBIAN CONSERVATION AND DECLINE IN ARGENTINA
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Of great importance to amphibians was the introduction of numerous species of fish of different types into lotic and lentic environments. These introductions were initiated at the beginning of the 20th century and constituted a policy sustained by various official agencies, at the provincial, national and even university levels. Such introductions have put two species of Argentine anurans in danger of extinction (Lavilla et al. 2000). The concept of "exotic species" is used here to include taxa coming from regions outside of the country as well as those within Argentina, but translocated to areas from which they had not been recorded previously. In the first category are included fish from various orders: Salmoniformes (Salmo salar, S. fario, and Oncorhynchus mykiss from Eurasia and Salvelinus frontalis from North America); Cyprinodontiformes (Gambusia aestiputius from St. Andrews, West Indies, Hypophthalamichthys molitrix from China, Cyprinus carpio from Europe and Carassius auratus from China and Japan); and doubtfully the Perciformes (Oreochromzs nzloticus, proposed by some provincial agencies as a resource for non-traditional fisheries, in spite of the well-known harm caused by tilapias in various regions of the world) (C. Buti, personal communication). Native taxa of fish that have been translocated include the orders: Perciformes (Percichthys aetispinnis, R colhuapiensis, R vicinguerrae and R trucha); Characiformes (Piaractus mesopotamzcus) and Siluriformes (Pseudoplatystom coruscans and Rhamdia quelen) (C. Buti, personal communication). Although some species are herbivores, others are carnivores and have been introduced into bodies of water that harbour (or did harbour) endemic amphibians. Given the concrete example of Laguna Blanca (Zapala, Neuquen), where introduced fish extinguished the local population ofAtelognathus patugmicw in less than 30 years, one can imagine the losses fi-om the Andean-Patagonian lakes, where the Salmoniformes were introduced more than a century ago. b
More recently, during the last decade of the 20th century, farms of the bullfrog (Lithobates catesbeianus) were installed at various places in the country. The problems resulting from the escape of individuals and the establishment of feral populations including those arising from competition, predation, and the potential dissemination of diseases are amply documented (Goldfeder 1995, and see next section). In Argentina, feral populations were reported Erom the provinces of San Juan (Sanabria et al. 2005), Misiones (Pereyra et al. 2006), Buenos Aires (Barraso et al. 2009), C6rdoba (Akmentins et al. 2009) and Salta (Akmentins and Cardozo 2009). Another way species are introduced is through the pet trade, still of incipient development in Argentina. The list of species already brought in and available in branch stores is rather extensive and includes members of various higher categories not represented in the country. A summary of the imports into the country in the past years is presented in Table 3. It is known that with a certain frequency and by different means the owners of pets release them after a time in captivity. The problem becomes even more complicated when it is taken into account that many of the introduced species prey on small vertebtrates.
7. Diseases Although the analysis of the role of disease in the demise of amphibians is just beginning in Argentina, alarming information was presented by Herrera et al. (2005), who recorded Batrachochytrium dendrobatzdis on individuals of Leptodactylus ocellatus from Buenos Aires, being the first evidence of this fungus in natural populations of frogs in the South American lowlands. Additional cases of chytrid infections were reported on individuals of Leptodactylus ocellatus from Buenos Aires (Arellano et al., 2006) and C6rdoba (Ghirardi et al. 2009), Leptodactylus gracilis in C6rdoba (Ghirardi et al. 2009), Elmutobius atacamemis and T. pisanoi from the mountains of northwestern Argentina (Barrionuevo and Mangione, 2006), Atelognathus patagonicus from the Patagonian Steppe (Fox et al. 2006) and in Elachistoclezi bicolor from the humid, subtropical lowlands of Misiones (Arellano et al. 2008).
AMPHIBIAN BIOLOGY
56
These records add to what was known for South America, including Brazil (Carnaval et al. 2006), Ecuador (Ron and Merino 2000), Uruguay (Mazzoni 2000), Pen3 (Seimon et al. 2005) and Venezuela (Guayasamin et al., 2002; Bonaccorso et al. 2003). In Ecuador chytrids were found in museum specimens that had been in collections since at least 1980, although the fungus was not detected otherwise until 20 years later. In Uruguay, very worryingly, active infections were reported in populations of Lithobathes catesbeianus in frog farms. Finally, Fox et al. (2006) reported the presence of a ranavirus in Atelognutus patagonicus, apparently the first documented case of morbidity and mortality associated with this virus in natural populations of a South American frog. International information on the pathology of amphibians in relation to their decline PHTM/frogs/ is being concentrated at the website (Berger 1999; Speare et al. 2001). 8. Increase in Ultraviolet (UV) Radiation
Information on the effect of ulraviolet radiation on the early developmental stages of amphibians is contradictory and it is likely that sensitivity to this type of radiation is speciesspecific. Actual levels of ultraviolet ( W ) radiation did not produce deleterious effects on Patagonian amphibians (Pleurodema bufoninum and Nannophryne variegata) (Young et al. 2001; communication by Stanley Fox at the "XV Reuni6n de Comunicaciones Herpeto16gicasn), and similar conclusions were reached in Canada (Davis et al. 1996; Grant and Litch 1996). Conversely, Nag1 and Hofer (1996), Lizana (1997), Lizana and Marco (2001) and others have reported harm caused by ultraviolet radiation (W-A and UV-B) to eggs, larvae, and adult amphibians. See Marco et al. (2009) for a review. The variability in results necessitates a deeper analysis of the relation between UV radiation and amphibians in Argentina. There are three relevant facts: (1) Ultraviolet radiation in various parts of Argentina is increasing (Orce and Relbling 1997). (2) Recent discoveries indicate that Carbaryl, a common insecticide, breaks down under the action of ultraviolet radiation into substances harmful to developing eggs and tadpoles. (3) Metophrene, a pesticide used in wetlands to retard the development of mosquitoes degrades into two by-products whose effect on the immature stages of amphibians is 100 times stronger than the original substance (Anonymous 2001). Although there are no available studies on the agrochemicals used in Argentina, this kind of evidence demands urgent attention. More information on this subject can be obtained from the following two websites of the United Nations Environment Programme (UNEP):
http:llwww.gcrio.org/ozoneltoc.html or http://www.gcrio.org/UNEP1998l
.
9. Global Climatic Change
The scenarios and predictions about the effects of global climatic change on habitats within the Republic of Argentina are relatively scarce (Labraga 1998; Moyano and Seoane 1998; Seoane and Moyano 1999; Hulme and Sheard 2000). Although the various scenarios proposed differ to varying extents, the sources agree that there will be an increase in temperature of 0.4"C per decade in the northern part of the country and of 0.25"C per decade in the south, while precipitation will decrease in the west and increase in the east. With these data one can predict diminutions in the number of sites suitable for reproduction by amphibians in the arid west of Argentina north of the 45th parallel (one degree north of the border between Chubut and Santa Cruz), the habitat of a relatively high number of endemics in the genera Atelognathus and Somuncuriu.
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On the global level, Beebee (1995) reported that over 17 years English amphibians advanced the initiation of their reproductive activities between two and seven weeks, and that this change was correlated with a mean increase of +O. 1°C per year in air temperature over the same period of time. 10. Commercial Trade in Amphibians
Various species of frogs are targets of formal or informal commercial activities that supposedly are of significant volume in Argentina. Although there are no national statistics, local populations of various species are being affected by collection for gourmet food (Leptodactylus ocellatus, L. chaquensis), scientific research (Rhinella arenarum) and for sale as pets. In the latter category, the following species have appeared in shops in the principal cities of the country: Rhinella arenarum, R . dorbigny, R . fernandezae, R. schneideri, various subspecies of Melanophryniscus (Bufonidae), Ceratophrys cranu~elli, Ceratoprhys ornata (Ceratophryidae), Leptodactylus ocellatus (also sold as live bait) (Leptodactylidae),Phyllomedusa sauvagii and Hypsibous pulchellus (Hylidae) (also sold as live food for captive snakes) (Pablo Llaver, in litt., Claudio Bertonatti, in litt.). In section IV-A-6 reference was made to the pet trade as a means of introduction of exotic species into Argentina, with the consequent threat it carries for the local batrachofauna. The other side of this activity is the commercialization of native species in the national and international markets. Although vendors insist their animals are raised in captivity, the business clearly is not regulated and controls are presumably weak. A superficial sample of vendors of pets at six internet sites (two in North America, two in Europe, and two in South America) revealed an offering of various taxa of Argentine frogs. They included, amqng others, Leptodactylus laticeps, Ceratophrys ornata, Ceratophrys cranwelli, Lepidobatrachus laevis, Rhinella spinulosa, R . schneideri, Melanophryniscus stelzneri, Phyllomedusa azurea, Phyllomedusa sauvagii and Dermatonotus muelleri. VIII. REGIONALIZATION OF THE HERPETOFAUNA AND PRINCIPAL THREATS On the basis of the formal geophysical regions, the eco-regions proposed by Olson et al. (1998 a,b) and Burkart et al. (1999), the phytogeographic regions of Cabrera (1976), the regionalization of wetlands by Canevari et al. (1999), the faunistic analysis of Yungas (Lavilla et al. 2000b), Chaco (Lavilla, in press), southern woodlands ( ~ b e d a1999) and central Argentina (Bridarolli and Di Tada 1994), as well as the environmental summary presented by Bertonati and Corcuera (2000) and the contribution of Lavilla (2001), it is possible to regionalize the Argentine batrachofauna and collate the principal environmental risks detected in each region. A. The Northwest, Sierras Pampeanas, and Cuyo
+
+
This area corresponds to the High Andean + Puna Yungas Forest Dry Chaco ecoregions (Burkart 1999), to the Chacoan (in part) + Yungas Prepuna + Puna + the northern part of the High-Andean biogeographic provinces (Cabrera 1976), and to the Southern Andean (Sarmiento et al. 1999) and Chacoan regions (Bucher and Chani 1999).
+
The elevational gradient in the northwestern part of the country produces a great number of environments, and consequently threats are diverse. In the forested mountains there are records of clear-felling, selective felling, urban growth, destruction of basins, contamination by pesticides, herbicides and fertilizers, introduction of exotic species, diminution of rainfall and effects related to mining activities. On the other hand, above the tree line several agents act against amphibians, including infection with Batrachochytrium dendrobatidis, the alteration of wetlands and other bodies of water, mining activities, introduction of exotic species, increase in ultraviolet radiation and lowered precipitation. The batrachofauna of the region includes Oreobates barituensis, Oreobates dzscoidalis,
AMPHIBIAN BIOLOGY
58
Gastrotheca christiani, G. chysosticta, G. gracilis, Dendropsophus minutus, D. nanus, Hypsiboas andinus, H. cordobae, H. marianitae, H. raniceps, Pseudis limellum, Phyllomedusa azurea, P boliviana, P sauvagii, Pseudis platensis, S c i m acuminatus, S. ficovarius, S. nasicus, S. squalirostris, Trachycephalus venulosus, hptodactylus bufonius, Leptodactylus chaquensis, L. elenae, L. fuscus, L. gracilis, L. laticeps, L. latinasus, L. mystacinus, L. ocellatus, L. podicipinus, Ceratophrys cranwelli, Chacophrys pierottii, Lepzdobatrachus asper, L. laevis, L. llanensis, Telmatobius atacamensis, I: ceiorum, T. contrerasi, I: hauthali, I: hypselocephalus, I: laticeps, 7: aff marmoratus, I: oxycephalus, I: pinguiculus, T. pisanoi, I: platycephalus, I: rubigo, I: schreiteri, I: scrocchii, I: stephani, Odontophynus achalensis, 0. americanus, 0 . cordobae, 0. lavillai, 0 . occidentalis, Physalaemus biligonigerus, P cuqui, P borellii, P cinereum, l? cordobae, P guayapae, l? kriegi, P marmoratum, l? nebulosum, l? tucumanum, Pseudopaludicola boliviana, Rhinella achalensis, R . arenarum arenarum, R. bergi, R . fernandezae, R. gallardoi, R. gnustae, R. major, R. rumbolli, R . schneideri, R. spinulosa spinulosa, Melanophryniscus klappenbachi, M. rubriventris, M. stelzneri spegazzinii, M. stelzneri stelzneri, Demtonotus muelleri, Elachistocleis bicolor and E. skotogaster (Argentinean endemics in bold letters).
