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-

l6

V. A. Bizikov

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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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T opisthoteuthrscaliJbrniana A 3peruii .t"::^11? yy 4Yl' BHr co cnHHHoi cropoHrr. B. il,r'ayrqar He3peraq
:le; its medial bridge is situatedclose to the aoex rrhile the lateral wings envelopethe mantle like a norse-shoe r.viththe lateralwings underlyingthe fins bases. In adult Opisthotettl.tisthe very thick gelatinous rntegumentdisguisesthe outline of the body and rrakes it appearflat. The anterior dorsal margin of the mantle.rvhich is tongue-shaped, almost reaches the bridge betw.eene1'es(Fig. 7A). The mantle is connecredwith the head b1 a pair of nuchal mus_ cles rilnning from its anteriordorsal mantle marsin t o r i a r dt h e a r m b a s e s . TOTAL C?O^SS-.SECTIONS.The secrion in sasrt_ tal plane (Fig. 8A.B) shows that adult OpisthotJut_ /ri.r is flattened against its r.ridell ,pr"ud arms. lts rnantleand visceraare reducedto a low hump above the arms and web. The muscularmantle is attached aroundthe whole gladius but does not oversrow it t F i g . 7 ) . T h e g l a d i u sd i v i d e st h e m a n t l ed o r i a l ( a o pearinganterior in the spreadposition) and ventral t appearingposterior in the spread position) parts. fhe long. tube-like funnel is turned 90o backward and fusesrvith the basesof arms IV along 2/3 of its length. The dorsalll.-positionedfins avJras.e77yo

ML in length,and abouttwo times the ML in their span.The headconsistsmainly of two large eyes. The brainis foreshortened andcompressed between thearmsbasesandthedigestivegland.Cephalicand ocularcartilagesareabsent.Theheadretractorslack musclesand are reducedto a film-like, collagen envelopeof the visceralsac;they attachingto tt.,. dorsaland ventralmarginsof the gladiuswings. The posteriormantlewall is very thick. It con_ sistsof outer and inner muscularlayersseparated by thick gelatinous, highly vacuolated tissue.The posteriormantlewall attachesto the gladiusalong the dorsalgroove of the saddleand ihe posterioi sidesof the wings. The anteriormantlewall. in contrast.is very thin. without distinctaxial vacuo_ latedtissue.It coversthe dorsalsideofthe visceral sacand attachesto the anteriorsideofthe eladius. mergingwith the posteriormantlebeyondlhetips of the horns.As a result,in the regionbetweenthe fin basesthe anteriorand posteriormantlesare separatedfrom one anotherby the gladius.The vis_ ceralsacis largeand occupiesmost of the visceral mass.The dorsalmantlecavity is a narrow slit be_ tween the anteriormantle wall and the dieestive

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FIG. 8. General anatom) of Opisthoteuthiscalilbrnicura.A. Latcral rres of a maturing male (,17 mm DNIL) afier rcmoral of the skin. arnts. mantle *all and the gill fiom thc leli side. B. Sections l. in median sagittal plane (ntaturingmalc: J9 ntm D\'lL). C. Scction f: transrcrsalsectiona1 the greatestllns tiidth (rmmalurc f'errale:-13 m n r I ) \ ' { L ) . T h e p o s i t i o no f t h e s e c t i o n sr s i n d i c a t e do n F i e u r e 7 . S c a l eb a r : I c n l . calilbrnrarn. A. Bn.r c5oxy (co:pcnaxrutniicarrcrt:.17 rrrr ,ll\4): c .retsoiieropurrbl PI,{C 8. ClpoeHue Oprsthoteutltis n.locKoerll p\KH. crcHKa\taHTHHu xadpa. B. Cpe: l:carurra-rsustficpe: g rre.fua-rsHoii KoxHbrc rror(poBbr. )Ja,leHbr (co3peBaHlilla.q carrxa: J9 rnr n\l). C. Cpe: 2: nonepevuuir cpe: Ha \ poBHe ItauSo.rrrueiiuIlpHHbt Il.taBIttilioB (co:penanutarcarrna:J3 vrr ,{\'1). flo.roxesue cpe3oBfioKa3attoHa Pnc. 7. Macrura6 : I crl.

Shell in Vampyropoda

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I iG 9 Relationship of the gladius rvith the soft bodf in opisthoteuthis calforniana. A. Fragment of' the median , sagittal preparation. illustiating attachnent of the mantle and runrief to trr"tl"oirr and the left t"ii..rii'orgun, lunnei retractorare cut:t.ar,l onll right pa1 ol the giadius ii-irr"*"1. e. rlagmeni oliiunrrl..r. -h;;n;-oT'iionru.rr. section at thc le'el of attachment of tunnel retractors to the l3tera_l oi trr. grdoiur. c. T.ug-.nt sectron at the Ie'el of the grearestfins ri.idth (section2: Fig. gc). scate uai:--l .rn. ?11C 9' B:anr'toornortleHuer'laJuvca u MtrrKolo reJa v opisthoteuthis calforniana. A.
,lland.The verrtralmantlecavity is reducedto a srnallspacebetweenthe visceralsacand the pos:eriormantlewall. The mediummantlesentumis r ery thin. The funnel retractorsare shoft and wide Fig. 8). They originatefrom rhe innerwall of the :unnel.passalongthe visceralsacandattachto the ateralhornsof the gladius(Fig. 9A). Tl-refrontalsection(Fig. 8C. 9C) illustrates the itructureof the fins and their relationship with the :ladius.Eachfin. in this section.consists of two :ruscularlayers(dorsaland ventral)separated by

axial cartilage.The fin carlilageis a flexiblesuppofiingstructure, thick and wide basally.gradually taperingdistally.The basalparrof rhe fin cafiilage is separated from the restof the caftilageas a more denseand stiff basalcarlilage,triangularin crosssection.Apex of basalcarlilageis insertedinto the fin cartilage,while its baseadherestightly to the shellsaccoveringflat outersurfaceof lateralwings of the gladius(Fig. 9.C).Basalpocketsareabsenr. Elevatoranddepressor musclesarethin andweakly developed. They originateon both sidesof the fin

V. A. Bizikov base and attach to the mantle above and belovv the gladius.The function of thesemusclesis apparentll to adjust position of the fins which otherr.viseis limited due to the absenceof basal pockets and tight fusion of fin basal cartilage to the shell sac. The mantle attachesto lateral u,ings of the gladius from their sidesi and the digestive gland adjoins it from the inner side. COMMENTS. Position of the gladius in Opisthoteezrlrls demonstrates its role as a supportingstructure. The solid attachmentof the fins to the shell is unique to the cirrates(with the possible exception of the paralarval fin of Vampvroteutftis)and is. apparently. neededfor their flapping. bird-like strokes that differ from the undulatorl' fin rrotion seen ln many decapodiformsand the more complex fin movement in VampyroteLtthis.

FIG. 10. Gladius of Grimooteuthisumbellata(immature female: ,16 mm DML). A, Anterior rieri (dorsal side donn): B. Lateral r,iew (anterior side right). Scale bar : I cm.

Grimpoteuthididae O'Shea,1999

PHC 10. f.,ra,ru)c Grimpoteuthis umbellata (ue:pe"ra.r carrxa: 46 rnr nM). A. Bu,r cnepeJn (.lopca"rurar cropoHa nuu:y): B. Bnl c6on (nepe,rH.sr croporra cnpana).Macrura6 - I crr.

Grimpoteuthisumbellala (Fisher, 1883) HABITS AND HABITAT. Most speciesof the genusGrimpoteuthis are poorly known. Thev inhabit bottorn and near-bottom \\'aters of bathl'al and ab1'ssalzones of ail oceans and rnostly occur at depthsbelou, 1000 m fNesis. 1982119811. G. umbellata is knou,n from the tropical to temporal Norlh Atlantic and the CaribbeanSea [Nesis. 1982119871. Direct underr.vaterobservationsshorv that although Grimpoteuthis.like Opisthotetthis.is closell, associatedwith the bottom. the forrner is a much better srvimmer than the latter [Villanueva er al.. 1997; V e c c h i o n eY . o u n g . 1 9 9 7 ; V e c c h i o n ee t a l . . 1 9 9 8 ) . Fin swimrning appearsto be the dominant mode of locomotionin Grintpoteurftis.rvhich is occasionallv assistedb,v medusoid contraction of the arm/rveb c o m p l e x[ V e c c h i o n eY . oung. 1997]. GLADIUS MORPHOLOGY. The gladius of Grimpoteuthis is thick. stout and deeply U-shaped(Fi_e. 10). Its rvidth is slightll less than its length. The saddleis thick. shoft. someu'hatcompressedlaterally'. Dorsal (outer) side of the saddle is nearlr flat; dorsal groove absent.Lateral vningslong. laterally' cornpressed. tenninate in tu'o lobes r.vithsmall indistinct horns on ventral side. Outer flattenedsides of tlie wings are nearly parallel to one another. MICROSTR(.CTLIRE OF THE GLADILTS in Grirnpoteuthrsis essentialll'the same as in Opistlnteuthis. EXTERNAL MORPHOLOGY.Soft bodr of Grunpotetthis ttmbellata (Fig. 1l) has the same gelatinous consistenc,vas in Opisthoteuthis but its fonn more closeh' resernblesthe typical cephalopodBa-

uplan. The mantle is bell-shaped, wide and confluent rvith the head. Its length averages 36ok of the

total length.The mantlecavity openingis reduced to a narrow slit aroundthe ventral surfaceof the funnel.Thefunnelprojectsanteriorlyfrom themantle. The fins arelarge,oar-shaped. with smalllobes at theiranteriorbases.They aresetobliquely(slightlf inclinedanteriorly)on the lateralsidesof the mantlein its anteriorhalf.The fin lengthisll-15ok ML and the fin width is about45ohML. The fin spanis 1.8-2.0timesgreaterthanthemantlelength. Thelongarms(ca.two timestheML) areimbedded in the web exceptfor short distal ends.The u'eb betrveenthe arms in Grimpoteuthisis thinnerthan in adult Opisthoteuthis. enablinga more fusiforn-r shapeduring fin swimming [Villanuevaet al.. 19971. Thegladius occupies subterminalposition on the dorsalside of the mantle.its saddleis visible throughtranslucent skin betweenand posteriorto thefins(Fig. l1B), whilethewingsprojectanteroventally'alonglateralsidesof the mantle. TOTAL CXO,S.S-S.ECTI ONS (Fi gs. I 2. 13). Mantle v,allof Grimpoteuthis is thicker.moremuscularand lessgelatinous thanin Opisthoteuthis. The relative11'thick. muscularanteriormargin of the mantle gradually'becomesthinnerposteriorly.The thicknessof the mantlewall is approximately uniform aroundits circumference. The muscularmantleis attachedaroundthe lvhole gladiusbut does not cvergrowit (Fig. 13A-C).Contraryto the descriptionsby Vecchione andYoung119911. theposterior endof the gladiusin Grimpoteuthis doesnot coincidewith the posteriorendof the mantle.but occu-

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FIG. ll. Grintpotettthisuntbellata(immature female: .19 mm DML). A. Ventral vieu. B. Dorsal vierv. Arro1r's',r'ith numbersindicatethe position of correspondingcross-sections shown in Fig. l2 and 13. Scale bar: I cm. FIG. ll. Grintpoterihisumbe.llata (ne:pe"rarcarrxa:;19rnr,{M). A. Bn.r c neHrpansnofi cropoHbr.B. Bul c,ropca-rrHoii c'l'opoHbl. Crpe.lxu c uuQpaMH\(a3brBatorrro.roxeHHecoorBercrBYrouHxcpe3oB.rroKa3aHHbrx na Puc.'12 u 13. = Macurad | cv.

pies a subterminalposition as in all octopods.The posteriorextensionof the thinning mantlesurrounds a gelatinous core (Fig. l3D). The dorsal manrle cavitv extendsfrom the nuchal region to the level of anterior margins of the gladius wings. At the level of the funnel, the dorsal mantle cavity encirclesthe visceralsacfor about2l3 of its circumference (Fig. 12A). The ventralmantlecaviw extendsposteriorly to the levelof saddleof the gladius(Fig. 14C). The visceral sac is spaciousand dominatedanteriorly by the large digestive gland (Fig. 12). At the level of stellateganglia, the visceral sac is broadly fused with the lateralmantle rvalls (Fig. 13C). In the middle of the mantle cavity'. thick mantle septlrm containing the mantle adductor muscle is present(Fig, 13A). Posteriorll,the sac is fused n'ith the mantle and the shell sac (Fig. l3B). Betrveen funnel and stellateganglia. the visceral sac is susp e n d e di n t h e m a n t l e c a v i r y ( F i g . 1 2 B ) , Structure of funnel is shown on the section 1 (Fig. 12A). Lateral rvalls of the funnel are rhick and relativelv muscular.Their inner parts aftachto the visceralsac while the outer parts continue into thin collar folds and attach to the lateral rvalls of the rnantle. At the sites of attachment of the funnel to

the visceralsac.the funnel also fuseswith the mantle forming the collar fusion. The ventral wall of the funnel is thin and less muscular. It joins with the lateral walls along the sides of the funnel. The cross-sectionshows the presenceof a distinct junction formed by muscular fibers of different orientation between the ventral and lateral walls of the funnel. The dorsal wall of the funnel is lined .,vith the thin muscularextensionof ventral median mantle adductor. The shor1.ribbon-like funnel retractors extend a l o n gv e n t r a l s i d eo f t h e v i s c e r a l s a c( F i g . 1 2 8 ) a n d attach to lateral mantle walls at the level of stellate ganglia (Fig. 12C). Head retractorsform the thin. muscularenvelopeof the visceral sac (Fig. 12A-C) and attach medially to the dorsal, ventral and anter i o r m a r g i n so f t h e g l a d i u sw i n g s ( F i g . 1 3 A ) . The structureof fins is similar with that of Opisthotettthis(Fi-q.1a). The basalfin carlilageis thick. but. unlike the carrilage in Opisthoteuthis. it is not clearly differentiatedfrom the axial cartilage.The axial cartilageis thinner than in Opisthoteuthlr.Widened base of the fin carlilage tightly adheresto the shell sac along outer flat sidesof gladius r,rings (Fig. 13B). Epithelial basal pockets are absent.

22

V. A. Bizikov

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tlG. 12. Scherraticcross-sections of Grtntpoteuthisuntbellcttdsofi bodl limmature female: ,19 mm ML) A. Secrion l . a t t h e l e r e l o f t h e f u n n c l .B . S e c t i o n2 . i m m e d i a t e l rh e h i n dt h e f u n n e l .C . S e c t i o n3 . a t t h e l e r e l s t e l l a rs a n s l i a . t h c p o s i t i o no f t h c : e c t r o n si s i n d i e a r e Ji n F i g . I I S e r l e h a r I cm PVC. 12. Cpe:u rtrrxoro rcta Grintpoteuthrs unbellato (He3pe.rar carrxa:'19 rnr .[\1). A. Cpe: l. Ha rponne BopoHKH. B. Cpe: 2. no:a:u BopoHKH. C. Cpe: 3. sa rpoBHc 3Be3-tr{arbr\ raHr"rHeB. flo.roxerruecpe3oBfroKa3aHo rra Prrc. ll. \lacLura6 I ert.

Shell in Vampyropoda

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FIG. l-1. Grintpoteuthisunthellata.sectionthrou-shthe long aris of fin at the level of its greatestlidth. Scale bar I cm. Pl'IC. 14. Grintpoteuthis untbelldta. cpe3 BJo.rb npo-to.rbHoiiocH n.raBHHKaHa vpoBHe ero Hal.r6o"uurefiuupunr,r. Macurra6 - 1 crr. -r 'rl nr

Musclesmonitoring position of the fins on the mantle are weakl)' developed.E,levatorand depressor musclesconsistof dispersedmuscularbundlesoriginating on the fin base and attaching to the mantle aboveand belou,the fins (Fig. 14). Anterior retractors spread alor-rgthe mantle from the fin basesto the level of the posterior end of the funnel (Fig. 12B.C). The muscular la1'ersin the fins of Grimpotetnhis are rnorphologically differentiated into proximal and distal pafts with different orientations of the mr.rsclefibers (Fig. la). In the proximal parr. the dorsal and ventral muscular la1'ersare composed predominantlv of longitudinal fibers (parallel to the long axis of the fin) and to a lesserextend b;" oblique fibers. In the distal part of the fin. muscular la1ers consistmainlr, of transversefibers oriented perpendicular to the fin surface. COMMENTS. The gladius rn Grintpoteuthis is thicker and bulkier than in Opisthoteuthis;its dorsal surfaceofthe saddleis nearll flat: the lateralrr ings are relatively longer and lateralh con.rpressed: the lateralhorns shorl and indistinct.The differencesin gladius rnorphology reflect the differencesin locomotion betu'eenthe t*o species.The fins \n Grintpotetrthisare much larger than rn Opistltoteuthis. The fin bases in Grimpotetttltisare closer to one anotherthan in Opisthoteuthis.and this is reflected in the shorlersaddleof the fbrmer. The surfacesof the fin bases are greater in Grimpoteurlris. u hich corresponds to the largerouter surt-aces of the lateral rvings.The larger fins. presurnabll. are responsible

for the thicker and stoutergladius.The weak development of the lateralhorns in the gladius of Grimpotettthis correlatesu,ith the weak funnel retractors, which do not attachto the gladius but to the mantle n'all. Unlike the saddle groove of Opisthoteuthis. the gladius of Grimpoteuthis has no special adaptations fbr the attachmentof the mantle muscles.

