The shell in Vampyropoda (Cephalopoda): morphology, functional role and evolution

/ssN 0136-0027 /sBN5-87317-182-3

V. A. BIZIKoV

T H E SHELL IN

VnMPYRoPoDA (cEPTTALOPODA): MORPHOLOGY, FUNCTIONAL ROLE AND EVOLUTION

Bcepocculr cxww HavqHo-I,{cc,rretroBare.'rscxuii zTHCTWTy r prr6noro xosqr4crBa r{ oKeaHorpaQtm (BHI4PO)

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B. A . Bvr3trr(oB

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PAKOBI4HA VAVTPYROPODA (CEPHALOPODA): Mop+ oilorvrfl' {yr*rlrdoHa

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Ruthenica,Supplement 3 Moscow + December,2004

CONTENTS Introduction N'laterial and methods R t . u l ts \1n rrt7tltrot eut Ii s i nfenn I i s Op i -*t In t eut lr is califontinn Grimpotcuthis un*ellata

3 5 8 B t4 ,n

Cin'oteuthis ntutIIet i Enteroctopus dofleiti Benthoctopus sibiricus

z+

Bathypofupus sslebro sus

29 35 40

Eledorrcnrcssyae

+.1

Alloposus mollis Ocythoetubet'culata

46

Argormuta

rtttdLtsn

Japetelladiaplnnn Antphitretus p elagicus

Discussssion

54 5B oz o.*

67

Variation of the shell stnrctr-rrc:ind shell-soft bodv relationship in Vampvropoda H o m o l o g i e s o f t h e s h c l l : r n r o n gV a m p v r o p c , d a The process of shell tr:ursformation Paleontological evidences Evolution of the shell in Vanrpvropocla R..-fcrcnces

6 7 -7 /1

1 A /-t

77 BO B4

Editor of the volurne: A, \'. Svsoev -Stntc ntu\(ruttof .\loscotr' Zoologicnl lJnirercitt' Camera-ready copy: Yu. I. I(antor, A.l'l.Severtzoy lrtstituteof Ecologt& Et,olutiort, Russimt Ac. Sci O \/. A. Bizikor,.200.1 A Rutheuicn, 200,{, design

The shellin Vampyropoda(Cephalopoda): morphology, functionalrole and evolution \rvacheslav A. BIZIKOV lll-Russian Research lryyjlyte of Fisherv and Oceanography(V\{IRO\, V.-Krasnoselskayastr., l'. Juloscow,107110, RUSSIA; E-mail; bizikovQgvniro.ru

The sltell of mollusks is the part that determines the yvhole. AdolfNaef, 1921 .\BSTRACT. Comparativefunctionalmorphologl andmicr-rrstructurc of internalshellvestigeshavebeenstudiedin l.l )peciesof recentVampvropodaincludingthe singlerecent representative of vampire squids. I hrzp_r,roteuthis infernalis t ' h u n . 1 9 0 3 . 3s p e c i eos f C i r r a t aa n d l 0 s p e c i eos f l n c i r r a t a . Rciationship betrveen the shellandthe soft bodr rvasstudied irn totdlcross-sections ofthe mantleat differentplanes.The studl' sho.,vsthat the shell plal s different role in diff-erent groupsof eight-armedColeoidea.and evolutionof the shell rras strpulatcd b1,evolutionof its function.In I'antptroteutirrs.an eari) evolutionan,offshoot of the Vampr ropoda.the .hcll represents a q'pical gladiusof the teuthoidtvpe thar pror ides aftachmentsites for the tlns. mantle. funnel and neadretractors. and the r,isceralsac.In cirrateoctopodsthe -:iadiusrepresentsa remnantof coneflags. ri in-esand lateral rlatesof r ampvromorphgladius.* hich is transfbrnted mos:lr ip16, 'fin support'.In the Incirratathe shell is reduced ro parredrods.sn lets.functioningas anchorssupportingthe lirnuelretractors.In sereraladVancedIinea,ees of Incirrata lhe shellhas beenlost completelr. Iiach lineageof recentoctopodilbrms- \/ampvromorphida.Cirrataand Incirrata- has its ou n characteristic t\ pe i,t shcll structurcand shell-sof'tbodr relationships\\ride

separation of stellategangliain all recentoctopodspresents morphologicaler.'idence that this group evolvedfrom some \ anipvromorph-like ancestorrvith u'ide middle plateof gladiusproostracum. Tri o crucialeventstook placein evolution of the shell in octopodianlineage:reductionof the middle plate of proostracumand conus resulting in transformation of vampvroteuthoid-like gladiusintothegladiusof thecirrate tl pe: and reductionofthe transversal connection(saddle)in the cirrate gladius resulting in its transformationinto paired sn lets of the Incirrata.In Incirratathe shell underrventgradual reductionuntil its completeloss in severalevoived fbrms. This last e'"ent.completedisappearance of the shell. hasoccurredindependentllin all threeprincipallineagesof Incirrata:Octopodoidea. Bolitaenoidea and Argonautoidea. In all casesthe final loss of the shell rvasaccompanied b1 the reductionof jet-suimming in connection*ith development of a 'rvalking'habrtinr olving the arms(benthicOctopodoidea)or heavv relianceon passir,efloatationin pela_eic Bolitaenoidea and Argonautoidea. The final lossof the shell r estigesin advancedIncirratadid not chansetheir soli-bod1 design.*hich remainedgeneralll the sameas in primirire benthrcOctopodoidea.

INTRODUCTION

comprisesless than 0,004% of the body mass disappear in [Zuev.1965].But eventhesevestiges someoctopodlineages:Bolitenoidea. Argonautoidea. someOctopodoidea [Robson,1932:Voight.

Octopods have the most unusual shell among cephalopodmollusks. It differs greatll frorn rhe clrambered,coiled shell of the pearl,v Natttiltrs. tl'om the calcareousbuoyant sepionof cuttlefishes. and from the ciritinoussuppofiing pen (gladiusl of teuthids.Reduction of the shell that occurs in all groups of Coleoideareachesits apex in the Octopoda. In finned octopods (suborder Cirratal the shell is representedb1, a saddle-.butterflr.,-or Usirapedstructul'elvhile in finless octopods(subor.ier Incirrata) it is reduced to a pair of u'idel) separatedspindle-like rods. or sl,lets. situatedobliqLrely on the dorsal side of the rnantle [Naef. 19211231. Tl-restylets are verv small: their mass

teel).

Origin of octopod shell is obscure.Its morphological elements reveal no apparenthomology to a n ) ' p a f i o f t h e s h e l l o f o t h e r c o l e o i d s .b o t h r e c e n t and fossil. There is no trace of a phragrnoconeor proostracum.The octopod shell is soft and cafiilage-like. w'hich differs fi'om the hard. chitinoussubs t a n c eo f t h e t e u t h o i d g l a d i u s .N a e f [ 1 9 2 1 / 1 9 2 3 . p . 6 5 7 1n o t e d .' i t h a s t o b e a s s u r n e dt,h a t t h e s h e l l (of octopods)consistsrnainly' of a remnant of the proostracumtrith a flatteredcone'. However. even if Neaf is correct. ue do not know. u'hat oarls of

\

.{

Bizikor

Tabie L List of speciesexamined in the -stud) l-a6-'ruuaL Cnucox Hcc.re-toBaHHbr\ Btr,loB.

ORDER FAN,lILY

\umber ot' specimensexamined f-emales

Spec ies

h range. mnr males

\"{NIPYRO}IORPHIDA V A \ I P Y R OI E L T H I D A E I'dmp\)roteuthtsinfernalis Chun. 1903 CIRRATA OPISTHOTEUTHIDAE Oprstltoteuthiscaliforniana Berry. l9-19 Grintporeuthisumbellara(Fisher. 1883)

53-70

25

7 z

C I R R Of E U T H I D A E Cirroreuthismuelleri Eschricht.1838 INCIR-R{TA OCI'OPODIDAE Enteroctopusdo-fleini(\\rulker. l9l0) Benthoctopussibiricus Lolning. 1930 Bdth,tpollpus salebrostts(Sasaki. 1920) Eledone messr,oeVoss. 196:l

females

40 -

6'1

8 9 I I

AT,LOPOSIDAE .-llloposttsnrol1i.rVerrill. 1880

1 3 560-

14 49

65 -

80

16 l6

l9

265 175

128

63

145 260 83 - 200 4'7 - 56 35

63.67

57

TREMOCTOPODIDAE Trentoctoptts violaceusChiaie. 1830

l

57.60

OCYTHOIDAE Oc'.vthoe tuberculdtoRafinesque.1811

2

96. 103

ARGONAUI'IDAE Argonauta nodosa Solander.1786

94.108

BOLITAENIDAE Japetelladiaphana Hoyle. 1885 AMPHII'RLTIDAE .lntphitretuspelagicus Hoyle. 1885

the coleoid proostracumevolved into the octopod shell and why. We also do not know what the homology is betrveenthe U-shapedshell of Opisthoteuthidae.the saddle- or butterfly-shapedshell of the Cirroteuthidaeand the dorsal st1,letsof finless octopods.Possibleclues for understandingthe ongin and evolution of the shell in the Octopodama)' come from its sistergroup. Vampy'romorphidaPickford, 1939. The single living vamp\,romorph. Vantpyrotetiltis infernalis Chun. 1903. has a set of characterscombining such 'teuthid' featuresas a well-developed.chitinous gladius rvith a generall)' octopod-like brachial crown fPickford. 1919]. Vampyromorphida and Octopoda have long been united into a singletaxon with differentnames.first on the basis of general similaritl': Octobrachia fYoung. 1989]. later on the basisof morphological and genetic cladistic anal,vses:Varnpvropoda[Boletzky. 1992; i9991. Octopodiformes IBerrhold. E n g e s e r .1 9 8 7 ; Y o u n g , V e c c h i o n e .1 9 9 6 ; C a r l i n i . Graves.1999; Haas. 20021.The name Varnpyropoda (Boletzky. 1992) seemsto be the most appropriate and u,ill be usedin the presentpaper.It alludes

57 26

to thevampvromorphs. on the onehand.andto the cirroctopods and octopods.on the otherhand. Knorvledgeof the highly variablemorphologv of the shell in the Octopodais fragmentarr,. The shell is befter knorvn in those finned octopods u,hereit is usedin svstematic analysis[Aldredel ql.. 1983:Nesis.198211987 Collins.Henriques. 2000:Villanueva e/ al..20021.1n finlessoctopods detailsof the shellvestigeshavebeentraditionalll' absentfrom svstematic descriptions, andtheirver,r,, presenceis rarell.mentioned[Akimushkin.1963: Voight. 19971. The innerstructureof octopodshell and its growth patternhave not beenstudied. Morphologicalvariabilityof the octopodshell indicates variabilityof its function.In finnedoctopodsthe shell is commonlyconsidered a fin support. its flattenedlateralparls servingas the attachmentsitesfor thefin basesfRobson,1932. Aldred et al.. 19831.The functionof styletsin finlessoctopodsis not clear.Akimushkin[963] considered them as merevestigeswithoutany specificfunctio n . N a e f I q : I 1 q 2 3 p. . 6 7 6 1b e l i e v e rdh e s r rl e t s 'servemainll as pointsof attaclmtent fbr the ret-

Shell in Vaniplropoda

ractorsof funnel and cephalopodium'.The shell is clearll, not a uselessvestige. at least in species rvhereit is verl' large. If it is a supportingstructure. horv can suppoft be provided when the shell disappearscompletely.?While the generalfeaturesof the shell in the Vampvropoda is knorvn throughoutthe rvork of Naef 11921119231. Pickford [1949] and orhers. no svstematic study has been attempted to determineits structure.function and evolution. The presentpaper describesmorphology'of the shell and its functional relationshin with the soft body'in all n-rajorgroups of the Vamplropoda. and proposeshl,pothesison possible evolution of the s h e l l i n V a r n p rr o p o d a .

MATERIAL AND METHODS Foufieen speciesrepresentingmost farnilies of recent Vampvropoda. were studied.These include the single vampyromorph. Varnptl.oteuthisinferna1r.r.3 genera of cirrate octopods (Opisthoteuthis, Grintpoteulhis and Cirrotetilhis) and 10 genera of incirrate octopods (Octoptts, Benthoctopus, Bat/4'polypus, Eledone, Alloposus, Tremoctopus, Oct.rlne, Argonauta, Amphitretus andJapetella')(Table 1). Only two rare families u'ere beyond the scope of my study: the Stauroteuthidae(Cirrata) whose gladii rvere anal;-zedusing literaturedata [Collins. Henriques.2000], and the Viterledonellidae(lncirrata) that lack the shell completely fNesis. 198211981 : Voight. 19971. Abbreviations for the institutes and museums that housed the octopods examined here a r e : V N I R O - R u s s i a nF e d e r a lI n s t i t u t eo f F i s h e lr and Oceanography.Moscow: SIORAN - P.p. ShirshovInstitute of Oceanologl,.Moscor.v:AtlanTNIRO - Atlantic ResearchInstitute of Fisheries a n d O c e a n o g r a p h yZ; M M U - Z o o l o g i c a l M u s e Lrrnof Moscorv State University: NSMT - Natiorral ScienceMuseurn.Tok1,'o;TIFA - Tromso InstitLrte of Fisheriesand Aquaculture.Norwa1..Other .rbbreviationsused in the text are: ML - dorsal rnantle length; TL - total length; GL - gladius length; SD - standarddeviation: R/V - research r essel;F/V - fishery vessel.

ce

caecufl

c e np

central thickenedpart (in the shell of cirrate octopods cone lla_qs collar folds cartrlaginouslaver of the fln base collar fusion cone collar fusion cartilage filling the scars left by the st1lets after their reduction collar pockets crop dermls dorsal aorta dorsal ,qrooveon the mantle r.vall(in .-lntphitretus) digestivegland ventral -qrooveon the mantle rvall (in .lntphitretus) distal transversalmuscles(in fins of cirrate octopods) dorsal longitudinalmuscles(in fins of cirrate octopods) depressorntuscles anterodorsalmantle adductor dorsal intermediatemuscular laver of fins dorsal ridge of the saddle (in the gladius of crrrateoctopods) surfacelaver of dense musculartissue of fins (dorsal) elerator muscle

CF cfold cl colf

co c ol f cont cp crop d da dgd dgl dgv distl dlm dm dmad dml dr dsm em eye fad fc fch fb fc fin fla fo fun func gl brgl gon gr qst

\bbreviation used on figures llC

:rfl It nl

,lpl ;tur bcf hnd l' [) l)rnt !ilf

axial cartilaginouscore of the fins lateral funnel adductor mantle arter\ apical line (in stvlets of incirrateoctopods and in gladii of some squids) auricle basal carrilageof the fins bend (morphologicpan of the stl lets of incirrateoclopods) basal pockets brachial hearr ccphalrccartilage

hy'dr hvp i n cI in c2 ink KA kn LA lh lig

funnel adductors fin cartilage flrst check delimiting the postnuclearzone (in the _sladiusof cirrate octopods) fln base fin cartilague 1-ins closer bond of the funnel lunnel organ funnel funnel corner gills brachial gland gonad dorsal groove (in the shell of cirrate octopocls) stellar -eanglia hl drostatrc organ h1postracum lst order incrementsin the shell 2nd order incrementsin the shell ink sac marginal asvmptote knob-like surfacesculpture(in the sflle1s of lnclrrateoctopods) lateral asl,mptote lateral horns of the shell (in cirrate octopods ) risceral ligament connectingthe funnel retractor$ith the Visceralsac (rn Treilloctopus)