B. Llanura Platense
This area corresponds to the eco-regions of Humid Chaco + Esteros of IberA + Monte of Sierras and Bolsones the northern part of Monte of Llanuras and Mesetas + Pampan + Espinal + the Delta and Islands of the Paranh River eco-Regions (Burkart et al. 1999), to the Chacoan Monte Espinal + Pampeana biogeographic provinces (Cabrera 1977) and to the Chacoan (Bucher and Chani 1999) and Pampan regions (G6mez and Toresani 1999). It is the most densely populated area of the country and coincides with the major agricultural, pastoral and industrial activities. For this reason the threats to amphibians are numerous, including infection with Batrachochytrium dendrobatidis, alteration of forested habitats, conversion of natural space into agricultural fields or pastures, alteration of wetlands, contamination by heavy metals, pesticides, herbicides, fertilizers, and organic industrial wastes, introduction of exotic species, and probably 3cid rain, although there is no reliable information on the last item. The batrachofauna recorded from this region includes Chthonerpeton indistinctum, Argenteohyla siemersi pederseni, A. siemersi siemersi, Dendropsophus nanus, D. sanborni, Hypsiboas albopunctatus, H. andinus, H. caingua, H. pulchellus, H. punctatus rubrolineatus, H. raniceps, H. riojanus, H. varelae, Pseudis limellum, Phyllomedusa azurea, l? sauvagii, Pseudis minutus, P platensis, Scinax acuminatus, S. berthae, S. ficomarginatus, S. fuscovarius, S. granulatus, S. nasicus, S. squalirostris, Trachycephalus venulosus, hptodactylus bufonius, L. chaquensis, L. diptyx, L. elenae, L. fuscus, L. gracilis, L. latinasus, L. mystacinus, L. ocellatus, L. podicipinus, Ceratophrys cranwelli, C. ornata, Chacophrys pierottii, hpzdobatrachus asper, L. laevis, L. llanensis, Odontophrynus americanus, 0 . barrioi, 0 . cordobae, 0. lavillai, 0 . occidentalis, Physalaemus albonotatus, P biligonigerus, P femndezae, P henselii, P riograndensis, P santafecinus, Pleurodema guayapae, l? nebulosum, l? tucumanum, Pseudopaludicola boliviana, P falcipes, l? mirandae, P mystacalis, Rhinella arenarum arenarum, R . bergi, R . dorbignyi, R . fernandezae, R. major, R . schneideri, Melanophryniscus atroluteus, M. cupreuscapularis, M. fulvoguttatus, M . klappenbachi, Dermatonotus muelleri and Elachistocleis bicolor (Argentinean endemics in bold letters).
+
+
+
C. Subtropical Plateau This area corresponds to the Paranaen Forest + Campos and Malezales eco-regions (Burkart et al. 1999), and the Paranaen biogeographic province (Cabrera 1977). The principal threats emanate from the destruction of forests (clear-felling and selective felling), contamination by pesticides, herbicides and fertilizers, introduction of exotic species, and contamination by organic residues, coming mostly from the paper industry. The batrachofauna recorded from the region includes Chthonerpeton indistinctum, Luetkenotyphlus brasiliensis, Siphonops annulatus, S. paulensis, Zschnocnema henselii, Aplastodiscus perviridis, Dendropsophus minutus, D. nanus, Dendropsophus sanborni, Hypsiboas albopunctatus, H. caingua, H. curupi, H. faber, H. pulchellus, H. raniceps, H. aff. semiguttatus, Ztapotihyla langsdor-i, Pseudis
LAVILLA and HEATWOLE: AMPHIBIAN CONSERVATION AND DECLINE I N ARGENTINA
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limellum, Phyllomedusa tetraploidea, Scinax acuminatus, S. aromothyella, S. berthae, S. fkcomarpnatus, S. JiLscovarius, S. granulatus, S. nasicus, S. perereca, S. squalirostris, S. uruguayus, Trachycephalus dibernardo, ?: imitatmjc, ?: venulosus, Hyalinobatrachium uranoscopum, Leptodactylus bufonius, L. chaquensis, L. diptyx, L. elenae, L. furnarius, L. fuscus, L. gracilis, L. labyrinthicus, L. latinasus, L. mystacinus, L. ocellatus, L. plaumanni, L. podicipinus, Limnomedusa macroglossa, Odontophrynus americanus, Proceratophrys avelinoi, I? bigibbosa, Physalaemus albonotatus, I? biligonigerus, P cuvieri, I? aff. gracilis, I? riograndensis, Pseudopaludicola falcipes, I? mystacalis, Rhinella azarai, R. bergi, R. fernandezae, R . icterica, R . major, R . ornata, R. schneideri, Melanophryniscus atroluteus, M. devincenzi, M. krauczuki, M. aff. tumifons, Crossodactylus dispar, C. schmidtii and Elachistocleis bicolo.1: D. Patagonia
This area corresponds to the Patagonian Woodlands + Patagonian Steppe + Southern part of Monte of Llanuras and Mesetas eco-regions (Burkart et al. 1999), to the Subantarctica + Patagonian + the southern part of Monte biogeographic province (Cabrera 1977), and to the Patagonian Region (Iglesias and PCrez, in Canevari et al. 1999). The principal threats (real or potential) include infection with Batrachochytrium dendrobatzdis and ranavirus, the alteration of forested environments, conversion of natural space into pastures, alteration of wetlands and other aquatic environments, urban growth, contamination by heavy metals, hydrocarbons, and industrial organic wastes, and the introduction of exotic species. The Patagonian batrachofauna is under the direct influence of the Antarctic ozone hole, but there still are no concrete proofs that the increase in ultraviolet radiation affects it (Harold Fox, personal communication). The following species have been recorded from this area: Atelognathus afJ: grandisonae, A. nitoi, A. patagonicus, A. praebasalticus agilis, A. praebasalticus dobeslawi, A. praebasalticus luisi, A. praebasalticus praebasalticus, A. reverberii, A. salai, A. solitarius, Batrachyla antartandica, B. fitzroya, B. leptopus, B. taeniata, Alsodes australis, A. gargola gargola, A. gargola neuquensis, A. pehuenche, A. verrucosus, Eupsophus calcaratus, E. emiliopugini, E. vertebralis, Hylorina sylvatica, Rhinoderma daminii, Leptodactylus bufmius, L. latimus, L. ocellatus, Odontophynus occzdentalis, Pleurodema bufoninum, l? nebulosum, R tucumanum, l? thaul, Somuncuria somuncurensis, Rhinella arenarum arenarum, R. arenarum mendocinus, R. rubropunctata, R. spinulosa papillosa and Nannophryne variegata (Argentinean endemics in bold letters). IX. CATEGORIES OF PROTECTION FOR THE ARGENTINE BATRACHOFAUNA There are diverse proposals for categorizing the Argentine herpetofauna at different ranks, including the global (IUCN et al., 2004), national (e.g. Bertonatti and Gonzhlez 1992; Bertonatti 1994; Lavilla et al. 2000), provincial (e.g. Chani et al. 1989; Tedesco et al. 1999), regional (e.g., Christie 1984), and local (e.g. Martin et al. 198'7; ~ b e d aet al. 1994) levels. The methods that were used were diverse and not always clearly explained, leading to discrepancies among specialists. In 1993, the "Direcci6n Nacional de Fauna y Flora Silvestres" [National Management of Forests, Fauna and Flora] decided to place the categories of conservation of the fauna of the country on an objective basis and originated the project "Recalificaci6n del Estado de Conservaci6n de la Fauna Silvestre Argentina" [Assessment of the State of Conservation of the Forest Fauna of Argentina] coordinated by Drs. Carmen ~ b e d aand Dora Grigera, and the method developed by Reca et al. (1994) was adopted and applied to tetrapods in general. In this context, a large group of specialists on different amphibian fauna1 regions developed a series of workshops and associated tasks from September 1998 to March 2000 to evaluate the Argentine amphibian fauna. They took upon themselves the mission of reaching agreement on the most precise methodology fitting the group in question; the results were published by Lavilla et al. (2000) and were adopted by the Argentine legislature as Resolution 1030/04. The 12 variables analysed were: (1) Continental Distribution (DICON): Evaluates the distributional amplitude of each taxon in South America. Considers four possible categories, established as a comparative variable
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by a series of graphs, with the following notations: 100-75% occupancy of the area of the continent = zero; 7450% occupancy = 1; 49-25% = 2; < 24% = 3. (2) National Distribution (DINAC): Evaluates the distributional amplitude of each taxon in Argentina. The notations for six possible categories were: 100-80% occupancy of the area of Argentina= a value of zero; 79-60% = 1; 5 9 4 0 % = 2; 39-20% = 3; 19-l%= 4; < 1% unable to map = 5. (3) Amplitude of Habitat Use (AHUA): Evaluates the capacity of the species to live in different habitats. Three categories are recognized: Capable of living in four or more different types of habitat = a value of zero; Capable of living in two or three different habitats = l ; Restricted to only one type of habitat, or needs more than one habitat sometime during its life =2. (4) Amplitude of Use of Vertical Space (AHUEVE): Evaluates the number of strata used for feeding and reproduction. Three categories are recognized: uses one stratum = a value of zero; can use two or three strata= l ; can use more than three strata=2. (5) Body-Size (TAM): Three categories of body size, taken as snout-to-vent length (SVL) are recognized: C 79 mm = a value of zero; 80-149 mm = 1; > 150 mm = 2.
( 6 ) Reproductive Potential (POTRE): This is expressed as the number of eggs laid per female per reproductive season. When information is lacking, estimates based on reliable data from congeneric taxa of comparable size and mode of reproduction are used. Three categories are recognized: > 1000 eggs = a value of zero; 999-100 = 1; < 99 = 2. (7) Trophic Amplitude (AMTRO): The majority of Argentine species that eat principally arthropods were classified as "generalist carnivores" (a value of 1 according to Reca et al. [1994]). Others (e.g. Ceratophrys and Lepidobatrachus), that eat small vertebrates were considered as "specialist carnivores" with a value of 2. ( 8 )Abundance (ABUND): Abundance is one of the most intuitive variables of the methods used, given the absence of population censuses for Argentine anfphibians. The assignment of a taxon to a particular category is grounded on the field experience of the convened specialists. Three categories are recognized: Abundant = a value of zero; scarce= l ; Rare to very rare =2.