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CirroteuthidaeKeferstein,1866 Cirroteuthismuelleri Eschricht, 1836

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HABITSAND HABITAT.Cirroteuthis muelleriis in a benthopelagic cirrateoctopodusuallyfor-rnd associationrvith the ocean floor at great depth in the North Atlantic. Arctic Ocean fNesis, 19821198'71. North Pacific [Guerra et al.. 19981 and off New Zealand [O'Shea. 1999]. In the Norlh Atlantic it occurs at depth between 700 and 4854 rn with the peak abundanceat 3000-3500 m [Collins et rzl.. 2001]. Speciesof Cirrotetrt|tisare the largestrepresentativesof Cirrata reachingup to 1.5 m in length [Nesis. 198211981].They are often found in deep uater su'irnming or drifting near the ocean floor [ V e c c h i o n eY . oung.2003a]. GLADIUS MORPHOLOGY. The gladius is a massive. translucentstructurevvitha short.thick rnedial saddleand broad lateralrvings(Fig. 15). The saddle has a uide 'u'entralbaseand a narro\!. dorsal longitudinal ridge. The w'ings are expandedboth anteri-

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IrlG 15. dlaclirs of Clirroteuthisrttttelleri(maturing female: 128 mm \,lL) A. Dorsal ,nie.,i(anteriorside is up) B Lateral rien (antcrior side is on the left: dorsal-siders Lrp) C. Posteriorvieu (dorsal side is up). Scale bai = I cln. Pt4(l l5 i-"ra:nrc C'irroteuthismuelleri (co:perarouarcarrr.ra: 128 rnr !N{). A. Bu,r c lopca.rruoii cropoHbr(nepe.tHhH KoHeucBepx\').B. Bur cix) lnepe:Hnii xoueu c.reBa:JopcarbHarcropoHacrep*1). c. Bu;r c3aJH(jtopca-rbHa, cropoHacBepx\').\4acura5 - I crr.

orlr,'and posteriorlv.They are situatedvery closeto one anotherand their ventrolateralmargins are alrnost parallel. The anterior and posterior edges of the rvings are bluntly rounded. and the wings are almost elliptical in lateral vieu. Lateral surfaceof eachwing is slightly concavesloping downrvardsat a n a n g l eo f a p p r o x i m a t e l l . 6 0 o , MICROSTRUCT(IRE OF THE GLADILTS. Cross-section tl-roughthe centralparl of the gladius is V-shaped.resemblingthe cross-sections of sorne I e u t h i dg l a d i i [ B i z i k o r , . 1 9 9 6 :F i g . t 8 C ] . C e n t e ro f grorvth is situatedin the rriddle of the saddle.The growth incrementsare u'ide. united into secondordercvcles.Microstructureof the gladiusis sirnilar to that of Opisthoteuthts. EXTERNAL MORPHOLOGY. The body' is gelarinous.very fragile. with short sac-shaped mantle and long arms (about twice the mantle length) embedded into a deep rveb except for the shorl distal ends t F i g . 1 6 ) .T h e h e a di s a p p r o x i m a t e l yr h e s a m e* , i d t h as the mantle. with small inconspicuouse1,,es. The rriantlelength cornprisesabout 1/3 TL. Mantle aperture is reducedto narro\\' semicircularslit around the funnel. The fins are large. oar-shapedand set \ er)' close to one anotheron the dorsal side in the rniddleparr of the mantle. Fin length is approxrrnateN' equal to the mantle len-eth.and the fin span is 1 . 9 - 2 . 0t i m e s t h e m a n t l e l e n g t h .T h e a n t e r i o rb l a d e of each fln has a srnall lobe at the base.Lonq axes , , f f i n s a r e n o t p a r a l l e lr o e a c ho t h e r b u t t i l t e J a n t e riorly forming an angle about 135o betu,eenthem. -l he funnel projectsanteriorlr.'frorn the mantle. It is long. tube-like and fused with the headon its dorsal

side.The gladiusoccupiesa subterminalpositionon the dorsal side of the mantle. The mantle bulges posterior to the gladius forming a dome-shaped apex. The axial part of the saddle and the dorsal margins of the wings can be seenthrough the gelatinous flesh on the dorsal side (Fig. 168). TOTAL CRO.SS-.SECTIONS. The most striking f'eature about Cirroteuthis anatomy is the lateral fusion of its visceralsacwith the mantle walls resulting in considerabledecreasein size of the mantle cavitl ( F i g s . l 7 B . C : l 8 A ) . T h i s f u s i o n s t a f i sa t t h e l e v e l near the collar folds (Fig. 178) and proceedsto the level of the gladius (Fig. 18A). The manrle in C'ir.rotetlhis is rather thick anteriorll, and gradually.becomes thinner posteriorly.Part of the head extends into the bodl'. so that its nuchal parl, including statocysts.is coveredby dorsalmantle wall (Fig. l7A). The mantleattachesto the gladiusalong the margins of the r.r'ings.The fin basesattach to the outer sides of the u'ings. On the dorsal side of the mantle. anteriorand posteriorparts of the mantle are fused o v e r t h e d o r s a lr i d g e o f t h e g l a d i u s( F i g . 1 8 C ) .T h e thicknessof mantleu'all is approximatelyequalaround its circumferenceexceptposteriorto the gladiLrs u'here the dorsal mantle rvall is about two tinres thicker than the ventral rvall (Fig. 18D). SLrbcutaneousgelatinollsla),er is about the same thickness as in Grimpoteutltis. The funnel consistsof a single muscular laver. Junctionsof muscular lavers between ventral and lateral ualls are absent. The anterior oart of the funnel is sr-rppofted by paired funnel adductormuscles that passfrom head retractorstou'ard dorso-la-

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V. A. Bizikov

FlG. 16. Citoteuthis ntuellert(immaturefemale:65 mm DIVIL).A Ventral vieu. B. Dorsal vier.".Arro*s rrith numbers (shonn in Figures l7 and l8). Scale bar: 1 cm. indicatethe planes of correspondingcross-sections PHC. 16. Cirroteuthisntuelleri (He:pe-:rar cropoHbr.B. Bu,t c.lopcarbHoii canxa: 65 rnr !M). A. Bur c neHrpa-rsnoii ua Pnc. l7 u 18. cropoHbr.Crpe"rxu c uuQpalrr.rvKa3brBarorrro"roxeHHecoorBercrB)roruHxcpe3oB.rroKa3aHHLIX Macurra6 - 1 cn.

teralrvallsof the funnel(Fig. 17A).Funnelorifice is extremely narrow and somewhat unusual in cross-section. In its anteriorpart a pair of coiled flaps (funnel organ?) protrudesinside the canal from the lateralwalls (Fig. 17A). ln the posterior pan of funnelthe flaps disappear. and funnelcanal (Fig. 178). becomestriangularin cross-section Collarfoldsarereducedto thin mLlscular stripsoriginatingfrom the ventrolateralsidesof the funnel andattaching to the lateralwallsof themantle(Fig. l7B). Attachmentsitesof collarfoldsto the funnel aremarkedby junctionsformedby muscularfibers with differing orientations.The funnel retractors are shoftand wide. They originatefrom posterior ventralcornersofthe funnel.follow theventralside of the visceralsacand attachto lateralwalls of the mantleat the level of stellateganglia(Fig. 18A). At site of attachmentthe mantlewalls are thickened. ln their middle parl the funnel retractorsare muscularflapshangingfrom the ventralwall of the visceralsacinto the mantlecavitl,(Fig. 17C).The

head retractors are thin. weak muscles. They form an envelopearound visceral sac (Fig. 178.C) and attach from inside to dorsal. ventral and anterior m a r g i n so f g l a d i u sw i n g s ( F i g . 1 8 B ) . Mantle cavity' is verl' small. The dorsal mantle cavity is a narrow slit in nuchal region (Fig. 17B.C). The short.thick saddlehas shifted visceral organs ventro-anteriorly.Posterior part of ventral mantle cavity has a shapeof narrow dorso-laterally squeezedtube. In contrastro Grimpoteuthis, venlral mantle cavity extends posteriorly beyond the glad i u s( F i g . 1 8 D ) . At the level of greatestfin width the V-shaped gladius is extremely thick and provides a rigid supporl for the fins (Fig. 18C). The fins in Cirroteuthis are larger than in Grimpoteuthis and Opisthoteuthis. A thick axial fin cartilage forms the core of each fin. The basal part of the fin carlilage is greatly expanded into wide flat basethat adherestightl) to the shell sac along the flat outer sidesof the wings (Fig. 18C). Elevatormusclesoriginateon the dorsal

Shell in Vampyropoda

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28

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trdl of Cirroteuthismuelleri sofi bodl (same specimenas in Fig. 17) A. Section'1. FIG. 18. Schematiccross-sections at the lercl of anterior margrn of the fins llerel of stellar ganglia) B. Section 5. at the level of anterior sinqs of the gladius. C. Section 6. at the lerel of the greatestllns sidth. (The slit beflreen tlns basesand gladruson this seciion is an anifact of sectionrng).D. Section7. behind the gladius.The position of the sectionsis indicated o n F i g . 1 6 . S c a l eb a r - I c m . PI4C 18. Cperrr rrllxoro re.ra Cirrotetthis muelleri (rn3elrn.rspror xe. qro Ha Puc. l7). A. Cpe: -i. ua rpoaHc () poBeHb3Be3.tqarbr\r'aHr-rHeB). B. Cpe: 5. Ha r poBllr- nepe-tHH\KpaeBKpbl.tl,eB nepeJHefoKpar n.taBHHKoB (Llle:tl rtex:1 ocHoBaHfirI\1H n.taBHt'lKoB u uHpHHbrn.raBHHKoB. r.,la{Hvca.C. Cpe: 6. Ha l ponHe HauSo.rsureil nprr petxe). D. Cpe:7. no:a:u r.ralulca. flo.roxeHnecpe3oB)Ka3attotla Prtc. r-na.1n1 corr apieSart. so.tHuriulrlii 16. \lacr,ura6: I crr.

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Shell in Varnpyropoda surface of fins in their basal part and attach to the gladius wings in the region of medial dorsal r i d g e . D e p r e s s o rm u s c l e so r i g i n a t e o n t h e v e n t r a l surface of the fins in their basal part and attach t o t h e g l a d i u sw i n g s b e l o w t h e f i n s . T h e m u s c u l a r lavers in the fins of Citoteuthis are more complex than in Grimpoteuthis and Opisthoteuthis.ln the proximal part of the fins. both dorsal and ventlal muscular layers consistof two layers each: a n i n n e r l a 1 , e ro f l o n g i t u d i n a l m u s c l e s ,a d h e r i n g t o t h e a x i a l c a r t i l a g e .a n d a n o u t e r l a y e r o f o b l i q u e m u s c l e sc o v e r i n g d o r s a l a n d v e n t r a l s i d e s o f fin (Fig. 18C). In the distal part of the fin, the r n u s c l e sc o n s i s tm a i n l y o f t r a n s v e r s ef i b e r s . a s i n Grimpoteuthis. COMMENTS. Prominent expansion of lateral rvings in both anterior and posterior directions is one of two unique elementsof the gladius in Cirroteuthis. The narrowing and increased depth of the saddleis the other. Both elementsreflect an irnportant change in the attachment of the fins to the g l a d i u s .I n C i r r o t e u t l r i s ,t h e f i n s a r e s e t t r a n s v e r s a l l v o n t h e w i n g s a n d t h e i r b a s e sa r e b r o u g h t c l o s e t o g e t h e r w h i l e i n t h e o t h e r c i r r a t e ss t u d i e d (.Opisthoteuthis and Grimpoteutlzis) the fins attach along the length of the wings and their b a s e sa r e s e t w i d e a p a r t ( c o m p a r e F i g s . 1 6 . I I and 7). On one hand, the change in fin-attachm e n t c h a n g e dt h e a n g l e o f t h e f i n s w i t h r e s p e c t to the body axis: in Opisthoteuthis the fins b a s e sa t t a c h t o t h e w i n g s a t s o m e a n g l e t o t h e body axis (Figs. 7. 8A), while in Cirroteuthis thev attach along the body axis (Fig. 16). On the other hand. the gladius in Cirroteutftis also c h a n g e di t s o r i e n t a t i o n : t h e a x i s f r o m t h e s a d d l e t o a n t e r o v e n t r a lt i p s o f t h e w i n g s m a k e s a s t e e _ p e r a n g l e r . v i t ht h e b o d y a x i s t h a n i n o t h e r c i r r a t e s s t u d i e d .T h e d e p t h o f t h e s a d d l ea p p e a r st o be tied to the depth of the broad wings. Narror v i n g o f t h e s a d d l e a n d i t s i n c r e a s e dd e n t h t r a n s f o r m e dt h e m i d d l e p a r t o f t h e g l a d i u s i n t o s t o u t s u p p o r t i n gb e a m . V - s h a p e di n c r o s s - s e c t i o nw, i t h t h e f i n a t t a c h e dt o i t s s i d e s ( F i g . l 8 C ) . Although the fins bases are fused with the s h e l l s a c . t h e i r p o s i t i o n o n t h e w i n g s a p p e a r st o be adjustable,perhaps through some elasticity in t h e s h e l l s a c .T h e p o s s i b i l i t yo f a d j u s t m e n ti s s u g gested by the vertical din-rensionof lateral wings, rvhich is greater than the thickness of the fins bases attached to then-r.The flat, cartilaginous bases of the fins would conform well to outer surfacesof the wings over this range. In addition the elevator/depressormuscles are larger than in opisthoteuthids.The differentiation of the muscular layers in the fins indicates they are capable of more complex movements. perhaps an increased ability for anterior/posteriorundulation. The gladius in Cirroteutllis has no special adaptations

29

for theattachment of mantleor retractor muscles. The weakfunnelretractors attachto the mantle walls,confirming theabsence ofjet-swimming. Indeed,thefunnelreminds onemoreof a nostrilthan a jetnozzle. SuborderIncirrata Grimpe, 1916 OctopodidaeOrbigny, 1845 OctopodinaeOrbigny, 1845 Enteroctopusdofleini (Wulker, l9l0) GENERALREMARK.The shellin the Incirrara consistsof a pair of narrowspindle-shaped carlilage-likerodsembedded in the muscletissueon dorsolateralsideof the mantle.Althoughthis unusual shell is terrned sometimes 'gladius' [Nesis, 19821198'71, it differs from the typical teuthoidgladius in many aspectsand deserves a specialterm: stylets[Robson,1932;Voight, 1997]. HABITS AND HABITAT. GenusEnteroctopusas well asothercloselyrelatedgeneraof Octopodinae includesfamiliar benthicmuscularoctopusesinhabiting a wide rangeof depthsfrom inrertidalpools to lower continental slopesdown to 800 m fNesis, 1982/19871. They inhabit all oceansof the world from equatorto high latitudesand occuron a wide rangeof habitatsfrom coral and rocky reefs,seagrass and algal beds,to sand and mud substrates fNormanet al., 1998].Speciesof the genusEnleroctopus primarily move via two methods: fl) crawling over the substrateusing the arms,and 2) jet propulsionusing the mantle-funnelcomplex [Normanet al., 19981.E. dofleiniis the largestrepresentative of Octopodinae, reachingup to 5 m in total length(60 cm ML) andup to 150kg in weight[Norman et al., 19981.E. do/leiniis found in the North Pacific,from the Bering Seain the norlh to the OkhotskSe4the Seaof Japanandthe yellow Seain the southwestand to Califomiain the southeast fNesis, 1982119871. Themaximumdepthof its occurrence is about400m [Filippovaet a\.,19971. SHELL MORPHOLOGY. The styletsin Enteroctopus aretwo thin translucentrods with pointed endslying on dorsolateral side of the mantleat a sharpangleto longitudinal axis(Figs.19,A;20A). Distancebetweenstyletsat the level of their anterior endsis about 50% ML. The styletsconsist of a cartilage-likechitinoussubstance that is laid down in concentriclayers.The length of stylets in adult octopusesrangesfrom 20.4Yoto 3I.B% ML (meanlengthis 24.3o/o; SD=3.4).Eachstylet is surrounded by a shellsacwith denseconnective tissueon the outer side of the sacand shell eoitheliurnon the inner side.Each stylet has a bend

30

V. A. Bizikov

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FIG. 19. St1lets of Etteroctopus dofleini. A. Ventral vicu of a pair of snlets from adult f-emale(21 cm N{L): rrght snlet is on the left: anterior end is up. The stvletsare shonn opaqueto rereal their surlace. B. Lateral r ieu of the right st1let from the same specimen(r'entralside il on the ri_sht).The str let is sho*n naturally transparentto rereal its gro\\th lncrementsand the rnitialshell(shi).Bold arro* s indicate 'C'. t h e p l a n eo 1 ' t h ec r o s s - s e c t i osnh o n n i n C. Crosssectionthrou_qhthe angle of the sqlet (rentral side i s u p : o u t e r s i d e i s o n t h e l e l t ) . . \ . B : s c a l eb a r - I c m . C : s c a l eb a r - I m m . PHC. 19. CrH.rersr Erteroc'topusdqfleint.A. llapa crurelon :pc.roiicarrxu (21 crr INI): nu.f c neHrpa-rsHoii croponLr (rrpaeuii crHrer c.reBa:nepe.tH.cq cropolra uanepry). Cru.rersr u:oSpaxeHu Henp03palrHhr\1.r. qro6sr uoxa:aru pe.rsetlru\ ttoBep\HocrH. B. Bu: cSoxv npaeoro crH-lera roii xe ocodu (acurpa-rrHa.r cropoHa cnpana). Cru.rer n:odpaxeH ecrecrBeHHo qroSsrnoralarb efo -rr'lHHu npo3paqHbr\r. uapacraHnt \Ka3brBar.or u 3apoJLIueB\rcpaKoBHH\(shi). Crpe.rxn 'C'. no"rroxeHue cpe:a. u:oSpaxeHHoroHa C. flonepevru,rficpe3 Ha vpoBHe\ r.ra crH.tera(BeHrpatbHat cropoHaHaBep\):BHeurH.sr cropoHac.resa).A.B: rracttrra6 = I crr. C: rraculaS : I rrrr.

in itsanteriorpartthatformsanobtuseangle( I 30'its 145")(Fig. 19B).At thebendthestyletreaches greatestthickness thatrangesfrom 5.1o/o to 8.4Yoof SD:0.86).Theapexof bend styletlength(ca.6.6%o; is dome-shaped and its surfaceis coveredwith numerousminuteknobstestifyingthe muscleattachment in this region.Indeed,during extractionof st)'lets.it is the bendthat is the most difficult to The benddividesthe separate from the softtissues. styletinto anteriorand posteriorparts(shoulders). The anteriorshoulderis short. about one half the lengthof posteriorshoulder.andnearlystraight.The posterior shoulder is longandslightlycurveddistally. Thedistalpartof theposterior shoulderis oftencurved in a zigzagpattem.recallingthe bladeof a Malaysian 'Kris'dagger. Althoughthe generalshapeof the styletsin E dofleiniis ratherconservative, their length.thicknessandrelativelengthofthe shoulders showconsiderableontogeneticand individual variability. Thegrorvthof styletsis negativelyallometric.Their relativelengthdecreases from28-32ohML at 13-17 cm ML to 20-260/o ML at 24-21cm ML. Proportionsof shoulders andthicknessof styletsapparently do not changewith age.The lengthof the anterior shoulderranges from 28o/oto 43o/oof the stylet length. averaging35.2% (SD:3.4). Sty'let thicknessvariesfrom 5.loh ro 8.4Voof the st1'let length.averaging6.6% (SD=0.85).There is also variabilitybetweenleft and right styconsiderable lets of the samespecimen.The lengthof stylets mal, differ up to 9% (average4.3%: SD:4.1): the lengthof the shoulders may differ up to 1lo/o(average4.8%: SD=1.5).and the thickness of stylets rnal' differ up to 33o/o(average11.5%;SD=9.6). Hou'ever.thereis no consistent differencebetween left andright st,""let: the averagesizeof the left and right st1'lets is the same. MICROSTRLTCTIIRE OF THE STYLETS. The grorvthof stvlet occursin layersthat are laid dow'non the outersurfaceof the previouslayer. As a result.the shapeof styletat earlierstages rnaybe reconstrllcted from its grolvthincrements visibleon intactstyletin transmittedlight. The apicesof previouslyformedlayersform tu'o thin apicallines divergingfrom the bend along the (Fig. 19B).In somestylets axesof bothshoulders lines u'hitishandopaoneor bothapical becomes que.apparentlldueto someinjury in the past.fhe thecenterofgrou'thand stl let bendthusrepresents contains theearliestincrements. includingthe embrl onicshell. A cross-section throughthe angleapexis roughl1 oval in shape(Fig. 19C).It is composed of numerous regular concentric increments.Tlie uidths of incrementsare 7-12 prm.averaging9.2 prn. Eachincrementconsistsof a glass-liketranslucentzoneconfinedb., a distinctrefractineborder.