V. A. Bizikor

LP lrr \IA mam mat mcart mcd mcv me ml mla mn mnd mnv mo mpa nfin n mu s np NS

nuf oe ost ot'a ovi per peri pz Ra rant rc rfcart

ren rec rf rm RO sant sca sdl slg spost sh sh sac shi soc st stat sut test tun tub vd

lateral plates latcral nings of the gladius median as\mptote \r'ntral medran mantle adductor , i n l a r ' 1 rcj I\ t e n s r o n so f r e n t r a l m e d i a nm a n t l e a d d u c t o rn r u s c l c s m i l n t l c c a r t i l a g eo c c u p li n g p o s t t i o no f t h c tormer sn lets mantle caritr dorsal milntlc ca\ it\ \'entral e r t r a o c u l a re r e m u s c l e muscular layer of the fin base closer bond of the rnantle mantle d o r s a lm a n t l en a l l ventral mantle nall lateral openinesof the mantle apefture(in .lntphirretus ) rncdian pailial arterr fin nen c nuchal muscles(anteriormantle adductor) p a l l i a ln e n e Necdham sac nuchal lusion of the visceral sac s ith the mantle (in .'lnrphitretus) esophagus ostracunr o\ ar\ oviduct nephrrdialappendages periostracum postnuclearzone rach is anterior retractors of fins cephalopodial(head) retractors cafiilage at the inncr rnargin of rhe funnel rctractor rcnal appendages l'ectulll

funnel retractors(: posterodorsal mantle adductorsin Octopodidae) cartilasinousrim of the shell sac rosirum antcrior shoulderof the snlet (in incirrate oc opods) mantle scars ntarking position of the former shell in some incirrateoctopods saddle(medial part of the gladius in cirrate octopods) salivarr glands posteriorshoulderof the str let (in incirrate octopo0s ) shell shell sac initial shell spermatophoncorgans compler stomach statoc\sts suture linc of the lisceral sac IESTES

colla-eentunic t u b e - l i k ee r t e n s i o no f r e n t r a l m a n t l c s a l l around the funnel (in Cirroteuthis\ clermal ."ern

t'en llm vmI Ypp vS

vsm

\\' \14

rreb $?o

\ ena ca\ a r e n t r a l l o n g i t u d i n am l u s c l e s( i n t i n s o f cirrate octopods) r e n t r a l i n t e r m e d i a tm e u s c u l a rl a r c r o 1 ' f i n s postenor pallial Yein r isceral sac surfacelal er of dense musculartissue of fins (r entral) ri ings a n t c r i o rp a r l i o l - t h e * i n g s i n t h e s h e l l o f crrrateoctopods interbrachialrieb (in cirrate octopods) \\ ater pores

Vampyroteuthisinfernalis Chun, 1903. Three specimens \\'ere studied.T*o immature females(53 n'rm and 60 mm N,lL; *ere kindll prorided b1 Dr. K.N. Nesis (SIOR.A\) The specrmens\\ere sampled fiom a catch 'l1na:' of mid-riater tra*I durin,eR.,V cruise ,\l 17 in S \ \ ' I n d r a nO c e a n 9 . D e c e m b e r1. 9 8 8 .i n p o s i t i o n3 2 ' 5 3 ' S . . 1 . 1 ' l 2 ' E .D e p t h o f p l a c e : 1 2 8 0 m : f i s h i n g d e p t h : 1 2 6 0 m. The third specimen.maturing female. approx. 70 ntnr N'lL. rias kindll provided by Dr. T. Kubodera (NSMI ) 'fhe specirnenrias caught in West Pacific Ocean.28 Oct o b e r . 1 9 8 8 .i n p o s i t i o n3 1 " 0 3 ' S . 1 3 3 ' 0 7 ' E . ? d e p t h .I s a aks-Kidd mid-nater tranl: res. ,rtcNSMT-Mo66708. Opisthoteuthis californiana Berry, 1949. 32 specrmens \\ere studied.All specimensr.r'erecollectedduring 'Tenyu-.)Iartt a surve) onboard FIY Io 78' in the Western Bering Sea in Jul1. 1998. The specimensu,ere samplcd 'Ihe from the catchesof t*o commercialbottom tra*ls. traul Nr: I rias pertbrmed 29 Jull'. 1998 in position 5 q ' 5 8 ' \ . 1 6 7 ' 5 9 ' Ea r d e p r h- 1 5 0m . l r r i e l d e dl 9 s p c c i n r e n s including 2 mature t-emales(36 mm and 41 mm N,lt.). I immature female 19 mm ML and 16 mature malcs ( 1 2 . - 1 1 .1 . 1 .+ 6 . 1 6 . 1 7 . 4 8 . ' 1 9 . 5 0 . 5 4 . 5 4 . 5 5 . 5 8 . 5 8 . 62 and 6"1mm \4L), The tra"r,lNc 2 nas made the sanre d a r i n p o s i t i o n5 9 ' 5 7 ' N . 1 6 7 ' 5 7 ' E a t d e p t h , 1 0 0m . I r l i e l d e d 1 3 s p e c i r n e ni sn c l u d i n g2 m a t u r ei e m a l e( , l l a n d - l - l m m i v I L ) . 2 m a t u r i n gl t m a l e s ( 3 5 a n d 3 6 m m N l t _ ) and 9 mature males (.10.-12..1.1.17. 19.50. 51. 53 and 5-1mm N'lL). Grimpoteuthis umbellata (Fisher, 1883). Tuo rmmature l'emales1,19and approx. 45 mm N,lL) ',r'erestlrdred. Both specimensriere kindl., granted b1' Dr, K.l.J.Nesis (SIORAN). Ther *ere sampledand identifledb1'Dr. Nesis tiom the same boftom traul during R/V 'l'itla,- crulse "\ 65. in CentralAtlantic (Cape Verde Basin).31 1\,larch. 1 9 ' 1 9 .i n p o s i t i o n- 1 1 ' l - 1 ' N .l - l ' 2 8 ' \ V . a t d e p t h 5 31 0 m . 'fhe specimen,19 mm \,lL *as in good condition *hile anotherspecimennas badlr damagedbut rias believed to belong to thc same species.Total cross-sections scre made iiom one of the spccimens(49 nim N4L). and the sladius \\as e\tracted liont another. Cirroteutltis muelleri Eschricht, 1836. Fire specimcns 'l'he (t\\o samples)*ere studied. llrst sample(l mrruring l e m a l e : 7 8 m m M L ) r ' a s k i n d l l p r o ri d e d b y D r . K . N . Nesis(SIORAN). The specimennas sarnpledliom a catch of pelagictranl ('Aeassiz't)pe) madeonboardNY' f'ctltu' Stenr' (crurseARK XL'1) in \orfh Atlantic. 10. Ar.reust. 1 9 9 5 .i n p o s i t i o n6 8 " l , l ' \ . 0 l ' 3 . 1 ' \ \ r .D e p t ho f p l a c e :3 0 5 0 nr: fishine depth: 1200 rn l'he secondsamplerias krndlr grantedby Dr. H. S Bjorke (1 IFA). The sanple included -l specrmens: I rmmaturef-emale65 mm ML: 1\\o ntaturinc females(105 and 128 mm I\4L) and l maturin,qmale 80 mrr \4L. All specimensriere collected fiom the samc 'G.O. pelagrctra*l during R'/V Sars' cruise in thc Norrr esian Sea. 2-1. Januarr'. 1999. in position 69"57'N.

Shell in Vampl'ropoda t t t ) ' . 1 0 ' ED e p t h o f p l a c e : 2 8 0 0 m : f l s l i i n s d e p t h : 1 1 0 0 rr. Ciencralr,ierr u as drau n on imnratuie fernale (65 nrm 1\4L)from the secondsample,The gladius \\as e\_ rractedand dra*n tiom trro maturing ftmales (65 and l18 mm N4L). both fiom the secondsample.Total crosssectionsucre made from maturing i'emale(78 mm i\,ll) liom the first sample and maturing nale (80 rrm \,{L) trom the secondsample. Enteroctopusdofleini (Wulker, l9l0). 21 specimens ri erestudred.AII specrmens ri ere sampledfrom the catches o1' commercial bottorn trat Is during a sur\e\ onboard 'Teny,u-Ilaru FY .\b 78' in the \\'eirern Berins Sea in . l u l r . 1 9 9 8 .T h e s a m p l e si n c l u d e dI: m a l e st 2 l 5 a n d 1 3 5 m m N { L ) c a p t u r e dl 3 J u l l . r n p o s i t i o n6 0 " 5 7 ' N . 1 7 g " 5 5 ' \ \ ' at depth 206 m: I male (250 mrr N{L). and 1 female t 2 l 0 m m M L ) c a p t u r e d1 , 1 J u l r . i n p o s r t i o n6 1 " 0 - l ' N . 1 7 8 ' 3 0 ' \ \ ' a r d e p r h 1 5 0 m : I f ' e m a l e( 2 6 0 m m l v I L ) c a p _ t u r e d l 5 J u l r ' . i n p o s i t i o n6 1 . 1 0 ' N . 1 7 8 " 3 7 ' \ \ ' a t d e p i h 1 6 7 m : , 1 m a l e s( 1 3 8 . 1 7 0 . 2 0 5 a n d 2 1 0 m m M L ) a n d 2 f ' e m a l e s( 1 8 3 a n d 2 1 5 m m M I _ ) c a p t u r e d1 6 J u l r . i n p o s i t i o r ro 0 ' 5 b ' \ . 1 7 9 1 6 ' 1 i a t d e p l h 3 5 5 m : I m a l r , s ( 1 8 0 a n d 2 1 5 m m N , l t - )c a p t u r e c2i l J u l l . r n p o s r u o n 6 0 " 5 6 ' N . 1 7 8 ' 5 5 ' \ V a r d e p t h 2 0 0 m : 3 m a l e s( 1 5 2 . 1 9 0 and 253 mm N,ll.) and I female (216 ntm N,IL)caprured 2 6 J u l y . i n p o s i t i o n6 0 . 3 2 ' N . 1 7 2 " 1 5 ' Ea r d e p r h. 1 0 0m : I f - e m a l e( 1 9 2 m m M I _ t c a p r u r e d2 6 J u l r . r n p o s r t r o n 6 0 " ' 1 2 ' N .1 7 2 ' 1 3 ' E a r d e p r h 3 1 0 r n : 3 m a l e s i l - 1 0 . l - 1 2 a n d 2 2 8 m m M L ) c a p t u r e d2 7 J u l l . i n p o s r t i o n5 9 " 1 1 . N . 1 7 0 ' 1 5 ' E a r d e p r h4 0 0 r n : I m a l e 1 2 6 : m m N I L ) a n d 2 f-emales(1.15 and 160 mm ML) captured 2g Jull . in p o s i t i o n6 0 ' 0 2 ' N . 1 6 8 " l 6 ' \ \ , a r d e p r h 3 6 5 m . Benthoctopussibiricus Lovning, 1930. 25 specimens *ere anahzed.All of these ucre collectedfrom catches of commercial boftont trarils during a sur\ev onboard FIY 'T'en,-u-]laru.\b 78' in the \Veirern Berine Sea ln J u l 1. 1 9 9 8 .1 ' h e s a m p l e si n c l u d e d :I m a l e 1 l 7 l i n m \ , { L ) c a p t u r e dl 3 J u l y . i n p o s r t i o n6 0 " 5 7 ' N . 1 7 9 " 5 5 ' \ \ ,a r d e p r h 2 0 6 m : I m a l e( 1 5 0 m n r N I L ) c a p t u r e dl . l J u l l . i n p o s r r r o n 6 1 " 1 0 ' N . 1 7 8 ' 3 0 ' \ \ ' a r d e p r h 2 3 0 n t : 2 m a l e s( 1 5 0 a n d 1 5 5 m m M L ) a n d 2 f e m a l e s( 1 3 0 a n d l g 0 m m N , l L ) c a p t u r e dl 5 J u l 1. i n p o s i t i o n6 1 " 1 0 ' N . 1 7 8 . 3 7 ' U ra r d e p t h 1 6 7 m : I f ' e m a l e( 1 2 0 m m M L ) c a p t u r e dl 6 J u l r . i n p o s i t i o r6r 0 ' 5 6 ' N . I ' q ( l 0 ' \ \ a r d e p r h3 5 5 n r . I m a l e s ( l l 5 a n d 1 7 5 m r n N , I L ; c a p t u r c dl 7 J u l l . i n p o s i t i o n 6 l ' 1 0 ' N . 1 7 8 ' 3 1 ' W a r d e p r h l 5 g m : 2 m a l e si 6 0 a n d 1 6 0 m m I V I L ) c a p r u r e dl 8 J u l y. i n p o s i t i o n 6 1 . 2 3 . N . 1 7 8 ' 0 9 ' \t a t d e p r h 1 . 1 8m : 2 m a l e s ( 1 5 5 a n d 1 7 5 m r n N,lL) and I fcmalc (200 rnm N4L) captured l9 .lult. in p o s i t i o n6 1 " 2 7 ' N . 1 7 7 . - 1 6 ' \ \ a' t d e p t h l 5 0 m : 5 m a l e s ( 1 0 3 . 1 , 1 2 .1 , 1 5 .l - 1 5 a n d l 5 l m r n L f L ) a n d 3 f - e m a l e s ( 1 1 5 . 1 5 3 a n d 1 8 0 m m M L ) c a p r u r e d2 2 J u l l . i n p o s i t i o n 6 l ' 2 5 ' N . 1 7 8 ' 0 9 ' \ t ' a r d e p r h1 5 5 m : I m a l e i l 0 0 m m M I - ) c a p t u r c d2 3 J u l r . i n p o s i t r o n6 1 " 1 6 ' N . 1 7 g . 0 7 ' \ \ ' at depth 150 m: I fcmalc (90 mm ML) captured 2.1 J u 1 1 .i n p o s i t i o n6 1 " 0 9 ' N . 1 7 8 . 3 8 ' \ \ ' a t d e p t i r 1 7 0 m . and I lemale (83 mm N,lL) captured26 july. in polt,on 6 0 ' 4 2 ' N . 1 7 2 " 1 3 ' Ea r d e p r h 3 1 0 m . Bathypol_y-pus salebrosus(Sasaki, 1920).The descriprion is basedon ,l specimens. collectedlrom catchesof commerctal botlorr tratrlsduring a suner onboardFN'Kar,o__llant.\b l8'in the \\iestemBering Seain December.1999:I temale (approx. ,17 mm ML) captured I December. in position 6 0 " 0 1 ' N .1 6 8 ' 0 1 ' Ea r d e p t h2 5 0 m : I f e m a l e( 5 6 m m M . ) captured4 December.in position61"0-l'N. li,l"2l'F. ar denth 130 m: I lbmale (5,1 mrn iv{L) capturerl05 Decemberin position6l'38'N. 175'01'Ear deprh180m. I i'emale(approx. 50 mm iVIL) capruredl0 Decemberin posrtion61"10'\. 1 7 a " 6 1 ' \ \ a r d e p r h2 3 0 n r . Eledone messlae Voss, 1964. Tuo sDecimens*.ere

studied:maturrng female. 35 mm ML: and adult male. 63 rrrn \'lL. Both specimensuere kindlv grantedbr Dr. Ch. \'1. Nigmatullin (AtlantNlRO). Thev riere sampled tionr a catch of the samebottom trar'"1during R/V patriot cruise ,\q .1. in SW Atlantic. 7 Ma1,. 1983: in posruon -16"0.1'S. 60"02'\\'. Depth of place: 680 m. Alloposus mollis Yerril, 1880. Three specimens u.ere srudied:rmmaturefemale. 57 mm ML: immature male. 6t) mm N,lL and tmmafuremale. 63 mm ML. Thev g.erekindh sranredbr Dr. Ch. M. NigmarullinlarlantNIliOl. All thrce speclmensuere sampledfrom a catch of the same pelasic trarrl (BPT-50 t1pe) during RN 'Gizhiga' cruise in \i\\' A t l a n t i c . 2 5M a 1. 1 9 8 3 i:n p o s i t i o n 1l"lj'N.64.21'W, Depth of place: 1200 m: tranling depthtunknonn. Tremoctopusviolaceus delle Chiaie, 1830. The description is based on the t\r'o immature female (57 and 60 mm ML) obtained from cephalopod collection of ZN,IN4U. Both specimenslr'eresampledb1,prof. A.p. Bog_ danov rn the region of Nice (France) in Jul1. 1gg4. Ocllhoe tuberculatoRafinesque,1814.Trio immarure fernales*ere studied:103 mm ML and 96 mm ML. -fhe tlrst female (103 mm ML) nas collected from a catch of pelagictran I during RA/ 'Od1ssel' cruisein the central part of the Indian Ocean.1,1November. 198,1.in position ? ? 1 7 ' 5 . 7 , 1 ' 3 0 ' E .D e p t ho f p l a c e :4 1 0 0m : t r a u , l i n gd e p t h : 100-0 m. The secondfemale (96 mm ML) ,nu, iu.pl.d tiom pelagrctra*l catchduring R/V .Vozrozshdenie'cruise in the SE Pacific Ocean27 October. 19g9.in position 7 - 1 " 5 6 ' \ \ 'D. e p r ho l p l a c e :3 6 4 0m : r r a r i l i n gd e p r h : l9 90'S l0-0 m. Both femaleswere kept in the cephalopodcol_ I e c t i o no l ' V N - l R O Argonouta nodosa Solander, 1786. Tr.vo mature f'emales uere studied:94 mm ML and 108 mm ML. Both specimenswere collectedfrom catchesof pelasic trarvl during R/V 'Vozrozshdenie'cruisein the SE Facilic ocean in October-December.1989. The first female (9,1 mm ML) uas sampled 27 October. in position 26"00,S. 7.1o5.1''*r. Depth of place 3900 m: traw.linsdeprh: l0_0 m . T h e s e c o n df e m a l e ( 1 0 9 m m M L ) \ \ ; s s a m p l e d3 December.in positicn 31"09'S. 84.55'W. Depth oi place 3850 m: trawling depth: l0-0 m. Both speCimen.,uer. k e p t i n t h e c e p h a l o p o dc o l l e c r i o no f \ r N I R O . Japetella diaphana Hoyle, 1885. The description is based on a sin_elespecimen.immature ttmale. 57 mm \{L kindll grantedb1 Dr. G.M. Vinogrador,.. The specrmen uas sampledfiom a catch of planctonicnet during RrV '.-lkademic .ll Kel$'sch 'cruise Nc 49. in equatorialEastern Paciflc. 8 September.2003: station N, 4630. in posuron 0 9 " 5 0 ' S . 1 0 ' l ' l 5 ' \ \ r D e p r h o f p l a c e :2 5 0 0 m l i r a r v l i n g d e p t h r a n g e :2 1 6 0 - 0 m . pelagicus Hoyle, 1885. The description .Amp,hitretus is based on a single specimen.immature male. 26 mnt ML kindh granred br Dr. K.N. Nesis (SIORAN). The sp_ecimen uas sampledfrom a catchof pelagictrau,ldurin-e '.lkademic RN Kurchatoy'cruiseNc ll. in SW Atlantic. 3l December.l97l: station ,\r 952: position unkno*.n: d e p t h o l p l a c e u n k n o sn : t r a \ \l i n g d e p t h :2 3 0 m .