(9) Taxonomic Peculiarity (SINTA): Taxonomic peculiarity is an indirect expression of the genetic distinctiveness of a taxon in relation to the number of species that make up higher taxonomic categories. Three categories are recognized: Absent=a value of zero; Belongs to a monotypic genus= l ; Belongs to a monotypic family=2. (10) Distinctiveness (SING): Two criteria were followed, one biological (peculiarities in the mode of development) and the other distributional. Species were considered peculiar (value of 1) if they hlfilled one or more of the following requirements: (a) endemic to Argentina, (b) viviparous, (c) young develop in a dorsal pouch or gular sac, or (d) direct development. (11) Effect of Collecting (AXECT): The following variables are recognized: Absent = value of zero; Induces fear, revulsion, or superstition, or is a pest, or is hunted on a small scale = 1; Hunted for sport, commercially exploited, or officially declared a pest = 2; Combination of two or more of the previous categories = 3; Intensive exploitation for leather, meat or other goods = 4; Irreversible destruction of the habitat = 5. (12) Protection (PROT): Those species that are found in natural areas under various jurisdictions in which effective control measures are in place are considered protected. Nominal parks and reserves, or those lacking effective management procedures, or whose small area does not guarantee significant protection for the species in question, were not taken into account in the assessment of this variable. Four categories are recognized depending on the number of natural protected areas in which the species is present: Three or more = a value of zero; Two = 1; One = 1; Not protected = 3.
LAVILLA and HEATWOLE: AMPHIBIAN CONSERVATION AND DECLINE IN ARGENTINA
61
Legislation by the Republic of Argentina established the following categories (Fauna1 Law 22.42 1181 and regulatory decree 666197): (1) In Danger of Extinction: Species that are in immediate danger of extinction and whose survival is improbable if the factor causing its decline continues to operate. (2) Threatened: Those species that through excessive hunting, destruction of their habitat or because of other factors, are susceptible to becoming in danger of extinction. (3) Vulnerable: Species that because of their population size, geographic distribution or other factors, although neither clearly in danger nor threatened, are at risk of entering these categories. (4) Not Threatened: Those species that are not in any of the above categories and whose risk of extinction or of being threatened is considered to be low. ( 5 ) Insuficiently Known: Species that, owing to lack of information on their degree of threat or risk, or because of their biological characteristics, cannot be assigned to any of the previous categories. According to resolution 1030104, all species not evaluated, described or recorded for the first time in Argentina after December 31, 2004. are included in this category. Lavilla et al. (2002), re-analysed the taxa considered "Insufficiently Known" by Lavilla et al. (2000), and established the category "Species that Merit Special Attention" (inspired by Maneyro and Langone [2001]), that has no legal status but does serve to call to the attention of herpetologists the need for studies of certain taxa. This category encompasses those species that are based on clearly identified reference material in museums, and that have a high index of categorization (18 or more), but have not been reported in nature for at least three decades+ The actual state of knowledge of such taxa does not permit elucidation of the reasons for the absence of recent reports. These could be, among others, errors in identiftring the original locality of collection, recent absence of collecting activity, or local extinction. The equivalency of the conservation categories of various proposals with those of Argentine legislation has not been defined. In order to correct this deficiency, Table 4 equates the categories of levels of risks between Argentine legislation and the classification adopted by the International Union for the Conservation of Nature (IUCN, 2001). When pertinent, the placement of Argentine amphibians in conservation categories was carried out at the subspecific level, based on their disjunct distributions. The distribution of taxa among conservation categories according to Barrionuevo and Ponssa (2008) and Lavilla et al. (2000, 2002) is as follows: (1) Species conszdered extinct: Telmatobius ceiorum and Telmatobius laticeps.
Table 4. Equivalency of the conservation categories contained in Argentinean legislation with those proposed by the International Union for the Conservation of Nature (IUCN) (2001). Level of Risk
Argentina
IUCN v. 3.1
Code
(4) Maximum
Extinct
EX
(3) Very High (2) High (1) Medium (0) Minimum (?) Unknown
In danger of extinction Threatened Vulnerable Not threatened Insufficiently known + S ~ e c i aattention l
Extinct Extinct in the wild Critically Endangered Endangered Vulnerable Least Concern Insufficient data Not evaluated
CR EN VU LC DD
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AMPHIBIAN BIOLOGY
Telmatobius ceiorum and Telmatobius laticeps, previously considered as Vulnerable (Lavilla et al., 2000) are considerd extinct by Barrionuevo and Ponssa (ZOOS), after four years of exhaustive surveys in the mountains of Tucumfin. ( 2 ) Species that merit special attention: Luetkenotyphlus brasiliiensis, Rhinella gnustae, Melanophyniscus stelzneri spegazzinii, Hypsiboas varelae, Crossodactylus dispar; Eupsophus vertebralis and Pseudopaludicola mirandae.
(3) Species in Danger of Extinction: Atelognathus patagonicus, Telmatobius atacamensis and Telmatobius pisanoi. The principal population of Atelognathus patagonicus was situated in Laguna Blanca, Zapala, NeuquCn, but disappeared, as already indicated, because of the introduction of perch (Percichthys colhuapiensis) and trout (Oncorhynchus mykiis and Salmo trutta). Today this frog is limited to small, peripheral bodies of water, most of them not protected. Telmatobius atacamensis was reported as probably extinct by Lavilla (in Frost 1985). A metapopulation was later found in 1989 in Pueblo Nuevo, near San Antonio de 10s Cobres, Salta, but it has not been seen there since then. Later, Barrionuevo and Mangione (2006) reported another population from Los Patos, Salta, infected with Batrachochytrium dendrobatidis. Telmatobius pisanoi is included here based on the authority of Barrionuevo and Ponssa (ZOOS), who found only a relictual population at the edge of its original area of distribution, the same previously reported as infected with Batrachochytrium dendrobatidis by Barrionuevo and Mangione (2006).
(4) Threatened Species: Hyalinobatrachium uranoscopum and Somuncuria somuncurensis. Hyalinobatrachium uranoscopum, the only centrolenid in Argentina, seems to be strongly associated with Araucaria forests in Misiones Province, a habitat that is fragmented and in definite decline. The monotypic genus Somuncuria is endemic toethe warm bodies of water of the Somuncurfi Plateau, where no effective protection is provided. Trout have been introduced in the lower parts of this small and closed basin, and throughout the region there is extensive rearing of cattle. ( 5 ) Vulnerable Species: Siphonops annulatw, S. paubnsis, Chthonerpeton indistinctum, Rhinella achalensis, R. arenarum mendocinus, R. gallardoi, R . rubropunctata, R. rumbolli, Melanophyniscus cupreuscapularis, M. devincenzii, M. rubriventris, M. stelzneri stelzneri, Aplastodiscus pervirzdis, Argenteohyla siemersi sienzersi, A. S. pederseni, Hypsiboas marianitae, Gastrotheca chktiani, G. chrysosticta, G. gracilis, Itapotihyla langsdor-i, Scinax perereca, Phyllomedusa boliviana, P tetraploidea, Alsodes gargola neuquensis, Atelognathus nitoi, A. praebasalticus praebasalticus, A. p. agilis, A. p. dobeslawi, A. p. luisi, A. reverberii, A. salai, A. solitarius, Batrachyla antartandica, Crossodactylus schmidti, Oreobates discoidalis, Eupsophus emiliopugini, Hylorina sylvatica, Leptodactylus labyrinthicus, L. laticeps, Odontophynus achalensis, Pleurodema kriegi, P marmoratum, Proceratophrys avelinoi, P bigibbosa, Telmatobius hauthali, T oxycephalus, 7: schreiteri, 7: stephani and Rhinoderma darwinii. The forms included in this category are ( 1 ) taxa strongly associated with forests (Paranense, Southern Cordilleran Forest, Yungas) whose habitats are threatened by human activities, ( 2 ) microendemic taxa, (3) taxa with particular reproductive modes (including viviparity and incubation of eggs in dorsal pouch or in gular sac), and (4) taxa subject to non-regulated commercial exploitation because of their value as pets. ( 6 ) Species that are Not Threatened: Rhinella arenarum arenarum, R. bergi, R . dorbignyi, R . fernandezae, R . icterica, R. major; R . ornata, R . schnezderi, R. spinulosa papillosa, R . S . spinulosa, Melanophryniscus atroluteus, M. klappenbachi, M. aff. tumifrons, Nannophyne variegata, Hypsiboas albopunctatus, H. andinus, H.
LAVILLA and HEATWOLE: AMPHIBIAN CONSERVATION AND DECLINE IN ARGENTINA
63
caingua, H. fabel; Dendropsophus minutus, D. nanus, D. sanborni, Hypsiboas pulchellus, H. cordobae, H. punctatus rubrolineatus, H. raniceps, H. semiguttatus, Trachycephalus venulosus, Phyllomedusa azurea, l? sauvagii, Scinax acuminatus, S. berthae, S. granulatus, S. fuscomarginatus, S. fhscovarius, S. nasicus, S. squalirostris, AAldes gargola gargola, Batrachyla leptopus, B. taeniata, Ceratophrys cranwelli, C. ornata, Chacophrys pierottii, Eupsophus calcaratus, Lepzdobatrachus aspel; L. laevis, L. llanensis, Leptodactylus bufonius, L. chaquensis, L. elenae, L. fuscus, L. gracilis, L. latinasus, L. mystacinus, L. ocellatus, L. plaumanni, L. podicipinus, Limnomedusa macroglossa, Odontophrynus americanus, 0. lavillai, 0. occidentalis, Physalaemus albonotatus, I? biligonigerus, l? cuqui, l? cuvieri, I? fernandezae, I? aff. gracilis, l? henselii, ET riograndensis, I? santafecinus, Pleurodemu borelli, I? bufoninum, I? cinereum, P guayapae, P nebulosum, I? thaul, l? tucumanum, Pseudopaludicola boliviana, I? falczpes, I? mystacalis, Dermatonotus muelleri, Pseudis limellum, Pseudis minutus, I? platensis and Elachistocleis bico1o.l:
(7) Species that are Insuficiently Known: Rhinella azarai, Melanophryniscus fulvoguttatus, M. krauczuki, M . cf. stelzneri (Tandil), H~psiboascurupi, Hypsiboas riojanus, Scinax aromothyella, Scinax aff. uruguayus, Trachycephalus dibemzardoi, i? imitutrix, Leptodactylus diptyx, Leptodactylus fimarius, ALsodes australis, A. pehuenche, A. verrucosus, Atelognathus a 8 grandisme, Batrachyla fitzroya, Ischnocnema henselii, Oreobates barituensis, Odontophrynus barrioi, 0. cordobae, Pleuroderna Cordobae, Telmatobius contrerasi, i? hypselocephalus, i? murmoratus, T pinguiculus, 7: platycephalus, 7: scrocchii, T rubizo and Elachistocleis skotogastel:
This category includes taxa that (1) have been described recently (2) have been recently incorporated into the batrachofaunal index of the country, (3) are not included in studies beyond their original description or their original listing for Argentina, (4) present unresolved nomenclatural problems, andlor ( 5 ) have more than one questionable entry in the table of conservation categories (Lavilla et al. 2002). In 2004, and after considerable effort, all amphibian species of the world were assessed (IUCN et al. 2004) following the IUCN Red List Categories and Criteria (2001). The information on Argentine amphibians appears in Appendix 1. Although there is an overall similarity between the two schemes, there are some discrepancies. The recorded differences between the Argentine (ST in Appendix 1) and the Global (STl in Appendix 1) schemes are due to diverse factors, including: (1) ST restricts analysis to those populations recorded in Argentina, while ST1 analyses the species in its whole range. For example, in Argentina Hyalinobatrachium uranoscopum is known from a restricted patch of forest in Misiones Province, and is the only centrolenid known for the country. Consequently, it is one of the two Threatened Species in Argentina. Conversely, this species has a wide range with several populations known from southeastern Brazil, and according to ST1 is a Low Concern taxon. (2) ST includes subspecies whereas the lowest category considered by ST1 is the species. An illustrative example of discrepancy is Rhinella arenarum. At the species level, it corresponds to the Low concern group of taxa, but when considering the subspecies, one (the nominal, with a wide distribution in southern South America) is included in Low Concern, whereas Chaunis arenarum mendocinus, restricted to a few areas in central-western Argentina is considered Vulnerable. (3) Categories in ST are the result of the summation of 12 variables; if two of them are unknown, the taxon is automatically included in the category Insuficiently Known. By contrast, the methodology used by ST1 allows categorization based on just one variable. Examples of discrepancies are particularly noticeable in Telmatobius, a genus with several species known only from the name-bearing types and from the data available in the original descriptions. According to ST they are Insuficiently Known, but are included in diverse categories of risk by ST1, based on their restricted distributions. (4) Other differences are due to the generation of new information in the years elapsed between the publication of the two methods. An example of this is Atelopthus patagonicus, considered by ST as in Danger of Extinction; due to its known occurrence in three lakes in a protected area; the status changes to Endangered in the ST1 assessment.