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I'l-reu'idth of each increment is approximatelv equalalong its perimeter.The centerof gro*th (init i a l s h e l l )i s s i t u a t e dc l o s et o t h e m i d d l eo f t h e c r o s s jcction. It is an amorphous.opaque.oval bod1,170190 prm in length. about 100 pun in u'idth. The rr idth of the growth incrementsdoes not vary signit'icantlv from the center toward periphery'.The growth zones. sirnilar to those describedin statol i t h s .a r e a b s e n t[ C l a r k e .1 9 7 8 ;A r k h i p k i n . B i z i k o v . 1991].Prirnar,uincrementsare clearl;-grouped into second-ordercycles. marked by prominent borders apparentlvreflecting some events in the animal's lif-e. fhe number of first-order incrementsin one second-orderc1'clevaried from 7- I 5 nearthe center to 25-33 in periphery.The minute knobs are located on the ventral (inner) side of the bend. rvhile the tiorsal (outer) side is smooth. The knobs can be traced on previously formed lavers: their marks tbrm twisted lines radiatins from the center of growth. EXTERNAL MORPHOLOGY. As E. dofleini is the first incirrateoctopod to deal rritlr in this study. this speciesu'ill be used as an exarnplein description of the general morphological Bauplan of the I ncirrata. 'fhe m a n t l e i n E d o f l e i n i i s m u s c u l a r .u , i d e . sac-shapedand broadll' fused rvith the head on t h e d o r s a l s i d e ( F i g . 2 0 A ) . A n t e r o d o r s a lm a r g i n of the mantle can be seen after removal of the skin from dorsalside.The margin is nearll,strai g h t a n d r e a c h e st h e p o s t e r i o r e d g e o f t h e e y ' e s . A r v i d e n u c h a l m u s c l e f a s t e n st h e d o r s a l m a n t l e w a l l t o t h e h e a d . T h i s r n u s c l ee x t e n d sf r o m t h e d o r s a lm a n t l e m a r g i n t o t h e b a s e so f a r m s I . M a n t l e i s t h e r n o s t t h i c k i n i t s a n t e r i o rp a r t . V e n t r a l r n a n t l ei s t h i c k e s ti n t h e r e g i o n o f g i l l s : t h e d o r s a l r n a n t l er v a l l i s t h i c k e s t i n t h e r e g i o n o f t h e d o r s a l r n a n t l ec a v i t y ( F i g . 2 1 A ) . P o s r e r i o r l vt h e m a n t l e b e c o r n e st h i n n e r a n d r e a c h e si t s r n i n i m u m t h i c k ness at the posteriorapex. The mantle aperture i s u ' i d e . e x t e n d i n g l a t e r a l l y ,t o t h e l e v e l o f e - v - e s . T h e m a n t l e c a v i t y 'i s r e l a t i v e l y s p a c i o u s ;t h e v e n tral part of the mantle cavitr is distinctlv larger t h a n t h e d o r s a lo n e . T h e f i n s a r e a b s e n t .T h e s t 1l e t s 1 i e o n t h e d o r s o l a t e r a sl i d e s o f t h e m a n t l e i n i t s p o s t e r i o rh a l f . T h e a n t e r i o r s h o u l d e r o f e a c h s t v l e t l i e s s u p e r f i c i a l l yo n t h e e x t e r i o r s u r f a c eo f t h e m a n t l e m u s c l e .r v h i l e i t s p o s t e r i o rs h o u l d e ri s e r n b e d d e di n t h e m a n t l e m u s c l e . The funnel is fused rvith the head and parth cmbeddedin it (Fig, 20C). The rniddle par-tof the funnel is fastenedto the head by a pair of lateral adductor muscles.The posterolateralr.vallsof the firnnel pass into muscular collar folds. The collar fblds surroundvisceral sac like a rvide bell-rnouth .jarand aftachto the dorsal mantle riall. The funnel arisesdeep lvithin the mantle cavity. and its posteloventral margin rests against the ventral mantle

3l

adductor(Fig. 21A). A funnel locking-apparatusis absent.but the posteriorcornersof the funnel bear small cup-like depressionscausedby contractionof funnel w'all over the head of the funnel retractors. The funnel retractorsare thick and stout. They'originate as r.videposterior extensionsof the dorsal wall of the funnel (Fig. 20C). run alongsidevisceral sac and adhere to the ventral sides of the sty,'lets (Fig. 21A). Muscle fibers of axial part of funnel retractors attach to the stylet in the region of its angle. while peripheralfibers diverge in a fan-like fashion and attach along the anterior and posterior s h o u l d e r so f t h e s t y l e t s( F i g . 2 1 B ) . Attachment of the visceral sac in the Incirrata i s u n i q u ea m o n gc e p h a l o p o d(sF i g . 2 0 B ; 2 1 A ) . T h e visceral sac. at its anterior end. is fused with the head and. at its posteriorend. it adheresto the mantle. In the middle part the visceral sac is suspended inside rnantlecavity by five adductormuscles:paired anterodorsalmantle adductors.paired posterodorsal mantle adductors (=funnel retractors) and an unpairedventral median mantle adductor(:mantle septum).Anterodorsalrnantleadductorsare formed b1' the outer layer of the head retractors that branches off at the level of stellate ganglia. Each adductor undergoesan 180o twist so that the anterior-most margin at the visceralsac becomesthe posterior-mostmargin at the attachmentto the mantle w a l l ( F i g . 2 0 B . C ) . T h e s t e l l a t eg a n g l i a a r e s i t u a ted on the inner surface of the mantle just lateral to the attachment of the anterodorsal adductors. A m o n g n u m e r o u sn e r v e sp a s s i n gt o a n d f r o m t h e s t e l l a t eg a n g l i a . t w o a r e r e l e v a n tt o t h i s s t u d 1 , :a p a l l i a l n e r v e p a s s i n gf r o m t h e b r a i n t o e a c h s t e l late ganglion through the anterodorsaladductors. and a "fin" nerve passing from each stellate gang l i o n p o s t e r i o r l ya l o n g t h e i n n e r m a n t l e w a l l t o t h e s t y l e t s ( F i g . 2 0 C ) a n d b e y o n d . A r r h e s t yl e t . t h e " f i n " n e r v e p e n e t r a t e st h e m a n t l e w a l l n e a r t h e p l a c e o f a t t a c h m e n to f f u n n e l r e t r a c t o r( F i g . 2 l B ) . P e r s i s t e n c eo f t h e ' ' f i n " n e r v e s i n i n c i r r a t e o c t o p o d si s q u i t e r e m a r k a b l e .a s t h e y r e t a i n t h e i r original position in relationthe shell. thus indicating the position of former fins. The posterodorsal adductorsare formed by the funnel retract o r s . T h e v e n t r a l m e d i a n - m a n t l ea d d u c t o r i s a t h i c k . r v i d e m u s c u l a rs e p t u m e x t e n d i n gf r o m t h e v e n t r a l m a n t l e r v a l l t o t h e v i s c e r a ls a c ( F i g . 2 1 A ) . I t i s u ' i d e a t t h e m a n t l e r . v a l la n d b e c o m e sp r o g ressivell narrower toward the visceral sac. The median mantle adductor divides ventral mantle cavity into left and right parts. Posterior to the a d d u c t o r .t h e m a n t l e c a v i t y ' i s u n d i v i d e d . CRO.SS-.SECTIONS.A section at the level of the funnel shou'sthat the visceral sac is enclosedby a thick muscularcover formed by the head retractors. The thicknessof head retractorsis greateston the lateral sides of the sac and least on the dorsal side

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I FIG 20. General anatomv tn Enteroctopusand Octopus.A. E. dofleini. dorsal viel (female: 2l cm N4L). The skin is removedto sho* thc outline of the mantle and positionof the shell vestiges.Bold arrons with numbersindicate the planes.of correspondin-e cross-seclions (sho*n in Fieure 22). B. O. vulgaris: dorsal r,ieu of a hall'-gro\\n animal. The muscular mantle is cut ofT from the dorsal side riithout changing natural topographl -aOOucror [from Naef.*1923: modified] C. E dolleini. rentral vre*. The mantle is open at the inserlionof ihe median mantte and spread. The gills i'u-rdlisceral or,sans(e\cept the dieestivegland and stomach)are removed. Scale bar I cm. Pl4C. 20. Crpoenue Enteroctopusu Octopus.A. E. dofleini: BHJ c.topcarsHoii cropoHu (carrna:2l crr IJM). Koxa Crpe.rxu vxa3btBarcT )JareHa. qro6tr noxa:arb KoHTvpttauruiinr,rxlrbrrlu H no.toxeHuepvJH\leHToBpaKoBHHbr. no"roxeHnecoo'rBercTBvtottIHX cpe3oB(noxa:ausrHa Puc. 22). B. O tulgaris: BH;l\to.toJoro xuBorHoro c .topca_tblrot"l cropoHbr.;ilopca-rrsalcreHxa lrarrrnH \.taieHa 5e: u:rrcnesur ro.toxeHHr BHvTpeHHHX opraHoB[u: Naet-. 1923: c n:rteHeHuli[r]. C. E. JoJltint. er: .' *.-urpanrHoiiclopoHu. \{aHrHq BcKpbrrac BeHlpa-rbHoii ctoporrsrelo.rr cpeJHet .lllHHu.orfe"leHa o1 \lefHa"turroiicenrsr H pacnpaB.reHa. rentral rre$. Xadptr H Bucuepa-tblrr,re opfaHbr (Kpo\re nuueBapHre.tbHoir xe.te:sr rr xe.lJxa). \,faculraS I crr. )Ja,'reHbr

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2l. B:aurtoorHottleHue \re;+i-t)ocrarKa\Ifipa(oBHHbr l \rqrKu\r retoy Enteroctopusdofleini (::pe"rsrii cayeu: lg0 rnr !M). A. Bn: c5oxr'. C .renoi cropoubr \.ta-reHbrKoxHbrefloripoBbr.rra*,inq u xadpli 'B. yse.-rnqeHHr,rii (tpanreHr sfiJa'A'. rloxa3btBarcuHil = npuxpen.reuHe \r\cK).toB K crH"tet\. iV{acru.rad I cri

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ventral llall of the funnel. and a pair of lateralfolds forming the dorsolateralu,alls of the funnel (Fi_e. 22A). Boundariesbetrveenventral and lateral*'alls of the funnel are markedby'thejunction of muscular fibers of different orientation.The inner margins of dorsolateralrvalls of the funnel attach to collagen tunic of visceralsac.The muscularcollar folds represent lateral extensionsof the dorsolateralwalls.

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Shell in Vampyropoda They pass alongside the visceral sac and attach to dorsolateralwalls of the mantle. Inner dorsal surface of the funnel canal is lined with a thick, glandular funnel organ. At the level of anterodorsaladductors the head retractors are thinner, especially ventrally (Fig. 22B). The paired anterodorsal adductors are seen to arise fiom the head retractors. The anterodorsal adductofsrepresentthe only attachment sites of the head retractorsto the mantle. Ventral median adductor is formed by two muscular layers diverging from the mantle wall to ventrolateralwalls of the visceral sac. The ventral adductorstraddlethe rectum and vena cava. The funnel retractors are wide. flat and parlly fused with ventrolateral walls of the visceral sac. At the level of attachment of the funnel retrac_ tors the mantle reachesits greatestdiameter. Vis_ ceral sac is relatively small here and occupiesapproximatelyhalf of the volume ofthe mantle cavity (Fig. 22C). Lateral sides of the visceral sac are fused with the funnel retractors which, in turn, attach to the stylets(Fig 22D). The funnel rerractors attachto the medial side of the stylets.Mantle walls attach to dorsal and ventrolateral sides of the sty_ lets. The furrow between mantle muscles over the st1,.let is filled with dense connectivetissue. Each "fin" nerve penetratesthe mantle wall near the anterior shoulderof a stylet. The gill basesattachto mantle near the funnel retractors(Fig. 22D) and thus receive indirect support from the stylets. COMMENTS. The most important function of stylets.one that determinestheir shape.is suppor.tof the funnel retractors.During contractionof the funnel retractorsthe bendsof the stylets sustainthe major load fi'om the contractionforces.Visceral sac also ieceives indirect suppoft from the sg,lets through the funnel retractors.The mantle attachmentto the styletsappa_ rently helps maintain some positioning betrveenthe vlsceraand the mantle.

BathypolypodinaeRobson,1928 Benthoctopussibiricus Loyning, 1930 HABITSAND HABITAT.GenusBenthoctopus in_

c l t r d easb o u 2t 6 s p e c i eosf d e e p - l i v i n b ge . n r h ioc c topodsinhabitingcontinental shelfand slopeof all oceans,frorn Arctic to sub-Antarctic[Nesis. 1982119811. Speciesof this genusoccurat depths belowzl00m in tropic and subtropiczones,while in theArcticseastheyascend to theshelfandlittoral Speciesof Benthoctopus [Nesis,1982119871. are generallymorefragileand lessactiveanimalsthan Octoptts.B. sibirictrs is the most cold-waterand shallolv-water speciesof this genus.It growsup to

J)

180mm ML andis knownfrom theseasof Siberian Arctic andthe BeringSea[Nesis.19821198]1. SHELL MORPHOLOGL Styletsin Benthoctopus are shofter.thicker and softerthan in Enteroctopus (Fig.23).Theyareembedded in dorsolateral mantle wall. The distance betweenanteriorendsof the styletsis about13%ML (Fig. 23A). Similar with Enteroctopus,the styletsconsistof semi-transparent cafiilage-like chitin laid down in concentric layers. The lengthof styletsrangesfrom j .6ohto l4%oML (meanlengthis 10%; SD:1.5). that is abouttrvo times smallerthan in Enteroctopu.r. Eachstylethas a bendin its anteriorparl that forms an obtuseangle (120'-130').Thebendis veryprominent, thick.eitherdome-likeor crest-shaped. At thebendthestylet reachesits greatestthicknessthat rangesfrorn 8% to 30ohof styletlength(mean ca. 16Yo:SD:4.6). The surfaceof the bendis faintly sculptured. while the rest surfaceof stylet is smooth.The anterior shoulderis curved.claw-like.Its lengthrangesfrom 16%oto 46Yo of stylet length, averaging 33% (SD:6.3).The posteriorshoulderis nearlystraight, sharplypointed.The apicallinesareratherdistinct. especiallyin posteriorshoulder. The stylets in Benthoctopusexhibit greater variability in size and shapethan in Enteroctopzzs.Among 25 specimensof Benthoctopusana_ lyzed, threemorphologicaltypes of styletswere found.The most abundant(14 specimens) were the styletswith high crest-likebendand long nearly straightanteriorshouldercomprising31% _ 46ohof stylet length (mean ca. 38oh;SD:3.1) ( F i g .2 3 D , E ) T . h e s e c o n di n a b u n d a n c(e9 s p e c i mens)werethick styletswith massivedome-like bend and short anterior shoulderrangins from 25%oto 35%oof stylet length lmean-cai 31%; SD=3.3) (Fig. 23A). Rarely encountered (two specimens) were styletswith low bend and almost straight short anterior shoulder ranging from 16%oIo lSoh of stylet length (Fig. 23C). Taxonomicstatusof abovedescribed morphological types is unclear. Accordins to Nesis [ 1 9 8 2 1 1 9 8 7a]n d K o n d a k o ve t a l . l t 9 8 t l . t h e genusBenthoctoplts needsa revision,and B. sibiricusin the westernBering Seamay combine 2-3 undescribed species. Variabilitybetweenthe left andthe right sty,lets in Benthoctopl.swas also higher than in EnterocIctpus.Althoughthe averagesizeof the left andthe right stylets(in relationto the mantlelength)rvas equal,the differencein lengthbetweenthem could reachedup to 20%o, differencein thickness- up to 2l%o.and differencein the length of anterior s h o u l d e- r u p t o 5 l % . MICROSTRUCTURE OF THE STYLETS. Crosssections of styletsat the levelof the bendareroughly oval or slightlytriangularin shape.consisting

36

V. A. Bizikov

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FIG 23. N{orphologicalrariability of sqlets in Benthocroptts. A. B. sibiricus.Ventral vierr of a pair of st1letsfronr mature male (1,15 mm \,lL) (right st1let is on the left: anterior end is up). Note curvature of the stllets and conspicuousventral angle in a shapeof bul_eingdome. Dark initial shell is r isiblc through semitransparent substance of the st1let. B. Left stl let frorr the same specimen:lateralr ieri form the inner side (r'entralside is on the right). C. Benthoctoprssp.: adult malc (150 mm l\4L), \'entral rieu of a right stllet. D-F. Right stllet liom Benthocropus sp. adult male (173 mm N,lL). D.Ventral rieri (anteriorend rs up: outer side is on the left). E. Lateral vieu fionl 'F'. F. the inner side (ventral side is on the left), Bold arroris indicate the plane of the cross-sectionshoun in Cross-section through the angle of the stllet (dorsal side is up: outer side is on the left). Scale bar: I mm. PHC. 23. Ir{optpo.roruuecnar fi3veHquBocrbcril"reroB Benthoctopus.A. B. sibiricus.BHg c neHrpa"rrnoiicropoHsr naphr crH.reroB3pe.rofocarrua (1-15rrrr ,[N'{): npaarrii crH.rer c.rcBa:rtepefHqr cropoHa HaBepx)'.Yro.'r clu.rela Hlreer BHJ lrllpoKofo BbrnrqHBarcuefocq K) no.ra.B ueHipatbuoil qacrn cru.rera lpocBequBaerre]\'rHarr 3apoJbrileBaq paKoBHHa. B.,rlesrrii cru-rer rofi xe ocodu: sH: cSori) c nHrrpenueiicropoHbr(BeHrparsHatc'ropoHacnpaea).C. cropourr. D-F. llpanui;i Benthoctopussp..B3poc.rbrii carrert(150 lrr rIlNl), Bu.r npanoro crri-rerac BeHrpa.:rbHoii cru"rer 3pe-roroca\{qa Benthoctopus cropoHbr(nepe:urii KoHeuHaBep\): ry (173 rnr rll\{). D. Bur c BeHrparLHoii \'Ka3brB?uor' BHeurHsq cropoHbr(neurpa-rruarcroporrac.-reaa). C'r'pe.rKI4 cropoHacrena). E. Bu: c6oxr c aHvrpeHHeii 'F'. lo"iroxeHuecpe:a. u:odpaxeHHoroHa BH.te F. IlorrcpevHuiicper Ha \poBHe)f.ra cru"rera(:opca,rsuarcropolra HaBep\\: BHeruH.s.q cropoHa c.resa).!lacrrlra6 - I rrrr.

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Pl4C 2l CTpoeuue Benthoctopussibirtcus.A. B:poc.rsrEcarreu(115 rnr Tlivl): nu.r c :opca*rruoii croporrBr.Koxsr,re noKpoBLI \taHTHti. Crperxn c uuQparlr \Ka3brBallrrro-ToxeHHe )JalcHbl.'iro6rt noxa3arb](oHT\pbt coorBercrB\K)tuqx cpe3oB(lIoKa3aHLI Ha Puc. 25). B. Bu: c5onr roir xc ocodu lcreHxa'rraHlHH u xadpsr c -reaoficr.opoHr,r 'B'. )Ja.rcHbr). C. Vse-tuqeHHsrfr rreHr su:a 'tofiaiorsarcruuii Npen.teHHe \lblrru K .teBolr\ crH-terr. A H B: rracurad : -rlpar I cn. Cl: rracurra6- I rrrr.

I

of numerousregulartransparent concentricincrements(Fig. 23F). Contoursof previousll,formed increments are similarto the outercontourof the section.indicatingthat the stvlet profile doesnot changesignificantll'duringgrowth.Microstructure of the increments is similarthroughoutthe section. The grorvthzonesare absent.Gror.vthincrernents rangein ri'idthfrorn 6 to 14 pm. averaging 1i pun.

The centerof grorvth(initialshell)is situatedclose to themiddleof thecross-section. It is roundor oval. rangingfrom 80 to 1601xnin greaterdiameter.Firstorderincrements aregroupedinto second-order cvcles.from 8 to 35 increments in onecycle.Ventralside of the bend(in the bottomof the section)is covered b1'minuteindistinctknobs.The knobsin Benthoctopt$ are lesspronouncedthan in Enteroctopraand

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of the soft bodl in Bentlnctopus srbiricus (matunng ttmale: 90 mm \{1.) .\' FIG. 25. Schematiccross-sections . . S e c t i o n3 . b c h r n t l S e c r i o nl . a t t h e l c r e l o f t h e 1 u n n e l .B . S c c t i o n2 . a t t h e l e r e l o f d o r s a lr n a n t l ea d d u c t o r sC D. SectionJ. at the lercl of attachmentof the tunncl rctractors.E. Enlargcd fragment anteriordorsal 'L)' adductors. shoriing attachmentof thc ntantle and funnel rctractorto the shell. Positionof sectionsis indicatcd of figure on Fig. 2-1.A-D. scale bar - I cnt. E: scal.' bar - I nlnl. PHC. 25. Cpe:rr rrrrxor-o re,'ta ISenthoctopus sibtrtctts(co3peBarcuatcarltia: 90 rrrr ,{\'1). A, Cpe.] l. Ha lponuc rJ-t\ r\lopoB.C Cpe:_3. no3a.lu-lopca.rsttr'tttt:lutttiittt'tr. \laHTllrluL,l\ uopoHxrr.B. Cpe: 2. na r poBHe.topca-rr,nbt\ 'D'. pclpariropoBBopoHxlt.I-1.\'se-rnqcrtrtltr"t iut.'l)KropoB.D. Cpe: 1.' irtr l poBue npKpcn,reHrrr Sparrtcttl eft-la K crti-rer). flo.toxeulte cpc30Bnolia3auotla Pttc. \raHllllr r1 pelpar\fopa BLrporrKIt llpllNperr,'reHue rroria3brBaruulrx 21. A-D: rtaculaS = I crr. E: rlacutraS- I rnt.