Definitionsof terms and measurements used here follow Robson 11929;19321,Roper. Voss The measurements [1983]and Nesis11982119871. of fin lengthand fin width were madeaccording to Voss.Pearcy[1990]:fin width was the greatest perpendicLllar distancebetweenanteriorand Dosrerior marginsof the fin. and fin lengthwasthe distancefrom the middle of the fin baseto the fin apex.In addition.fin spanwasmeasured according

V. A. Bizikor to Guerra et al. 11998]as the distancebetu'eenthe tips of the fins. Tri'o basic measurements.lerrgtlt and u'idth. r.veremade for the gladius of cirlate octopods.The gladius width w'as measuredas the distance betu,eenanterior rnargins of the ri in-ss. while the length was measuredas the distancefrom p o s t e r i o rt i p o f t h e g l a d i u s t o t h e l i n e c o n n e c t i n g a n t e r i o rm a r g i n so f t h e u i n g s .C r o s s - s e c t i o nosf t h e shells of octopodsand varnpire squids uere made accordingto the techniqueselaboratedb1 the auth o r f B i z i k o v . 1 9 9 0 : 1 9 9 1 ] .T h e s h e l l sw e r e r e m o ved from fresh or forrnalin-preservedanirnalsand storedin ,l% buffered fonnalin. The inner structure To make of the shell rvasstudiedon cross-sections. the shell was squeezedby hand becross-sections. tween two piecesof st.vrolfoam and then cut lnanually r,rsinga microtome knit'e. Relationshipsof the sl-rellrvith the soft bodl' u'ere studiedon anatomical preparationsand entire cross-sections. E,ntire cross-sectiorrs of octopods!veremade using the fbllorving procedure: an intact folmalin-preserved specimenrvas soaked in fi'esh uater. then spread on a flat surt'aceand fi'ozenat -2.1oCfbr 3-6 hours. dependingon the animal size. After complete fi'eezing the specimen\\'as cross-sectionedmarruallv rvith a sharp heavy knife rvith strai_rhtblade, The s e c t i o n s( 0 . - tr r r r t o 1 . 0 m r n t h i c k ) r i e r e t h a u e d o n 'SZHa glassplate r.vithrvaterand drau n using a 10 O 1 1 ' r n p L rzso' o m - m i c r o s c o p eI n. V a r n p v r o m o r p h i d a and Cirrata. the sections.,r'erernadeat tlie tbllol.ring levels:the funnel. behind the funnel. attachrnentof the funnel retlactors. greatestu idth of tl-reflns and b e h i n dt h e f i n s . l n I n c i r r a t at.h e s e c t i o n sn e r e m a d e at the level ofthe funnel. behind the funnel (ventral adductor).anterior dorsal adductorsand postefior dorsal adductors(: funnel retractors).

RESULTS OrderVampvromorphida Pickford,1939 Vampyroteuthidae Thiele,in Chun, 19l5 Vumpyroteutltisinfernalrs Chun, 1903 I-untptroteutlrl.r. or HABITS AIYD HABITAT. v a r r p i r e s q u i d . i s a b a t h l - a b y s s o p e l a g i cs p e c i e s inhabitingtropical and tenrperate\\'atersolall oceans at depths fronr 800 rn to 2000 rn [Nesis. 1 9 8 2 / 1 9 8 7Y: o u n g . 1 9 9 8 1 U . n d e r \ \ a t e ro b s e n a t i o n s f } o m s u b m e r s i b l e sf H u n t . 1 9 9 6 ] s h o r . r e dt h a t I"antpt'rotetrftrscan s*irn surprisinglr fast for a gelatinous animal acceleratingup to tu o bodr lengtUsecin about 5 sec.Fast suimming consistsof quick movementof the fins tou'ardthe funnelalternating rvith a-ietlrorn the mantle.Su imming in this rr ar . the vanrpiretakesa seriesof quick turns in an enatic escaperoute [Hunt. 1996]. The varnpireappearsto ri ith the olient r.nostcomrnonlv in a horizontalattitLrde

arrns spread fonvard to fonn. together with the i.veb. an umbrella-like posfure [Hunt. -1996]. GLADIUS MORPHOLOGY. The gladius of farnp)l'oteltthis is a broad. chitinous. transparent plate ly'ing along the dorsal surface of the body beneath the skin and a thick layer of loose connectivetissue *ith a dermal netrvork of muscle fibers (Fig. 1). lt is thin and flat anteriorly.gradually becoming thicker and stronglv archedposteriorly.Posteriorto the tlns. the gladius encirclesthe body for about I 80o then terminates in a broacl of its circurnt-erence conusand rostrum.The structureof vampire gladius is tvpicalll' teuthoid: it is slightly longer than the nantle (the mantle terrrinateson the anterior edge of the conus). it consists of three morphological parts- dorsal plate (proostracum).conus and rostrurn. and it is formed by three shell layers: middle la1'er (ostracum). inner layer (hypostracum) and outer layer (periostracum).Teminology of the gladir,rsparls is given hereaccordingto Jeletzky[1966] and Bizikov [1996].The problem of homological betweenstructuralpartsof the same correspondence n a m e si n t e u t h o i da n d b e l e m n i t o i ds h e l l sl i e s b e 1 ond the scopeof the presentstudy. The rnost developed layer rn Vampvroteuthisis ostracum. Being corrposed of chitinous substance.it takes paft iu formation of the dorsalplate and the conus.Hypostracum and periostracumare somewhatcaftilaginous: the former is laid dorvn on the ventral side of the ostracurnand provides the thickening of the posteriorpart of the gladius: the later lies dorsall;' and posteriorll' and forms the small spine-sl-raped rostrum situatedapicalll' on the conus.The baseof the rostrum forrns a shallow thin-walled cup. the alveolus. over the apex of the conus and extends forvn'ardalong the cone flag. The proostracum consists of five longitudinal elements:the rniddle plate (rachis).two lateralplat e s . a n d t v n ou ' i n g s ( F i g . 1 A ) . A l l p a r r so f p r o o s t racum are separatedfrom each other by as)'mptotic lines iormed by sharp bending of the gladius gror,rthlines: a pair of median asymptotesseparates the rachisfrom lateralplates.a pair of lateralasr nrptotes separateslateral plates from wings. and a pair of rnarginal as)mptotes separatesthe u'ings from conus.The rachis is broad. uniformly rvidens anteriorlr,.rvith a broad. blunt anterior end. The dorsal surfaceof the rachis bears narro\\,parabolic grou'th lines repeatingthe shapeof its anteriormargin. The anteriorparr of the rachis.the free rachis. extends be1'ondthe lateral plates. The free rachis in llantprroteuthis comprisesabout 25% of the gladius length (GL). The lateral plates are narro\\. * ith concave anterior margins and densely spaced hy'perbolicgrorvth lines. They are distinctly'delineated from the rachis by median asymptotic lines but less clearll' separatedfrom the u'ings. as the lateral as1rnptotes.delirniting lateral plates fronr

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t h e w i n g s m a v b e i n d i s t i n c ti n s o m e s p e c i m e n s l P i c k i o r d . l 9 - 1 91 . T h e r , ri n g s a r c m o r e r h a n t \ \ i c e as vvideas the lateral plates.uniforrnll' convex (vieu,ed dorsally').and make the greatest w,idth of vamprre gladiLrs.approrimatelr-"31% of the GL. 'fhe dorsal surfaceof the u ings bears convex obliclr-re gror.l'thlines that are spaced more sparselv then those on the lateral plates. l - h e c o n e i s a u , i d e .s h a l l o u . c u p - s h a p e ds t r u c ture enclosingthe posteriorapex of the I'iscera.It is separatedfrorn proostracumb\ the pair of rnarginal asl,mptotes.Junction of the conus u,ith the u'ings is rnarked b1 slight constrictionof the _eladir,rsthat separatestr.voahnost equal maximums of the gladius width: anterior. lbrmed b1' wings. and posterior.formed b1"the cone. The apical angle of the cone is broad.No trace of a chamberedphragr n o c o n ee x i s t s .T h e v e n t r a ln a l l o f t h e c o n ei s s h o n .

*'ith shallowincisionin the middle.Dorso-lateral wallsof the cone.or conefields,accordingto Naef are long and wide. They projectan[192111923]. teriorly alongthe proostracumand form the posterior expansion of thegladius.Therostrumis a short. laterally compressed. cartilage-likespine tapering posteriol)'frorn the conusapex.Its lengthis about 5% ofthe proostracum length.The degreeofrostrurn development is variablein Vampyroteuthis andit na,r be absentin somespecimens [Pickford.1949]. RELATIONSHIP BETWEEN THE GLADIUS AND THE SOFT BODY. Typicallyin coleoids. the soft parlsdo not contactwith the gladiusdirectll, bllt attachto theshellsacthatsurrounds thegladius. The outersideof the shellsacis formedby fibrous tissuewhile its innersideis linedby shellepithelium that secretes the gladius.Whenthe shellsacis

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FlG. 2. Relationshipbenveen the shell and soli bodl in I'antpvroteuthisinfernalis (immature female: 53 mm Mt,) A Ventral viel . the mantle cavitv is opened:the visceral organs are removed. B. Dorsal view'. the skin is sho*n (shorvnon Fig. 3 and I-ig. transparent. Arrous nith numbers indicatethe position oi correspondingcross-sections 5). Scale bars - I cm, PI4C.2. B3aurroorHoueHr4elrexJv rJaJH)coll H u.qrKnlr retott l'amptroteuthis infernalis (ue:pe.'rar cartxal 53 r'trt nN'l) A BHg c reurpanruoii cropolrrr: vaHruiiHac no.rocrb BcKpblralBucueparbHbreopfaHbr )',larleHbr.B. Bnrr c KoHr)poM.Crpe.rxu c uurppauu )Ka3brBarcr no.rnpo3paqHbrM lopca.rlnoli cropoHbriKoxHbrenoKpoBbrnoKa3aHbr o x e r { } r sc o o r B e r c r B ) r o u l ucxp e 3 o B( n o r a : a s s s r xn a P u c , 3 u P u c . 5 ) . M a c u r a S : I c n .

intact. it adhers to the gladius so tightll' that attachment of soft parts to the sac is functionally equal to their attachmentto the gladius itself. In Vampvrr.tteuthis the mantle muscles follou the contour of the gladius. attachingto its margin from ventral side (Fig. 2B). At site of mantle attachment.the shell sac is reinforcedb1' cartilaginous rim first mentioned by Pickford [1949]. The head attachesto the gladius b1' paired cephalopodium retractors (head retractors). and nuchal muscles (Fig. 2B). Although the head and the mantle in adult Vampyroteuthis are fused. the means of fusion is unlike that of octopods.A vestigialnuchal cartilageis presentin the headjust under the anterior pafi of the free rachis. On the dorsal surface of the head there is complex nuchal rruscle sheath including the fibers that pass from the shell sac to the cephalic cartilage. from the shell sac to the base of the arms and frorn the nuchal cartilage to the baseof the arms. The head retractorsare thin sheets. They' pass from the cephalic cartilage.make a thin muscularenvelopearound the visceralsac and attachto the anterior rrarsins of the lateral olates.

The funnel retractorsare shoft, ribbon-like. They' originate from the ventral posterior comers of the funnel. extend posteriorly along the visceral sac and attachto the anteriormargins of the wings (Fig. 2A). The r.veakly-developed stellateganglia appearas slightly enlargedknots on the pallial neryes and are situated laterally'to the wide gladius at the level of its lateralplates(Fig. 2A). The fins attachnearthe dorsal side of the gladius.near cone fields. The fin basesare not fixed in their position rigidly, but are anchored by muscles(Fig. 2B). Vedical adjustmentof the fins is accomplishedby fin elevator and depressormuscles. Elevator musclesform thin muscular sheet,overlaying posterior arial part of the gladius. and unite the fin bases.Depressormuscles originate from the ventral side ofthe fin basesand run in a posteroventral direction.tow'ardthe margins of cone fields. Depressormusclesapparentlyserve to adjust the fins position in both vertical (ventral) and longitudinal (posterior) directions.Longitudinal adjustmentin antenor direction is ensuredby paired anterior retractormuscles radiating from the fin basesto the dorsal side of the gladius in the area of wings.

Shell in Vampyropoda

il

mpa i;lG. 3. Schematiccross-sectionsof the sofi body o1' I'ampt,roteuthisrnfbrna,lis(immature f-emale; 60 mm ML). A . Section l. at the level of the funnel. B. Section 2. imniediatell behind the funnel. C. Section 3. at the levil of aftachmentof the funnel retractors.Position of rhe st-crionsis indicated in Fie. 2. Scale bar - I cm. l'l.lC. 3. Cpelu :nr.rrxorore-ta I'antpt'rotetrltis rnfernalts (ue:pe"rarcavxa: 60 rnr !M), A. Cpe: l. ua',,ponue BopoHri[. B. Cpe: 2. nosa,fn BopoHrlr.C. Cper 3. ui ypoaHe frpuripcrr.teHHq BopoHorrHbrx perpaxTopoB,floloxeuue cpe:oe : vKa3aHosa Puc. 2, N{acutraS I cv.

t2

V. A. Bizikov

rant

FIG. 4. I'antprroteuthisiry'brnalis.Enlarged part of the section 3 (Fig 3C) sho*ing attachmentof muscles to the gladius margin. Scale bar : 1 mm. npuxpen.leHxe NI}'cK}.roB PHC..l. I-antprt'oteuthis infernalis.Vse:uqeHHrrii{parueur cpe:a 3 (Puc. 3). rroKa3blBatorlt{ii K KpaHl rJa.tu)ca. MacuraS : 1 rnr.

CRO,SS-SECTIONS(Figs, 3-5). Functionalrelationships between the gladius and soft body in I"i infernalis are best understoodfrom entire cross-sect i o n so f t h e b o d y ( F i g . 3 - 5 ) . P o s i t i o no f t h e s e c t i o n s is shown by arrows in Fig. 28. Section 1 (at the level of funnel) illustratesthe attachmentof soft pafis to the fiee rachis (Fig. 3A). At this level the rachis is u'ide. thin and nearly flat u'ithout pronouncedribs. It is composedof the ostracumonl1',The visceral sac abuts the ventral side of the rachis. its dorsal rvall being actuall,vfused u.ith the shell sac. Dorsal and lateralwalls of the visceral sac are forrred bv thin head retractor muscles and collagen fibers.The ventral rvall ofthe visceralsac servesfor attachmentof the funnel. At the sites of funnel attachmentthe ventral wall is thickenedbut no cartilage is present.Two muscular folds (collar folds) originate fiorn lateral walls of the funnel. Upper marginsof collar folds attachto the nuchalcartilage and the shell sac anteriorly and to the visceral sac posteriorl)'.The collar folds confine a pair of spacious cavities(collar pockets)on both sides of the visceralsac.The rnantleattachesto the carlila-einous rin of the shell sac fi'orn the ventral side.The rialls of the mantle.funnel and the collar. each consistof (inner and outer)separated tlvo thin muscularla,r,ers by a thick highly vacuolatedgelatinouscore.