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IX. REFERENCES Acosta, R., Mesones, R. V and Ndtiez, A., 2005. Fauna de anuros en la cindad de Salta, Argentina. Reuista de Biologia Tropical 53: 569-575. Aguiar, O., Bacci, M., Lima, A.E, Rossa-Feres, D.C., Haddad, C.F.B. and S.M. Recco-Pimentel, C.F.B. 2007. Phylogenetic relationships of Pseudis and Lysapsus (Anura, Hylidae, Hylinae) inferred from mitochondrial and nuclear gene sequences. Cladistics 23: 1-9. Akmentins, M. S. and Cardozo, D. E., 2009. American bullfrog Lithobates catesbeianw (Shaw 1802) invasion in Argentina. Biological invasions, DO1 10.1007// S10530-009-95 15-3 Akmentins, M. S. and Vaira, M., 2009. Amphibia, Anura, strabomantidae Oreobates barituensis: distribution extension, a new rpvincial record and geographical distribution map. Check List 5: 216-217. Akmentins, M. S., Pereya, L. C. and Lescano, J. N., 2009. Primer registro de una poblaci6n asilvestrada de rana tor0 Lithobates catesbeianus en una provincia de Cbrdoba, Argentina. Notas sobre la biologia de la especie. Cudernos de Herpetologia 23: 25-32. kvarez, B.B , Cespedez, J. A., Lions, M. L., Hernando, A. and Aguirre, R., 1996. Herpetofauna de las provincias de Corrientes, Chaco y Formosa (Argentina). FACENA 12: 119-134. Anonymous, 2001. http://www.dnr.state.wi.us. February 19, 2001. Arellano, M. L., Ferraro, D. E, Steciow, M. M., Lavilla, E. 0 . and Ramirez Barrios, L., 2008. Primer registro de quitridiomicosis e n Elastocleis bicolor (Anura: microhylidae) para el Bosque Atlintico de Misiones, Argentina. ZX Congreso Argentina de Herpetologh, San Luis. Arellano, M. L., Agostini, M., Nerrera, Steciow M,, Lavilla, E. 0 . and Barraso, D., 2006. Nuevo hallazgo de quitridiomicosis en el noreste de la provincia de Buenos Aires. VIZ Congreso Argentino de Herpetologia, Corrientes: 124. Baldissera, F. A., Caramaschi, U. and Haddad, C. F. B., 2004. Review of the Bufo crucqer species group, with descriptions of two new related species (Amphibia, Anura, Bufonidae). Arquiuos do Museu National, Rio de Janeiro 62: 255-282. Baldo, D. and Basso, N. G., 2004. A new Species of MelanoPh~iscus (Anura: with comments on the species of the genus reported for Misiones, northeastern Argentina. J Herpetol. 38: 393-403. ~ ~ l D.; d ~~ , ~ C, and~ segalla, ~ M, V,~ 2008, i Amphibia, Anura, Leptodactylidae, Leptodactylus furnarius: New country record, geographic distribution map and advertisement call. Check List 4(2): 98-102. Barrasso, D. A., Cajade, R., Nenda, S. J., Baloriani, G. and Herrera, R., 2009. Introduction of the American bullfrog Lithobates catesbeianus (Anura: Ranidae) in naturil and modified environmdnts: an increasing conservation problem in Argentina. Sth Amer J . Herpetol. 4: 69-75.
Barrionuevo, J. S. and Ponssa, M. L 2008. Decline of three species of the genus Telmatobius (Anura: Leptodactylidae) from Tucumin province, Argentina Herpetol. 64(1): 47-62. Beebee, T. J. C., 1995. Amphibians and climatic change. Froglog 1 2 : 1. Berg, C., 189697. Batracios Argentinos. Enumeracidn sistemitica, sinonimica y bibliogrifica de 10s batracios de la Repdblica Argentina. An. Mus. Nac. Buenos Aires (Ser. 2) 5: 147-226. Berger, L., 1999. Amphibian disease website. Froglg 32: 2. Bertonatti, C., 1994. Lista propuesta de anfibios y reptiles amenazados de extinci6n. Cuadernos de Herpetologia 8: 164-1 7 1. Bertonatti, C. and Corcuera, J., 2000. "Situaci6n Ambiental Argentina 2000". Fundaci6n Vida Silvestre Argentina, Buenos Aires. Bertonatti, c. and G o d e z , E, 1992. "Lista de Vertebrados Argentinos Amenazados de Extinci6n". Fundacidn V& Silvestre Argentina Boletin Tlcnico No. 8: 1-32 B6, R. F. and Quintana, R. D., 1999. Actividades humanas y biodiversidad en humedales: El caso del Bajo Delta del Rio Parani. Pp. 291-315 in "Biodiversidad y Uso de la Tierra. Conceptos y Ejemplos de AmCrica Latina", ed by S. D. Mateucci, 0 . T. Solbrig, J. Morello and G. Halffter. EUDEBA, Col. CEA 24. Bonetto, A. A. and Hurtado, S., 1999. Regi6n 1. Cuenca del Plata. Pp. 33-72 in "Los Humedales de la Argentina: Clasificaci6n, Situaci6n Actual, Conservaci6n y Ltgislaci6n", ed by E Canevari, D. E. Blanco, E. Bucher, G. Castro and I. Davidson. Wetlands Zntl. Publ. 46. Bonin, J., Ouellet, M., Rodriguez, J., Desgranges J.-L. and Sharbel, T F., 1996. Measuring the health of frogs in agricultural habitats subjected to pesticides in southern Quebec. Froglog 16: 2. Bonaccorso E., Guayasamin, J. M., Mendez, D. and Speare, R., 2003. Chytridiomycosis in a Venezuelan amphibian (Bufonidae: Atelopus cruciger). Herpetol. Rev. 34: 331-334. Brailovsky, A, E. and Foguelman, D., 1992. Agua medio ambiente e n Buenos Aires. Ed. Fraterna, Buenos Aires. Bridarolli, ~ ,M. E. and Di Tada, I. E., 1994. Biogeografia de 10s anfibios anuros de la regi6n central de la Repdblica Argentina. Cuadernos de Herpetologia 8: 63-82. Brown, A., Martinez Ortiz, U,, Acerbi, M. and Corcuera, J. (eds), 2005. "La Situaci6n Ambiental Argentina 2005". Fundaci6n Vida Silvestre Argentina, Buenos Ares.
Barrionuevo, S. and Baldo, D., 2009. A new species of Telmatobins (Anura: Ceratophryidae) from Northern Jujuy Province, Argentina. Zootaxa 2030: 1-20.
Brown, A. D. and Pacheco, S., 2006. Propuesta de actualizaci6n del mapa ecorregional de la Argentina. Pp. 28-31 in "La Situacidn Ambiental Argentina 2005", ed by A. Brown U. Martinez Ortiz, M. Acerbi and J. Corcuera. Fundaci6n Vida Silvestre Argentina, Buenos Aires.
Barrionuevo, S. and Mangione, S., 2006. Chytridiomicosis in two species of Telmatobius (Anura: Leptodactylidae) from Argentina. Dis. Aquat. Organ. 73: 171-174.
Brusquetti, F. and Lavilla, E.O., 2006. Lista comentada de 10s anfibios de Paraguay. Cuadernos de Herpetologia 20 (2): 3-79.
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Stetson, R. E., 1994 b. Nuevo aporte a1 conocimiento de anuros urbanos. Primera cita de Bufo pygmaeus Myers y Carvalho (Bufonidae), y Leptodactylus chaquensis (Cei, 1950) para Misiones. Notas Cientifias 2: 1-5. Tedesco, M,, Alvarez, B., Cespedez, J. and Morand, M., 1999. Estado de conservacidn de la fauna de saurios, anfisbenidos y anfibios de la provincia de Corrientes, Argentina. F! 111 i n "Abstracts of V Congreso Latinoamericano de Herpetologia". Tyler, M. J., 1997. Herbicides kill frogs. Froglog 21: 2. ~ b e d a C., , 1999 ("1998"). "Batracofauna de 10s Bosques Templados Patagbnicos: Un Enfoque Ecobiogeogrifico. Unpublished Doctoral Dissertation. Facultad de Ciencias Exactas y Naturales, Universidad Nacional de Buenos Ares. ~ b e d a C. , A, D. Grigera, D. and Reca, A., 1994. Estado de conservaci6n de la herpetofauna del Parque y Reserva Nacional Nahuel Huapi. Cuadernos de Herpetologia 8: 155-163. UICN, 2001. Categorias y Criterios de la Lista Roja de la UICN: versi6n 3.1. Comisi6n de Supervivencia de Especies de la UICN. UICN, Gland. i-ii + 1-33. USGS, 1999. USGS News Release: 10 September, 1999. Froglog 36: 1-2. USGS, 2000. USGS research finds that contaminants may play an important role in California amphibian declines. http:/~.usgs.gov/publidpresdpublic~~airs /press-releaseslpr 1338m.html.
LAVILLA and HEATWOLE: AMPHIBIAN CONSERVATION AND DECLINE IN ARGENTINA Vaira, M., 2002. Variacibn de la coloracibn en poblaciones argentinas de Melanophryniscus rubriventrir (Vellard, 1947). Cuadernos de Hwpetologia 16: 151-163. Vaira, M. and Ferrari, L. 2008. A new species of Oreobates (Anura: Strabomantidae) from the Andes of northern Argentina. Zootaxa 1908: 41-50. Valetti, J., Salas, N. E. and Martino, A. L., 2009. A new polyploid species of pleurodema (Anura: Leiuperidae) from Sierra de Comechingones, Cbrdoba, Argentina and redescription of Pleurodema kriegi (Muller, 1926). Zootaxa 2073: 1-21. Vervoorst, F., 1982. Nomeste. Pp. 9-24 in "Conservaci6n de la Vegetacibn Natural en la Republica Argentina, Serie Conservaci6n de la Naturaleza", Fund. M. Lillo 2.
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Woodwell, G. M,, 1983. Global deforestation: contribution to atmospheric carbon dioxide. Science 222: 1081-1086. Yanosky, A. A., Dixon, J. R. and Mercolli, C., 1993. The herpetofauna of El Bagual Ecological Reserve (Formosa, Argentina) with comments on its herpetological collection. Bull. Maryland Herp. Soc. 49: 160-170. Young, B. E., Lipps, K. R., Reaser, J. K. Ibanez, R., Salas, A. W., Cedefio, J. R., Coloma, L. A., Ron, S., La Marca, E., Meyer, J. R., Muiioz, A., Bolanos, F., Chaves, G. and Romo, D., 2001. Population declines and priorities for amphibian conservation in Latin America. Cons. Biol. 15: 1213-1223.