Shell in Vamp.vropoda occllp\ minor pafi of the section.The knobs can be traced on previouslr.'formed increments as radial rnarks. forming a sector of about 60o. EXTERNAL MORPHOLOGY. The bodv in Berztltctctctpus is more gentle and less rnusculir than in Enteroctopu.s. The mantle is elongated oval. The nuchalrnuscleis u'ell developedspreadingfrom the rnantle margin to\\'ard the bases of arms I (Fig. IJA). The mantle n,all is the most thick in anreflor part. gradualll' becoming thinner posteriorl\..The dorsaland the ventral mantle u,alls are approximatelv equal in thickness.The n-rantleapefiureis narrorverthan in Enteroctoplrs.its lateral margins are situatedbelou' the e1'es(Fig. 2,18). poster.oventral rnarginof the funnel restsagainstthe ventral mantle adductor.The mantle cavitl,'is occupiedalmost entirely bl the visceral sac. Free spaceofthe ventral rnantlecavity' is greatlv reducedas comparedil'ith Enteroctopus.The ventral median-mantleadductor is rvide. The anterodorsalmantle adductorsare situated at some distancefrorn posterior margins of the collar folds. The funnel is narrow and long. reaching the bases of the ventral arms. A funnel locking-apparatusis absent.The funnel retractors are narro\\'er and longer than in Enteroclopus. They, attachto the st1,'lets in a similar wav as in Enterocroptrs(Fig.24C). The "fin" nervesstartoff the stellar ganglia.run posteriorlytou ard attachmentof the tunnel retractorsand pierce the dorsal rnantleu,all nearanteriorends of the stvlets. CRO.SS-.SECTIONS. The rnanrle and the funnel consistof trvo surfacemuscularla1,.ers separatedby, thick middle laver of vacuolatedconnectivetissue t F i g . 2 5 ) . T h e d e n n a l i n t e g u r n e nits s m o o t h .t h i c k and gelatinous.especiallvnearthe posteriorapex of the mantle. The mantle cavitv is relatively,small; its ventralparl is larger than the dorsalone. In the region betw'eenanterodorsaland posterodorsaladductorsthe dorsal and ventral parts of the rnantle - cavin' meroe alongsidethe visceralsa. (pi-e.25C;. The visceralsac is large at the level of the collar tblds. occupy'ing most part of the mantle cavitv ( F i g . 2 5 A ) . P a l l i a l n e r v e sa r e s i t u a t e do n d o r s o - l a teral sides of the visceral sac. betueen salivarv s l a n d sa n d t h e d i g e s t i v eg l a n d ( F i g . 2 5 A ) . T h e r e c tum and the vena cava are situatedon ventral side of the sac. projecting inside the funnel canal. The ink sac is absent. The head retractorsrnake muscularu,alls of the visceral sac at the level of the funnel (Fi-e.25A). The thicknessof head retractorsis less than in Ent erocI ctpus.The anterodorsaladductorsdifferentiate fiom the head retractorsat the level of the stellate ganglia (Fig. 25B), At rhis level the head retracrors becornethinner. especially on the ventral side of the visceral sac. The stellateganglia are relativelv srnall. Thel are situatedon the mantle rvall. late-

rallv from the anterodorsal adductors. Posteriorll, the head retractorsextendto the level of the mantle s e p t u m( F i g . 2 5 C ) . The median mantle septum consistsof two thin adductormusclesdiverging in V-like pattern from the ventral mantle wall to ventro-lateralwalls of visceral sac (Fig. 25B.C). Inner spacebetweenthe adductor muscles contains the vena cava and the rectum.Anterior extensionsof the adductorsextend anteriorlv forming a part of the dorsal funnel rvall (Fig.2sA). The muscular portion of the funnel in its anterior pafi consistsof a single muscularlaver. ln post e r i o r p a n o 1 't h e f u n n e l . b o u n d a r i e sb e t u e e n i t s ventral and lateralwalls are marked by the junction of muscular fibers with different orientation (Fig. 25A). The muscularcollar folds originate as extensions of dorsolateralwalls of the funnel and attach to dorsolateralrvalls of the mantle. T h e f u n n e l r e t r a c t o r so r i g i n a t ea s p o s l e r i o re x tensionsof the dorsolateralrvalls of the funnel (Fig. 25B). They run obliquely alongsidethe visceralsac and attach to the stylets embeddedin the dorsolateral rvalls of the mantle (Fig. 25D). The funnel retractorsare wide and thick. Inner side of the funnel retractorsattach to the lateral walls of the visceral sac along their entire length. At the level of attachmentof the funnel retractors the stylets. like in Enteroctopus.provide supporl for the mantle. funnel retractorsand gills (Fig. 25D). The visceral sac is the largesthere. occup1,,ing the mantle cavitv almost entirelv. The funnel retractorsattachto the medial inner side of the stvlets (Fig. 25E). Mantle w,allsattach to dorsolateral sides of the sty'lets.leaving narrow furrows over them. The visceral sac attach to inner side of the funnel retractors.while the gill basesattach to the outer side of the funnel retractors. COMMENTS. Relative size of stylets in Benthoctoptts is much smaller than in Enteroctopu.s. compr i s i n g i n a d u l t s7 - 1 1 % M L a n d 2 0 - 3l o / o M L . r e s p e c tivell'. Adhesion of the funnel retractorsto the str,,lels in Bentltoctoplts is weaker. If one tries to tear the funnel retractorsoff the mantle in fresh animals. in Enteroctopusthel' usually detach together with stvletsattachedto them. r.vhilein BenthoctopusIhe st;-letsas a rule remain inside the mantle rvall. But the most important sign of vestigial state of the str lets in Benrlrcctopzrs is their high morphological variabilitl. especiallr variabilitl' between left and right stl,let of the same specimen.Such variability could not be possible in functionally, important structure.It testifiesthat the styletsin Benthoctopus are not an) more the subjectsfor stabilizingpressure of natural selection.Thus. Benthoctopusrepresents an example of octopod rvith greatly,reducedshell. uhich apparentlyrvasstipulatedb1,thegeneraldecreaseof animal activit\ .

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^TIICROSTRL"CTU'RE OF THE STYLETS. The grouth pattefn of st1lets is similar to that in Entet'octopus and Benthoctopus. The stylets gro"l b1 c o n c e n t r i cl a r e r s .T h e i n i t i a l s h e l l i s s i t u a t e di n t h e areaof the bend. Apices of grou'th incrementsfol'trl apical lines visible through semitransparentsubst a n c eo f s t l l e t s .

F I G . 2 6 . S q l e t s i n B a t l n p o h p u ss t t l e b r o s u(si e m a l e :- 1 7 mm \{L). A. Ventral lie* of a pair of sn lets: rte.hl stylet is on the leti: antcrior end is up. B. I-ateral /, ( o u t e r )r ' i e * o f t h e r i g h t s n l e t ( \ c n l r a l s i d e i f o n t h c right: anteriorend is up1. Scale bar - I mnt. PI4C. 26. C lr'r.relrrBathtpolT l:us salehrosus(cartna.J7 crourr ANI). A, Bn.r napbrcrn.reroBc BeHrpa*tbHoii poHbr:npaBr,riicrH-rer c.reBa:IIepe.tHttcropoHa Haneprr. B. Bu: c Soxy (orap);.tiH)npaBoro crrr.rera (BcHTpa*rbHat cropoHa cilpaBa:nepetHHitlir)lteuHa- I rnr. Bepx\). lV1acrrrra5

Bathypolypus

salebroszs (Sasaki, 1920)

HABITS AM HABITAT. B. saiebrosusis a srrall ( u p t o 5 0 m m M L ) d e e p - u a t e rb e n t h i co c t o p u st h a t i s t 1 ' p i c a l l l f' o u n d a t d e p t h s 1 5 0 - 6 0 0r n i n t h e O k hotsk Sea.Bering Sea.off the easterncoastsof the K r - r r i l eI s l a n d s . H o k k a i d o a n d H o n s h u [ N e s i s . \ 9 8 2 1 1 9 8 7 1I n . t h e B e n n g S e a i t r n o s t l l o c c u r so n rnud bottom of the continentalshelf and slope. Bio l o g l ' a n Ce c o l o g l o f t h i s s p e c i e sa r e p o o r l l k n o u n . SHELL MORPHOLOGY. Stl lets in Batln'polvpus are two carlilage-like chitin rods uith protninent t h i c k e n e db e n d i n a n t e r i o rp a n ( F i g . 2 6 ) . T h e l l i e on dorsolateralsidesof the mantle at a sharp angle t o t h e b o d y 'a x i s ( F i g . 2 7 , A ) .T h e l e n g t ho f s t l l e t s i n a d u l to c t o p u s e cs o m p r i s e sa p p r o x i m a t e l ll T % M L . Distancebetlveenstyletsat the level of their altteriof e n d si s a b o u t5 2 % M L . T h e b e n d b e t u e e na n t e r i o r a n d p o s t e r i o rs h o u l d e r si s v e r r p r o l n i n e n t r. a n g i n e b e t r v e e n1 1 0 ' a n d I 1 5 ' . A p e x o f t h e b e n d i s t h i c k . d o m e - s h a p e db.e a r i n gd i s t i n c tk n o b - l i k e s c u l p t u r e . The greatestthicknessof each st1let (at the level of the bend) comprisesapproximatell 14% of stl lets length.Anterior shoulderis about tuo times shofier than posterior.Both shouldersare thick. smoothand pointed.Posteriorshoulderis faintll curved in zigzas Dattern.

The mantle is MORPHOLOGY. EXTERIIAL densell spacedderu ide. globular and covered b1 ( F i g . thick in its m o s t 27). It is the rnal papillae postefiotgradually' thinner becoming anteriorpafi. i n t he region u ' a l l i s t h e t h i c k e s t l r . D o r s a lm a n t l e riall mantle ventral the of the dorsal mantle cavity: mantle the ventral region of is the thickest in the adductor.Mantle apertureis wide. Its lateral margins are situatedbelorv the e1'es.The ventral median-n.rantleadductor is thick. muscular alld rathel' narrow. Its anteriormargin is at some distancefi'om ventral margin of the mantle (Fig. 27B). The fitnnel is shor1.conical. It arises deep within the ntantle cavitr. and its posteroventralmargin rests against the ventralmantle adductor.A funnel locking-apparatus is absent. The posteriorlateralrvalls of the funnel pass into muscular collar folds. The funnel retractorsare uide and ribbon-shaped.Thel run obliquell from posterior corners of the funnel tou ard the stl letsembeddedinto dorsolateralrvallsof the mantle. Visceral sac is very' Iarge. The anterodorsalmantle adductorsare shifted anteriorl)'to the ler''elof collar folds (Fig. 27B). Each adductorLrndergoesan 180otrvist so that the anterior-mostmargin at the visceral sac becomesthe posterior-ntost margin at the attachmentto the mantle \\all. CRO,SS-,SECTIONS.The rvalls of mantle and funnel consistof tu'o layers of muscularfibers separat e d b 1 t h i n r n e d i a nl a y e r o f c o n n e c t i v et i s s u e( F i g . 28). The mantle and funnel are more muscularthan The lateralrvalls of the mantle are in Benthoctopu.s. slightll thicker than the dorsal and ventral u'alls. The mantle cavitl is approximatell.'thesarneslze as in Benthoctopr.i:its dorsal parr is smaller than tlte r,'entralone. The dorsal mantle cavity' is best deleloped in the area of collar folds. extending posterio r l l t o t h e l e v e l o f t h e s t y ' l e t s( F i g . 2 8 D ) . T h e v e n tral r.nantlecavitf is the largestimmediately behind the funnel (Fig. 28A.B) extendingposteriorlyto the level of gonads.In the region bet*'een the antelodorsal and posterodorsaladductorsthe dorsal ancl ventral par-tsof the mantle cavity merge alongside t h e v i s c e r a ls a c ( F i o . l 8 C ) . T h e v i s c e r a ls a c o c c L t p i e sa b o u to f t h e m a n t l ec a v i t v r e a c h i n gt h e g r e a t e s t size at the ler el of attachnrentof the funnel l'etfact o r s ( F i g . l 8 D t . T h e p a l l i a l n e r v e sa r e v e r ; ' l a r g e . between salivarl oval in cross-sectionand sitr-rated g l a n d sa n d t h e h e a dr e t r a c t o r s( F i g . 2 8 A ) . B e t i i e e r l the anterodorsaland nosterodorsaladductors the v i s c e r a ls a c i s o c c r : p i e dm a i n l r b y l a r g e d i g e s t i r e

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FI(l 2T General anatomr',.of Barhrpolvpussalebrosus.A. Adult female (-17 mm ML). dorsal vieg. The skin is remoredto sho* the outlineof the maniie.Bold arro*s *ith numbers indicate*re franei oTcoii.rfonolng cross-secrions (shorin in Fig 28) B Adult female (50 mm 1r'1L).lateral rlre*l iiai ..*orit of the mantic *.all and gill fiom the lelt side. Scale bar : I cnr PLLC.27.Clpoeulie Bathpohpus salebrostts.A. B:poc.ra.a carrxa(_17rnr nivl). BHJ c JopcatbHoiicropourr. KoNHrre Ilo^poBbl)ra-leHI'l'q'o5rr noxa:arbKoHr\DslrraHiurt,c-rpe.rrH g,ryirlpalru)Ka3brBaror no.roxeH'ecoorBercrBlRrr'rJ\ cpe3oB(rro*a3aHl'r Ha Prrc. 28)..13.B:poi.rar carrxa (50 vrr ,qriii:-i;r .'6o^, noir. i;;i;;;; \raHrHHu xaopsr c -reBoiicropoHr,r.\4acura6 - I crr.

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E D of the soli bodl in Bathtpoltpussalebrosus(adult t'emale:5'1 mm lvll) A. Sectiorr IrlG. 28. Schcmaticcross-sectrons l. at the lerel of anteriorpart of thc funnel.B. Section2. at the lerel of anteriordorsal mantle adductors(posterior mantle adductors.D. Section,1. at the level of attachment part of the funnel). C Seition 3. behind anteriordorsal 'D' shosing aftachmentof the mantle and tunnel retractor bf the tunncl retractors.F-. Enlargedtiagmcnt of figure t o t h e s h e l l . P o s i t i o no f s e c l r o n si s i n d r c a t e do n F i g 2 7 . A - D : s c a l eb a r = 1 c m . E : s c a l eb a r : I m n l . cartra: 5-l r.1\rn.M). A. Cpe: l. ua rpoaHe nepe:Heir (B3poc.rac PI,IC.28. Cpe:u rrl|xoro reta Bathrpoltpussalebrosrrs rracrli BopoHKu.B. Cpe:2. Ha ypoBHc nepeJHH\-topca-rbHhrr rrasruiiuux ar't)'KropoB(:a{ull.lacrb BopottKH). perpaxropoBBopollKu. a.1t)KropoB.D. Cpe: -1.ua vponne npHxpen"reHxq C. Cpc: 3. no:laLl Jopca.tbHbt\rrarrrniiusrr 'D'. \laHTHHH perpaKTopaBopoHKHK crrller\. npnxpen.reHHe noria3brBaHrLrHii E. )'se-rlqeHrluit(rparrrcur su:a flo"roNeHnecpe3oB) Ka3aHoua Pttc. 27. A-D: rtacutra6: I crt. E: rtacura6 : I rnt

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Shell in Vampyropoda gland (Fig. 28C). The ink sac is absent.Posteriorro the styletsthe visceralsac is fused r.viththe mantle. The head retractorsmake thick muscular rvalls of the visceral sac at the level of the funnel (Fig. 28A). Posteriorly thel' gradually become thinler. I'he anterodorsaladductors separatefrom the head fetractorsat the level of the stellate ganglia (Fig. 28B). The stellateganglia are larger ihan in BentItoctopus.The,vlie on the lateral mantle ',vallsventrallv from the attachment of anterodorsal adductors.The anterodorsaladductorsare unusuallythick and nrn obliquely upward from ventrolateralsides of the visceral sac to the dorsolateralr.vallsof the rnantle.E,achadductor is surroundedb;- thick gelatinousdermal integurnent.Posteriorextensionsof inner la1'ersof the head retractorscan be traced behind the anterodorsaladductorsas thin muscular c n v e l o p eo f t h e v i s c e r a ls a c ( F i g . 2 8 C ) . 'lhe medianmantle septumconsistsof two thick adductormusclesdiverging in a V-like patternfrom the midline of the ventral rnantle r.vall(Fig. 28C). ,Anteriorextensionsof the adductorsextend anteriorlv forming a part of the dorsal funnel w'all and the 'uvallof the visceral sac (Fig. 28B). The muscular portion of the funnel in its anterior parl consistsof a single circular muscularla1,er tFig. 28A). In posteriorpart of the funnel. boundaries betrveenits ventral and lateral u'alls are marked b1' the junction of muscular fibers of different orientation (Fig. 288). The collar folds originate as extensionsof the dorsolateralw,alls of the funnel and attachto dorsolateralu,alls of the mantle. The tunnel retractorsoriginate as posterior extensions o f d o r s o l a t e r awl a l l s o f t h e f u n n e l ( F i g . 2 8 8 ) . T h e y rLrnobliquely alongsideof the visceral sac and attach to the st;-lets embedded in the dorsolateral * a l l s o f t h e r n a n t l e( F i g . 2 8 D ) . I n n e r s i d e so f t h e lirnnel retractorsattachedto the lateral walls of the r isceralsac along their entire length. The styletsare enclosedinto thick cartilaginous shell sac (Fig. 288). The funnel retracrorsanach ro the ventral side of the st1,'lets. r.vhilethe mantle attachesto their lateral sides leaving wide break on their dorsal surface.At the level of attachmentof the lunnel retractorsthe gills atlach to the funnel fetractorsventral to the stvlets (Fig. 28D). COMMENTS. The stvlets in 3o7/11;pol,pas fit u'ell irrto the row of gradual reduction of the shell in Octopodidaeoccupying inrermediateposition bet\\een well developedstl,lets of Enteroctopasand \ estigial ones of Benthctctopus. Relatil,e lengrfi sf ihe st),lets in Bathvpoltpus 117%) is somewhere betr.r'eentl-rat of Enteroctopus (20-32% ML.1 and Btnthoctopus (7.6-11%). Sculptured knob-like .urface of the bend in the stvlets of Bathpolttpts indicate that these structures provide substantial )Llppoft for the funnel retractors. unlike soft and srnoothsty'letsin Benthoctopus.On the other hand.