On the section 2. behind the funnel (Fi-e.3B). the gladius is thicker. u'ider and slightly arched.Its section consistsof a thin axial parl corresponding to the rachis.and thickenedlateralparts corresponding to the lateralplateson Fig. 1C. Margins of the lateral plates are encasedin cartilageto u'hich the mantle and head retractors attach. The mantle attacheslaterally'to the margins of the lateral plates ivhile the head retractorsattachto them from ventral inner side. The head retractors form the lateral walls of the visceral sac. The funnel retractorsappear at this level as a pair of thick muscular flaps attachingto the lateral rialls of the visceral sac. Section3. at the ler,'elof attachmentof tl-refunnel retractors(Fig. 3C). shows the gladius at the gfeatestriidth of the uings. The lateral regions of the gladius are thicker and wider here than in previous sections.The inner areas. correspondingto the lateral plates.are not distinctly separatedfrom the outer areas.correspondingto the wings on Fig. 1 C . A l l m u s c l e sa t t h i s l e v e l a t t a c ht o t h e t h i c k e n e d l a t e l a l r n a r g i n so f t h e u i n g s ( F i g . 4 ) . T h e m a n t l e attachesto the dorsolateralside of the rvings rvl-rile the funnel retractorsattach to their ventrolateral side. The dorsal side of the wings provides attachment for loose muscLtlarfibers. Theserepresentthe anterior loneitudinal retractorsof the fins, shown

Shell in Vantpyropoda

l3

SN

hyp ost

B hvp

FIG 5. Schematiccross-secrions of the sott bodl of I'ctnptl.oteuthis tnlirnolis (contrnuedfiom Fie. j t .\ Seerion 1. at the greatestriidth of the fins. B. Section-5.at the'middle pan bf the fin b;.i a i;;tioi o. ar rhc posre..o; parts of the fln bases.D. Section7. through posteriorpart of ihe rnantlebchind the f'in basc:. Scale bar: - I ir1 PHC 5. Cpe:r't rtlnxoro ii -re:a I'antptroteuthrstnlbrnttlts(flpoloJxer{rrr'Prrc. -i ) .{. Cpr'; J. ua r poBsc Hasa)o-rLure lxllpHHbln'laBHuKoBB Cpe: 5. a cpc:neri qacrr L)cHOBasrrr"r rr.rasHnxna. C. Cpcr 6. ri ;a:rrlir !{acrrrocuoBarurr LIacru\raHnlr no3iltlt ocHOBarnril n'iIaBIItlKoB. D Cpe: 7. e :a-tHer"t n-raeultnoe.\laculra6 - I err

l4

V. A. Bizrkor

also in Fig. 28. At the site of muscularattachnent. the shell sac is reinforced by cartilage w'hich is thicker on the lateral side of the gladius than on its dorsalside. Inner structureofthe visceralsac is not shor.vnon this and the tbllou'ing sectionsdue to its poor preservationin sectionedspecimen. At the level of the fins. the gladius provides indirect support for the fin basesand mantle (Fig. 5A). The gladius here is strongly'arched and t'uvolal'ered: the hr:postracumappearson ventral side of the shell. increasingits thicknessin axial region. In this sectionthe thin marginal partsof the gladius correspondto the cone fields: the thickened lateral pafis correspondto the n'ings fused r.r'iththe lateral plates.and sharpchangein thicknessbetweenthem marks rnarginalas1'mptote.Tl-reventral sidesof the cone fields serve for attachmentof the rnantle.The fin baseslie on the dorsal side of the *ings and cone fields. Sharpbendsseparatethe basefrom the rest of the fln. Each base consistsof tu'o lay'ers. approximatel;-equal in thickness:a ventral cartilaginous la1'er.near the gladius.and a dorsal muscular la1'er.Elevator muscles connect the inner margins of the fin basesand overlay the dorsal surface of the gladius.Depressormusclesstarl originateon the ventral side of the fin basesand adhereto the rnargins of cone fields. Additional fixation ls accornplishedby bundles of connective-tissuefibers that bind tl-refin basesrvith lateral mantle walls. A pair of epithelial sacs (basal pockets).uhich rray' representseparatedporlions of the shell sac. are situatedbetrveenthe fin basesand the gladius.The sac walls presurnablyprovide gliding surfacesduring rnovernentof the fins. According to Bandel and Boletzkl' U919). basalpocketsdevelop during embrvogenesisas a differentiationof the secondarl' shell sac epitheliurn. At the level of greatestfin rvidth the basal pockets occup)' onll' part of the spacebetrveenthe gladius and fins bases.the rest is filled b1' highly vacuolatedconnectivetissue. At the level of posterior part of the fin bases epithelialbasal pocketsmerge into one large basal sac spreadingover the u'hole dorsal surfaceof the gladius (Fig. 5B). The posterior region of the fin basesare roughly triangular in cross-section.with carlilaginousventral and muscular dorsal components.Thev occupy shallou'concavitieson the dorsal side of the cone fields and are held in position b1' elevator and depressormuscles. The elevator muscles attach to the muscular dorsal side of the fin bases u'hile depressorrnusclesattach to their lateral side. Highl;" vacuolated connective tissue fills the space betu'eenthe fin bases.The gladius is thicker rvhere the hvpostracum extends to the margins of the cone flags. The mantle attachesto ventral side of cone flags. In the posterior parl of the bodv. the gladius is arch-shaped.occupy'ingdorsal half of the bodl cir-

cumference (Fig. 5C). The mantle aftachesto the gladius ventralll'. along the margins of the cone fields. The fins bases here are flat and wide and consist entirely' of vacuolated cartilage. Basal pockets are absent. Elevator muscles are separated from one another in the arial region over the gladius. Depressor muscles connect the lateral sides of the fin basesrvith the outer margins of the cone fields. Depressormuscles spread posteriorly almost to the end of the gladius (Fig. 5D) and apparently act also as posterior longitudinal retractors of the fins. Posterior apex of the body is cupped by another muscle that is missing on my sectionsbut was describedin details by Young [1964]. According to Young. this muscle forms a cone of ver"r delicate circular muscle fibers and covers the apex of the bodl' except for a srnall pore at the most posterior point. The anterior edge of this muscle attachesto the border of the conus ventrallv and the shell sac dorsally. COMMENTS. Attachment of fins to the gladius in Vampyroteutlzisis different from the one reporled earlier.Pickford [1940. p. 1761wrote that in Vantpvroteuthis "the fins rest directly on the shell sac whose wall is thickenedto form what appearto be carlilaginoussupport."Apparently Pickford missed the basalpockets.which are difficult to seeon gross anatomicalpreparations.but are clearly apparenton the cross-sections. Our data show that articulation of fins with the shell and mantle in Vampvrotettthis follows the same basic coleoid pattern described e a r l i e r i n t e u t h i d s[ N a e f . 1 9 2 1 l 1 9 2 3 :f t g . 6 6 ] a n d s e p i i d s[ N a e f . 1 9 2 1 / 1 9 2 3f:r g . 2 9 0 l . l t i s e s p e c i a l l y closeto condition found in some oegopsidfamilies, for example. E,noploteuthidae. where the gladius occupiessuperficialposition and the fins basesrest on its dorsal side. separatedfrom the shell sac by' basalpockets fNaef. 192111923:fig.66a]. Reportedhere for the first time. in addition to the more complete description of the muscular attachment to the gladius. are the presenceand description of the three layers of the shell. the presenceof the lateral platesof the gladius and their asymptotes.the three-dimensionalshape of the gladius. the ventral incisionofthe conus,the presenceofa basalpockets.

Order OctopodaLeach,1818 SuborderCirrata Grimpe, 1916 Family OpisthoteuthidaeVerrill, 1896 Opisthoteuthiscalifurniana Berry, 1949 GENER4LREMARK.Differenttermsareusedin cephalopod literature for the shellof cirrateoctopods:dorsalcarlilage[Hoyle. 1886;ljima. Ikeda. 18951: internalshell[Appellcif, 1899];shellvestiee Robson.1932];gladius[Nesis. fNaef.1921/1923:

Shell in Van-rp-vropoda 1 9 8 2 / 1 9 8 7o1r f i n s u p p o r t[ A l d r e d e r a l . 1 9 8 3 ] .I 'gladius' to emphasizeits origin frorr-r frefer to r-rse .'iongateinternal shell of the early coleoids. HABITS AND HABITAT. Opisthoteuthis califorttiana.or Californianflapjack devilfish. is a benthopclagic cirrate octopod inhabiting near-bottomuaters of the outer shelf and continentalslope (front 1 1 5 m t o 1 1 0 0 m ) i n t h e N o r r h P a c i f i c .f r o m t h e Bering Sea to the Sea of Okhotsk to off central Honshu in the northw'esternPacific and to off southern California in the noftheasternPacific [Nesis. 1 9 8 2 1 1 9 8 1V; e c c h i o n e e t a l . 2 0 0 3 1 . S r v i m m i n _ q rtrodeand behaviour of flapjack devilfishes vr,ere observedfrom a manned subrnersiblein O. califort t i a n al A l e x e e ve t a | . . 1 9 8 9 1 .a n d i n s i r n i l a rs p e c i e s . ( ) a g a s s i z i .I V e c c h i o n e ,R o p e r . 1 9 9 1 ] .O b s e r v a t i ons shorved that Opisthotettthis srvims mainll' by contractionof the arm-web corrplex added b1,frequent fin strokes (2-3 fin strokes per er,ery *eb contraction).During swimming the posterior apex of the mantle is oriented obliquely upward toward the direction of the swimming, and the octopod perfbrms gentle thrusts by' its arm-ueb complex. rnoving along a sinusoidaltrajectory. GLADILTS MORPHOLOGY. The gladius of Opisr l t o r c f i h i si s a t h i c k c a n i l a g e - l i k eb. r o a d l . vU - s h a p e d structurelaf ing transversalll'on the dorsal surface of the mantle (Fig. 6). Its u'idth is much greaterrhan rts length.The gladiusconsistsof a medial transverse paft (saddle) and enlarged. thickened. lateral parls (wings). The r.vingsterminatein pointed flexible lateral horns that protrude from ventral region of tlre wings in an anteroventraldirection.Morphological parls of the gladius are not distincrll separatedfrom one anothir. Ast,mptoticgrowth linesare absent.The saddleis rather thin. rounded in crosssection.with deep groove on the dorsal side. Lolv ribs are sometimespresenton the dorsalconvex side of the saddle and extend onto the lateral u ings. Lateralwings are thicker and rvider than the saddle. The outer sides of tl-rewings are slightly' concave: the inner sidesare convex. strengthenedb1,the lou keels.The outer.concavesidesofthe rvings are not parallelto one anotherbut diverge torvardthe tips. The width of the gladius.measuredbet'uveen the tips of the horns. is 70-80 % of ML. The height of the gladius is about 33 %. and the anterior-posterior d i m e n s i o no f t h e s a d d l ei s 6 - 1 5 % . D u r i n g g r o u ' t h the gladius becornesrelatively thicker. its lateral horns becomeshorter.and the dorsal groove in the saddlebecomesnearlv flat. MICROSTRUCTURE OF THE GLADILTS, Atthe m i d l i n e o f t h e g l a d i u s .c r o s s - s e c t i o ins U - s h a p e d . r.viththe concave dorsal side correspondingto the dorsalgroove (Fig. 6D). Numerous regular concentric incrementsof carlilage-likesubstanceare seen in the sections.Each increment consistsof a r.vide

t5

glass-liketranslucent zoneand a peripheral narro\\' opaquezone.The centerof grorvth(initialshell)is situatedin the lor.ver partof the section.It is a srnall flat body.580-620pm in width.24-30prmin height. andcomposed ofanamorphoussubstance withoutany, traceof grorvthincrements. Theinitialshellis surroundedby'a postnuclear zone(890-900prmin width: 290-3I 0 prmin height)separated from the outerzone bv prominentline or first check(Fig. 6F). From 12 to 19 faint uniformincrements wereobservedr.vithin postnuclear zone.eachwith a maximumrvidth 15-20pm. Bey'ondthe postnuclear zonethe incrementsbecomemoredistinctandtheirwidth graduallv increases towardperipheryup to 25-30;.rm.In the outerzonethe increments wereclearlygrouped into second-order cycles.from 7 to 25 increments in onecycle.The outlineof the growth increments presumablv repeats the shapeof the gladiusat earlier stagesof its development. The microstructure of the gladiusof Opisthoteuthis is very similarin the width andconsistency of increments and in the second-order cyclesto thatofthe innershelllayer. the hypostracum. in the gladiusof recentsquids to squids. [Arkhipkin.Bizikov.1991].ln contrast horvever. the increments in the gladiusof Opisthoteutisarecontinuousand eachincrementmakesa closedenveloparoundthe shell. SOFT BODY MORPHOLOGY AIVD ITS RELATIONTSHIPWITH THE GLADI{/S. The cephalopodianBauplanis difficultto recognizein the pancake-shaped bodyof adullOpisthoteuthis (Fig.7A). but the young stagesretain more featuresof the generalcephalopod organization. Duringthe cruise aboardthe F/V 'Tenyu-Maru Ne 78'in July, 1998. one specimenof Opisthoteuthis (immaturefemale, 19 mm ML) rvasretrievedalive (trawl J\l 1), and observed andpicturedin a shipboard aquarium. The mainmeansof locomotions was swimmingby rnedusoidcontraction of thearm-webcomplexalternating periodicalllwith shorrperiodsof fin-swirnming.Sirnilarbehaviorhasbeendescribed for opisthoteuthids previously[Pereyra.1965;Vecchione. Roper.1991; Vecchione. Young. 1997;Villanueva. 2000:Hunt.19991. In producing themedusoid stroke. the animalbroughtthe armsand web together. acquiringthe positionin which its cephalopodian planeof structurebecameapparent(Fig. 78). The bodl' of young Opisthotettthis consistsmainly of long arrnsunitedalmostcompletelyby a thick web. The head is small.confluentwith the arms.The mantlehas a shapeof small conicalcup on the posteriorpartof the body.Its lengthcomprises 2325o/oof the total length.On the dorsalside,the mantleis fusedwith thehead.On theventralsideit formssrnallmantleaperture closelysurrounding the funnel.Thefinsarerelativelysmall,oar-shaped and setobliquelyon the lateralsidesof the mantlein its anteriorpart.Thegladiusliesobliquelyin the man-

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F FIG.6. Cladius of Opisthoteuthiscalifornialo, A. Anterior rieu ldorsal side is up). B. Lateral vien (anteriorsrdc is on the ieft). C. Dorsal r ies (posteriorside is up). Bold arrows indicatethe planesof the cross-sectionshori'n in D-F. D. Cross-sectionl. through the middle part of the gladius (dorsal side is up: anterior side is on the lcli). E. Cross-section 2. throrgh the'rniddle patt oi'the lateral *rng (dorsal side is upi anterior side is on the right). 'D' F. Enlareedfragment of Il-eure (section 1). sho*in-e initial shell and postnuclearzone. A-C: scale bar: I cm: D-F: scalc bar I rnm. PIIC 6. l ,raJH)c Opistltotettthts caltJbrruana. A. Bu-r crrcpcJu(Jopca.rbHar cropoHaHaBep\\').B. Bnr c5oxl (nepelurr clopoHac:eea). c. Br: c -topca.rsuoii cropoHr,r(3a-tHcccTopoHaHaBep\)). cTpe.rxu\ Ka3brBaroT froJ.roxeHHe cpe3oB. IloKa3aHHbl\ Ha Bua\ D-F. D. Cpe: l. ca|nlra"ruHrrircper B cpelHetiqac.lur'.ra-trl) ca (topca:rrHarcropoHaHaBepx): ilepeJHt,{cropoHilc.reaa).E..Cpe: 2. s cpe:ueii qrcrH .rarepa-rbHoro (:opca.rrHa.n KpLr.ra cropoHacBep\}: rrepeJHrt 'D' cropoHacnpana).F. Yne.rtj'retttrurii rlparrrenr slrJa tapollsruen_r xt (?) paxoer.iHvu lCpera l). roxa3brBaH)ruHii n o c r H v K - r e a p H )3l o r r ) . A - C : r r a c u r a 6 : 1 c r r : D - F : r r a c u r a 6 = 1 r n r .