APPENDIX 1 Distribution, habitat and conservational status of the amphibians recorded from Argentina up to 31 July, 2006 Key to Abbreviations: DISTR: Distribution by political units (Provinces) in Argentina, and by countries when the taxon is not endemic. ECOR: Eco-regional distribution following the scheme of Burkart et al. (1999). S T The status of the taxon according to Argentine legislation, following Lavilla et al. (2000, 2002). The code is: CR: in danger of extinction; EN: threatened; VU: vulnerable, LC: not threatened, DD: data deficient. The code DSA is employed for those taxa that, although formally considered as data deficient, deserve special attention (see Table 4). ST1: The status of the taxoh according to the results of the Global Amphibian Assessment (http:I/ www.globalamphibians.org),accessed on July, 30th, 2006. Code is: CR: Critically Endangered; EN: Endangered; VU: Vulnerable; LC: Least Concern; DD: Data Deficient; NE: Not evaluated. Taxa in boldface are endemic to Argentina.
APODA CAECILIIDAE
Siphonops annulatus DISTR: Argentina: Misiones. Also in Bolivia, Brazil, Colombia, Ecuador, Guayanas, Paraguay, Peh, Venezuela. ECOR: Paranaen Forest. S T VU ST1: LC Siphonops paulensis DISTR: Argentina: Corrientes, Msiones. Also in Bolivia, Brazil, Paraguay. ECOR: Paranaen Forest, Campos and malezales. S T VU ST1: LC Luetkenotyphlus brasiliensis DISTR: Argentina: Misiones. Also in Brazil, Paraguay. ECOR: Paranaen Forest. S T DSA ST1: DD TYPHLONECTZNAE Chthonerpeton indistinctum DISTR: Argentina: Buenos Aires, Chaco, Corrientes, Entre Rios, Santa Fe. Also in Brazil, Paraguay, Uruguay. ECOR: Humid Chaco, Esteros of Iberi, Campos and Malezales, Delta and Islands of the Parani River, Espinal. S T vu ST1: LC
ANURA BRACHYCEPHALIDAE Zschnocnema henselii DISTR: Argentina: Misiones. Also in Brazil. ECOR: Paranaen Forest. S T DD ST1: LC STRABOMANTIDAE STRABOMNTZNAE
Oreobates baritrensis DISTR: Argentina: Jujuy, Salta. ECOR: Yungas Forest. ST. DD ST1: NE Oreobates discoidalis DISTR: Argentina: Jujuy, Salta, Tucumin. Also in Bolivia. ECOR: Yungas Forest. S T vu ST1: LC
AMPHIGNATHODONTIDAE Gastrotheca chtistiani DISTR: Argentina: Jujuy, Salta ECOR: Yungas Forest. S T vu ST1: EN Gastrotheca chrysosticta DISTR: Argentina: Salta. Probably in Bolivia (?) ECOR: Yungas Forest. S T vu ST1: VU
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AMPHIBIAN BIOLOGY
Gastrotheca gracilis DISTR: Argentina: Catamarca, Salta, Tucumin. ECOR: Yungas Forest. ST: vu ST1: W HYLIDAE Aplastodiscw perviridis DISTR: Argentina: Misiones. Also in Brazil. ECOR: Paranaen Forest. S T vu ST1: LC Argenteohyla siemersi siemersi DISTR: Argentina: Buenos Aires, Entre Rios. Also in Uruguay ECOR: Pampa. S T vu ST1: Subspecies: NE; the species is considered EN Argenteohyla siemersi pederseni DISTR: Argentina: Corrientes. Also in Paraguay. ECOR: Esteros of Iberi. S T vu ST1: Subspecies: NE; the species is considered EN Dendropsophw minutw DISTR: Argentina: Jujuy, Misiones, Salta. Also in Bolivia, Brazil, Colombia, Ecuador, Guayanas, Paraguay, P e d , Trinidad, Uruguay, Venezuela. ECOR: Yungas Forest, Dry Chaco, Paranaen Forest. S T LC ST1: LC Dendropsophw n a n w DISTR: Argentina: Buenos Aires, Chaco, Corrientes, Entre Rios, Formosa, Misiones, Salta, Santa Fe, TucumPn. Also in Bolivia, Brazil, Paraguay, Uruguay. ECOR: Yungas Forest, Dry Chaco, Humid Chaco, Paranaen Forest, Esteros of Iberi, Campos and Malezales, Delta and Islands of the Paran5 River, Espinal, Pampan. S T LC ST1: LC Dendropsophus sanborni DISTR: Argentina: Buenos k r e s , Chaco, Corrientes, Entre Rios, Formosa, Misiones, Santa Fe. Also in Brazil. Paraguay, Uruguay. ECOR: Humid Chaco, Paranaen Forest, Esteros of IberA, Campos and Malezales, Delta and Islands of the Paran5 River, Espinal, Pampan. S T LC Hypsiboas albopunctatw DISTR: Argentina: Corrientes, Misiones. Also in Bolivia, Brazil, Paraguay, Uruguay. ECOR: Humid Chaco, Paranaen Forest, Campos and Malezales. ST: LC ST1: LC Hypsiboas andinus DISTR: Argentina: Catamarca, Jujuy, Salta, TucumPn. Also in Bolivia. ECOR: Puna, Monte of Sierras and Bolsones, Yungas Forest, Dry Chaco. S T LC ST1: LC Hypsiboas caingua DISTR: Argentina: Corrientes, Misiones. Also in Brazil, Paraguay. ECOR: Humid Chaco, Paranaen Forest, Campos and Malezales. ST: LC ST1: LC
Hypsiboas cordobae DISTR: Argentina: Cbrdoba, San Luis. ECOR: Dry Chaco. S T LC STl: DD Hypsiboas curupi DISTR: Argentina: Misiones. Also in Paraguay. ECOR: Paranaen Forest. S T DD STl: NE Hypsiboas faber DISTR: Argentina: Misiones. Also in Brazil, Paraguay. ECOR: Paranaen Forest. S T LC ST1: LC Hypsiboas marianitae DISTR: Argentina: Salta. Also in Bolivia. ECOR: Yungas Forest. ST: vu ST1: LC Hypsiboas pulchellus DISTR: Argentina: Buenos Aires, Chaco, C6rdoba, Corrientes, Entre Rios, Formosa, La Pampa, Misiones, Santa Fe. Also in Brazil, Paraguay, Uruguay. ECOR: Humid Chaco, Paranaen Forest, Esteros of IberP, Campos and Malezales, Delta and Islands of the ParanP River, Espinal, Pampan. ST: LC ST1: LC Hypsiboas punctatw rubrolineatus DISTR: Argentina: Chaco, Corrientes, Entre Rios, Formosa, Santa Fe. Also in Bolivia, Brazil, Paraguay. ECOR: Humid Chaco, Delta and Islands of the ParanP River. ST: LC ST1: Subspecies: NE; the species is considered LC Hypsiboas raniceps DISTR: Argentina: Chaco, Corrientes, Entre Rios, Formosa, Jujuy, Misiones, Salta, Santa Fe, Santiago del Estero. Also in Bolivia, Brazil, Colombia, French Guayana, Paraguay. ECOR: Yungas Forest, Dry Chaco, Humid Chaco, Paranaen Forest, Esteros of IberA, Campos and Malezales, Delta and Islands of the ParanP River. ST: LC ST1: LC
Hypsiboas riojanus DISTR: Argentina: Catamarca, La Rioja. ECOR: Monte of Sierras and Bolsones. ST: LC ST1: DD Hypsiboas semiguttatus DISTR: Argentina: Misiones. Also in Brazil, Paraguay (?). ECOR: Paranaen Forest. ST: LC ST1: LC
Hypsiboas varelae DISTR: Argentina: Chaco. ECOR: Humid Chaco. ST: DSA ST1: DD Itapotihyla langsdorfii DISTR: Argentina: Misiones. Also in Brazil, Paraguay. ECOR: Paranaen Forest. ST: vu ST1: LC
LAVILLA and HEATWOLE: AMPHIBIAN CONSERVATION AND DECLINE IN ARGENTINA Pseudis limellus DISTR: Argentina: Buenos Aires, Chaco, Corrientes, Entre Nos, Formosa, Santa Fe. Also in Bolivia, Brazil, Paraguay, Uruguay. ECOR: Dry Chaco, Humid Chaco, Esteros of Iberi, Campos and Malezales, Delta and Islands of the Parani River, Espinal, Pampan. S T LC ST1: LC Pseudis minutw DISTR Argentina: Buenos Aires, Corrientes, Entre Nos, Santa Fe, Santiago del Estero. Also in Brazil, Uruguay. ECOR: Humid Chaco, Delta and Islands of the Parani River, Pampan.. S T LC ST1: LC Pseudis platensis DISTR: Argentina: Buenos Aires, Chaco, Corrientes, Entre Rios, Formosa, Santa Fe. Also in Brazil, Paraguay. ECOR: Humid Chaco, Esteros of Iberi, Delta and Islands of the Parani River, Espinal. S T LC ST1: NE. Scinax auminatus DISTR: Argentina: Chaco, Corrientes, Entre Rios, Formosa, Santa Fe. Also in Bolivia, Brazil, Paraguay. ECOR: Dry Chaco, Humid Chaco, Esteros of Iberi, Campos and Malezales, Delta and Islands of the Parani River, Espinal. S T LC ST1: LC Scinax aromothyella DISTR: Argentina: Misiones. AIsU in Uruguay; Probably in Brazil and Paraguay.. ECOR: Paranaen Forest. ST: DD ST1: DD Scinax berthae DISTR: Argentina: Buenos Aires, Chaco, Corrientes, Entre Rios, Misiones, Santa Fe. Also in Brazil, Paraguay, Uruguay. ECOR: Paranaen Forest, Esteros of Iberi, Campos and Malezales, Delta and Islands of the Parani River, Espinal, Pampan. S T LC Scinax fxscomarginatus DISTR: Argentina: Chaco, Corrientes, Formosa, Santa Fe. Also in Bolivia, Brazil, Paraguay. ECOR: Humid Chaco, Esteros of Iberi, Campos and Malezales, Delta and Islands of the Parani River, Espinal. S T LC ST1: LC Scinax fwcovariw DISTR: Argentina: Chaco, Corrientes, Formosa, Jujuy, Misiones, Salta, Santa Fe, Santiago del Estero, Tucumhn. Also in Bolivia, Brazil, Parguay, Uruguay. ECOR: Yungas Forest, Dry Chaco, Humid Chaco, Paranaen Forest, Esteros of Iberh, Campos and Malezales, Delta and Islands of the Parani River, Espinal. ST. LC ST1: LC Scinax granulatw DISTR: Argentina: Buenos Aires, Entre Rios, Misiones. Also in Brazil, Uruguay. ECOR: Paranaen Forest, Delta and Islands of the Paranh River, Pampan. S T LC STl: LC