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FIG. 29. Stylets in Eledone nrcssyae.A. Dorsal vreu of a pair of sq lets from adult male (63 mm ML): anterior end is up. B. Lateral (outer) vieu of the right str let of the same specimen(ventral side if on the right: anterior end is up). Scale bar : I mm. PVC. 29. Cru.rerst Eledone messyae. A. Bul c ropcalr,HofrcropoHbrrrapbrcrHneroB3penofo canua (63 rr:'r !M): nepe.tHqrcropoHaHaBepx).B. Bnl c6oxr lcHapvxn) npaBorocruiera roii xe oco6u (nertrpa.riHaccropoHacnpaBa:nepelHH)iKoHeuHaBepxr) Macil'rao

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the stvletsin Bathypolypas could not be aseffective supportingstructuresasin Enteroctopusdueto their smallsizeandsofterconsistency. Eledoninae Grimpe, 1921 Eledone messloe Voss, 1964 HABITS AND HABITAT. Liltle is known aboul habitatand biology of E. messyae. Accordingto Nesis[1982/1987]. it is a benthicspecies inhabiting uppershelfof Brazil.Uruguay,ArgentinaandTrinidadIslandin depthrangefrom 30 m to 160rn. It is a smalloctopod.growingup to 75 mm in mantle length[Roperet al.. 1981]. SHELL MORPHOLOGY.Thesfyletsarelong.slenderandneedle-shaped chitinrodslying on thedorsolateralsideof themantle(Fig.29).Theyaresetwidell apaftfrom one another:distancebetweenthe stvlets at the level of their anteriorendsis about80% ML (Fig. 30A). The lengthof styletscomprises approx-

V. A. Bizikov

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FIG. 30. General anatom)' of Eledone messyae.A. Dorsal vierv of a maturing female (35 mm ML). The skin is removedto show the outlineof the mantle.Bold arrowsr."ithnumbersindicatethe planesof corresponding cross-sections (shor.vnin Fi-e.3l). B. Lateral vierv of an adult male (63 mm ML) after removal of the mantle r.valland gill from the lefi side. Scale bar I cm. PI4C. 30. CrpoeHue Eledone messyae.A. flopca-rsurrii sur co:pesarcuteii cauxu (35 vv [M). Koxsue noKpoBbr y,la"rreHbr..{ro5sr noxa3arL KoH'r}'pMaHTurr.Crpe,rrrl c uur}palrn )'Ka3brBarcT flo.roxeHne coorBercrBy]oulux cpe3oB (norasauu Ha Puc.31). B. Bl,r c6on1'(n:poc"rsriicalreul 63 nrr lM) noc.re)'.raJeHu.f, creHKr.r MaHr[n u xa6pu c Jeeofi cropoHbr.Macuna6 - I crr.

imately 11% llL. The bendis low. obtuse,ranging from 125'to 130".Surfaceof thebendis smooth.as well as the restof the stylets.Greatestthicknessof styletsis situated at thelevelof thebendcomprising aboutlYo styiet length.Anterior and posteriorshouldersare slightly archedinsidethe mantle.The anteriorshoulderis relativelylong, approximately 40o/oof styletlength.The distalparl of both shoulwithoutzigzagcurvature. dersis straight. MICROSTRUCTURE OF THE SZYZEZS. Mic-

rostructure the sameas of the styletsis essentially in Benthoctopas.The stylets grow by concentric layersof semitransparent chitin.The initial shellis situatedin the areaof the bend.Growth increments andapicallinesareclearlyvisibleinsideboth sholight. uldersin transmitting EXTERNAL MORPHOLOGY. The mantle is wide.globularandcoveredby thick gelatinous dermal integument with prominentpapillaeon thedorsal side(Fig. 30).It is the mostthick in its anterior

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FIG. 31. Schematiccross-sections of thc soft bodl in Eledone nrctssrae (rraturing f'emale:35 mm ML). A. Secrion l. at the level of antcriorpart. 01'the funnel. B. Section2. at the ielel'of anterlordorsal ntantle adductors(posterior part.of thc funnel). C. Section3. behind anteriordorsal mantle adductors.D. Section,1. at the level of atiachrncnt of the funnel retractors,E. F-nlargedtiagment of figure 'D' sho*ing attachmentof the mantle and funnel retractor to the left shlet. Position of seciionsii indicated6n Fig. 30 A-D: scale bar : I cm. E: scale bar : I mm. PLIC 3l Cpc:rr rltlxofo teta Eledone massrde (co:penarouar car,rxar35 ulr !M). A. Cpe: l. Ha l,poane nepe:rueri qacrfi BopoHKu.B. Cper 2. ua IponHe flepe.tnu\ -]opcarbHblxnauruiluslx a1:I],K.ropoB (:agrur qacrb Bopo]rKfi). no:a*lIl.{opca"tl,t{blx lrarlluiiHr'ri a::1 xlopbn, D. Cpe:'1. Ha rpoaue Kpen.reHr.ir perpaKi.opoB 9 !p..3. BopoHKH. 'D'. E. Vee.quqeHHsrii tpparr,rerrr Bnjla uoKa3;rBarculhr"i xpen.rcune\ltllrurl H perpaKTopa BopoHKH K .reBo\{\crn.tct.\. flo"rroxerrue ope3oBfroKa3asoua Puc. 30. A-D: rracura6 : I c\r. E: rracurra6: I uM.

V. A. Bizikov part. gradually becoming thinner posteriorly.Lateral rvalls of the mantle are thicker than dorsal and ventral u'alls. The mantle apefture is relatively srnall:its lateralmargins are situatedwell below the e;'.es.The ventral median-mantleadductor is thick and rvide. It attachesto the visceral sac from the level of the anterodorsaladductorsto the level of the stvlets(Fig. 30B). Anterior margin of the ventral median-mantieadductor is at some distancefrom ventral margin of the mantle. The funnel is long, tube-like.fused with the head approximatelyalong of its length.The funnel arisesdeepwithin the mantle cavity. and its posteroventralmargin restsagainst the ventral mantle adductor.A funnel-mantlelocking apparatusis absent.The funnel retractorsare long. rvide. ribbon-like. The anterodorsaladductorsare situated at the level of posterior margins of the collar folds. They have a shapeof shortribbon-like muscular ligamentstwisted in the sameway as in other Incirrata. Tlre visceral sac is fused with the mantle posterior from the level of the stylets(Fig. 30B). CRO^SS-.SECTIONS.The walls of mantle and the funnel consistof two thick surfacemuscularlayers separatedbv ver1, thin layer of connective tissue ( F i g . 3 l ) . I n a n t e r i o rp a r l o f t h e m a n t l e i t s l a t e r a l walls are slightly thicker than dorsal and ventral rvalls.The dermal integumentis very thick. Its surface bears prominent papillae covering the mantle entirely. The mantle cavity is relatively small. At the level of the funnel the dorsal mantle cavity is larger than the ventral one. Posteriorfrom the funnel the dorsal mantle cavitl, is smaller than the dorsal one. Between the anterodorsal and posterodorsal mantle adductors both ventral and dorsal mantle cavitiesare fusedtogetheralongsidethe visceralsac ( F i g . 3 1 C ) . T h e v i s c e r a ls a c i s r e l a t i v e l ys m a l l i n anterior parl becoming very large posteriorly. Betweenthe anterodorsaland posterodorsalmantleadductorsthe visceralsac is occupiedmainly by large d i g e s t i v eg l a n d ( F i g . 3 i C . D ) . T h e i n k s a ci s i n u n u sual position. deeply embedded inside digestive gland from the ventral side. Head retractorsrnake thick rnuscularwalls of the visceral sac at the level of the funnel (Fig.31 A). At this level they consistof thick inner and thin ollter muscular layers. The anterodorsaladductors differentiate from the outer layer of the head retractorsat the level of the stellateganglia (Fig. 318). The anterodorsaladductorsare unusually oriented running obliquel,v downward from dorso-lateral r.vallsof the visceralsacto lateralwalls of the rnantle. The stellateganglia are large. situatedon lateral walls of the mantle just below the sites of attachment of the anterodorsaladductors.Posteriorlythe head retractorsextend to the level of the median mantle septlrm(Fig. 31C). The median rnantleseptllm consistsof two thick adductor musclesdiverging in a V-like pattern from the midline of the

mantle toward the visceralsac.Inner spacebetween the adductor muscles contains the duct of the ink sac. vena cava and the rectum. Anterior extenslons of the median mantle adductor form a parl of the d o r s a lf u n n e l w a l l ( F i g . 3 l A , B ) . The muscular portion of the funnel consistsof s i n g l e c i r c u l a r m u s c u l a rl a y e r ( F i g . 3 i A . B ) . T h e collar folds originate as extensionsof the lateral walls of the funnel and attach to lateral walls of the mantle. The funnel retractors originate as posterior extensionsof dorsolateralwalls of the funnel. They are thin. flat and ribbon-like in the middle par1. gradually becoming thicker posteriorly (Fig. 3lC). Inner side of the funnel retractors is attachedto the visceralsac.At the sitesof attachmentto the stylets the funnel retractors are thick, wide and triangular i n c r o s s - s e c t i o(nF i g . 3 l D ) . T h e w i d e m e d i a l s i d e of each base attachesto lateral side of the visceral sac, while the narrow outer apex attaches to the medial half of the stylet(Fig. 3lD,E). The stylets are embeddeddeep inside the mantle wall. Their greatestdiameter is about 1/3 the thicknessof the mantle wall. The mantle attachesto the dorsolateral sidesof the styletswhile the funnel retractorsattach to the ventral side of the stylets (Fig. 31E). The "fin" nerve is small, passing between the funnel retractorand mantle wall. ventrally from the stylets. The gills attachto the mantle wall ventral from the styIets. COMMENTS. Extremely narrow needle-like shape differs the stylets in Eledone from those in other octopodidsstudied.At the level of the greatestdiameter the stylets in Eledone comprise lessthan l/3 of the mantle wall thickness.Weak expressionof the bend, relatively small size and smooth surface of the styletsin Eledone indicateto the reductionof supportingrole of the styletsin this species.On the other hand. the styletsin Eledone apparentlyretain their role of structural centersuniting the mantle. funnel retractors,visceralsacand the gills. Widened inner basesofthe funnel retractorsapparentlyensure strong connectionbetween the visceral sac and the mantle. Reductionof supporling role of stylets in Eledone may be causedby decreaseof its swimrning activity in the courseof adaptationto benthic (crawling and hiding) behaviour.

AlloposidaeVerrill, 1881 Alloposusmollis Verrill, 1880 HABITSAND HABITAT.A. mollisis a benthopelagic octopod.inhabitingnear-bottomwaters of continentalslopesin all oceans,from tropicalto high latitudesfYoung, 1996].Body tissuesaregelatinous.Fernales arevery large.reaching400 mrn ML or a total lengthup to 2 m [Nesis.1982/19811.

=

Shell in Vampy'ropoda Males are much smaller than fernales.but thel are no dr.vartt like in other representativesof argonautoid families [Young. 1996].According to Nesis !9751. the deep umbrella formed by' the arms and rveb servesAlloposus as its main organ of locomot i o n .A b i l i t l , f o r t h ej e t - s wi m m i n s i s a p p a r e n t hl o s t . Recentll'this was confinned by' direct submersible obserr,'ations of Alloposussu'imming n ith slou medusoid motion of its umbrellajust above the ocean f ' I o o rf Y o u n g . 1 9 9 5 ] .

t'7

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SHELL MORPHOLOGY. Sn'lets in Alloposus r r e r ef l r s t d i s c o v e r e db i ' V o i g h t 1 1 9 9 7 1 u h od e s c r i bed tl-remas 'gelatinous masses'. situated 'in the dorso-lateralmantle'. Stvlets in ,lllctpctsusare unllsual in their shapeand structure(Fig. 32). Ther are r e l a t i v e l vs m a l l .w i d e a n d t h i c k d r o p - l i k eb o d i e so f soft consistencl'ernbeddedin the lateralrl,allsof the rnantle. In forrnalin-storedspecimens st) lets are transparent.soft and flexible. like rvater-filledballoons. The lengths of st,v-lets comprisesabout l0% VL. As the srylets lie on the lateral sides of the rnantle.the distancebet'uveen thern eoualsthe mantle u'idth at that level. cornprisin-eabout 54% ML. In each st,vletthe anterior and posterior shoulders fbrm an obtuse angle of about 135o-145obetrveen thern.The shorteranterior shoulderis roundedand uide; its length comprisesabout 33%oof the stl let length.The posteriorshoulderattenLlates to a point. I'he bend is low and dome-shaped:its surface is snrooth.The greatestu'idth of the stl,lets (at the level of the bend) corrprisesapproximatelr 46% of :ty let length. The inner side of each stl let bears a prominent ridge ending in a prominent dome jLlst a b o v et h e n u c l e u s( F i g . 3 3 C ) . T h e s u r f a c e so f t h e -it\lets are smooth. Dorsal side of each st1let bears a shallowgroove betu'eenthe anteriorand posterior shoulders. UICROSTRLTCTLTRE OF THE S?YZEZS. As in other incirrates.the st;-letsin Alloposttsare composed of concentriclayers growing around an initial .hell, fhe latteris visible in transrnitringlight uithin ihe bend.However.all attemptsto make cross-section ot'thesestructuresfailed. as the sryletslost their shape lnd releasedr.vaterr.vhentheir surfaceis broken. EXTER IAL MORPHOLOGY. The bodr. is smo.rth and u'ith gelatinousintegurnentconcealingthe r L n d e r l l , i n rgn u s c u l a t u r e( F i g . 3 3 ) . T h e m a n t l e i s .hor1.rvideand cup-shaped:its lengthaverages380% I L. Dorsal rnargin of the mantle fonns *ide : o n g u e - l i k ep r o c e s sp r o j e c t i n g a n t e r i o r l y .V e n t r a l ;nargin of the rnantleis shallovvconca\/e.The man:le apeftureis u,ide: its lateral rnarginsare situated rt the level of ey'es.The long. ri ide. tLrbe-likefunnel :s completelyernbeddedin the head.Its u ide nozzle opens anteroventrallyto the e1'es(Fig. 33B). A n eak funnel locking-apparatusis present.It consists rf hook-like muscular folds on the funnel corners

FIG. 32. St1lets of .'llloposnuol/is(immaturc male: 60 rnm 1\{L).A. Inner lateralvie* of the lcft strlet (antcrior end is up: r entral side is on the rilht1. e. Inner lateral vieu of the rieht str let (anteriorend is -left1. 'C. up: r entral side if on the Dorsal r res o1 the right sn lct (anteriorend is up: inner side is on the left). D. Inner lateralvie* of the right st\ let (samc 'B'). orientatronas in A.B the sn lets are drarin naturallr transparent to sho* their grosth increments. C.D the st\lcts are drann oDaoueto rereal their : u r l ' r c e .S c a l . ib l r s I mm. PI,IC.i2. Cru.reru ,-llloposnrol/rs(He:pe.rtriicarreu:60 rrrr ,1\1). A. Bn: .teBofo crH.terac6oxr' (u:rlr lpH): fIepeJHHi{ KoHcr]HaBepx]:BeHTpiLtbHar cropoHacflpaaa. B. Bnr npaBofo cru"tera c6oxy (u:u1rpr): lrepe-tHuiiKoHeuHaBep\\':BeHTpa-tbHar cropoHac"leBa. C. Bu-r npaBolocru.terac :opca-rsuoiicropoHrr(ncpc.tHHilKoHeurraBep\\: BH\rpeHrJrrcropoua c.rentr). D. Bu: npaBolo crn.tera c5oxr (HrHvrpu):opueHra'B'. uurr ra xc. qro sa A.B - crn.rerrr u:o6paxeHrr ecTecTBellrlo ilpo3paqHhr\tti.rtToobrrroKa3aTb il\ c.toH ruapacraHHr. C.D crH.terbru:odpaxeurr HenpolpaqHurru. qlo6rr noKa3arbpe-rretpHXnoBepxHocru. N4acnra6 : I rnr.

V. A. Bizikov

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FIG. 33 General anatoml of ,llloposus mollis. A. Dorsal rieri (immature male: 60 mm ML) B Sam: specimel: (shorvnin Fig. 31I q cross-sections lateralricg. Bold arro*s *ith numbers indicatethe plane of correspondin-e Lateral \ieg of a immature male (63 mm \{L) altef removal of mantle *all and gill from the right side. Scale bars = I cm. PI,{C.33. Crpoenye ,llloposus mollis. A. Bnl c:opcanruoii cropoust (He:pe,rslficarreu: 60 vrr nM). B. Tor xe no.roxeHuecoorBcrcrB)lotuu\cpe3oB([oxa3aHblHa Pnc ,*aaynr"p, su-t c5ori.. Crpe"rrorc urrspatrn ) Ka3brBaKlr \raHrHHu xadpsr c npaBorrcropoHbl(ne:pe-rsriicarteu: 63 rl:rt tll\'I) 3-l). C. dn,r cdonl ,io..-rey-ta-r."uq crcHKr.r Nlacura5 = I crt.

Sheli in Vampyropoda

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I IG. 3l Schematiccross-sections o1'the soft bodl in ,1llt:,posus rrol/rs iintmature ltmale: 57 ntm I,lL). A. Section l . a t t h e l e v e l o f a n t e r i o rd o r s a l m a r . - e ionl ' t h e m a n t l e . ' 8 . S e c t i o n2 . a t r h e l e r e l b e h i n dt h e t u n n e i . C. Scction 3. at the lerel of anteriordorsal mantli adductors.D. Section1. behind anreriordorsal mantle adductors. E. Sectron tlt 5. at thc level of attachnlcntof the funnel rerractors.. F Enlarged tiaernent of tl_eure iiroirin-s unacl1nrcnio1 the mantle and funnel retractorto the leli srl let. Posirionof sictions"is rndicated-o" rie 1:. A-E: scale bars I cnt. F: :eale bar = I nun. :'llC. 3'1. Cpe:st rtlrxoro re-ta_ .llloposus rrollrs (ue:pe.rarca\rKa:57 rnr illM). A. Cpe: l. sa r poBrrerepeJHcro Jopcarr,HofoKpa.s\laHrHH.B, Cpe: 2. no:alu BopoHxrl.c. cpe:3. ua rpoage rrepe.rHu\.-ropcarLHbrx rrasrurissrr -1. al:1 xropoe no3aln .topca-tust'tx rtaHruirshr\r-LrlKropon E. Cfir 5. Ha rponHc npnuip.n.,.rtu"plTparil-opoB -D Cpel BopoHKH. F. Yee,rrl.rerrrmrii (rparrrerrrB[:Ia'E'. nor(a3brBanorulfi npurpen.rcHue\taHrHHu perpah-ropa BopoHKnK _teBo\r\ cru'rler\.flo'roxeuue cpe3ourtoxa3asoua Puc.33,;\-E: rracurla6I I crt. F: rracurrad': I rrrrl

V. A. Bizikor and correspondingridge/grooves)'stemon the mantle. Visceral sac is rather small. Inli sac is present. The median rnantleseptum is rvide but feebly'rnuscular. Its anterior margin is at the anterior ventral margin of the mantle. The funnel retractorspass nearl,vlongitudinalll' along lateral sides of the visceral sac. The anterior dorsal mantle adductorsare long and narrow. running almost parallelto the funnel retractors(Fig. 33C). CROSS-.SE'CTIONS.The rvalls of mantle and funnel arethin and rveakh'muscular.Dorsal rvall of the mantle projects furlher anteriorN than the ventral r.vall.so tl-ratthe latter is absenton the section at the level of the funnel (Fig. 3aA). The dorsal mantle wall that confinesthe dorsal mantle cavit,vis conspicuously'thinnerthan lateraland ventral con"valls fining the ventral mantle cavity (Fig. 34C.D). The rnantle cavitf is spacious:the dorsal part is larger thanthe ventralone.The dorsalmantle cavitv is best developedin the areaof collar folds. while the ventral parl reachesthe greatestsize immediatell beh i n d t h e f u m e l ( F i g . 3 5 C . D ) .V i s c e r a ls a co c c u p i e s about 2/3 of the mantle cavity'. Posterior part of digestivegland is divided into left and right lobes (Fig. 3aC,D). The ink sac is enbedded betweenthe two lobesof the digestivegland. An elongatedh,vdrostaticorgan lies in the rniddle part of the visceral sac.along its dorsalmidline. next to digestivegland (Fig. 3aC.D). Numerousfolded and branchedmembranesproject inside the organ from its walls. Head retractorsare thin. shoft and rveak.They do not fonn a complete muscular envelope around the anterior part of the visceral sac. like in octopodids. but run along lateralsidesofthe visceral sac as a pair of thin muscularbands.Posteriorlythe headretractors gradually'become thinner and disappearby the level of stellateganglia(Fig. 3aA-C). The anterodorsalmantle adductorsare peculiar in shapeand structure.They'separatefrom the head retractorsverv early. at the level of the funnel. Here they'have the shapeof lou' ridges on the ventrolateral sidesof the visceralsac(Fig. 3'1A).Each ridge consistsof a series of muscular bundles surround i n g a p a l l i a l n e r v e , T h e l a t t e r o c c u p i e su n u s u a l position in Alloposus. lying external to the head retractors.At the level of collar folds. the bridges containing the anterior adductors increasein size and their lateral sides fasten to the inner sides of the collar folds by' thin ligamentstherebv dividing the collar pocketsinto dorsaland ventral pafts (Fig. 34B). Further posteriorly'the bridges attach to the outer sides of the funnel retractorsand the separated adductor bundles merge into single muscular layersthat attachto the lateralrnantleri'alls behind the stellateganglia (Fig. 3aC). Thel are situatedso lorv in lelation to the visceral sac that should be 'anterolateraladductors'. termedmore correctly'the The median mantle senturr consistsof tr.rothin

adductormusclesrunning along the lateral sidesof a gelatinouscore containingthe rectum, vena cava. mantle arlery and the duct of the ink sac (Fig. 34B.C). Anterior extensionsof the adductorsform a lorv ridge that extends anteriorly forming part of the dorsal funnel wall and the ventral side of visc e r a ls a c ( F i g . 3 a A ) . The muscular portion of the funnel consistsof one ventral and two dorsolateralmuscular walls (Fig. 3aA). Boundaries between these walls are marked by the junction of muscular fibers of different orientation.The collar folds originate from the lateral rvalls of the funnel, pass alongsidethe visceral sac and attachto dorsolateralwalls of the mantle. The funnel retractorsare thick and wide. The;" attach to the visceral sac along their dorsal margins.while the ventral margins hang free inside the mantle cavit;- (Fig. 34C.D). At the sites of attachment to the stylets. the funnel retractors are oriented obliquely from dorsolateralsides of the visceral sac to the dorsomedialsides of the stylets. which are situatedlow on lateralwalls of the mantle (Fig. 34E). The stylets are much thicker than the musclesattachingto them. The mantle attaches to the dorsaland ventral sidesofthe styletsleaving rvide break on their outer surface (Fig. 34F). The gills attachto the mantle wall ventral to the stylets. COMMENTS. The stylets in Alloposus are unique among octopodsin being soft. gelatinousand unusually'large. Such structurescould not provide support for the funnel retractors and apparently serve as a hydroskeleton.variable in shape but constant in volume. betweenthe major musclesof the bod;,. Reductionof the styletsin Alloposttswas apparently stipulatedby the loss of jet-swimming. However. the presenceof a rvell-developedfunnel locking apparatusin Alloposus suggeststhat it is derived from a more muscularancestor. Another characteristic feature of Allopostts rs the presenceof a hydrostaticorgan. which is reported here for the first time. Until now. hydrostatic organ of sirnilar structure was repofied only for Oct'thoe IPackard. Wurtz. 1994]. The presenceof hydrostaticorgan implies Ihat Alloposus can attain neutral or near-neutralbuoyancy passively. Development of a nerv septum between anterior dorsal adductorsand the collar folds may suppoft the anterodorsaladductorbridge.