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l(t T opisthoteuthis calijbrniana. A. Dorsal viev' of a. mature.male; 49 mm DML. B. Lateral view of a swimming

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B of urustrlG. 38. Schematicscctionsshoning attachrnent t'iolaceus.A. Loncles to the shell in Trentoctoptts gitudinal sectionof the mantle along the lefi sn let. Anterior end is on the leti: dorsal sidc is up. B. 'fransversal through the right st) let (encross-sectior.r largedliagment of Section5: Figure 37E). Dorsalsidc is up: outer side is to the rrght. Sealebar - | mnt. PllC.38. Kperr.rcnnc\rhrrlu K paKoBr.inc7i'entoctopus violaceus.A. ilpo:o,rsuuii cpe: rtaHrun B.lo.tb.teBofo crr{.Tera.Ilepe:uuii KoHeuc.reBa:.topca.rbHatclopoHa uaBep\\'.B. flonepeurrutilcper veper npeastiicru.rer (r ne.nrvcrrrr,rri rlrparrreHr cpera5: Puc.37E).!,opca-rrcropoHacnpaua.N'IacHaqcropoHaHaBep\):BHeuHt.q UTAO

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This rnuscle extends along the mantle u'all both anteriorl)'and posteriorll from the region of attachment to the visceral sac. Dorsalll' the adductor divides into t*o la1'ersthat diverge onto the sides ofthe visceralsac.The spacebetrveenthe diverging m u s c l e si s o c c u p i e db 1 t h e r e c t u m a n d v e n a c a v a . Anteriorll the adductor muscles extend into the funnel as a thin muscularlal er coveringthe rectunt. v e n a c a v a a n d t h e d r - r cot f t h e i n k s a c ( F i g . i 7 A ) . T h e f u n n e l c o n s i s t so f s i n g l ec i r c u l a rm u s c u l a r layer: its ventral and lateralualls are fusedtogether w i t h o u t b o u n d a r i e s( F i g . 3 7 A ) . C o l l a r f o l d s o r i g i nate from the dorsolateral*alls of the funnel. pass along the sides of the visceral sac and attach to dorsolateralu'alls of the mantle. A funnel lockingapparatusin Tremoctopzrsis rvell developed and

hook-like folds consists of car-tilage-strengthened pocketsin corresportding of the funnel cornersand ( F i g . r v a l l 3 7 B ) . t h e v e n t r a lm a n t l e Funnel retractors are rvide. thick. tnuscular bands on the lateral sides of the r isceral sac (Fig. 37D). They fuse with the visceral sac along the dorsornedialof their rvidth. rvhile the ventral quarter hangs freely' inside the tnantle cavitr'. At their sites of attachmentto the stylets the funnel retractors are thick and triangular in cross-section(Figs. 3 7 E : 3 8 8 ) . T h e u i d e m e d i a l s i d e o f e a c hb a s ep r o jects into the mantle cavitl'. rvhile the narl'ow outer apex attachesto the rnedial half of the stylet. The dorsal side of each retractor base connectsto the v i s c e r a ls a c b y a r n e m b r a n e( F i g . 3 7 8 ) . T h e g i l l s attach to the mantle r'vall r.'entralto the attachment of the frrnnel etraclors. Attachment of the musclesto the stylets in Trentoctopusis unusual.Longitudinal preparationshoned that each stylet is obliqueiy oriented in the animal body': its posterior parl is embeddedin the mantle muscle.rvhile the anterior paft projects into the funnel retractor(Fig. 38A). Comparedro Octoprs. the sty'letsare thick in relation to the mantle. The mantle musclesforrn a break over the stylets. that is clearly visible on both longitudinal and trans v e r s a ls e c t i o n s( F i g . 3 8 A . 8 ) . COMMENTS. Straight stylets in Tremoctopus are not anchoredin the mantle as effectively'as studlike sti'lets of benthic octopods. Instead.thev are inserledin the mantle rvall like obliquely knocked n a i l s ( F i g . 3 8 A ) . T h e s m o o t hs u r f a c eo f t h e s t y l e t s and the absenceof the bend suggestthat muscles This reduction is compensaattachmentis r.r'eaker. ted. at least parrly. bl the special,well-developed funnel locking-apparatus.rvhich easesthe role of the funnel retractorsin holding the funnel during jet-sn'imming. Obviousll,. Tremoctopus cannot srvim. like Allopostts.rvith medusoidmovement of its arm crown. as its interbrachialweb is incomplete (absenb t e t r v e e na r m s I I I a n d I V ) . S i n c ej e t p r o p u l s i o n i s i t s o n l l ' m e a n so f l o c o m o t i o na n d i t p o s s e s s e s st1'lets a large.muscularmantle and r.vell-developed \\'e assumethatTremoctopusis capableof relativelr, s t r o n gj e t - s u i m r n i n g . The hi drostaticorgan that is reporledfor Tremoctopu.sfor the first time representsan important adaptation for pelagic life and implies that the octopuscan attain neutral or near-neutralbuol'anc;' passivel1,.

Oc1'thoidaeGra.v,1849 OcythoetuberculataRafinesque,1814 HABITS AIVDHABITAT. Little is knownabout the life stl le and ecology'of Ocythoetuberculala. waters This pelagicoctopodoccursin near-surface and regionsof all oceans to temperate in subtropical

Shell irr Vanrpvropoda

55

l1 12

\

mcv

FIG 39 GeneralanatonlYof oct'rhoe tuberculata.A. Dorsal rieu after removal of the skin from the mantle and head (immature female: 96'm Mr-). sota ai.oiils rtitn numbers indicate the p.lanesof corresponding cross-sections (sho*'n in Fig 'll) B. l-ateralrlie* afier remolal of ti-remantte^":rrr'""4 gill from the left iide lrmmaturetemale; 1 0 3 m m M L ) . S c a l eb a r s - I c m . PI'1c' 39 c'poeulle oclthcte ltrberctlatct,A. Bnr c:opca-rsHo.ii cropoH'r .,oc"re]-ra-reHu.sKoxHbrx noKpoBoBc NraH.'rr ll ro-jloBhl(lJe3pe-latcartxa: 96 r^r nNI) crne-rxu c ur0par'i \ Ka3brBaro'r [o]oxeHue coorBercrByrorqxx -.ropoHu cpe3oB

::i,lfitlb! 1?r,ti'n;i'i0"3;j$t:'?"1,

fiocre]rareH'.screHKH \raHrH'N xa6prr. ..,."oii

has often been caughtby drift nets and pelagic trawlsin upper10m of waterat night fRoper.Swe_ eny. 1976;Mangoldet al.. 1996b1.The dayrime habitatis unknown.Females reachabout30 cm ML. whiletheadultmalesaredwarf.approximately one tenththe lengthof the females.The mantleis mus_ cularandthe octopod.presumably. is an excellent swimmerfMangoldet al .1996b1.Malesandyoung femalesareoftenfoundresidinginsidethe testsof salps [Nesis. 198211987]. Femaleshave unusual hydrostatic organ,whichis locatedin therniddorsal regionof thevisceralmassfpackard.Wunz: 1994]. EXTERNAL MORPHOLOGY OF FEMALES. The stl,letsareabsentcompletely,. andonly rluscu_ larscarson thedorso-lateral sidesof themantlewith the "fin" nervespenetrating them indicatethe for_

(Herpe.rar

mer positionof the shell (Fig. 39). The mantleis ovoid.denseandmuscular. Themantlelengthcom_ prisesabout 25% TL; the mantlewidth is approx_ imatell' 75% ML. Anterior dorsalmarsin of the mantleis fastenedto the headby wide n,i.hrl Inrrcle. Arms are long (about 1.8 ML), ventraland dorsalarmsare rnuchlongerthan lateralarms.The rvebbetweenarmsis completelyreduced. A pairof waterporesis situatedat the basesof ventralarms. Funnelis very long, projectingbeyondthe arms bases. Proximalof thefunnelis fusedwith thehead. Funnellocking-apparatus is ver),strong.forrnecl b1 rigid cartilage-like cornersof the funneltharcoil outuardlike a spiralhooksand insenfrrmlr rnro correspondin_u depressions in the manrleuali 1Fig. :l0B). The distal parrsof the funnel corners are suollenriherethel resideinsidethe rnantleensu_

V. A. Bizikov

56 &

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ink

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Irlti. -10. Oc't'thoetuberculattt.A. Gcncral lateral vie* of an adult lemale. Note tubercleson ventral surlace of the mantlc. Il. Vcntral vieu o1-an adult female: ventral parl of mantlc rcmolcd to shori thc structureof mantlc car itr and lirnncl lockine-apparatus [fiom Naet. l92ll19231 rnodificd]. Scalc bars - 2 cm. Pl4C. 10 Ocythoeluberculdta.A, 3pe;ar ca\rKa:BH! c6ox1. BeHrpa"rbHaq cropoHa\raHrnu froxpbrraceruarorlcxl .rurrrlpoii. B. 3pe:ar ca\IKa: Bu.t c BeHrpa-rr,Hoii c'ropouu. BeH'rparsHarcreHKa \{aHrHu )'.fareHa: Bx.tHo crpoeHue rraurHriHo-sopollorrrroro MacuraS : 2 cr'r. 3a\lr,rKafe.rblrolo arrrrapara[u: Nael-. l92ll1923: c n3\relrerrHqNrn],

ring permanent. solid connection betrveen the funnel and mantle.The mantleapeftureis wide: its lateralmarginsaresituatedwell abovethe levelof e)'es(Fig.398). The visceralsacis small.The anmantleadductors havethe shapeof twisterodorsal ted.wide bands.l'he medianmantleseptumis wide andmuscular.Its anterodorsal marginis rvellanterior to anteroventral mantle margin (Figs. 398;

passobliquelyfrom thecor40B).Funnelretractors nersof the funnel alongsidethe visceralsac and attachto dorso-lateral r.vallsof the mantle. CROSS-^SECTIONS. The mantle wall consistsof the innerand outermuscularlayersseparated by a (Fig. al), The thin sheetof connective tissue outer muscularlayeris thickerthanthe inneroneandthe

Shell in Vantpyropoda

57

mat aql Y".

/

U )rsr FIC. 11. Schematiccr.oss-sections of the sofi bodl of Oc:,,-thoe -ttrberctrlatn lsamespecrmenas in Fig. 39A). A. Section l' at the lerel of the funncl B. Section2. it the r.u.r or anteiior"Jorrutmantle adductors.c. section 3. at the lerel of attachmentof the lunnel t.t.oitori. o p"JuGq i;g.;";tiecrion 3. showing anachmentof.the funnel retractorto the mantle. Position o1'sectionsis indicied t-D, ;;.-';;;;: i;. E: scale bar : I ""-Fle.':U. Pl4c ll cipe:sr \rqfKoro re-la ocvthoe tttberc'trlata (l^3c'rnirrp ror xe. qro Ha ?uc 39A). A. cpe: l. Ha ypon'e Bopollrir'B Cpe: 2' rra.1ponHenepe-IHHX -lopca"t,Hhrx rra'rH*s'x a,,lJ)Kropots. c. cpe. 3. ua 'pouue rrp,Kpe,'"rreH',, pcrparir'opoBsopoHKH.. 1.. yae:rilqeHrr;riirpp_ar-rre_rr cpc.rl 3. noi"ri,"ii"u,ru npuKpen.reHuepel.panropaBopoHriun rraurnn. llo.roxeurle cpc3oBroKa3aHona-puc. 39 A_D: .,";;;;-6-^_'i c]I. h: Nracrurad: I 16r.

58

V. A. Bizikov

dorsalmantle wall is slightlv thinner than the ventral and lateralwalls. The dermis is thin and smooth on the dorsalside of the mantle.graduallybecoming thicker and ridgedtoward the ventral side.The mantle cavity is large: its dorsal pan is much smaller than the ventral one. Visceral sac is relativelv compact in anterior and posterior parts (Fig. alA.C), srvollen in the m i d d l e p a r t ( F i g . 4 1 B ) . D i g e s t i v eg l a n d o c c u p i e s most pafi of the visceral sac in its anterior and rniddle portions. Ink sac is large. triangular in cross-section.embedded into the digestive gland frorn ventral side. The hydrostatic organ is larger than in Alloposus and Trentoctoptts.but similar in structure(Fig. alA-C). It is an elongatedthin-walled muscular sac situatedin the middorsal region of the visceral sac. above the digestive gland, The interior of the hy,'drostatic organ in its anterior paft is paftl)' filled by branchingmembranesprojecting insidefrom the ventral wall (Fig. 4lA). The posteriorparl of the comb-like. membranous organ is occupiedby loosel,v" tissuenot seenin the othertwo genera(Fig. alB.C). Head retractors are thin. wide and muscular. The1,forn-ra muscular envelopeof the visceral sac and spread from the head to the level of stellate ganglia. Near the base of the funnel the head retractorsconsistof tlvo layers (inner and outer) u'ith differentorientationof their muscle fibers.The pallial nerves lie inside the inner layer of the head fetractors.lateral to the visceral sac. Posterior to the collar fblds. the outer head retractorsbranch outrvardfrom the visceral sac and form the anterodorsaladductorsthat attacl.rto dorsolateralu'alls of t h e m a n t l e ( F i g . , 11 B ) . A n t e r o d o r s a la d d u c t o r si n Oc1ll1rrcare thick and muscular. uith the pallial n e r v e p a s s i n gi n t h e i r m i d d l e p a r 1 .T h e i r u n u s u a l s h a p ei n F i g . 4 1 B i s a r e s u l to f t h e s e c t i o np a s s i n g through the tu'isted rnid-portion of the adductors. The stellateganglia are situatedposterolateralll,to the attachrnentsite of the anterodorsaladductors. Ventral median rnantle septum is thin and Vs h a p e di n c r o s s - s e c t i o(nF i g . 4 1 8 ) . I t i s f o r r n e db 1 t\\'o verv thin adductor musclesthat diverge from the nidline of the ventral mantle uall and attach to the ventral side of the visceral sac. in the region of the ink sac. The spacebetrveenthe ventral adductofscontainsthe rectum.\'ena cava and the median pallial after) embeddedin vacuolatedconnect i v e t i s s u e .T h e a n t e r o d o r s ael r t e n s i o no f t h e I e n tral adductorspreadsinto the funnel as a thin rnuscular lay'ercovering the rectum and vena cava. The firnr-rel is l'er1 uide and semicircularin crosss f t u o d o r s a l u a l l sa n d s e c t i o n( F i g . a l A ) . I t c o n s i s t o wide. arc-likeventrolateralualls. the lafterare fused rvith the collar folds into singlemuscularlalers. The junctions of muscularfibers of different orientation mark the sitesof attachmentof the dorsalu alls to the *alls of the funnel.The collar folds are r,entrolateral

wide and muscular. They originate from the ventrolateral wall of the funnel and attach to the dorsal wall of the mantle, forming spaciouscollar pockets on both sides of the visceral sac. The funnel retractors are thick. wide. muscular ribbons attachedto the visceral sac along their medial margins (Fig. a1B). The usual position of stylets at the sites of attachment of the funnel retractors is occupied by dense cartilage. probably the remnant of the shell sac. which is wedged into the mantle wall on its inner side (Fig. 41C.D). A break in the mantle muscle occurs over the cartilage.The medial side of the cartilagetogether with the adjacent mantle wall form a shallow groove for attachment of the funnel retractors. At their attachment each retractoris irregularly triangular in cross-section. rvith a long. ventral apex projecting inside the mantle cavity. a short inner dorsal apex facing the visceral sac. and an outer dorsal apex inserling into the mantle rvall. The gills fastento the mantle wall ventral to the funnel retractors. COMMENTS. Although there are no reports of ir .sitrzobservationson the swimming mode of Ocythoe. rhe adult females are undoubtedly good jetswimmers as indicatedby the muscularmantle.the strong funnel locking-apparatus and the spacious ventral mantle cavity. On the other hand. the presence of well-developed hydrostatic organ or "swimbladder"in Ocythoefemalesindicatethat this speciesapparentlydoesnot needto swim constantly to maintain position in the water. There is an apparentcontradictionbetweenthe absenceof styletsand the ability for jet-srvirnming in Ocvthoe. The loss of stylets means that the attachment of the funnel retractorsto the rnantle is u'eaker.The main function of the funnel retractors is to hold the funnel during jet propulsion.Apparentl)'. the funnel retractorshave partially relinquished their role in Oc-,-thoeto the strong funnel locking-apparatusthat prohibits movernent betueen the mantle and the funnel. This is confirmed b1 the thin structure of the retractor muscles. A c o m p a r a b l es i t u a t i o ni s s e e ni n s o m e s t r o n g - j e n i n g ommastrephidswhere the retractorsare small and the funnel and mantle are permanentlyfused togeth e r . O t h e r u i s e r e d u c t i o no f s t y l e t sd i d n o t i n d u c e m a j o r m o r p h o l o g i c acl h a n g e si n O c t , t h o e . l ng e n e ral. this speciesretainedthe same octopodianBau p l a n .t h o u g h u ' i t h o u tt h e s h e l l . Argonautidae Trvon, 1879 Argonauta nodosa Solander, 1786 HABITS AND HABITAT. Argonauts. or paper nautilusesa . r e m u s c u l a re p i p e l a g i co c t o p o d si n h a b i ting subtropicaland tropical surface waters of all oceans.but only rarely'encounterednearshore[Nesis.