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Scinax nasicw DISTR: Argentina: Bnenos Ares, Cbrdoba, Chaco, Corrientes, Entre Rlos, Formosa, Jujuy, Misiones, Salta, Santiago del Estero, Santa Fe, Tucumin. Also in Bolivia, Brazil, Paraguay, Uruguay. ECOR: Yungas Forest, Dry Chaco, Humid Chaco, Paranaen Forest, Esteros of Iberri, Campos and Malezales, Delta and Islands of the Paranh River, Espinal, Pampan. S T LC STI: LC Scinax perereca DISTR: Argentina: Misiones. Also in Brazil. ECOR: Paranaen Forest. S T vu ST1: LC Scinax squalirostris DISTR: Argentina: Buenos Aires, Chaco, Corrientes, Entre Rios, Formosa, Misiones, Santa Fe. Also in Bolivia, Brazil, Paraguay, Uruguay. ECOR: Dry Chaco, Humid Chaco, Paranaen Forest, Esteros of Iberi, Campos and Malezales, Delta and Islands of the Parani River, Espinal. S T LC STI: LC Scinax uruguayus DISTR: Argentina: Corrientes. Also in Brasil, Uruguay. ECOR: Paranaen Forest, Campos and Malezales. S T DD ST1: LC Trachycephalus imitatrix DISTR: Argentina: Misiones. Also in Brazil. ECOR: Paranaen Forest. S T DD ST1: LC Trachycephalw venulosus DISTR: Argentina: Chaco, Corrientes, Entre Rfos, Formosa, Jnjny, Misiones, Salta, Santiago del Estero, Santa Fe. Widespread in Middle and South America. ECOR: Yungas Forest, Dry Chaco, Humid Chaco, Paranaen Forest, Esteros of Iberi, Campos and Malezales, Delta and Islands of the Parani River. S T LC
PHYLLOMEDUSINAE Phyllomedwa azurea DISTR: Argentina: Chaco, Corrientes, Formosa, Salta, Santiago del Estero, Santa Fe. Also in Bolivia, Brasil, Paraguay. ECOR: Dry Chaco, Humid Chaco, Esteros of Iberi, Delta and Islands of the Paranh River, Espinal. S T LC (as Phyllomedwa hypochondrialis azurea). ST1: NE. Phyllomedwa boliuiana DISTR: Argentina: Jujuy, Salta. Also in Bolivia, Brasil. ECOR: Yungas Forest, Dry Chaco. S T vu ST1: LC Phyllomedusa sauvagii DISTR: Argentina: Cbrdoba, Chaco, Formosa, Jujuy, La Rioja, Salta, Santiago del Estero, Santa Fe, San Luis, Tucumin. Also in Bolivia, Brazil, Paraguay. ECOR: Yungas Forest, Dry Chaco, Humid Chaco, Esteros of Iberi. S T LC ST1: LC Phyllomedwa tetraploidea DISTR: Argentina: Misiones. Also in Brazil, Paraguay. ECOR: Paranaen Forest. S T vu ST1: LC
72
AMPHIBIAN BIOLOGY CENTROLENIDAE
Hyalinobatrachium uranoscopum DISTR: Argentina: Misiones. Also in Brazil. ECOR: Paranaen Forest. S T EN ST1: LC
LEPTODACTYLIDAE Leptodactylw bufonius DISTR: Argentina: Catamarca, Cbrdoba, Chaco, Corrientes, Entre Rios, Formosa, La Rioja, Mendoza, Misiones, Salta, Santiago del Estero, Santa Fe, San Juan, San Luis, Tucumin. Also in Bolivia, Brazil, Paraguay. ECOR: Monte of Sierras and Bolsones, Yungas Forest, Dry Chaco, Humid Chaco, Paranaen Forest, Esteros of Iberi, Delta and Islands of the Parani River, Espinal, Monte of Llanuras and Mesetas. S T LC STl: LC Leptodactylw chaquemis DISTR: Argentina: Catamarca, Cbrdoba, Chaco, Corrientes, Entre Rios, Formosa, Jujuy, Salta, Santiago del Estero, Santa Fe, Tucumin. Also in Bolivia, Brazil, Paraguay, Uruguay. ECOR: Monte of Sierras and Bolsones, Yungas Forest, Dry Chaco, Humid Chaco, Esteros of Iberi, Campos and Malezales, Delta and Islands of the Parani River, Espinal. S T LC Leptodactylus diptyx DISTR: Argentina: Corrientes, Chaco, Entre Rios, Formosa, Misiones, Santa Fe. Also in Bolivia, Paraguay. Brazil (?). ECOR: Humid Chaco, Paranaen Forest, Esteros of Iberi, Delta and Islands of the Parani River. S T DD ST1: LC Leptodactylus elenae DISTR: Argentina: Chaco, Corrientes, Entre Rios, Formosa, Jujuy, Misiones, Salta, Santa Fe, Santiago del Estem. Also in Bolivia, Brazil, Paraguay. ECOR: Yungas Forest, Dry Chaco, Humid Chaco, Paranaen Forest, Esteros of Iberi, Campos and Malezales, Delta and Islands of the Paranh fiver, Espinal. S T LC ST1: LC Leptodactylus firnarius DISTR: Argentina: Misiones, Also in Bolivia, Brazil, Paraguay. ECOR: Paranaen Forest. S T DD ST1: LC Leptodactylw f w c w DISTR: Argentina: Chaco, Corrientes, Entre Rios, Formosa, Jujuy, Misiones, Salta, Santiago del Estero, Santa Fe, Tucumin. Also in Bolivia, Brazil, Colombia, French Guiana, Guyana, Panami, Paraguay, P e h , Surinam, Tobago, Trinidad, Venezuela. ECOR: Yungas Forest, Dry Chaco, Humid Chaco, Paranaen Forest, Esteros of Iberi, Campos and Malezales, Delta and Islands of the Parani River, Espinal. S T LC ST1: LC Leptodactylus gracilis DISTR: Argentina: Buenos Aires, Catamarca, Cbrdoba, Chaco, Corrientes, Entre Nos, Formosa, Jujuy, La Pampa, Misiones, Salta, Santa Fe, San Luis, Santiago del Estem,Tucumin. Also in Bolivia, Brazil, Paraguay, Uruguay.
ECOR: Yungas Forest, Dry Chaco, Humid Chaco, Paranaen Forest, Esteros of Iberi, Campos and Malezales, Delta and Islands of the Parani River, Espinal, Pampan. S T LC STl: LC Leptodactylus labyrinthicw DISTR: Argentina: Corrientes, Misiones. Also in Bolivia, Brazil, Paraguay. Venezuela? ECOR: Paranaen Forest, Campos and Malezales. S T vu STl: LC Leptodactylus laticeps DISTR: Argentina: Chaco, Cbrdoba, Formosa, Salta, Santiago del Estero, Santa Fe. Also in Bolivia, Paraguay. ECOR: Dry Chaco, Humid Chaco. S T vu ST1: NT Leptodactylus latinasus DISTR: Argentina: Buenos Aires, Catamarca, Cbrdoba, Corrientes,Chaco, Entre Rios, Formosa, Jujuy, La Pampa, Salta, Santa Fe, Santiago del Estero, Tucumin. Also in Bolivia, Brazil, Paraguay, Uruguay. ECOR: Yungas Forest, Dry Chaco, Humid Chaco, Esteros of Iberi, Campos and Malezales, Delta and Islands of the Parani River, Espinal, Pampan, Monte of Llanuras and Mesetas. S T LC STl: LC Leptodactylus mystacinw DISTR: Argentina: Buenos Aires, Catamarca, Cbrdoba, Corrientes, Chaco, Chubut, Entre Nos, Formosa, Jujuy, La Pampa, Misiones, Rio Negro, Salta, Santiago del Estero, Santa Fe, San Luis, Tucumin. Also in Bolivia, Brazil, Paraguay, Uru uay ECOR: Yungas Forfst, b r y Chaco, Humid Chaco, Paranaen Forest, Esteros of Iberi, Campos and Malezales, Delta and Islands of the Parani River, Espinal, Pampan. S T LC ST1: LC Leptodactylw ocellatus DISTR: Argentina: Buenos Aires, Cbrdoba, Chaco, Corrientes, Entre Nos, Formosa, La Pampa, Mendoza, Misiones, NeuquCn, Rio Negro, Santa Fe, San Juan, San Luis. Also in Bolivia, Brazil, Colombia, French Guiana, Guyana, Paraguay, Suriname, Tobago, Trinidad, Uruguay, Venezuela. ECOR: Dry Chaco, Humid Chaco, Paranaen Forest, Esteros of Iberi, Campos and Malezales, Delta and Islands of the Parani River, Espinal, Pampan, Monte of Llanuras and Mesetas. S T LC ST1: LC Leptodactylw plaumanni DISTR: Argentina: Misiones. Also in Brazil. ECOR: Paranaen Forest. S T LC ST1: LC Leptodactylw podicipinus DISTR: Argentina: Chaco, Corrientes, Entre Rios, Formosa, Misiones, Santa Fe. Also in Bolivia, Brazil, Paraguay, Uruguay. ECOR: Dry Chaco, Humid Chaco, Paranaen Forest, Esteros of Iberi, Campos and Malezales, Delta and Islands of the Parani River. S T LC ST1: LC
LAVILLA and HEATWOLE: AMPHIBIAN CONSERVATION AND DECLINE IN ARGENTINA CERATOPHRYIDAE CERATOPHRYINAE Batrachylini Atelognathus afi grandisonae DISTR: Argentina: Santa Cruz. ECOR: Patagonian woodlands. S T DD ST1: NE. Atelognathus nitoi DISTR: Argentina: Rio Negro. ECOR. Patagonian woodlands. S T vu ST1: VU Atelognathus patagonicus DISTR: Argentina: Neuqutn ECOR: Patagonian steppe. S T CR ST1: EN Atelognathus praebasalticus praebasalticus DISTR: Argentina: Neuqutn (Laguna del Teru). ECOR: Patagonian steppe. ST W ST1: Subspecies: NE; the species is considered EN Atelognathus praebasalticus agilis DISTR: Argentina: Neuqutn (Meseta Casa de Piedra). ECOR: Patagonian steppe. S T vu ST1: Subspecies: NE; the species is considered EN Atelognathus praebasalticus dobe$awi DISTR: Argentina: Neuqutn (Barda de Santo Tomis). ECOR: Patagonian steppe. S T vu ST1: Subspecies: NE; the species is considered EN Atelognathus praebasalticus luisi DISTR: Argentina: Neuqutn (Lagnna Overa, CantaLil). ECOR: Patagonian steppe. S T vu ST1: Subspecies: NE; the species is considered EN Atelognathus reverberii DISTR: Argentina: Rio Negro. ECOR: Patagonian steppe. ST W ST1: EN Atelognathus salai DISTR: Argentina: Santa Cruz. ECOR: PaGgonian woodlands. S T vu Atelognathus solitarius DISTR: Argentina: Rio Negro ECOR: Patagonian steppe. S T vu ST1: VU Batrachvla antartandica DISTR: h e n t i n a : Neuqutn, Rio Negro, Chubut. Also in Chile. ECOR: Patagonian woodlands.