TremoctopodidaeTryon, 1879 TremoctopusviolaceusChiaie, 1830 or blanHABITS AND HABITAT. Tremoctopus. ket octopus.is an epipelagicoctopod inhabitingtropical and subtropicalsurface waters of all oceans [ T h o m a s . 1 9 7 7 : N e s i s . 1 9 7 5 : 1 9 8 5 ] . F e m a l e sa r e larse.up to 500 nrm ML:the malesare drvarf.about

Shell in Vampyropoda

5l

15 mm ML. Direct underw,ater obseruations showed that this animal can jet-swim [Young, 1995]. In othercasesTremoctoptswas foundswimmingnear tl-reshallowoceanfloor with its long dorso-lateral arms and web spreadwide apart [Mangolde/ a/., 1996a1.

Right

SHELL MORPHOLOGY. The styletsare straight, thick and relativelystiff sausage-shaped rodswith slightlypointedends(Fig. 35). They lie on the Iateral sidesof the mantle(Fig. 36A,).Distancebetrveenthe anteriorendsof the styletsis about45% ML. The styletsconsistof carlilage-like chitinthat is laid down by concentriclayers.The centerof growth(initialshell)is situatedin anteriorl/3 of the stylets.Lengthof the styletsis aboutl/6 ML. Each styletis slightlycompressed in its middlepafi and somewhat swollenin its anteriorandposteriorparts (Fig. 35A). The bendis absent.The surfaceof styletsis smooth.The greatestwidth is situatedin the posterior1/3and comprises approximately 18%of theirlength. MICROSTRUCTURE OF THE STYLETS. Crosssectionsin the middle part of styletsare roughly oval in shapeandconsistof numerous regular,concentric.translucent layers(Fig. 35C).The centerof growth is situatedapproximately in the middle of the section.Contoursof the growthincrements are sirnilarthroughoutthe section.indicatingthat the stylet shapedoesnot changesignificantlyduring growth. Growth zonesare absent.The width of growth incrementsrangesfrom 7 pm to 15 prm, averaging 9 pm. First-order increments aregrouped into second-order cycles.from 5 ro 32 increments in onecy'cle. EXTERNAL MORPHOLOGY OF FEMALES. Body is dense,muscularand smooth.Mantle is elongated, roundedposteriorly(Fig. 36,4).Anterior dorsalrnarginof thernantleformswidetongue-shapedprocess. projectingto the levelofeyes.Ventral antefiormarginof the mantleis even.Mantleaperture is wide; its lateralmarginsare situatedabove the levelof eyepupils(Fig. 368). The positionof the styletsis visible on intactanimalas a pair of longitudinal grooveson lateralsidesof the mantle. Dorsal arms I and ll are very long (n-rorethan 2 timesthe mantlelength)and connected by a large interbrachial web.Ventro-lateral armsIII andIV are muchshofterthanthedorsalonesandnot unitedby the web. A pair of water poresis situatedat the basesof dorsaland ventralarmsleadinginto large subcutaneous cephaliccavities.Funnelis long and tube-like,embedded in the headdorsally.The nozzle of the funnel is free, narrowand situatedanreroventallyfrom the eyes.Funnelcornersarefolded outwardandform funnellocking-apparatus that fits into corresponding pocket-likeslitsin the mantle.

B

c

FIG. 35. St1lets in Ttremoctopusviolaceus. A. Dorsal vier.v of a pair of stylets fiom immature feniale (60 mm ML); anterior end is up. B. Lateral vier.v from inner side of the right stylet (ventral side if on the lelt, antenor c-nd is up) Arrows indicate thc plane of the cross-sectionshor.vnin 'C'. C. Cross-sectron of the right sf'let (dorsal side is up: outer side is o n t h e l e l t , 1S. c a l eb a r s l m m . PHC. 35. Clulersr Ttremoctopusvirtlaceus.A. Bur c cropoHbrnapbrcrilJeron ne:pe;oii cauxH ,to-pcanbHoti (6_0nr,r [M): nepe,ruu cropoHa uaaepxy. B. Br.,t c6ox1' c auvrpeuneil cropoHbrrrpaBorocrn.'rera(eeHr_panLHa.f, cropoHa cneBa;rlepe,IHHfrKorreuuanepxr.). LTpe,rKHvKa3r,rBarorno.rroxeHuecpe:a. n:odpaxeu_ Horo Ha sulle 'C'. C. flonepeuHsuicpe: rrpaBofocru,rera (nopcanbHarcropoHaHaBepx);BHeilHrr{cropoHa c;reea).Macmra6: I I,rrvr.

CRO.S,S-SECTIONS OF FEMALES. The mantle wall is thick andmuscular.Its outerandinnermuscularlayersareseparated by a thin layerofconnective tissue(Fig. 37).The lateralwallsof themantle areslightlythickerthanthedorsalandventralwalls.

52

V. A. Bizikov

FIG.36. General anatomv of Trentoctopustlolaceus (immature female: 57 mm lt'll-). A, Dorsal vieu. B. Lateral vle\\ (shown in Fig. 37). Scalebar - I clTl. Bold arro*s *ith numbersindicatethe planesof conesponding cross-sections PI4C.36 C'rpoeuue Trentoctopustiolaceus (He3pe.rarcarrira:57 rnr I|\,l). A. Bru c .ropcansHoficropoHbr.B. Bur c6ox1 Crperxu c un$parlr )Ka3brBarcrrro.roxeHuecoorBercrB\roruu\cpe3oB(noxararrsrrra Puc. 37). Macmra6: I clr.

Dermis is thin and smooth. The mantle cavit\ is relativell' small: the dorsal part is larger than the ventral one. The visceral sac occupiesabout 2/3 of the rrantle cavitl'. Digestive gland is not divided posteriorl)'and occupies most of the visceral sac anteriorl)'.Ink sac is large. triangular in cross-section. embeddeddeep into the digestivegland from v e n t r a l s i d e ( F i g . 3 7 8 - D ) . A h v d r o s t a t i co r g a n i s presentin the middle pafi of the visceral sac on its dorsal side. It is situatedposteriorto the digestive gland and above the stomach and has the shapeof a wide. flattened.muscularsacu ith numerousbranc h e d m e m b r a n e sp r o j e c t i n g i n s i d e f r o m i t s u a l l s ( F i g .3 7 E ) . The head retractors are thin and u ide. Thev form the muscular lateral ualls of the visceral sac and almost merge dorsalh and ventralll (Fig. 37A.8). Posteriorll the head retractorsgradualll become thinner and final11 disappearat the level of the stellateganglia. In the region of the funnel the head retractorsconsistof inner and outer layers rvith different orientation of their muscular fibers

(Fig. 37A). The pallial nerves occup)' position betueen lavers of the head retractorson the lateral s i d e so f t h e v i s c e r a ls a c .A t t h e l e v e l o f t h e c o l l a r fblds. the outer muscular layer of the head retractors branchesoutuard and forms anterior the anterodorsal mantle adductors containing the pallial n e r v e ( F i g . 3 7 B ) . U n l i k e A l l o p o s u s .a n t e r o d o r s a l adductorsin Tremoctoprlsare not connectedwith the collar folds. Anterodorsal adductorsattach to the mantle imrnediately behind the funnel (Fig. 37C). At the sites of attachmentthey are thicker and more muscular. The lateral end of each anterodorsaladductoraftachesto the lateralmantle $all uhile the medial end attachesto the ventrolateral side of the visceral sac. close to the funnel retractors. The stellate ,eangliaare situated below and posteriorlr the sitesof attachmentof the anterodorsal adductors. Ventral median mantle septum is thick. muscLll a r a n d Y - s h a p e d i n c r o s s - s e c t i o n( F i g . 3 7 8 . C ) . V e n t r a l l r t h e s e p t u mi s c o r n p o s e do f a s i n g l e .t h i c k adductor muscle that attachesto the mantle uall.

Shell in Van.rpyropoda

,

53

,1,)(

/'ti

"/f'$ ./

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brgl hydr

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rl

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irlG 3T Schematiccross-sections of the soti bodl ^ot' .Trenoctopus t'tolacetts(immature female: 57 mm ML) A. Section 1. at the level of the funnel. Il. Secriori:. ueirinJ ine"i;;;.1."b Secrion3. ar rhe ler.el of anreriordorsal mantle adductors l). Section'1. behind dorsal mantle tr'.'rt.rr.; i"'igir.r'e. Secrion5. ar rhe 1,1i";i;rtlGi:;i level of afiachmentof the lunnel retractors.Positionof "r sections'isindrcateo on Fig, 36. Scale bars : I cm. I'l'1c 37 cpe:rt rtrl xoro re.ta Trenoctopust'iolacetLs (He3pe.rar car.rxa:57 rrrr ,il\{). A. cpe: l. ua r ponrreBopoHKH. B. Cper 2. ro:a-tu BopoHriu.C Cpe: 3. sa rpoBHe rrepeJHu\ .topca_tbt{brr rrasrnlisrix a-Lt}.I(ropoB. D. Cpe.r:1. no3al''lopca"rruux tt'ttttttiir:]:.Til1:!"8 {Ha \poBHe3Be3rqarbr\raHr.rnt-e).E.4;.,-5. riil'poo,,. npu.perr.reHH, p e r p a K r o p 0 B O p O H K lUl o. . r o x e s r . r cep e 3 o B\ K i u a H o H a p u c . 3 6 . \lacur-rao: I c\{.

V. A. Bizikor

lrq ..

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Er-=.-: :

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t otn' "'',',,,.--'

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

:

I

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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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's'*

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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

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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

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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

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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

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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

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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.

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\'

.\. 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<*

18

Thickness of stl lets (in 7o of st1'let length)

66

l6

l.+

Anterior shoulder length (in 7o of st1'let length)

33

33

33

10

33

33

Angle betrveen shoulders

1'10'

I25"

112"

121"

13 5 0

I 80'

sculptured

smooth

Surface of angle Consistencv

stiff

soft

sculptured moderately soft

smooth

smooth

smooth

soft

gelatinous

moderatell soft

Remarks:asterisk(*) marks position of stl lets on lateral side of the mantle. In these casesdistancebetrveensnlets is equal to the mantle uidth. flpurreuaHue: (*) norreveuul crfiJerbl. pac|Io"toxeHHbteHa 5oxoertx cropoHax ]IaHTul4.B lrnx c,l)'qatx paccrotHHe Irex.I)'

HHN,Ilr COOTBeTCTB]eT [IHpHHe

]laHTHH.

boderaet Okutani. 1986) has the gladius with markedly weakenedmedial parl and thickenedsigmoidal lateral wings (Fig. 49 I). Such a shape of the gladius is unique among recent octopods.but it is strikingly similar to the gladius of fossil Palaeocopus nev,boldi(Woodward. 1896).the earliestincirrate octopodfrom the late Cretaceous(Fig. 55E.F). Another congenericspecies.C. hochbergrO'Shea. 1999. has the gladius with long rod-like lateral wings. rvhich diverge in a V-like pattern and are distinctly'bent in their distal parls (Fig. 49E.F). The bendof tlre wings in C. hochbergiapparently'marks the placesof attachmentof the funnel retractorsand correspondsto characteristicbend in incirrate sty'lets.Gladii of C. antarctica and C. hochbergi illustrate hou the transforrrationof cirrate gladius into incirratesty'letscould happenin evolution. Butterfll-like gladii of CirroteLttftisand Citothatnta representthe rnost evolutionarl' advanced stage of the shell in Cirrata. Flared lateral \\ines providing support for the fins. become the most prominent element of the gladius. The saddle is very narrow and deep.The funnel retractorsdo not contact rvith the gladius. but attach to the mantle rvall. Incirrata Of the genera examined.Enteroctoptrsappears to be the most prirnitive in respectto the shell as it is the genus rvith the most u'ell-developedshell and associatedmuscles;the shells of all other ge-

nera appearto be derived via reduction.The characteristicsof the Incirratathat are consideredto be primitive and perlinent to this study are the follow i n g ( T a b l e2 ) : 1. The shell is reducedto a pair of stylets each u'ith a shell sac. The stylets are thin carlilage-like rods with pointed ends lying on dorsolateralside of the mantle at sharp angle to longitudinal axis. Each stylet is bent in its anterior part into obtuse angle with the apex directed inside the mantle. 2. The styletsgrorv by concentricincrementsof cartilage-likesubstancewith the center of grorvth (initial shell) for each stylet in its bend. 3. The styletsoccupy subterminalposition.The mantle attachesto the stylets along their entire periphery. Both anterior and posterior ends of each sty'letare embeddedinside the mantle wall, rvhile the middle part occupiesa superficial position. zl. The funnel retractorsattach to the inner sides in the anterior half of the stylets. At the sites of attachment the st-vletsmay' be bent inu'ard. 5. The head retractorsare thick and muscular anteriorly. but become thinner posteriorly'.At the level of stellateganglia.the outer layersof the head retractors branch off the visceral sac forrning the anterodorsalmantle adductors.Each adductor exh i b i t s a t r v i s to f a b o u t 1 8 0 " . 6. A dorsalmantle cavity extendsfrom the nuchal region to the level of posterior margins of the st1,lets.Dorsal and ventral mantle cavities are broadly' confluent on lateral sides of the visceral sac

Shell in Vampyropoda

73

N :\\\

S-'\.rr\\

2))))l)\)l :

\:,--l

-:,

lll /

/

FIG

NIorp-hological rariability of the shell remnants - Enterocropustlofleini (\\,ijlker. .5.0-. -(stlle!) in Incirrara..\. B l 9 l 0 ) . C . D - B e n t l t o ' r o p t t s . s t b r r i c u s ^ L o r n i1n9- e 3 .0 .E . F - B a t h t p o h p u st " t r o i i i , t i s r " i u r i . r s z o t . c . H Trentoctopus t'iolaceusdellc Chia.ie.l83U i.J -- Eledoneilpsstae rroii. iSO+ K - .1tt;p;;;s nrollis Verril. lgg0. A. C. E and G - rentral r-ieri of a pair of sr-iletslanterroi end is donn). I - dorsal'rlieri.of pul1u oi rt1,i.t, (anterlorend tn do$n). K tnner lateralrie$ o1--apair of strlets (rentral sides of both strlets face inside:anterior end is doun) B.D.F. H rind J lateral rrerr lanteiior cnd is dorin: renrral side is on ihe iigtrt). A.B: scale bar - I crn. C - K: scale bar - I ntrr. All ligures madc b1 the author.

PllC-. 50. ;L1op(to.torH,reglgc (prfurrerrros paxoBuHbr) uHuupparHLr\ocsrrHHoroe. A. fTi.9g,"pa3He B E n t e r o c t o p . udso 1 / e t r t(t\ \ u l k e r . l 9 l.napH^br\_crH-rcrots 0). C. D_ n- Li nog1. f S j d . E . r Batl*poltptLs , , B e n t h ' ' o i t o p u s . s i b i r i c u s salebrosus(Sasaki-1920).G- H^-. Trenroctopustiolotetts delle Chia.;e.1830 I:J -- Eleclonenlessraevoss. 196.1. K 'lllopostts ntollis Yerril. 1880. A. C. E u G BH-r-c BeHrpa.rbHoii cropoHsr(neperur.r cropoHa nHnry.).I BH.l c .lopca-]LllollcropoHt'l-(nepe-lHttcropoHa BIIn3)). K - snl napbr c-rH.terosc5oxr (n:H1rpn): BeHrpa-lr,Ha, ' cropoHa oSoux cru-reron oSpaueHaBH)rpb: rrepefrrqqcropoHa sHn:lr. B.D.F. FI s J' .Oirn1 tniper"r, cropoHaIlHlJ3\':BeHTpa.lbHat cropoHacrtpaaa).A.B: rracurra6= I crr. C - K: rracurraS: I "r^r rrrr. PHciuxu iuropa.