Shell in Vamp-vropoda

mcd

gst

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59

mnd

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nmus

---.-.-OVd

-mcv

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FlG, 12. Cenerirlanatoml of ..lrgoncura..\. .Aduit fbmale of .lrgorrcnttaLtrgo ' B o ljn d normal strinrntin_gposition Itrorl N a e f . 1 9 2 3 1B . . l \ l a t u r el t m a l e o f . 1 n o d o s u( 1 0 8 n r r n \ { L ) : d i i r s a lr i e * arroris nith numbcrs indicittcthe planes of cross-sections (shosn in Fig, .{3). Cl. \,lature lemale (9J mn \lL ): lateral r icrr afier remoral of the m a n t l e* a l l a n d t h e g i l l f ) ' o r nt h e l e f t s i d e . S c a i eb a r s l c m . PHq ^^-l^2:Crp^oeuue ..lrgonoutct..{. B:poc:a-r carrna 'lrgonauta .z/g.o.n"lblB\iltaq B ecrecrBeHHoiilo:e [u: \ael. 19231.B. 3pe-rarcarrxa .,1.nodosa (108 rnr I\{): srrj c :opcanuuoil cropoHbr.Crpe.rru c uuQparru\Ka3blBarof no-roxeHHecoorBercrB\roiuH\ cpe3oB(nona:laHut sa Puc. 13t. C 3pc.ral carrxa (9-1 rrrr .illVl): sH.r cSoxv rroc-te 'l crr. )la,reHnn creHKl \raHruu u xa6psr c .resoii cropoHu. \lacurrad -

1982119811. Femalesreachl0 cm ML and build the 'shell'upto 30 crn in length.Malesareduart approximatell'onetenththe sizeof females.and havebeen reportedliving n itlln salpsfBanaset a/.. 1982].Argonautsarepool s\\'irrlrners. at leastfentales.

EXTERNAL MORPHOLOGY OF FEMALES. Thestvletsareentirehlacking.A pairof breaksin themuscular tissueon thedorso-lateral sidesin the posteriorl/3 of the mantleindicates tlie fbrrrerpositionof theshell(Fig.a2).AlthoLrgh thetrLreshell

60

V. A. Bizikor

fun

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rlnl "Y'-\

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F l ( j . - 1 3 .S c h e n r a t rccr o s s - s c c t i o nosf . 1 . n o c l r : s t(tn l a t L l r el t m a l c : 1 0 8 n r r r \ 1 1 - ) .- { . S e c t i o n l . a t t h e l e l e l o f t h c l i r n n c l .l l . S c c t i o n2 . a t t h c l c r c l o t ' d o r s a ln r a n t l ea t l c i u c t o r C s .. S c c t i o ni . a t t h c l c r c l o f a t t a c h m e not f t h c f u n n c l r c t r a c t o r sD. . E n l a r e e dl i a s m e n t o 1 ' I ' i e u r c ' C s h o r i i n g a t t a c h n r c ' o n ft t h c f u n n e l r e t r a c t o rt o t h e m a n t l e .P o s i t i o n o l t h e s e c t r o n si s i n t l i c a t e do n F i e . l l . S c a l cb a r s - I c n r . (3pe.rarcarrna: 108 rrrr J\1r. -\. Cpe.r l. ua y poBrrcBopoHKu.[3. C.pc.l2. ua r ponHe PI4['. -13.Cpe:u ,]. nct,:losu pcrpaKTOpoB rrepeJHri\-topca-rbHbr\ a-fl\ KTOpoB. C. Cper i. rra r poBlrenprlNpen,reHnr BOpoHKn. D. \'Bc.rrlrcHHrrii ( t p a i r r c r r rs r r l a ' ( - ' . i r u K a l b n a r i ) r n nr in r K f r ! ' n . r e H npee r p l l K r o p at s o p o H KKr l \ r a H T n l lf.l o - r o x e H t t ec p e l o B[ o K a ] a n ( ) H a P r l c . - 1 2 .\ l a c r r l r a 6- l c r r .

Shell in Vaupl'ropoda

6l

is absent.f-emalessecretea thin externalcalcareous Head retractors are very thin and narrow. They sheltero . f t e n c a l l e dt h e ' s h e l l ' . i n u ' h i c h r h e 1 ,l i' v e do not form a complete muscular envelopearound a n d b r o o d e g g s f N e s i s .1 9 8 2 1 1 9 8 7 T 1 .h i s . s h e l l ' i s the visceralsac. but run along its sidesas a pair of a planispiral. lateralll compressed. boat-shaped thin muscular bands (Fig. a3A). posteriorly they structure lrith paper-thin. ribbed u,alls. The rveb gradually become thinner and disappear by the b e t r v e e na r m s I I - I V i s d i s t i n c tb u t s h a l l o w .D o r s a l level of stellate ganglia. Posterior to the collar arms of fernaleshave large sail-like vu'ebs. The inner folds. the external of the two head retractors seDasurfaceof the rveb is covereduith glandulartissue ratesand forms anterodorsalmantle adductors(Fig. and is responsiblefor secretionand shapins of the 43B). The latter are long and very thin. They are 'shell'. T l p i c a l l l ' r h e f e m a l es i t si n t h e : s h e ] l ', r i t h oriented obliquely and pass from the ventrolateral the beak facing or-rtuard. its dorsalarms curvedback sidesof the visceral sac to the dorsolateralwalls of u ith the n eb expandedor,'erthe 'shell' and all other the mantle. The pallial nerves are small and indisa r m s i n s i d et h e ' s h e l l ' h o l d i n g o n r o i t ( F i g . a 2 A ) . tinct. Anteriorly they are situatedon the inner sides T h e m a n t l e i s m u s c u l a r .s m o o t h .e l o n s a t e da n d ofthe headretractors.Posteriorlythey passthrough ovoid. Posteriorparl of the rnanrle is cuived dorthe anterodorsaladductorsand into the stellategansalll'. rihile its middle parl forms distinctdorsal glia at the sites of attachmentof the anterodorsal s n ' e l l i n gg i v i n g t h e a n i m a l h a r n p b a c ka p p e a r a n c e adductorsto the mantle. ( F i g . 4 2 A ) . T h e m a n r l el e n g t hi s c a . 2 l o / oT L : m a n Median mantle septum is thin and weakly rnust l e u i d t h i s a b o u t4 1 % M L . A n t e r i o r d o r s a lr n a r g i n cular (Fig. 438). Ir is fonned by two very thin o f t h e m a n t l e h a s a s h a l l o * , i n c i s i o ni n t h e m i d d l e adductormuscles.which originate on the midvenseparatin_e tu o anteriorly projecting lobes. Each tral mantle wall, passalmost parallelto one another lobe is connectedrvith the head b1' a narror.vand and attachto ventral side ofthe visceral sac. Space l o n g n u c h a lm u s c l e( F i g . a 2 B ) . T h e h e a di s s l i g h t l y of the adductorsis very small, containingsolely the narro\\ierthan the mantle. Water pores are absent. rnedianpallial ar1er1. The rectum, ink sac and vena Funnel is ver.ubr.oadand long. projecting rvell cava are shifted toward the visceral sac. The me_ bevond the arm bases.Its distal half is free from dian adductormusclesdo not extend anteriorlv into the head for about of its length. proxirnal part of the funnel. the funnel is fused rvith the head and fastenedto The funnel is semicircularin cross-section(Fig. the basesof ventral anns by a pair of long. strip-like 43A). Its ventrolateralwalls are fused with the colIateralfunnel adducrors(Fig. a2C). The funnel loclar folds into thick muscular layers. Dorsal walls king-apparatusis similar.to that of squids: it conof the funnel are less muscular. than the ventral sistsof oval depressionson the funnei cornersand one. The parts of the dorsal walls close to the vis_ correspondingcartilage-like knobs on the mantle. ceral sac are membranous.They attachto the venThe rnantle apeftLlreis very rvide: its lateral martrolateralsides of the visceral sac. in the region of glns are situatedrvell above the level of eves. The the head retractors.The lateral parts are more mus_ antelodorsal mantle adductors are tu isted long cular. Thev adhereto the ventrolateralwall of the bands. Ventral median rnantle septum is narror,r.. funnel and disappearon its inner surface.The collar Anterior margin of the septurnat its ventral attac_ folds are thick and muscular. They originate from hment is at some distancefrom the anteroventral the ventrolateral wall of the funnel and attach to margin of the n-rantle.The mantle rvall adiacenrro the dorsalrvall of the mantle.forming spaciouscolthe ventral adductorbearsdeep transversalgroove. lar pocketson both sides of the visceral sac w h i c h l o o k s a s c o n s p i c u o u sc o n s t r i c t i o no n l o n g i The funnel retractorsare thick. muscular ribt u d i n a l s e c t i o n( F i g . a 2 C ) . bons fusedto the visceralsac along their inner marCRO.SS-.SECTIONS.The mantle wall is muscular: gins (Fig. 438). The funnel retractorsare highly its inner and outer muscular layers are approximamodified as comparedwith other octopods:anteritely' equal in thicknessand separatedby a very thin orly they attachto the visceral sac by thin connecIayer of connectivetissue. Where the anterodorsal tive-tissuemembrane;posteriorly they attachthroadductorsattachto the rrantle. the mantle rvalls are ugh specialsupportingcartilages.oval in cross-secslightll' thicker than the dorsal and ventral walls tion. Inner side of each supporling car-tilageis ern( F i g a 3 B ) I n p o s t e r i o rh a l f o f t h e m a n t l e .i t s u . a l l b e d d e di n t h e c o n n e c t i v e - t i s s ueen v e l o p eo f t h e v r s is thinner and approxirnatelyunifonn in thickness ceral sac. while its outer side attachesto rhe funnel a r o u n di t s c i r c u m f e r e n c e ( F i g . 4 3 C ) . T h e d e r m i si s retractor.At the site of attachmentto the rnantlc. tl-rinand slnooth. The mantle cavitv is large. Antee a c h f u n n e l r e t r a c t o fi s t r i a n g L r l airn c r o s s - s c c t i o l t . riorlv the rnantlecavity,is somewhatlarger dorsallr u i t h t h e l o r i o u t e r a p e r i n s e r l e di n t o t h e l l a n r l c . than ventralll' (Fig. 43A.B). posteriorlr,. ihis proport h e l o n e d o r s a l a p e x c o n n e c t e dr i i t h t h c -r i : c e r a l tion is reversed (Fig. a3C). Anrerior parr of the s a c .a n d t h e l o n s . r e n t r a l a p e r h a n u i n c l i e c l - r i n t r r visceral sac is ahnost entirel-r'occupred br large t h e m a n t l ec a r i t l ( F i g . - l l C t . B r e a k s i n t h e r n a n r l e digestivegland. The hydrostaticorgan is absent. n r u s c l ea t t h e s i t e so f a f t a c h r n e not f t h e t i r n n c .rl e r -

6l

V. A. Bizikot

ractors mark the normal position of st1lets. Each break is filled by cartilage. probably'the remnant of the shell sac (Fig. ,13D).The lateral sidesof the cartilage attach to the mantle ualls. u'hile inner concaveside of the cartilagetogetheru ith the mantle u'all. fbrm a shallou concar,'itr'.in rihich the funnel retractol'sare inserted.Thus. the funnel retractorsattachto the inner side of the cartilage the salne wav thel' attach to the st1'letsin other shellbearing incirrates.The gills fasten to the rnantle wall belorv the attachmentof the funnel retractors. COMMENTS. General rr-rorpl-rologicaldesign of Argctnauta shorvs manl' features of adaptation to epipelagicrnode of life. This speciesdoes not have a lr1'drostatic organ like Oct'lhoe.Trentoctopusand 'shell' , l l l o p o s u s ,b u t i t i s k n o u n t o t r a p a i r i n i t s fbr buoyancy'fYoung. 1960].Comparingu ith Ocr'tirr.,e.muscularcomponentsin all adductorsin,lrgoncttio are much r.veakerindicating its less reliance on strong jet-srvirnming.The furtnel retractorsare connectedrvith the visceral sac through thin conn e c t i v e - t i s s um e e m b r a n e( a n t e r i o r l )l a n d u n u s u a l c a r t i l a g e( p o s t e r i o r l)l ( F i g . a 3 A . B ) . V e n t r a lm e d i a n nrantle adductor at the site of aftachmentto the r i s c e r a sl a c i s t h i n a n d n a r r o u ( F i g . a 3 C ) a n d d o e s not extendvery far (Fig. -+3C). Anterodorsalmantle adductorsare verv u'eak as thel' consistpaftl) of a t h i n m e r n b r a n e( F i g , 4 3 B ) . R e d u c t i o no f m u s c l e tissuernakesthe animal body' fragile and unableto producerapid jet thrusts. Reduction of st1'lets tn Argr.nauta. sirnilarly rtith Octthoe. is compensatedb1' the development of a strong funnel locking-apparatusof teuthidt) pe and b1''unusualstrengtheningof the attachmentof the funnel retractorsto the visceral sac. As r^,'ith Ocythoe,reduction of stvlets in Argornuta did not induce an1'major morphological transformation. Bolitaenidae Chun, l9ll Japetella diaphanu Ho1'le, 1885 HABITS AND HABITAT. Japerella diaphun is a meso-bathy'pelagic octopod inhabiting tropical and ternperate zones of the u orld oceans [Nesis. 19821811. Adults occur at depths from 600 rn to 1050rn and apparentll'do not perfonn diLu'nalrnigr a t i o n s[ Y o L r n g 1 . 9 7 8 ] .T h i s o c t o p o dg r o u ' su p t o 1 0 cm NIL. EXTERIVAL MORPHOLOGY. The bodl is u'eakl y m u s c l e da n d j e l l y ' l i k e( F i g . a a ) . D e r m a l i n t e g u ment is gelatinousand thick. especialll on the dorsal side of the headbetrveenthe e1'es.u hereit forms hood-like cover. Eyes are relatively large (about 15% ML) and locatedat the dorsolateralsidesof the head.The funnel is short. embeddeddorsallf in the head along nearlv its entire length. A funnel loc-

l,l

11,

a

\i \

I 12 13

B FIC. -11. Gcneral anatoml of Japetella diaphana (irttmaturefemale:57 mn'rN'IL).A. Dorsalvicn. B. l.ateral vies. Bold arroris with numbersindicateposition ot' t h e c r o s s - s e c l i o n( s h o r i n i n F i g . ; 1 5 ) . S c a l eb a r s : 1 crr. ca\tKa: Pl-lC. ll. CrpoeHue Japetella diaphana (He3pc-'rat 57 rnr ;rlN'l).A. Bu.r c Jopca-rruoii cropollLt. B. Bu:t no.roxeHile c6ox1. Crpe"rxu c rtuQpartHvKa3brBarcT coorBercrBlroruHXcpe3oB(nona:ausr ua PHc. .15). Nlacrura6: I crr.

king-apparatus is absent. Arms are shorter than the mantle. The web is relatively deep. connecting all arms for about 2/3 of their length. The nantle is elon-eated-ovoid. corrplising approxirnatel,v 55% TL. The stl lets are absent. and breaks in the mantle rnusculature are barell' visible on the posterolateral rnantle. Mantle aperture is rvide. reaching lateralh.

(Fig.aaB). the levelof e1'es I^ITERNAL STRUCTLTRE.The walls of mantle and highll' vaand funnelarethick.but gelatinous tll'o ver-uthin larThe mantleconsistsof cuolated. gelatinoby a thick ersof circularmuscleseparated of radialfibers us la1er containingthin trabeculae (Fig.a5).Bothendsof thetrabeculae branchasthel'' approachtouard inner and outer surfacesof the ualls of mantleandfunnel.The dermalintegument is thick. Mantle cavity is very large and alrnost endof themantle.Middlepart the posterior reaches of thevisceralsacis occupiedalmostentirel)'b) the digestiveglandu'hilethe anteriorparl is filled b1'a gelatinous. water)'core containingthe esophagtts.