Batrachyla fitzroya DISTR: Argentina: Chubut. ECOR: Patagonian woodlands. ST: DD ST1: VU
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Batrachyla leptopus DISTR: Argentina: Neuqutn, Rio Negro, Chubut. Also in Chile. ECOR: Patagonian woodlands. S T LC ST1: LC Batrachyla taeniata DISTR: Argentina: Neuqutn, Rio Negro, Chubut. Also in Chile. ECOR: Patagonian woodlands. S T LC ST1: LC
Ceratophryini Ceratophrys cranwelli DISTR: Argentina: Cbrdoba, Chaco, Corrientes, Entre Rios, Formosa, Jujuy, Salta, Santiago del Estero, Santa Fe, Tucumin. Also in Bolivia, Brazil, Paraguay. ECOR: Dry Chaco, Humid Chaco, Esteros of Iberi, Espinal, Monte of Llanuras and Mesetas. S T LC ST1: LC Ceratophrys ornata DISTR: Argentina: Buenos Aires, Cbrdoba, Entre Rios, La Pampa, Santa Fe. Also in Uruguay, Brazil. ECOR: Espinal, Pampan. S T LC ST1: NT Chacophrys pierottii DISTR: Argentina: Catamarca, Cbrdoba, Chaco, Formosa, La Rioja, Salta, San Juan, San Luis, Santiago del Estero. Also in Bolivia, Paraguay. ECOR: Monte of Sierras and Bolsones, Dry Chaco. S T LC ST1: LC Lepidobatrachus asper DISTR: Argentina: Chaco, Cbrdoba, Corrientes, Formosa, Santa Fe, Santiago del Estero. Also in Paraguay. ECOR: Dry Chaco, Humid Chaco, Esteros of Iberi. S T LC ST1: NT Lepidobatrachus laeuis DISTR: Argentina: Corrientes, Chaco, Formosa, Salta, Santa Fe. Also in Paraguay, Bolivia. ECOR: Dry Chaco, Humid Chaco. S T LC ST1: LC Lepidobatrachw llanensis DISTR: Argentina: Catamarca, Cbrdoba, Chaco, Formosa, La Rioja, Salta, Santiago del Estero. Also in Paraguay. ECOR: Monte of Sierras and Bolsones, Dry Chaco, Humid Chaco. S T LC ST1: LC
TELMATOBIINAE Telmatobius atacamensis DISTR: Argentina: Salta. ECOR: Puna. S T CR ST1: CR Telmatobius cewrum DISTR: Argentina: Catamarca, Tucumin. ECOR: Yungas Forest. ST: EX ST1: EN
AMPHIBIAN BIOLOGY Telmatobius contrerasi DISTR: Argentina: San Juan ECOR: High Andean. ST: DD ST1: DD Telmatobius hauthali DISTR: Argentina: Catamarca. ECOR: High Andean. S T vu ST1: VU Telmatobius hypselocephalus DISTR: Argentina: Jujuy. ECOR: Puna. S T DD STI: EN
CYCLORAMPHIDAE Alsodes awtralis DISTR: Argentina: Neuquen, Chubut. Also in Chile ECOR: Patagonian woodlands. S T DD ST1: DD Alsodes gargola gargola DISTR: Argentina: Rio Negro, Chubut. ECOR: Patagonian steppe, Patagonian woodlands. S T LC STI: Subspecies: NE; the species is considered LC Alsodes gargola neuquensis DISTR: Argentina: NeuquCn. ECOR: Patagonian woodlands. S T vu ST1: Subspecies: NE; the species is considered LC
Telmatobius laticeps DISTR: Argentina: Tucumin. ECOR: Puna. S T EX ST1: EN
Abodes pehuenche DISTR: Argentina: Mendoza. ECOR: paGgonian steppe ST: DD
Telmatobiw marmoratw (?) DISTR: Argentina: Jujuy, Salta. Also in Peni, Bolivia, Chile. ECOR: Puna. S T DD ST1: Argentinean populations NE.
Alsodes uerrucosw DISTR: Argentina: NeuquCn, Rio Negro. Also in Chile. ECOR: Patagonian steppe, Patagonian woodlands. S T DD ST1: DD
Telmatobius oxycephalus DISTR: Argentina: Jujuy, Salta. ECOR: Yungas Forest. S T VU ST1: VU
Eupsophw calcaratw DISTR: Argentina NeuquCn, Rio Negro, Chubut. Also in Chile. ECOR: Patagonian woodlands. S T vu STI: LC
Telmatobius pinguiculus DISTR: Argentina: Catamarca. ECOR: Puna. S T DD ST1: DD
Eupsophw emiliopugini DISTR: Argentina: Chubut. Also in Chile. ECOR: Patagonian woodlands. S T vu ST1: LC
Telmatobius pisanoi DISTR: Argentina: Catamarca, Tucumin. ECOR: Puna. S T CR ST1: EN
Eupsopw uertebralis DISTR: Argentina: Rio Negro. Also in Chile. ECOR: Patagonian woodlands. S T DSA ST1: NT
Telmatobius platycephahs DISTR. Argentina: Jujuy. ECOR: Puna. S T DD ST1: EN
Hylorina sylvatica DISTR: Argentina: NeuquCn, Rio Negro, Chubut. Also in Chile. ECOR: Patagonian woodlands. S T vu ST1: LC
Telmatobius rubigo DISTR: Argentina: Jujuy. ECOR: Puna. S T DD ST1:NE Telmatobius scrocchii DISTR: Argentina: Catamarca. ECOR: Puna. S T DD ST1:EN Telmatobius schreiteri DISTR: Argentina: La Rioja ECOR: Puna. S T vu ST1: EN Telmatobius stephani DISTR: Argentina: Catamarca. ECOR: Yungas Forest. S T vu ST1: EN
Limnomedwa macroglossa DISTR: Argentina: Entre Rlos, Misiones. Also in Brazil, Uruguay. ECOR: Paranaen Forest. S T LC ST1: LC Odontophrynus achalensis DISTR: Argentina: Cbrdoba, San Luis. ECOR: Dry Chaco. ST: VU ST1: VU
Odontophrynw americanw DISTR: Argentina: Buenos Ares, Catamarca, Cbrdoba, Chaco, Corrientes, Entre Rios, Formosa, Jujuy, La Pampa, La Rioja, Misiones, Rio Negro, Salta, Santiago del Estero, Santa Fe, San Luis, Tucumin. Also in Brazil, Paraguay, Uruguay. Bolivia (?). ECOR: Yungas Forest, Dry Chaco, Humid Chaco, Paranaen Forest, Esteros of Iberi, Campos and
LAVILLA and HEATWOLE: AMPHIBIAN CONSERVATION AND DECLINE IN ARGENTINA Malezales, Delta and Islands of the Parani River, Espinal, Pampan. ST: LC STl: LC Odontophrynus barrioi DISTR: Argentina: La Rioja. ECOR: Monte of Sierras and Bolsones. S T DD ST1: DD Odontophrynus cordobae DISTR: Argentina: Cbrdoba. ECOR: Dry Chaco, Espinal. S T DD ST1: LC Odontophrynus lavilhi DISTR: Argentina: Chaco, Jujuy, Salta, Santiago del Estero. Also in Bolivia, Paraguay. ECOR: Dry Chaco, Humid Chaco. S T LC ST1: LC Odontophrynus occidentalis DISTR: Argentina: Buenos Aires, Cbrdoba, La Pampa, La Rioja, Mendoza, Neuquen, Rio Negro, San Juan, San Luis. ECOR: of Sierras and Bolsones, Dry Chaco, Espinal, Pampan, Monte of Llanuras and Mesetas. S T LC ST1: LC Proceratqph~saavelinoi DISTR: Argentina: Misiones. Also in Brazil, Paraguay. ECOR: Paranaen Forest. S T vu ST1: LC C Proceratophrys bigibbosa DISTR: Argentina: Misiones. Also in Brazil. ECOR: Paranaen Forest. ST W ST1: NT Rhinoderm darujinii DISTR: Argentina: Neuquen, Rio Negro. Also in Chile. ECOR: Patagonian woodlands. ST. vu ST1: VU
LEIUPERIDAE Physalaemw albonotatus DISTR: Argentina: Buenos Aires, Chaco, Corrientes, Entre Nos, Formosa, Misiones, Santa Fe. Also in Bolivia, Brazil, Paraguay. ECOR: Humid Chaco, Paranaen Forest, Esteros of Iberi, Campos and Malezales, Delta and Islands of the Parani ~ i v e i Espinal , S T LC Physalaemus biligonigerus DISTR: Argentina: Buenos Ares, Catamarca, Cbrdoba, Chaco, Corrientes, Entre Rios, Formosa, Jujuy, La Pampa, La Rioja, Misiones, San Luis, Salta, Santiago del Estero, Santa Fe, Tucumin. Also in Bolivia, Brazil, Paraguay, Uruguay. ECOR: Yungas Forest, Dry Chaco, Humid Chaco, Paranaen F o ~ s t ,Esteros of Iberi, Campos and Malezales, Delta and Islands of the Parani River, Espinal, Pampan. S T LC ST1: LC Physaluemus cuqui DISTR: Argentina: Formosa, Jujuy, Salta. Also in Bolivia. ECOR: Yungas Forest, Dry Chaco. S T LC ST1: LC
75
Physalaemw cuuieri DISTR: Argentina: Corrientes, Misiones. Also in Brazil, Parguay. ECOR: Paranaen Forest, Campos and Malezales. S T LC ST1: LC Physalaemus fernanderae DISTR: Argentina: Buenos Aires, Entre Rios. Also in Uruguay. ECOR: Espinal, Pampa. ST: LC ST1: LC Physaluemw aff. gracilis DISTR: Argentina: Misiones. Also in Brazil, Uruguay. ECOR: Paranaen Forest. S T LC ST1: LC Physalaemw hemelii DISTR: Argentina: Buenos Aires, Entre Rios. Also in Brazil, Uruguay. ECOR: Pampan. S T LC ST1: LC Physalaemus riograndensis DISTR: Qentina: Chaco, Corrientes, Entre Nos, Formosa, Misiones, Santa Fe. Also in Brazil, Uruguay, Paraguay. ECOR: Humid Chaco, Paranaen Forest, Esteros of Iberi, Campos and Malezales, Delta and Islands of the Parani River, Espinal, Pampan. ST: LC ST1: LC Physalaemus santafecinus DISTR: Argentina: Chaco, Corrientes, Entre Nos, Santa Fe. ECOR: Humid Chaco, Esteros of Iberi, Delta and Islands of the Parani River. ST. LC ST1: LC Pleurodema borellii DISTR: Argentina: Catamarca, Jujuy, Salta, Tucumin. Also in Bolivia. ECOR: Yungas Forest, Dry Chaco. ST: LC ST1: LC Pleurodema bufoninum DISTR: Argentina: Mendoza, Neuquen, Rio Negro, Chubut, Santa Cruz. Also in Chile. ECOR: Patagonian steppe, Patagonian woodlands. ST: LC ST1: LC Pleurodema cinereum DISTR: Argentina: Jujuy, Salta. Also in Bolivia, Peni. ECOR: High Andean, Puna. S T LC ST1: LC Pleurodema cordobae DISTR: Argentina: Cbrdoba. ECOR: Dry Chaco. ST. DD ST1: NE Pleurodema guayapae DISTR: Argentina: Catamarca, Cbrdoba, La Rioja, San Juan, Santiago del Estero. Also in Bolivia. ECOR: Monte of Sierras and Bolsones, Dry Chaco. S T LC ST1: LC
76
AMPHIBIAN BIOLOGY
Pleurodema krieai DISTR: Argentina: C6rdoba. ECOR: Dry Chaco. ST: VU ST1: NT Pleurodema marmoratum DISTR: Argentina: Jujuy. Also in Bolivia, Chile, P e h . ECOR: High Andean, Puna. S T vu ST1: LC
Pleurodema nebulosum DISTR: Argentina: Catamarca, C6rdoba, La Pampa, La Rioja, Mendoza, Rio Negro, Salta, San Juan, San Luis, TucumPn. ECOR: Monte of Sierras and Bolsones, Dry Chaco, Espinal, Monte of Llanuras and Mesetas. S T LC ST1: LC Pleurodema thaul DISTR: Argentina: Neuqutn, Rio Negro, Chubut. Also in Chile. ECOR: Patagonian woodlands. ST: LC ST1: LC