-7

1

V. A. Bizikov

anteriorly and posteriorly to the anterodorsaladductors. 7. The stellateganglia are set uidely' apaft ll ing on the inner surfaceof the mantlejust lateralto the attachmentsites of the anterodorsaladductors. 8. The anterodorsalmantle margin is fused uith the head. Q T l r e " . ^ o ' ' - a . o i n S O f t h e C O l l a rf O l d Sa t t a C h to the mantle. 10. The fins are absent. COMMENTS. Relativell' long. stiff. moderatell' thick and distinctly'bent sty'letsof Octopodidaeapparently representthe most primitive condition of incirratet,'''peof shell. Such styletscould be evolved directly'frorn primitive gladius of cirratetype tlx'ough leduction of median transversal connection (saddle).In benthic shallorv-rvaterEnteroclopus the stylets are stiff. rvith r.vell-developedsculptured bend (Fig. 50A.B). The stylets in Enteroctopusare the largestamong Incirratareachingup to 30 o/oN4L (Table 3). In deep-seaoctopodidsthe sty'letsdecrease in size. become softer and sometimessmooth. In Benthoctopusthey retain considerablethickness ( c a . 1 6 o ho f s t l l e t sl e n g t h ;T a b l e 3 : F i g . 5 0 C . D ) a n d rvell-developedbend. but lack sculptureand become soft. St.vletsof Bathy,poltpils occup.vintennediate position between well-developedstyletsof Enterocloplts and reduced ones in Benthoctoptts(Fig. 50E,F). The stylets in Eledone are ver)1 narrow (their greatestwidth is about 7o/oof their lengthl. soft. smooth and almost straight(Fig. 501.J). Among pelagic octopods of Argonautoidea cladethe styletsare found in two primitive families only: Alloposidae and Tremoctopodidae.In both casesthe)' shorv signs of deep reduction. ln Alloposas the stylets lost stiffness and became gelatinous. water-rich and inflated (Fig. 50K). As a result, rvidtl-rof the stylets in Allopos us reaches46%o of their length. the greatestvalue among Incirrata. In Trentoctopasthe st1'letsare straight. moderatell soft and smooth (Fig. 50G.H). Attachment of the funnel retractors shifted torvard anterior end of the stylets.resulting in reductionof the bend. In Oq'thoe and Argonauta the stylets disappear.leaving just srnall mantle cartilagesin placesof attachrnent of the funnel retractors.Pelagic octopodsof Bolitaenoideaclade also lost the stylets. Remarkably'. redr"rction of st1-letsin both pelagic clades (Argonautoideaand Bolitaenoidea)did not result in transformation of their muscular arrangement.which remainedgeneralll''the same as in benthic Octopodidae. Homologies of the shell among Vampyropoda The onl-v evidence available for determining the homologiesof the shellsamon-qthesetaxa restsu ith

the position of the fin and the sitesof attachmentof the mantle rnuscleand the head and funnel retractors to the shell sac (Fig. 5l). Sincethe ancestral incirrateshad fins as testifiedby the presenceof fins in Paloeoctopusnert'boldi (Woodward 1896). we assumethat recentfin-bearing cirrateshave a shell that is closestto the ancestraloctopod shell. The paralarval fin in Vampyroteutlris lies over the u'ings of the gladius.We can assurle.therefore. that the wings and the region of the shell (rachis) betrveenthem evolved into most of the cirrateshell as the cirrate fins occupy much of the dorsolateral surfacesin the cirrate rvings. ln Vampyroteuthistne mantle muscle attachesaround the periphery of the shell (rachis.lateralplates.wings and conus)except for the anterior free end of the rachis (Fig. 5lA). In the primitive cirrate the same situation occurs although without a gap to representthe free end of the rachis. Presumably.all of these regions contributed something to the cirrate shell. In Vampyroteuthisthe headretractorsattachto the lateralplates ofthe gladius and the funnel retractorsattachto the a n t e r i o rr e g i o n so f t h e r . ri n g s . In cirrates the head retractors attach to the periphery' ofthe rvings and the funnel retractorsattach to the anteroventraledges of the wing horns (Fig. 5lB). This confirms the homology with the lateral plates and anterior wings of Vampyroteuthls.but since the muscle attachmentsto the cirrate shell do not maintainthe samepositionalrelationships.furlher refinementof areasof homology is not possible. The evolution of the incirrateshell from the cirrate-typeshell involved the loss of the saddlelpresumabll, mostly rachis-homologue)and a general decreasein the size of the remaining pans. In the incirrate stylets.the funnel retractorsattach to the bend and anterior shouldersof the stylets wl-rich, presurnably.are the homologuesof the horns in the cirrategladius.rvhile posteriorshoulders,rvhich are embeddedin the mantle. representthe remnantsof l a t e r a lr v i n g s( F i g . 5 l C ) . The octopod shell may' be mostly the homologue of the gladius hypostracumas the cirrate shell has thicknessand consistencl'similar to the hy'postracum in some teuthoids. The process of shell transformation Here we explorethe stagesin the transformationof the shell and the formation of the dorsal mantle in Vampyropoda.The gladius in Cirrata apcavit,v-' parentl)'evolved through the reduction of the free rachis and conus and the loss of the rostrum. The anteriorloss ofthe free rachisrvould expand dorsal spacebetu'eenthe free mantle margin and the nuchal cartilageto form a nuchal cavit.v.Such a cavitv presently'exists in Spirula due to the loss of its proostracum and the expansion of the muscular

Shell in Varnpyropoda

75

A

-t

\,\4,

/{tj

ili,\

/,/" f

$

# rin-ffi\ ' m n - ,'-^.\

r'

C

- n.' \' .

\d'

6, ll

l \i\/

\1

--1.l mn/ {+ 1:f .t!

$: tttt..,trrl:l:.|]e L.

( /a/r/)i15.

illustratinsaftachment of main musclesto the shellin Varrprropoda.A. L'antp)rorettthis. ts. opisrhoreuthi.;

l-eft coiurnn: A.C - tentral rieu (antenor cnd is up): B - dorsal rieu (anterror '-^ end rs un). R i _ s h rc o l u m n : l a t e r a l r i e r r f i o m t h e l e l i s i d c ( d o r s a i s i d e i s o n r f r . i i g t i i PHC 5l Crcrra.H-l"lrccrpHp\rcua.c|IptlKpen.reHHe\ibur]uKpaKoBHHeVamprropoda.A. I'antpt,roteutltis.ts.Opislhoteuthis. C. Octctotts. ilesaq rio.rotltia:A.C B I l r c B e H r p a - r b H o r -crr o p o H r , r ( t t e p e . ] H r l i i x o r r c u H a a e p r l BlrJ c Jopca.rrHoil c'opoHsr ): B ( r r e p e - t l r H t ix o H e t t H a s e p x r ) . l l p a n a l K o . t o H K a :e r u i o o x . c . r e e o r j c r o p o H b r ( - t o p c i r t b H a l l c r o p o H a c n p a B a ) .

V. A. Bizikov

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I-lG. 52. Diagram shouing attachmentof the head retractorsin difl'erenteroups of Vamprropoda.A. I'amptroteuthis. Dorsal r ieu (the mantle is shosn transparent).Arro* s indicate dircction of h1potheticaltranspositionof inner anteriormargins of the head retractorsduring reductionof the middle plate of the gladius.B. Grintpotertfirs.Dorsal riew (the mantle is sho*n transparent). C. Octopus.Dorsal rieu (the muscularmantle is cut off to show attachrnent of the r isceral sac to the mantle). Abbrerialions: IA. inner anterior margins of the head retractors:C)P. outer posteriormargins of the head retractors:sh - shell (eiadius or sn lets): dmad - anteriordorsal mantle adcluctors. perpiuropoBro-roBr,r Ozu.ru""r,J*ynnn Vunrpyropoda. Pl4C. 52. llptrxpen-reHne A. I utrtptroteutltis. tsn: c .topca-rbHor-r " Crpc.rxu \Ka3LrBalornarrpaB-rcHue cropoHbr(\raHTurlr:o5paxeua nporpavHoii). runolcrHqccKoroc\lerucHHrnepe.tHero Kpat perparTopoBfo.roBbrfrpli pe-t)Kunn \reJfia-rbrrorln.racluxrr r.raLrrlca. B. Grintpoteuthis.Bru c :opclr-rrrioir cfopoHr,r(rrarlrnr n:o6paxeHa rpo:pauHor'i).C. Octoptts.Bu: c:opcanrHoii cropoHu (-topca-rbHarcreHKa\raHrriu noxa3arbKpen.reHrie Bucuepa-rbHor-o \reulKa).)'c.rosHsre o5o:saqesxq:L\. nHrlpeuHnerepe.lHueKpaq ).tarerri1..rro5sr perpaxTopoBfo"roBbr:OP. eHerxHle3atHHcKpa.cpcrpaKTopoB ro.roBr,r:sh - paxonuHu (r','ratn\c n.rH clu.r!'r'br):dmad nCnd.lHHC .tOf\CiLIhHl-lC \tJHIHIlHblC

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mantle dorsalll' to form an anteriormuscularc) lind e r f C h r - r n1 9 1 0 - 1 9 1 5 ] I. n o c t o p o d s .f u s i o n o f t h e dorsal mantle mar-qinand head uould create the dorsalmantle cavit\,. Reductionof the conus resulted in the developmentof posteriormantle u all that forms the dorne-shapedposteriorape\ of the bod). T h i s d e v e i o p m e n tr e s u l t e d i n U - s h a p e d c i r c u l a r musclefibers ri ith endsattachedto the cirrateshell. Further clues to the transforrnationof the shell and the formation of the dorsal mantle cavitv are

found in the characteristictu,isting of anteriof dors a l a d d u c t o r si n I n c i r r a t a( F i g . 5 2 ) . T h e i n n e r m a r gins of the head retractorsin ['amptroteLrhis allach t o t h e g l a d i u sa n t e r i o r l l t o t h e i r o u t e rm a r g i n s( F i g . 5 2 A ) . I n C i r r a t a .r e d u c t i o no f t h e m i d d l e p l a t e i n the gladius causedtranspositionof the attachment sitesofthe headretractorsto inner surfaceoflateral u i n g s o f V - s h a p e dg l a d i u s( F i g . 5 2 B ) . A s a r e s u l t . the attachmentof the head retractorsbecarnelnvert e d : t h e i r i n n e l r n a r g i n sa t t a c ht o t h e g l a d i L l sp o s -

Shell in Varnpyropoda teriorly frorn the outer margins. Finally'.in Incirrata head retractors formed the anterodorsal adductors. rvhich attachto the mantle w.allanteriorto the shell remnants(Fig. 52C). But orienrationof the attachrnent of theseadductorsremainedas in the Cirrata: the inner margins of the adductorsattachedto the mantle rvall far posteriorh, from the outer margins giving the adductorsnearly a 180" tr.vistin a clockr.r,ise (left adductor)or counter- clockrvise(right adductor)direction. It seernslike the anterodorsal addr-rctors in Incirrata.having lost connection*,ith the shell. retainedthe former orientationas if thel are still attachedto the gladius of cirrate type. Apparentll,,at some stage of incirrate evolution expansionof dorsal mantle cavity' resulted in for_ mation of tu'o dorsolateralepithelial septapasslng from the stellateganglia tor.vardthe sites of attachuient of the funnel retractors.As the exnansion continued.these septa uere perforated.and dorsal and ventral parls of mantle cavity' merged together in the branchial region isolating the anterodorsal adductors.According to Naef 1192111923: p. 65g1. lepetition of this processcan still be traced during ontogeneticdevelopmentof 1,oungOctopus. Iladicalreductionof the gladius of teuthoidtvpe into a U-shapedstructureis not unique for Cirrata. S i m i l a r r e d u c t i o no f t h e g l a d i u so c c u r r e di n r e c e n t m esopeIagic oegopsi d squid B a t h ctt h a an a lyt.onutta Chun. 1906 (family. Cranclriidae.). ln Bdrltotl.tatuna the rachis separatedfrom the conus and reducedto a nan'o\\' and feeble needle-like rod embeddedin anteriol dorsal par-tof the rnantle(Fig. 53). Ventral paft of the conus lost completell, and the dorso-la_ teral parts unfolded into U-shapedplate providing suppol-t1br the fins on posterolateralsides of the m a n t l e ( F i g . 5 3 C ) . A t t h e f i r s t g l a n c e .t h e g e n e r a l morphologicaldesignof Bathothauma doesnot differ frorn that of Cirrata.However. the principal differenceis a position of the stellateganglia that are set close and connectedto each other in Bathotha_ unta and u,idely separatedin Cirrata. The fact that all other representatives of familt,Cranchiidaehave t1'picalteuthoidgladii indicatesthat transforrnarron of gladius into U-shapedtransversalplate in Batltt,ttltaumaapparentlyr,rasa result of a sinsle structural mutation rather than a gradual evolutionart trend. Palaeontological evidences According to the opinion currentlv accepted by many paleontologists.extant Vampyrornorphida and Octopodaorigin frorn "Fossil Teuthids": a prirnitive group of Triassic - Cretaceouscoleoids. rvhichhad gladii u'ith parlll' decalcifiedfive-par.ried proostracum IBerrhold, Engeser. 1987: Engeser. B a n d e l ,1 9 8 8 :D o 1 ' l ee r a l . 1 9 9 4 :H a a s .2 0 0 2 1 .R e markablediversitr of the rnorphologl of the gladii

71

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FIG.5.3 Pelagicsquid Bathothaumalyroma Chun. 1906 (adult female: 192 mm DML). A. Dorsal vierv. B. D o r s a lr i e u o f r h e g l a d i u ss h o r r n g i l s s e p a r a t i oinn t o t\\o parts: anterior axial rod (rachis) and posterior transversalband (unfolded; representingthe remnant of conus and conus tields;. C. posteri6r part of the mantle from the lateral side. Scale bar -^l cm. PHC. 53. Ile.raruqecxuii Kanbt\tap Bathothauma lyromct Chun. 1906 (r:poc.tar cavxal 192 rvnrAM). A. Brzr c :opcanrHoii c-ropoHbr.B. Bn,l r.'ra.{ilycac ropcarb_ Hoii cropoHbr.I-.raanyc pa3leneH Ha .lBe qacru: ne_ peJHrorooceB),rcrrJacrhHKv (paxuc) tr 3arHrorc no_ rrepeqH)'ro n.[acrHHK!' (pa:repuyra). rtpe.ncraBnr]o_ ur1rc co6oii p).tulreHr KoHycan ero r|.raion). C. Brz;r 3alHei .lacru vaHTHrzc6oxy. Macurra6 - I cu.

in "FossilTeuthids"indicatea greatvarietyof life st)'les(Fig. 54). Phylogenetical affinity of .,Fossil Teuthids"to eitherOctobrachiaor Decabrachia has been controversiallydiscussedfor many years. Someauthorsassigned someof theseformsto tenarmedTeuthidaon the basisof similarityof their gladiiwith thoseof recentsquidsandindistinctirnprintsinterpreted astentacles[Naef, I 92111923: JeIetzkv,1966;Donovan,1977;1983;Vecchione e/ a/. 19991.Othersassignedall "Fossil Teuthids"to ancienteight-armedVampyromorphida on the basis of rareand indistinctimprintsinterpreted asthe eight armsunitedby interbrachial web,uniserialsessile suckerswithouthomy rings,two rows of cini alonglateral edgesof the oral surfaceof the arms and nvo

V. A. Bizikov

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J\/ FIG 5-1 Gladii of Jurassicand Cretaceous.'Fossil Teuthids".\. Geoteuthissintplex(Voltz 18.10)iiom late.lurassic ('l'ithonian).B. Paraplesioteuthis (N,Itinsterl8]3) liom late Jurassic(Tithonran).C. BoreopeltissagiuLtto sagttttLtcr (\ael'. 1921) fiom late .lurassic(Tithonian).D. Plesioteutlisprisca (Rtippell 1829) tiorn late Jurassic(Tithonian). F,. .\laioteuthisntorrctertsis Reitner et I-.ngcser.1982 liom earll Cretaceous(Barremian\.F. Loligoseptaaalensis (Zieten.1830)fiom earlr JurassiclToarcian|.G. .\lastigopltora hret:rpinnis Onen. 1856fiom middlc Juiassii(Callovian). H. Trachitettthis hasti-forntes lRLippcll.1829) fiom earlr Jurassic(Toarcian).l. Teudopsissubcostata(\4unster.l8-13) tiom earlr Jurassic(1'oarcian).L Leptoteuthisgigas \Ie1cr. 183-l tiom carlr Jurassic(Toarcian).K. Celaenoconica Nliinsterl8-12from earh Jurassrc(Toarcian).L. Puluectloligo oblonga \\'aener (1860) fiom earlr Jurassic(l'oarcian). M. .\[orekitesvitrorensis(Fritsch. l9l0) tiom earl] Cretaceous(Barrcmian).\. Eoteuthoidescaudctta(Fritsch. l9l0) lrom earlr Cretaceous(Barremian).'l-hegladii marked br asterisksrepresentposslbleancestorsof resentVamplromorphidaand Octopoda.Thc rest gladii belone to representatires of other coleoid lrneages.A. B. D. F. ll. l. J. K and L alier Nacl-. 1922: C aiter Enseser.1986: E - atier Reither. Enseser.1982: G after Donoran. 1983: Nl. \ after Kostak. 2002.

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FIG 55. Rcconstructlons of fossrl octopodsand rarrpvromorphs.A.B ProteroctopLts riberr Fischer et Riou l9g2 liorn rniddlc Jurassic(Callorian). C.D I'ampt:ronassirhodanica Fischer et Riou 2002 hom middle Jurassic (Callorian). E.F Paleoctop_us ne,vboldi 1\\'obdriard 1896) from late CretaceouslCampanian).A. C lateral vrerv. B.D. F - dorsal riew. E - shell remnants(st\lets). A-B - after Fischir. nl"r.-is8i.-'C.u atter Fischer. Rrou. 2002 E.F after Haas. 2002. Phq^:: PexoucrprK_uHH HcKoraeltbt\ocb\rHHoroBH BallnHporrop$.A.B Proteroctopusriben Fischer et Riou 1982 n: cpeluefr H)psr: Ke.r.roneiicxniieex. C.D I'aip_t,rinisso. rhctdanica Fischer'et Riou 2002 Laz +.r".1 K)pu: Ke-r:roqciicxuii. ser E.F Paleocropusnevbolcli (iVoodqard 1896) u: no3JHeroMe-ra: Kar.rnaHcKnii sex. - BH_t.c.topca-rsuoii .\. L Bri-lcoori\ u.u....1_ cropoHbr.E p.:urresrbr paxoBuuLr(crurerrr). A.B u: Fischer. Riou. 1982 C.D- H: Fischer.Riou. i002 E.F n: Uaas. ZCi02-

pairs of fins [Bandel. Leich. 1986; Doy.leet al 1994; Donovanetal.2003: Fuchsel a1.20031. The presentstudl' of the shell-softbody relationship in recent vampire squid and octopodsprovide ner'v data for phylogenetic comparison between extant and fossil coleoids.Reduction of the middle plate in the gladius of pre-octopodsdid not change position of the stellateganglia that remained lying on lateral sides of the mantle posteriorlv frorn the funnel folds. Wide separationof the stellate ganglia in all recent octopodsrepresentsconclusive evidencethat this group evolved from some vampvromorph ancestorswith rvide middle plate of proostracum. The forms rvith narro\'!'middle plate of proostracLuxlike Plesioteutltis.Celaeno.

palaeololigo, Eoteuthctiesand orherscould not pos_ sibll be ancestorsof recent Octopoda. as all of thern apparentlyhad the srellateganglia set close to each other. The fbrms lvith wide middle plate of proostracum (Loligosepia, Trachitetrhis, ieuclopsis.Leptotetrthis,etc.)iould possibly belong to oitopodian evolutionarl, stem. Among theie. the forrns like TeuclopsisMr,nster. 1g42 (familv Teudopseidae)from the early, Jurassic(Toarcian). in rn! opinion. seemsto be the most likelir ancestors of recentOctopoda.as they had wide thick gladius with partly reducedmedial plate (Fig. 54 I). The fossil records of undoubted octopods and octopod-like vampvromorphs are extremelv rare. Only three fossil octopod species.proteroctopLts

PIjC 54. f.ra,lu)'cst.top*cKHX 14\te.roBbr\"Hcxoflae\rbr\Ka-rb\rapoB". A, Geoteuthrs sintpler (Voltz 18,+0):rro:rHrr K)pa: Turoscxnii serc'B. Paraplestoteuthissagittata (iVliinsterl8-lj): no::Hss IOpa: TuroHcxrri sex. C. Bor:eopeltis ,ngitt'ntn (Nael 1921): ilo3JHtt [Opa: Turorrul.rii eex. D. Pl,e^sio^teuthis prisca thrippell fS:9f no3-rn"r tOpa: ruro-ncngii -i ser. E llaiolettthis ntorroensis Reitner et En-sesrr. 1982: pauur.rii\'{e"r: Eipperrc^uli'rex. 7 olig'osepicrartlensis (Zieten.1830)lpaHnqq.IOpa-: Toapcxlt:iaex. G-,\^lasrigophor'o-bretipinnts O"iir. rSi6,.p-i"tr topul x.i..rro"eiicxuii sex. IL Trachitettthisl.tasttforntes(Rrippell. 1829): paHHqqIOpa: ioapcxHir eex. I. Teticlopsis,r,brortotn (Miinster. 18'13);paHHrn lO^pa:Toapcnli u.^._i.' Leptoteurhiigrgas tvliler. 183-l: paHHrr IOpa: T6apcrufi aex. K. Celaepo coirica Miinster l8'12: paHH,rqK)pa: Toap*iuil sex L.-Falaeololigo oblonga \\'agncr itAOO1,punnm tOpa: Toapcx1ir eeri. M. '\larekites vinarensis(Fritsch. l9l0): paHHuii l\'Ie.r:Eipperrcxuii sex. N. Eoteuth'oicles catthatt lf i.itsch. l9l0): pauHui Me.r: Eapperrcxufiee,x f"ra*rn-\'cbr. or\ieqcHHbre 3Be3.foqxoii. rronrlB.urbcr Bo3\ro;,r\HbrlrH npe.f1a\rx coBpe\leHHbl\ Vampl romorphidaandOctopoda.OcranuHrter.raJu\cbr npfiHaJ.rexalK HHbr\rrBo.rrounoHHbr\r .'rhHHr\r. A-B.D.F.H-I..l-KuL u z r - a e f .1 9 2 2 C : - r r : E n g e s i r . t g b OE : u r R e i t h e rl .n g e i e r 1 9 8 2 G : v3 Donolan. 1983: N{. N - u:t Kostak. 2002.