Shell in Vamp-vropoda

63

mcd

np cfold dgl

gst

ink

mam

FIG '15. Schernaticcross-sections of Japetelladiaphana lrmmature temale: 57 mm \'1L) A Section l. at thc lerel of the lirnnel. B. Section2. at the ler:el of dorsal mantle adductors,C. Section3. benreen dorsal mantle adductors and lirnnel retractors.D. Section -1. at the lerel of attachmentof the funnel retractors.posrtion of sectionsis rndicatedon Fig. -l-1.Scalc bars = I crr. Ptiqr l_i cpe:sr rr.rrxo'o re-ra Japetelladictphana(Heipe.raqcarrxa: 57 rrrr ,l!11. .A. Cpe: l. sa r poBHcBopoHKrj. B . C p e : 2 . n a I p o n u e n e p e - t H l \ . t o p c a , t b H br rt a\ H r u i i u i na r " . t l K r o p o B C.. C p e : 3 . r r e x - t r ' : o p c a - t b H b r \rnr ai u u l i u s r r u r -1. ua rpoaHe ilpuKpen.terulrperpax'ropoBtsoporifil.IIo-roxenrrc alJ)tiropa\Ifi rl pcrpaKropa\Ill D. Cpe: ,BopoHKtl, cpe3oBnoxa3aHoua Pric. l.l. \lacura6 - I crr.

o+

\'

.\. Bizikor

d o r . . i , . i . . 1 1aan d a p a i r o f l a r g e p a l l i a l n e r v e s( F i g . l-< \ \ hr drostaticorgan is absent. i lcr.l retractorsare thin and barelv visible in the c r ' . : : - ) ec t i o n s .T h e l d o n o t f o r m c o m p l e t ee n t ' e l o pe .tr.r.\:in t hJe r i s c e r a l s a c b u t r u n a s a p a i r o f t h i n i t b a r - , . it:r r . r s l a t e r a ls i d e s( F i g . . 1 5 A ) .B e h i n d c o l l a r lblJ: the head retractorsgive origin to the anterod o r s a lr n a n t l ea d d u c t o r s( F i g . a 5 B ) . T h e l a t t e ra r e shr)r1.leebl\ muscularand extend bettveenthe dorsolat.-rll sides of the visceral sac and the lateral u a l l : o 1 - t h er n a n t l e .T h e s t e l l a t eg a n g l i a l i e o n t h e lrantle ualls just ventral to the attachmentsites of anterodorsaladductors 'l'he nredian rnantle septurn is relativeh thick. b u t r i e a k l r r n u s c u l a rI.t i s f o r m e d b 1 t u o t h i n a d ductor rnusclesthat diverge from the middle line of the rentral mantle u,all touard ventral side of 'lhe rectum.vena t h e v i s c e r a ls a c ( F i g . 4 5 8 . C ) . cava and the ink sac are situatedbetrveenand are e m b e d d e di r r c . e l a t i n o ucso n n e c l ier t i s s u e . The funnel is broad and its ventral and dorsol a t e r a lu a l l s l u s e i n t o a s i n g l em u s c u l a rl a 1e r ( F i g . '15 A). The fi-rnnelrvalls attachto the ventrolateral sides of the visceral sac just ventral to the head retractors.The w'alls here are approximately'trt ice as thick as the ventral rvall of the funnel. Collar folds originate from lateralnalls of the funnel. run alongsidethe visceral sac and attachto dorsal rvall of the mantle. Muscular la;'ers of the collar folds and funnel are fused and the boundariesbet'ul'een them are apparent onlv in the orientation of the r a d i a lm u s c l e s . The firnnel retractorsin Japetella are unusual in shape.Thel are ver) u'ide. thick. long and broadll tirsedu'ith the viscelal sac along their entire length ( F i g . 4 6 C . D ) . D e s p i t el a r g e s i z e .t h e f u n n e l r e t r a c tols are rveakll, muscular.their nearly'rvhole volurne is occupied by' gelatinous tissue riith sparse. thin. r'adial muscle-fibers crossing into it. The cross-sectionsof the funnel retractorsremind me o f a p a i r o f h u g e b a l l a s tt a n k s i n a s u b r n a r i n e( F i g . 15C). The gills are srrall and fragile: thel fasten to the lateral mantle rl'alls b1' thin li-earnents. Attachrnent of the funnel retractorsto the mantle occurs unusualll, far posterior.in the posterior q u a r l e ro f t h e m a n t l e ( F i g . a 5 B ) . A t t h e s i t e o f attachmentthe funnel retractol'sextend horizontal1 1 ,t.o t h e l a t e r a ls i d e so f t h e v i s c e r a ls a c( F i g . ; l 5 D ) and form an unusual horizontal pafiition of the rlantle cavitl'. The funnel retractors are slightll' . h e m a n t l em u s c l e s t h i c k e rt h a nt h e m a n t l er n u s c l e T and funnel retractorsare fused togetheru'itliout irttelnal boundariesother than provided b1 the orrentation of the radial muscles.Supponing canila,qes are absent.The mantle does not have a break at the site of attachment.but its outer side bears distinct indentation indicating the normal position for a s h el .

COMMEI,ITS. Soft body anatomy of Japetella exhibits a number of featuresindicating that this species evolved mainh' as passivedeep-rvaterfloater. Its funnel fuseswith the headalong its entile length ( F i g , a a B ) . M a n t l e m u s c u l a t u r ei s g r e a t l y r e d u c e d a n d c o n s i s t sm a i n l l o f r a d i a l t r a b e c u l a e( F i g . 4 5 ) . The u'eak nature of virtually all musculatureindicates reduction in animal activity. On the other hand. the presenceof huge vacuoles in nearll' all muscle tissue suggeststhat this gelatinoustissue is positivelybuol'antand actsas a floating device.The funnel retractors therefore. may truly be ballast tanks.Attachmentof the funnel retractorsto mantle is verv rveak. It is not supportedeither by shell or by' connectivetissue. Reductionof sty'letsin Japetella did not induce an,l'major transformationin its general morphological design. Despite some specializedcharacters. Japetellaretainedty'picalincirrate Bauplan.Unlike representativesof Argonautoideaclade. reduction of st1'letsin Japetella r.vasnot coupled rvith deveiopment of an1 functional substitutes(funnel locking-apparatus.mantle caftilages etc.). replacing the stylets.Such a reductionwas apparentll'caused bv general decline in animal activity. associated ivith pelagic life in the deep ocean.

AmphitretidaeHoyle,1886 AmphitretuspelagicusHoyle, 1885 HABITS AND HABITAT. Lirle is knownabout biologl' and ecology' of Arnphitretus. lI is a rare rneso-bathlpelagic octopod inhabiting tropical and subtropical \\ aters of the u'orld oceans [Nesis. It has transparent.gelatinousand near1982119871. lv colorless bod1, and reachesup to 90 mm ML [Nesis. 198211987].Young Amphitretus occur in upper mesopelagicdepths dr"rringthe day. judging by a fer.rcapturesfYoung et al.. 1996]. There is nrr report on observationsof this speciesfrom submer'sibles.but it has beenobservedin shipboardaquaria [Young er al.. 19981. EXTERNAL MORPHOLOGY. Bod,r" is rveakl;and nearll' cornuscular.jelll like. semitransparent lourless.The dermal integumentforms a ver)' thick. gelatinouscover over the body disguisingits outline (Fig. 46). The stl,letsare absent.and the breaks in the mantle are not visible. The arms are long. about 1.5 ML and are connectedb;' a deep transpal'ent ueb for approximately'2/3 of their length.Anterior r,entralualls of the mantle fuse r.r'iththe funnel and head.As a result of this fusion. the mantle aperlure is reducedto t$o small openingson the lateralsides of the headthrough rihich the rl'atercan be punped inside the mantle cavitl . The funnel is verl long. tube-like and fused dorsalll uith the head for about o f i t s l e n g t h .T h e e y e sa r e s i t u a t e do n d o r s a ls i d eo f

Shell in Vampyropoda

65

FIG 16 Laleral Vier'" of Amphitr,etuspelagicus (immature male: 26 mm DML). Bold arror.vsrvith numbers indicate position of the cross-sections shou,n onTig. 47. Scalc bar - I cm. PIAC.16. BHI c6ox) Arnphitretusp-elagicus(He:pe.ruii cavcu: 26 lrrv [M). Crpcrxu c quQpayH vxa3brBarorrro,'roxeHue coorBerc'fBvrorrlxx cpe3oB.u:o6paxeHurrxua pl.rc.47. Macurr.a6: I crr.

the head.their basesbeingin directcontact.They areunusllalin shapeandorienteddorsally. CROSS-SECTIONS. A strikingfeaturein Amphitretl$ anatonlyis the presenceof broad fusion betweenthe anteroventral marginsof the mantle,the collarfoldsandthe lateralsidesof the funnel(Fig. 47A) and betweenthe posterolateral pafts of the collarfoldsandthevisceralsac(Fig. 478).Amphitretus is the only incirrateoctopodhavingsucha fusionwhich is strikinglysimilar in positionand structurewith the collar fusion found in cirrates (e.g.,Grimpoteuthis, Fig. 12,A;Cirroteuthis,Fig. 178,C)but differsin n-raintaining lateralopenings to the mantlecavity.The fusionbetweenthe funnel andmantlehasthe effectof eliminatingthe mantle wall beneath the funnel,lvhichformsa deeoincisio n i n t h er e n t r am l a n t l e\ \ a l l . Funnelis wide but thin-walled.Its ventraland lateralwalls are forrnedby singlemuscularlayer that differs from the dorsalrvallsin the orientation of rnusclefibers(Fig. 47A). The collar folds representdorsolateral extensions of the dorsalwallsof thefunnel.Theypassalongside thevisceralsacand attachto the dorsalmantlewall forming spacious

collarpocketson bothsidesofthe visceralsac.The lateralsidesof the funnel and adjacentpar-tsof the collar folds are fusedwith the mantle.posteriorly the collar folds fuseboth with the mantleand with thevisceralsac(Fig.47B).Herethe fusionbetween the collar and the visceralsac is very thick and consists of an outerthin muscularlayeranda thick innervacuolated, gelatinous core.The coreis pierced by radial muscle-bundles running from the outerlayerto the visceralsac(Fig. 47B). The walls of mantleand funnelarethin, gelatinous and weakly muscular.The mantle bearsa wide longitudinalgrooveon its dorsalside and a narrowgrooveon its ventralside definedby the mantlethicknessin theseareas(Fig. ,17C-E).The mantlewall in the dorsalgrooveis approximately half as thick as the adjacentareas.The thickness of the dermalintegumentis roughly equalto or greaterthan that of the mantle.Mantle cavity is very largebut the visceralsacis rathersmall.The digestivegland is elongatedverlically,so it looks disproporlionately largeon cross-sections. The anterodorsalparl of the visceralsacis fusedwith dorsal mantlewall (Fig. 47A). The stomachoccupies

66

V. A. Bizikor

nuf sgl

aa

r{nl

colf

dmad

rt' dgl

mam

F I G . 1 7 . S c h e n r a t iccr o s s - s c c t i o ncst l , l n t p l t i t e t t t sl t e l L t g t c u( isn r m a t u r er r a l e : f 6 m m D \ l l - ) . . A . .S e c t i o nl . a t t h e l e r e l o f a n t e r i o rm a r g i n o f t h e m a n t l e .B . S c c t i o n2 . a t t h e l e r e l o f t h e p o s t e r i o rp a r r o f t h e f u n n e l .C . S e c t i o ni . a t lhe lerel of dorsal mantle adcluctors.D. Sectron-1. behrnd dorsal mantle adductors.Fl. Section 5. at the lcrel of attachmentof the lunnel retractors.Positionof sectionsrs rndrcatedon Fi_e.-16.Scale bars: I cm. PhC. -17.Cpe':u rt.rrnorore-ra -trilpliitretuspel0giurr'(He3pe.'rbrr"r caveu: 26 rnr.il\l).,\. Cper l. ua rposrrc ilcpcJHcro xpat \raltruu. B. Cpe: 2. Ha r poauc ratrrcl"r.racrlrBopoHKrr. C. Cpe: -i. Ha r poeuenepeJHr\ .fopca,rbHbl\ \lilullllrbr\ a.],t\KropoB.D. Cpe: -1. nora:u lopca.rbHbr\rrasrrrirHsrra.lt\ KropoB.I:. Cpe: 5. Ha I poaHe upHKperr"leHfiq pcrpaxropoBBopoHKrr. flo.roxeune cpc3oBrroria3auoHa Prrc 16. \lacuLra6 : I crr.

Shell in Vampyropoda a positionon the dorsalside of digestivegland (Fig. + 7 B . C ) . A h r d r o s t a t i co r s a n i s a b s e n t , The head retractorsare very thin and barely visible in the cross-sections. They,,run along the lateral sidesof the visceral sac as filrn-like muscular bands (Fig. ,17B). Posterior to the funnel they branch outrvard forming anterodorsal adductors (Fig. a7C). The latterare thick but weakly muscular c o n s i s t i n gm a i n l l ' o f g e l a t i n o u sc o n n e c t i v et i s s u e . Thel' extendobliquely,betr.veen the visceralsac and the dorsolateralwalls of the mantle. Anteriorlv the s r n a l l p a l l i a l n e r v e s a r e s i t u a t e do n d o r s o l a t e r a l sides of the visceral sac. The nerves pass through the collar muscle and the anterodorsaladductors and enter the stellateganglia. The latter occup,r'the typical position adjacentto the attachmentsites of anterodorsaladductorsto the mantle. The rnedianrnantleseptum is thick. broadlv trianguiarin cross-section. and rveakly muscular(Fig. ,17C.D). It is formed b1. two verv thin adductor rnuscles.that diverge from the mid-line of the ventral mantle rvall tou'ard ventral side of the visceral sac.Betweenthe adductorsare the ink sac.intestine and vena cava embeddedin gelatinousconnective ti ssue. The funnel retractorsoccupy unusualpositions: they originate from the dorsal walls of the funnel. pass along lateral sides of the visceral sac to its dorsal side Lvherethe1,,merge together forming a single muscr,rlarlayer over the visceral sac to their attachmentsiteson the mantle (Fig. 47E). The mantle wall exhibits no modificationsu'herethe retractors attach. Supporting carlilages are absent. COMME|\,ITS. General rnorphological design of Amphitretus shows a unique set of adaptationsto planctonic life in deep ocean waters. Watery consistencvof the body and the loss of heavv rnusculature apparentlycontributesgreatly to buoyancl,. However. the structurethat provides some positive buoyancl, is unknown. The mantle cavity is more complex in Amphitrelzzsdue to the fusion of the collar folds with the mantle and visceral sac and verlical orientation of the digestive gland (Fig. 47A.B). The latter is achieved by special muscles that activell' maintainthe digestivegland in verlical position in different posturesof the anirral fyoung et al.. 19981.Functional meaning of the fusion between the ventral mantle lvall with the funnel and collar folds is unclear.It rnay help to optimize respiration flows at low energy costsand/or fix position of the funnel. Presumablvthe primary locomotion for Amphitretusis slow swimming with medusoid contractionof its deep umbrella. Despitemany specializedcharacters.Amphitrelzs retained typical incirrate plan of structure and. a c c o r d i n gt o N e s i s L 2 0 0 2 1 a n dV o i g h t [ 1 9 9 7 ] .e v o l ved apparentlyfrom benthic incirrate octopods.all of them having open mantle apefture.Fusion of the

67

mantle and funnel means that there was no more need to anchor the funnel retractors in the mantle by st1'lets.and the latter became redundant and was lost. The role ofthe funnel retractorschangedfrom supportofthe funnel to supportfor the visceralsac. This nerv role is the most obvious at the level of attachment of the funnel retractors to the mantle. where the funnel retractorsfuse together making m u s c u l a r' r o o f a b o v e t h e v i s c e r a ls a c ( F i g . 4 7 E ) . Like in other shell-lacking incirrate octopods,position of the former stylets in Amphitretas mal be spotted b; attachment of the funnel retractors. General morphological design of mantle complex in Amphin'etus representsthe most specializedstate among the speciesdescribedin the presentstudy. The means by which the peculiar funnel mantle fusion occurs is describedfor the first time.

DISCUSSION Look around and see all thejelllfish. You sayin'.flotation is groovy, baby. J i m i H e n d r i x .' P o w e ro f s o u l ' Variation of the shell structure and shell-soft body relationship in Vampyropoda In order to determinethe evolution of the shell i n o c t o p o d i f o r m st.h e s p e c i e sw i t h t h e m o s t p r i m i tive shells in each group will be selectedand its perlinent characterslisted. Vamplromorphida A single representativeexists. The cnaracteristicsof the vampyromorph that are considered to be prirnitive and pertinentto this study are the following (Table2): 1. The length of the gladius is about equal to the mantle length. 2. The gladius consistsof three rnorphological parts (dorsal plate. conus and rostrum). is built of three shell lay'ers(ostracum.hypostracum.and periostracum). and its dorsal plate (= proostracurn) c o n s i s t so f f i v e l o n g i t u d i n a el l e m e n t s m : iddleplate (rachis).a pair of lateralplatesand a pair ofuings. All elementsof the proostracumare delimited by asymptotic borderlines.I call this combination of charactersthe 'teuthoid plan'. 3. The rniddle plate (rachis)is wide and rongueshaped.It is the longest part of gladius proostracum. Lateral plates of proostracumare much narrower than the rvings. 4. The growth of the gladius occurs by adding layersto each of the three shell layers.The middle layer (ostracum)grows by incrementsadded from the anteroventralside and arrangedin tile-like pat-

V. A. Bizikor

68

ltatures of the shell and its relatronshrp*ith the sofi bodl in Vamplropoda. Table 2. Clharacteristic qeprbr crpoeHur paKoBHHbl c \l.qrKH\lre"lolt ) Vampvropoda H ec B3au\roorHoueHut TaS"ruua2, XaparirepHbre Character

In c irrata

Cirrata

Vamp.v-'romorphida

Shell condition and structure: P r e s e n c co f t h e i n n e r s h e l l

present

present

presentor absent

Conditionof the shell

longitudrnalchitinousplate

trans\ersalcanilage-likeU-

{ g l a d i u ts

shaped plate

a pair of cartilage-like rods 1st1 lets.;

Shell length

appror

less than the ML

less than the N{L

Shell structure

erttire

entire

divided in the median pan

Structural pafts: proostracum. conus and rostrunr 'l'he shell layers (ostracum. h1postracunl and periostracum)

present

absent

absent

all three shell lalers are present

one shell laler is present (hl postracum?)

one shell laler is prescnt (hl postracum?)