Pleurodema tucumanum DISTR: Argentina: Catamarca, C6rdoba, Chaco, Jujuy, Mendoza, Salta, Santiago del Estem, San Juan, San Luis, TucumPn. ECOR: Monte of Sierras and Bolsones, Yungas Forest, Dry Chaco, Espinal, Monte of Llanuras and Mesetas. ST: LC ST1: LC Pseudopaludicola boliuiana DISTR: Argentina: Corrientes, Chaco, Formosa, Santa Fe. Also in Bolivia, Brazil, Colombia, Guyana, Paraguay, Surinam, Venezuela. ECOR: Dry Chaco, Humid Chaco, Esteros of IberP, Delta and Islands of the ParanP River. S T LC ST1: LC Pseudopaludicola falcipes DISTR: Argentina: Buenos Ares, Chaco, Corrientes, Entre Rios, Formosa, Misiones, Santa Fe. Also in Brazil, Paraguay, Uruguay. ECOR: Humid Chaco, Paranaen Forest, Esteros of IberP, Campos and Malezales, Delta and Islands of the Parani River, Espinal, Pampan. S T LC ST1: LC
Pseudopaludicola mirandae DISTR: Argentina: Corrientes. ECOR: Esteros of IberP. ST. DSA ST1: DD Pseudopaludicola mystacalis DISTR: Argentina: Corrientes, Misiones. Also in Bolivia, Brazil, Paraguay. ECOR: Humid Chaco, Paranaen Forest, Esteros of IberP, Campos and Malezales, Delta and Islands of the ParanP River, Espinal. ST: LC ST1: LC
Somuncuria somuncurensb DISTR: Argentina: Rio Negm. ECOR: Monte of Llanuras and Mesetas. S T EN ST1: CR
BUFONIDAE Melanophrynircus atrolutew DISTR: Argentina: Corrientes, Entre Rios, Misiones, Santa Fe. Also in Brazil, Paraguay, Uruguay. ECOR: Humid Chaco, Paranaen Forest, Campos and Malezales, Espinal. S T LC ST1: LC
Melanophyniscus cupreuscapularis DISTR: Argentina: Corrientes. ECOR: Humid Chaco, Esteros of IberP. S T VU ST1: NT Melanophryniscus devincenri DISTR: Argentina: Misiones. Also in Uruguay ECOR: Paranaen Forest. S T vu ST1: EN Melanophryniscw jkluoguttatus DISTR: Argentina: Formosa. Also in Paraguay ECOR: Humid Chaco. S T DD STl: LC Melanophrynircus klappenbachi DISTR: Argentina: Chaco, Corrientes, Formosa, Santiago del Estero. Also in Paraguay. ECOR: Dry Chaco, Humid Chaco, Esteros of IberA. S T LC ST1: LC Mehnophryniscw krauczuki DISTR: Argentina: Misiones. Also in Paraguay, ECOR: Paranaen Forest. S T DD STl: DD Melanophryniscus rubriventris DISTR: Argentina: Jujuy, Salta. Also in Bolivia (?) ECOR: Yungas Forest. ST. vu ST1: LC
Melanophyniscus stelzneti stelznwi DISTR: Argentina: C6rdoba, San Luis. ECOR: Dry Chaco. ST: vu ST1: Subspecies: NE; the species is considered LC Melanophyniscus stelzneri spegazzinii DISTR: Argentina: Salta. ECOR. Yungas Forest. S T DSA ST1: Subspecies: NE; the species is considered LC Melanophryniscus aff. tumzfrom DISTR: Argentina: Misiones. Also in Brazil, Paraguay. ECOR: Paranaen Forest. S T LC ST1: LC. Nannophryne uarkgata DISTR: Argentina: NeuquCn, Rio Negro, Chubut, Santa Cruz. Also in Chile. ECOR: Patagonian woodlands. S T LC ST1: LC
Rhinella achalensb DISTR: Argentina: Cordoba, San Luis. ECOR: Dry Chaco. S T vu ST1: NT
LIVILLA and HEATWOLE: AMPHIBIAN CONSERVATION AND DECLINE IN ARGENTINA
77
Rhinello arenarum arenarum DISTR: Argentina: Buenos Aires, Catamarca, Cbrdoba, Chaco, Chubut, Entre Rios, Jujuy, La Pampa, La Rioja, biendoza, NeuquCn, Rio Negro, Salta, Santiago del Estero, Santa Fe, San Juan, San Luis, Tucumin. Also in Bolivia, B r a d Uruguay. ECOR: Yungas hrest, Dry Chaco, Humid Chaco, Delta and Islands of the Parani River, Espinal, Pampan, Monte of Uanuras and Mesetas. ST: LC STl: Subspecies: NE; the species is considered LC
Rhinella rubropunctata DISTR: Argentina: Neuquen, Rio Negro, Chubut. Also in Chile. ECOR: Patagonian woodlands. ST: VU ST1: VU
RhincUa arenarum mendocinus Dim Argentina: Mendoza. ECOR: Patagonian Steppe. ST: \v STl: Subspecies: NE; the species is considered LC
Rhinella schnezderi DISTR: Argentina: Catamarca, C6rdoba, Chaco, Corrientes, Entre Rios, Formosa, Jujuy, Misiones, Salta, Santiago del Estero, Santa Fe, Tucumin. Also in Bolivia, Brazil, Paraguay, Uruguay. ECOR: Yungas Forest, Dry Chaco, Humid Chaco, Paranaen Forest, Esteros of Iberi, Campos and Malezales, Delta and Islands of the Parand River, Espinal. ST: LC ST1: LC
Rhinella bergi DISTR: Argentina: Cbrdoba, Corrientes, Chaco, Formosa, Santa Fe. Also in Brazil, Paraguay. ECOR: Dry Chaco, Humid Chaco, Esteros of Iberi, Campos and Malezales, Delta and Islands of the Parani River, Espinal. S T LC ST1: LC Rhinella dorbignyi DISTR: Argentina: Buenos Ares, La Pampa. Also in Brazil, Uruguay. ECOR: F'ampan. S T LC STl: LC Rhinella fernandeze DISTR: Argentina: Buenos A r e s , Cordoba, Chaco, Corrientes, Entre Rios, Formosa, Santa Fe; La Pampa (?). Also in Brazil, Paraguay, Uruguay. ECOR: Dry Chaco, Humid Chaco, Esteros of Iberd, Campos and Malezales, Delta and Islands of the Parani River, Espinal, Pampan. ST: LC S T l : LC Rhinella galla~doi DISTR: Argentina: Jujuy. ECOR: Yungas Forest. S T vu STl: EN Rhinella gnustae DISTR: Argentina: Jujuy. ECOR: Puna. S T DSA ST1: DD
RhineUa major DISIE Argentina: Chaco, Corrientes, Formosa, Jujuy, Salta, Santiago del Estero, Santa Fe. Also in Bolivia, Paraguay. ECOR: Dry Chaco, Humid Chaco, Esteros of Iberd, Campos and Malezales, Delta and Islands of the Parani River, Espinal. S T LC ST1: Subspecies: NE; the species is considered LC Rhine& icterica DISTR: h e n t i n a : Corrientes, Misiones. Also in Brazil, Paraguay. ECOR: F'aranaen Forest, Campos and Malezales. S T LC Rhine& m t a DISTR: Argentina: Corrientes, Misiones. Also in Brazil, Paraguay. ECOR: Paranaen Forest, Campos and Malezales. S T LC (as Bufo crucifer). ST1: NE
Rhinella rumbolli DISTR: Argentina: Jujuy, Salta. ECOR: Yungas Forest. ST: vu ST1: VU
Rhinella spinulosa spinulosa DISTR: Argentina: Catamarca, Jujuy, La Rioja, Mendoza, San Juan, Salta, Tucumin. Also in Peni, Bolivia, Chile. ECOR: High Andean, Puna, Yungas Forest. ST. LC ST1: Subspecies: NE; the species is considered LC Rhinella spinulosa papillosa DISTR: Argentina: Neuqutn, Rio Negro, Chubut, Santa Cruz. Also in Chile. ECOR: Patagonian steppe, Patagonian woodlands. S T LC ST1: Subspecies: NE; the species is considered LC HYLODIDAE Crossodactylw dirpar DISTR: Argentina: Misiones (?). Also in Brazil. ECOR: Paranaen Forest. S T DSA STl: DD Cro~sodact~lus schmidtii DISTR: Argentina: Misiones. Also in Brazil. ECOR: Paranaen Forest. S T VU STI: NT
MICROHYLIDAE GASTROPHRYNINAE Dermatonotw muelleri DISTR: Argentina: Chaco, Corrientes, Formosa, Jujuy, Salta, Santiago del Estero, Santa Fe. Also in Bolivia, Paraguay, Brazil. ECOR: Dry Chaco, Humid Chaco, Esteros of Iberi, Delta and Islands of the Parani River. S T LC ST1: LC Elachistocleis bicolor DISTR: Argentina: Salta, Buenos Ares, Cbrdoba, Chaco, Corrientes, Entre Rios, Formosa, Misiones, Santiago del Estero, Santa Fe. Also in Bolivia, Brazil, Paraguay, Uruguay. ECOR: Dry Chaco, Humid Chaco, Paranaen Forest, Esteros of Iberd, Campos and Malezales, Delta and Islands of the Parani River, Espinal, Pampan. S T LC ST1: LC Elachistocleis skotogaster DISTR: Argentina: Salta. ECOR: Yungas Forest. ST: DD STl: DD
AMPHIBIAN BIOLOGY
APPENDIX 2 Recent changes in the nomenclature of Argentine amphibians
Lavilla and Cei (2001)
Frost et al., 2006; Grant et al. 2006; Aguiar et al., 2007; Chaparro et al., 2007; Hedges et al., 2008.
Gymnophiona
Typhlonectidae: Chthonerpeton
Caeciliidae: Chthonerpeton
Bufonidae: Bufo (part)
Bufonidae: Rhinella
Bufonidae: Bufo (part)
Bufonidae: Nannophryne
Hylidae: Gastrotheca
Amphignathodontidae: Gastrotheca
Hylidae: Hyla (part)
Hylidae: Dendropsophus
Hylidae: Hyla (part)
Hylidae: Hypsibom
Hylidae: Osteocephalw
Hylidae: Itapotihyla
H~lidae:Phrynohyas
Hylidae: Trachycephalw
Pseudidae: Lysapsw
Hylidae: Pseudis
Pseudidae: Pseudis
Hylidae: Pseudis
Leptodactylidae: Eleutherodactylw (part)
Brachycephalidae: Zschnocnem
Leptodactylidae: Eleutherodactylw (part)
Strabomantidae: Oreobates
Leptodactylidae: Atelognathw
Ceratophryidae: Atelognathus
Leptodactylidae: Batrachyla
Ceratophryidae: Batrachyla
Leptodactylidae: Ceratophrys
Ceratophryidae: Ceratophrys
Leptodactylidae: Chacophrys
Ceratophryidae: Chacophrys
Leptodactylidae: Lepidobatrachw
Ceratophryidae: Lzpidobatrachw
Leptodactylidae: Telmatobius
Ceratophryidae: Telmtobiw
Leptodactylidae: Alsodes
Cycloramphidae: Alsodes
Le~todactylidae:Eupsophw
Cycloramphidae: Eupsophw
Leptodactylidae: Hylorina
Cycloramphidae: Hylorina
Leptodactylidae: Limnomedwa
Cycloramphidae: Limnomedwa
Leptodactylidae: Odontophrynw
Cycloramphidae: Odontophrynw
Leptodactylidae: Proceratophrys
Cyclorarnphidae: Proceratophrys
Leptodactylidae: Crossodactylus
Hylodidae: Crossodactylus
Leptodactylidae: Physalaemw, Pleurodema, Pseudopaludicola and Somuncuria.
Leiuperidae: Physahemw, Pleurodema, Pseudopaludicola and Somuncuria.
Rhinodermatidae: Rhinoderma
Cycloramphidae: Rhinoderma
The W: ISBN Q 949324 53 1 this Volume: ISBN 978 O 9803113 4 1