Shell gro$1b pattem

tile-like pattem (ostracunr and hrpostracurn) and concentric pattern (perrostracum )

c o r r c e n t r i cp a t t e m

concentric pattem

Position o1- shell in the body

superficial, terminal

supert-rcial.subterminal

superficial. subten.ninal

Funnel retractors

attach to the \ings

attach to anteroventral parts of the uings

attach liom inside to anterior half of the stllets

Head retractors

attach to the lateral plates

attach lrom inside to anterior. dorsal and ventral margins of the \\tngs

attach to the mantle

Upper margins of the collar fblds

attach anteriorl) to iateral sides of the nuchal caftllage

posteriorll to the shell sac and the visceral sac

attach to the mantle

Nuchal fusion between the mantle and the head

flsed in roung and adults

fiee in paralarrae

fused at all stages

Stellateganglia

closell situated in paralan ae

uidell

wideh separated

Dorsal nrantle cavity

absent

prescnt

present

Anterodorsal nralitle adductors

absent

absent

present

\urrrber ol lins

t\\u ncirs

one pair

llns absent

Articulation of the flns

fin bases are separated liom the shell sac b1 epithelial basal pockets

fin bases are fused uith the shell sac. Basal pockets absent

equal to the NIL

\Iuscle attachment:

Soft bodl nrorphologl:

Ventral median mantle adductor absent I"unnel locking-apparatus

present.prinritire

tern: each next increment is shifted anteriorl)'against the previous increment.As a result. the thickness of the ostracum graduall)' increases rvith grou'th. r.vhilethe earlier regions of the ostracum lose contactwith tl-reshell epithelium and stop growing. Growth of the inner la1'er(hypostracurn)occlrrs b) adding of cartilaginous-likematerial to the ventral surfacein the posterior half of the proostracllm. The incrementsof the inner la1'erare slightly shifted forward against each other. and everv newh' secretedlay'er overlaps the anterior margin

s e p a r a t e di n a d u l t s

prescnt

present

absent

absent in priniitive fomis

of the previous la)er while posteriorly it gradllallv wedges in the region of the cone flags. Outer layer (periostracurn)grows by concentriclayers of conical shapethat are laid dorvn on the outer sltrface of the previous la)'er.Center of growth of all three lal,ers(initial shell) is situatedin the apical paft of the conus fBizikov. 1996]. 5. The gladius occupiesa superficial position: the mantle musclesattachto the ventral (inner) side of the gladius along its entire periphery,except fbr the anterior margin of free rachis.

Shell in Vanipyropoda

6. l'he funnel retractors attach to the anterior r n a r g i n so f t l r e w i n g s . 7. The head retractorsattach to anterior marsins o f t h e l a t e r a lp l a r e s . 8. The visceral sac is fused with the shell sac along its entire length. Dorsal mantle cavitl and anterodorsalmantle adductors are absent. 9. The headoriginally is not fusedrvith rhe mantle. In adults the head is fused; however. in paralarvae, anterior dorsal margin of the mantle is not fused with the head in the nuchal region fyoung. V e c c h i o n e .1 9 9 9 1 . 10. The shell sac is fused with the visceral sac tl-rroughoutits length (i.e.. a dorsal mantle cavitv is absent.;. 1 1. The stellateganglia are situatedon both side of the gladius at the level of lateral plates and in adults are widely separated. 12. Tu'o pairs of fins are present:a paralarval pair that is eventualh'resorbedand a juvenile/adult set that develops later and more anteriorly,,fpickford. 1940: 1949]. Paralarvalfins. rvhich are consideredthe primitive fins. lie over the u.ings of the gladius and attachto the shell fyoung. Vecchione. 19961.The adult fins are separatedlrom the shell sac by epithelial basal pockets. 1 3 . U p p e r m a r g i n s o f c o l l a r f o l d s a t t a c ht o l a teral sides ofthe nuchal cartilageand the shell sac anteriorlv and to the visceral sac and the shell sac posteriorlr'. COMMENTS. Pickford [1949] found rhat development of fins in Vampvroteutllisis unique among cephalopods. In this species earlv paralarvae (Pickford's "stage I larvae") have one pair offins. T h e n t h e s e c o n dp a i r o f f i n s d e v e l o p sa n t e r i o r l l o f the first pair. and the number of fins reachesfour ("stage2"), As developmentproceeds.the first pair of fins gradualll' resorbs and finally disappears. u'hile the secondpair increasesin size ("stages3 and 4''). The first pair of fins is proved to be homologor"rsto the fins of other cephalopods[young. V e c c h i o n e .1 9 9 6 ] .O u r d a t a s h o u t h a t a r t i c L r l a t i o n of adult flns Lviththe shell and mantle in [/antpt,roteutltisfollou,s the same basic coleoid patterndesc r i b e de a r l i e ri n t e u t h i d s[ N a e f .1 9 2 ] / l 9 l j : F i g . 6 6 l a n d s e p i i d sf N a e f . 1 9 2 1 1 1 9 2 3 F :i g . 2 9 0 ] . I t i s e s p e c i a l l l c l o s et o c o n d i t i o nf o u n d i n s o m e o e s o o s i d families. for example. Enoploteuthidae.uhJre the g l a d i u s o c c u p i e ss u p e r f i c i a lp o s i t i o n a n d t h e f i n basesreston its dorsalside.separatedfrom the shell s a c b l b a s a lp o c k e t s[ N a e f . 1 9 2 1 1 1 9 2 3F:i g . 6 6 a ] . Aparr fiom the fin structure.I'antpt.roteutltisparalarvaeare verv siurilar to adults in other respects. On the contrar\'.the hatchlingslook r,erv different. exhibiting a nurnber of archaic featuresthat disappear during later development.Young and Vecchione [999] describedrecentlr hatched llamptt.otetutltis(8 mrn ML) that had large funnel. rrhich uas

not embeddedin the head, no fusion of the mantle and head. no thick gelatinousintegumentcovenns the body. short arms. no web between arms. thick filaments that rvere approximately equal to the arrrrs in length and situatedin one circle with the other arms. and the gladius with 'somewhat narro*er median field' (Fig. 48). The gladius of Vcnnpt,roteuthis hatchlings deservesa special attention. ln contrast to adults, it has narrow rachis (median plate). which has long anterior free par1.The lateral plates and wings are shoft, weekly developedand fused with the cone flags forming posteriorextension of the gladius. The rostrum seemsto be very small. Position of wings in posterior half of the gladius means that the funnel retractors in hatchlings should be much longer than in adults. The structure of gladius in Vampyroteuthis hatchling is surprisingly similar to the gladii of some recent o e g o p s i ds q u i d s . Another remarkable feature of Vampyroteuthis is that its stellateganglia are weakly developedand apparentlyshift their position during ontogeny.position of stellate ganglia is different in teuthoids and octopodifonns.Being situated laterally of the s h e l l i n a l l c o l e o i d sf N a e i l 9 2 l l 1 9 2 3 ] . r h e s t e l l a t e ganglia in teuthoidsare locatedextremely close to one another and are connected by an interstellate connective Ivanov. Strelkov. 1949]. In octopods they' are set u'idely apart and are not comected. In Vantpvrotetillls the interstellate connective is absent. and the stellateganglia apparentlyshift their position during ontogeny in accordancewith ontogenetic rvideningof the gladius. In hatchlingsthey are apparentlysituatedcloser to each other. like in teuthoids.r.vhilein adultsthey are set widely apart. l i k e i n o c t o p o d s( F i g . 2 , A ) . Thus. ontogenetic data show that recenl Vamplroteuthis apparently evolved from some tena r m e d f o u r - f i n n e d c o l e o i d sw i t h f r e e f u n n e l a n d free anterodorsalmantle margin. In general. [/ampvroteurlis exhibits basically the same patt e r n o f g l a d i u s - s o f tb o d l ' r e l a t i o n s h i pa s t h e o n e d e s c r i b e de a r l i e r i n s o m e e g o p s i ds q u i d s [ B i z i k o v . 1 9 9 6 :B i z i k o v . A r k h i p k i n . 1 9 9 1 1 O . bvrousl1'.it is verl' closeto the ground coleoid pattern o f s h e l l - s o f tb o d y r e l a t i o n s h i p .I n O e g o p s i d at h e m u s c l e a r r a n g e m e n ti s t h e m o s t c l o s e t o V u n t p t : r o t e u t l t i s* i t h r e t r a c t o r so f t h e h e a d a n d t h e f u n n e l a t t a c h i n gc o r r e s p o n d i n g l yt o t h e l a t e r a lp l a t e s a n d u i n g s o f t h e g l a d i u s .a n d t h e f i n s l y i n g o v e r t h e u i n g s o f t h e g l a d i u s a n d a t t a c h i n gt o i t t h r o u g h t h e e p i t h e l i a lb a s a lp o c k e r sI B i z i k o r , . 1 9 9 6 : F i g . a O l . l n M 1 ' o p s i d ar h e m u s c l ea r r a n g e m e nirs s i r n i l a re x c e p tf c r t h e f i n s t h a t d o n o t c o n t a c t\ \ i t h t h e s h e l l b u t l i e o v e r t h e m a n t l er i a l l a n d a t t a c h t o i t t h r o u g h t h e b a s a l p o c k e t sI B i z i k o r . 1 9 9 6 : F i g . 3 9 ] . T h r s a n o t e u t h i d sh a v e u n i q u e p a r r e r nL ) t m L l s c l ea r r a n g e m e n t r. . r , i t ht h e h e a d r e t r a c t o r sa t -

-0

V. A. Bizikov

dra*ings of I'antptroteuthis infernalis hatchling illustratingpositron and shape of its gladius FIG. 48. Schen.ratic [redra*n from Young. Vecchione.1999]. A. Lateral rien fiom right side. B. Dorsal vien. C. Ventral vie"r of the gladius. PHC. 48. Bseuuuil BH.f .tHrrHHKti I'antptrotettthis infernalis HelocpelcrBeHHoIIoc.re BbtKreBa.u.rrrccrpHplHrLttuii rra,lrl)ca [u: Young. Vecchione.1999] A. Bu: c npanoii cropoHbr.B. Bu.r c,'topcarbrroii rfopvl H fro.'roxeHue cropoHLr.C. Bu: r"'raJhlcac BeHrparbHoilcropourt.

taching to extremely u'ide anteriorly protruding 'wings' and long funnel retractorsattachingto the ' c o n ef i e l d s ' I B i z i k o v . 1 9 6 6 :F i g . 3 8 ] . T h e f i n s i n Thisanoteuthidaeattachto the mantle the sameu'a",' as in M.vopsida. Cirrata Of the generaexamined.Opisthoteuthisappears to be the most primitive in respectto the shell as it is the onh' taxa that has the funnel retractors of the Cirattachedto the shell, The characteristics rata that are consideredto be prirnitive and perrinent to this studv are the follorving (Table 2): 1, Gladius is thick cartilage-likeU-shapedstructure without asyrnptotic lines 11ing transversalllon dorsal side of the mantle. 2 . G l a d i u s g r o u ' s b r c o n c e n t r i ci n c r e m e n t so f cartilage-likesubstance.The centerof grouth (initial shell) is situatedin the medial part of the gladius. 3. The gladius occupiessuperficialsubterrninal position. The mantle attachesto the gladius along its entire peripherl. including anteriorrniddle parr. 4. The funnel retractorsattach to anteroventral parls of the rvings that sometimesma1 be extended 'horns'. into flexible

5. The head retractors attach from inside along periphery'of the wings (dorsal.anteriorand ventral margins of the wings). 6. A dorsal mantle cavity is present.It is a narrow slit between the visceral sac and the dorsal mantle wall that extendsposteriorly between stellate ganglia almost to the level of the shell and connectslaterally to the ventral mantle cavity'.Anterodorsalmantle adductorsare absent. 7. The stellateganglia are set widely' aparl h ing at the junction of the visceral sac and the lateral m a n t l ew a l l s . 8. The anteriordorsal mantle margin fused rvith the head. 9. The fins basesadheretightll' to the shell sac over flat outer surfaceof lateral rvings of the gladius. Basal pocketsare absent. 10. Upper margins of collar folds attach to the mantle. COMMENTS.In recentCirrata.primitive rvide Ushapedgladii rvith relatively'long and narrow lateral rrings are found in Opisthoteuthis. Grimpoteuthis. Cirroctoptrs, Ltrettthis and Stauroteuthis (Fig. 49'). Among the generalisted.Cirroclopzrsdeservedspecial attention as it includes the species with the gladii exhibiting transitionalfeaturesbetween Cirrata and Incirrata.For example.C. antarctica (Ku-

Shell in Van.rpl'ropoda

7l

om //

t

/

H €--: /

/

-

(ll \

\/

\

tu

N \.l

l tlllt.l: -\+;+

1111:i

j:-

:l

FIG Opisthoteuthis californianctBerrl . 19.19 .49 N{orphological.rariabjlitrof gladii in Cinata (not in scale).A. B C' D Cirroctopus hc,c'hberg,O jh.u. i0'0t. C. H --'l.,r,tnlr,,t,i, ^Grintpoteuthislntbellata (Fischer. 1883) E. F 'rlrrzlsii O'Shea et Lu. 2002. I Cirroctopus antarctica Kubodera et Okutani. 1-SSO. :. K - Staurotetihis st,rtensts Verrill. 1879: L. M Ciryothaumannirati Chun. lgll \. O - Ci.roreuthismuelleri Eschncht. lg3g. A. C. E. G. I and J a n t e r t o rr i e r i l d o r s a l s i d e i s u p ) . L . N d o r s a lv i e u ( a n t e r i o re n d i s d o n n ) . g . O . " F . f i . ( N'l and O - lateral rie* (anteriorend is on the'lett: dorsal sidc is up') [,+-D. I- and M ]'figur., of ihe author: E-H after Vecchione.Y.oung.2003b: I after Kubodera.Okutani. iSSO:t. K - afrer Collini. Henriques.2000: f-. N{ - alier Aldred et al.. 19831. PHC_ '19 lloptlo.roruuecxoe pa-:uoo6pa3uef-raJulcoB_unpparHbl\ ocb\rHuoroB (rracl-rra6 ue cod.rrcJeu) A. B 'Cirrioirot,r, 19,19 C. D - Grinryoteurhisun$ellatct lFischer. iSSjl. E.'F ?1,1,!:l:i,!::,.,calrtbrniqrn^Berrr. hoL'hbergiO'Shea. 1999. G. H Luteutltisslrrislii O'Shea et Lu. 2002. I - Cirroctopui antorctica Kubodcra et Okutani. 1986. J. K Stauroteuthiss,r'rtarzsis Verrill. 1879: L. \1 Cirrothauna iturrati Chun. l9l I N. O. ('i'roteuthis nuellet.i Eschricht.l8j8 ,\. C. E. G. I u J BH-tcnepe_lutropii,iru".ibpo"u rraaeprr). L. N Bll.l c .lopca"lbHoiicropollbl (nepe:Hlr cropoHa auu;y). B. D. F. H. K. \4 and O - eHJ cSoxr''(nenc-rHq.q cropoHa c-leBa:JopcathHaq.cropoHaHaaeprl) [A-D^ L_.u \,1 - pHc\HKrlaBropa: E-H - u: Vecchione.young. 2 0 0 3 b :I u r K u b o d e r a .O k u t a n i .1 9 8 6 :j . i ( - - n : C o l l i n s .H e n r r q u e .2s 0 . 00: 1..M - n: Aldred et al.. 19831.'

V. A. Bizikov

72

of stl lets in Incirrata(averagevalues), Table 2. Principal morphologicalcharacteristics crH.teroB Incirrata (cpe,ruue 3Ha'{eHHq). Ta5;rnua 2. OcrjoeHrrevoptporrerpuvecKfiexapaKTepr'{crnxtl

St)'lets length (in % of ML) Distance between st1'lets (in % of N{L)

+-l

i,.1 *

52

..t