V. A. tsizikov

80

Medianfield

"Trachyteuthimorpha" and Vampyromorpha

Trachyteuthis

Cirrata

ralll octopod-like habitus u'ith short sac-shaped m a n t l ef u s e du ' i t h t h e h e a do n d o r s a ls i d e .* e l l - d e v e l o p e d t r i a n g u l a rt e r m i n a l f i n s . l o n g f i e e f u n n e l and verr long arms *'ithout interbrachialrieb (Fig. 55A.B). Each arm bore a single rou of suckers *itliout stalks and rings. According to Fischer and Riou [1982]. the n-rorphologlof Proteroctopttsdenotesa necto-epipelagicmode of life. I''antptt'onassa exhibitedcharacteristicvamp)'romorphfeatures. including eight arms and t\\'o filaments (modified secondpair of anns). deep interbrachialu'eb. Lrniserialsucker* ith borderingcirri on eacharm. elongatedrnantlethat \\as fused r.viththe head on dorsal s i d ea n d n i o o a r - l i k es u b t e r m i n afli n s ( F i g . 5 5 C . D ) . B a s i n g o n g e n e r a lr n o r p h o l o g l ' .F i s c h e ra n d R i o u f2002] tentativell suggested IhaL l:ampt'ronu.\'su \\'as a mesopelagicanimal. Palaeoctopusnetboldi lrom the late Cretaceousof Lebanon is commonll' consideredto be the earliest representativeof Inc i r r a t a [ E n g e s e r .1 9 8 8 ] . T h i s a n i r n a l h a d u i d e a l rrrost sphericalrnantle. fused rvith the srnall head on the dorsal side. r'erv long arms rvith uniserial s u c k e r st.* o s r n a l lt r i a n g u l a rf i n s a n d n o i n t e r b r a c hial rieb (Fig. 55F). The rnost striking f-eatureo1' Palaeoctopu.s is the structlrreof its gladius that nas recentlr described b1 Haas 120021.The gladius consistedof tlr'o sigmoidal-lanceolate conchyolin platesseparatedfrom eachother in the rniddle (Fi-u. 558). Separationof lateral halves in the gladius of Palaeoctopusclearll testifiesits affinitl' to lncirlat a . I t p r e s e n t sc o n c l u s i v ee v i d e n c et h a t d i v e r g e n c e of octopod stern into Cirrata and Incirrata had alreadl occurredbv the late Cretaceous.

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riberti Fischer et Riou. 1982. I'antplroussa rhodanica Fischer et Riou. 2002 and Palaeoctr.,pus nev'boldi (Woodu'ard. 1896). have been described (Fig. 55). l'he flrst tu'o speciesare kno\\'n from the Middle Jurassic (Callovian) of France [Fischer. Riou. 1982; 2002]: the latter uas reponed from the Late Cretaceous(Campanian)of Lebanon fWoodr v a r d .1 8 9 6 :N a e f . 1 9 2 2 ] .A l l t h r e ef o r r n s\ \ e r e p f e servedb1' organic caststhat reflect rnanv important featuresof their soft body but conceal completelr the structureof gladius. Proteroctopus had gene-

Evolution

of the shell in Vampyropoda.

B a s i n gr n a i n l yo n p a l e o n t o l o g i c a l d a t a H.a a s[ 2 0 0 2 ] p r o p o s e dt h e o r i g i n o f t h e s h e l l o f r e c e n to c t o p o d s f i ' o r nt h e g l a d i i o f ' ' F o s s i l T e u r t h i d s ("T r a c h rt e L r t i rnorpha) throLrghreduction of the n-rediantleld of proostracumand conus(Fig. 56). He sr"rggested that the step-u'isereductionof the gladius in Octopodir"'asprobabll' stipulatedbv increasirrs folm linea_ee s * i m m i n g a c t i v i t ) . S a g i t t a li n t e r r u p t i o no f t h e g l a diLrsin Palaeoclopus.accordingto Haas.has improved the capabilitl' of its muscular mantle for rnore vi,{orous inflation and deflation durin-esrvimnring and breathing. In mv studr the generalschemeof evolLrtionof the shell in Vampvropoda u'as made on the basis ol broad comparison of the shell structure and s h e l l - s o f bt o d y 'r e l a t i o n s h i pi n r e c e n tv a m p i r es q L r i d a n d o c t o p o d s( F i g . 5 7 ) . T h i s s c h e m es u p p o r l st h e conclLrsiorlof Haas 12002)on origin of Varnpr rop o d af r o r n ' F o s s i lT e u t h i d s 'u ' i t h u ' i d e m i d d l e p l a t e of proostracurnand partly redr-rced conus.Houel'er. i n m 1 o p i n i o n .r e d u c t i o no f t h e g l a d i u si n O c t o p o d a d i d n o t i m p r o v et h e i r s u i m m i n g a n d b r e a t h i n gp e r -

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5l

\/. A. Bizikov

formance and apparentl)'\\as determinedbr other reasons. Trvo crucial events took place in evoh-ttionof t h e s h e l l i n O c t o p o d i a nl i n e a g e : 1. Redr-rction of the middle plate of proostracurn and conus in the gladius of vampl'roteuthoidt\ pe resulting in its transformation into tlte -eladiusof clrratet!'pe: of transvet'salconnection(saddle) 2. Redr-rction in gladius of cirrate tr pe resulting in its transtbrmation into paired st1'letsof Incirrata. The first event \\'as the most important as it p r e d e t e r m i n e dt h e r v h o l e f o l l o u i n g e v o l u t i o n o f o c t o p o d s "l t s e e m s s u r p r i s i n g .h o u t 1 ' p i c a lt e u t hooid gladius of ancient vamp) romorplis could t r a n s f b r r ni n t o a b i z a r r e U - s h a p e g l a d i t r s o f c i r r a t e t ) ' p e l a c k i n - ed i s t i n c t i v e s t r r . r c t u r ael l e m e n t s . W h a t w e r e t l i e p o s s i b l ec a u s e so f s u c h t r a n s f o r m a t i o n ? W h a t a d v a n t a g e sg o t a n a n i t n a l h a v i n - e r i d d e n o f r n e d i a lp a r t o f p r o o s t r a c u m ?T o a n s ue r t h e s eq u e s t i o n sl e t u s c o n s i d e rt h e p o s s i b l es e q u e n c e so f s u c h r e d u c t i o n .R e d L r c t i o no f t h e m e d i a l part of proostracum meant that the tnantle ceased t o h a v e f i x e d l e n g t h . i t s a n t e r i o rm a r - e i nl o s t s u p p o r t . b u t t h e b o d y ' p l a s t i c i t y 'e n h a n c e d .S u c h a t r a n s f o r m a t i o nc o u l d h a p p e n ( a n d b e s u p p o r t e d b)' natural selection) onl1,'in slou-s"vimmin-s fbrms. in lvhich dorsal anterior Inantle margin had alreadl' been fused with the head. and the fins (not tl-re mantle) rvere the main means of l o c o m o t i o n .R e d u c t i o no f m e d i a n p l a t e o f p r o o s t r a c u m c o u l d n o t h a p p e ni n a j e t - s u ' i m m i n g n e k t o n i c c o l e o i d . b e c a u s ei t t r a n s f o r t n e dt h e a n i m a l from a jetting torpedo into soft salrsage.Thr-rs.it l n c e s t o r so f s e e m sv e r v l i k e l l ' t h a t h y ' p o t h e t i c a a O c t o p o d as u ' a m s l o u l y ' u s i n g t h e f i n s a n d h a d t h e mantle fused uitli the head on dorsal side. Apparentll'.these animals evolved tou'ard pelagic ( b e n t h o - p e l a g i c ?l)i f - ef o r m . a n d t h e p r e s e n c eo f r . l i d e h e a ' n , rg,l a d i u s o f v a m p v r o t e u t h o i dt y p e b e c a r r r ea n o b v i o u s o b s t a c l e o n t h i s e t ' o l u t i o n a r ' 1 pathwa,v. G l a d i i o f " F o s s i l T e u t h o i d s "u e r e b u i l t b 1 't h i c k densechitin that apparentll'had substantialnegative buo,vancy'. Such gladii u'ere adequatefor active necto-benthicfonns but rveretoo hear"vfor pelagic tbrms. Lightenin-eof the gladius could be achieved either through genelal reduction of the ueight ot through reduction of some rnorphological pafts. Apparently both u'a1s u'ere explored in evolution. The first way' (generallightening of the gladius)led to recent Vaurpyroteuthidae.The gladius in ['anrp)l'oteuthis decreasedin thickness and its dense heavy modification of chitin rias substitutedb1 its loose rvater-rich rnodification u ith nearll neutral buol'anc1'.Lightening of the gladius in vampl'romorphs resulted in decrease of its rnechanical strengthand correspondingdecreaseof its suppor-

ting function. The generalplan of gladius structure \\as conservedand did not changeconsiderably'during subsequentevolution of this group. As a result. tlre gladius in recent l/amplt'oteutftis is strikingl,r: s i m i l a rt o t h e g l a d i i o f s o m e" F o s s i lT e u t h i d s "f r o m the Lor.rer Jurassic.Despite its apparentfragilitl . the gladius of Vampt'rotetihis has most of the muscular attachrnentsfound in decapodiforms.It provides support for fins that have become the ntain organ of locomotion in this animal and can propel it at surprisingly fast speeds.It also serves as a 'backbone' ofthe soft bodl' but less as a rigid support than as a structurethat provides supportthrough its resistanceto stretching.Another impofiant function of varnpire gladius is strengtheningtlte attachmentof the head and mantle. The rostrum underrventradical reduction in Vantpyroletillis. Its absencein sorneindividualssuggeststhat it no longer has a function. Lightening of the gladius of the ancestralteuthoid plane together u'ith other adaptations enabledvamp)'romorphsto evolve pelagic lbrms. as testifledb1 a single living representative. Houever. this evolutionarl line turned out to be a dead end. When the finfishes entered the seas in vampyromorphsapparentthe Jurassic-Cretaceous. ly could not competervith them and survived only' in bathl'-pelagicrefLrge, Another means of lightening the shell. its radical reduction. \\'as realized in evolution of octopods. In course of this reduction. the medial pan of proostracum(rachis and. probably. lateral plates). conus and rostrum 'uverelost. The ostracurn and periostracum\\'erealso reducedand the gladiLrs transformedinto the shell of cirrate type: a carlilage-iike U-shapedstructure.composedb1' concentAs a result of such reric layers of h1.'postracum. 'backbone' for duction the gladius lost the role of the rrantle musculaturebut retainedits function of the fin suppofi. Reduction of proostracum.apal't fi'om lightening the shell. greatly'increasedflexibility of the bodl'. u'hich r.vasan imporlant preadaptation for the settlementon the ocean floor. The habit to explore large objects u'ith the arms \\as another preadaptationthat predeterminedan oralend-dou'napproachof"pre-octopod" to the bottom [YoLrnget al.. 19981. As testified by the fossil evidences(Palaeocto' pus). the divergence of pre-octopod lineage into Cirrata and Incirrata occurredbefore the Late Cretaceous.Ancestors of cirratescontinued to evol'n'e rnainll' as bentho-pelagicforms relying on swlrnm i n g u i t h f i n s . T h e g l a d i u si n c i r r a t e se v o l v e dn t a inll as the structure suppofting the fins and connecting the mantle. fins and the visceral organs. of basalpocketsin this lineage\\'as proRedr-rction babll stipulatedby' developmentof a ne'urbird-like wal of slvimrning u'ith fins. that required stronger connectionbetu,eenfin basesand the gladius.Tlio

Shell in Var.npyropoda evolutionarvlineagesmav be tracedu'ithin Cirrata. In one lineagethe animals adaptedro quasi-benthic life acquiring oral-end-dorvnorientation and flat cake-likebody (Grimpoteuthisand Opisthoteuthis). The gladiLrsin this lineage remained rvide and retained some primitive ancestralcharacters:the presenceof lateralhorns serving for attachrnentof the funnel retractorsand the presenceof dorsal groove on the saddleserving for attachmentof the mantle. Another lineage of cirrates led to bentho-pelagic forrns like Cirroteuthis and Cirrothaunn. Evolulton in this line .uvas associatedr.vithsr.rimrr-ring u'ith fins, and the gladius evolved exclusivell as the fins suppoft.The lateralu'ings of the gladius came closer togetherand greatlv expandedto provide effective suppofi for increasingfins. Axial part of the g l a d i u s b e c a m ev e r l ' t h i c k a n d r i g i d . E v o l v i n g i n this r.vay.the gladius transformed into perfect fin suppofi. It allowed pelagic cirratesvirtually to fly in the water by' powerful fin stroke. like the birds fl1, in the air. Ancestorsof incirratesdescendedto the bottom in oral-end-down position and began to adapt to cryptic benthic life associatedrvith cra.,rlinglrovement with the use of the arrns. Apparenth flrst incirrateswere shallo.ur,-water forms *ith u,ide Ushaped gladius and u'ell-developedoar-like fins. However. it seemsthat the life on the bottom 'u,,as not easy in Cretaceousseasrvherethe key posirions were gradually taken bv nevn'evolving predators. the finfishes.For animals unprotectedby the shell. adaptationto benthic environmentrequired enhancementof the bod1,'flexibilit_rto lride in erer_r.possible minute shelter on the bottom. The fins and suppoftingit rigid U-shapedgladius becarrean obstacleand had to be reduced.These reasonsstiplllated the second major event in evolution of the octopodianshell: reductionof the transr,,ersal fusion in U-shapedgladius and its separationinto paired lateralrods. sty,'lets. The first knorvn representativeof incirratelineage. Palaeoctopltsney'boldi. still exhibited sorne characteristicfeaturesof Cirrata: presenceof fins. t h i c k g l a d i u s a n d c i r r i o n t h e a r m s f H a a s .2 0 0 2 ] . However. the fins in Palaeoctoplzsshou.eddistinct signs of reduction:they were relativelv small and lacked solid supporl as rhe gladius had alreadv separated in the middle, In course of evolution of incirrateoctopodsthe fins reducedcompletelr'.and the gladius changed its function from the fin suppofi to suppofi for the funnel. The reductionofthe shell in Incirrataappearsto significantly affect their capability for jet-swimrning. Reduction of entire shell prohibits octopods from fixing their mantle length and streamline shape during srvimrnin_9. When inhaling. Octopttsdecreasesits length b1,'1214ok lZuev, 19651.Thick ventral mantle adductor diminishes the volume of ventral mantle cavrn

83

considerablr,'. Unique pattern of attachmentof the visceralsacto the mantle b;- meansof five adductor muscles found in cctopods is much rveaker than complete fusion of the visceral sac to the shell as found in vampvromorphs. Hou'ever. this pattern e n s u r e di n c r e d i b l em o b i l i t i , o f t h e v i s c e r a ls a c i n side the mantle cavin. that \\,asan imporlant adaptation to the benthic 'ura1'of life. Together rvith the a b s e n c eo f f i n s . i t m a d eo c t o p o db o d y v i n u a l l l ' s h a p e l e s s .I t a l l o u ' e d t h e a n i m a l s t o h i d e i n n a r r o u , cracks and slits in rocks and to squeezeoneself 'pan b) paft' through chinks r',,iththe rvidtlr jLrst 1/10 of the animal manrle length [Akimushkin. 1 9 6 3 1 .R e d u c t i o no f t h e m e d i a n c o n n e c t i o ni n t h e gladius and deep reorganizationof the body plan predeterminedthe evolution of Incirrata. On the one hand. it prohibited this group to evolve active nektonic life forms. On the other hand. it opened for ancient incirrates netv possibilities to evolve benthicand later bentho-pelagiclife forms and laid dorvn the basisfor contemporary, biological success of this group. Er,'olutionof Incirratawas associatedlvith pr.o_ur e s s i v er e d u c t i o no f t h e s h e l lu n t i l i t s c o m p l e t el o s s i n s o m e l i n e a g e sB . e n t h i cs h a l l o u - u a t e rO c t o p o d i dae retainedthe most primitive stl lets reachins sometimes up to 24'r/oML (Enteroctoptr.s). Gra.lual r e d u c t i o no f t h e s t r , l e t si n d e e p - * a t e rO c t o p o d i d a c \\'as apparentl;"stipulatedbr the seneraldc-clinr.tri' their activit'r'.In Benthocto7tu.s. Btttlt.t,prt1.1 f ,i.7t11t. done, Pareledone. Tett'ucltelerLtrte.I-alrtl, ttt,t ll)e s t 1l e t s d e c r e a s e di n s i z e a n d b c c a n t cs- o t i r - .ur l t i l e in Eledonella and Gratteletlt.tne the shell has bec-n lost completell IVoighr. 1997].Some muscular slrallorr'-riaterOctopodidae (.4meloctopus,Hapulr.,cltlaetta, etc.) have also lost the stylets fVoight. 19971.Together with stylets.these forms apparentl1 lost ability for jetting swimming as tesrifiedbv decreasedsize of their mantle in relation to the arms. At least tuo independentlineages of Incin.ata r e - i n r , ' a d etdh e p e l a g i c r e a l m : B o l i t e n o i d e a( C t e noglossa)and Argonautoidea.In both lineagesdeveloprnent of pelagic forms r.vasaccornpaniedb1 complete loss of the gladius. Bolitaenoidearepresents a more specializedpelagic lineage than Argonautoidea.The st1.,lets in this lineageare missirrg alreadv in primitive forms (Japetel/a).u'hile in the advancedform (Amphitretus) even the breaks in the mantle musculaturemarking location of the forrner shell have been lost. In Argonautoideagradual reduction ofthe stl.letscan be traced in Trentoctopus and ,llloposlrs until compete loss of the shell in Oct'thoe and ,4rgonaura.In this clade reductionof the shell \\,as accompanied bl, development of strong funnel locking-apparatus ofteuthid type that substitutedthe shell functionally. T h u s . t h e l a s t e v e n t i n e v o l u t i o no f t h e s h e l l i n

V. A. Bizikoi

Vampyropoda.its completeloss.repeatedly'and independentlyoccurredin Incirrata.In benthic Octopodidae (Ameloctopus. Hapalocltlaena) reduction of the stylets was caused by' abandonmentof the jet-swirnrning and development of crar.vlinghabit with the use of arms. In pelagic clades(Bolitaenoidea. Argonautoidea)the main causesof the complete loss of sty'letswere either the loss of abilitl' for jet-swirnming (Alloposus, Antpl'titretus) or developmentof strong funnel locking-apparatus/fusion betrveenthe firnnel and the mantle (Octlhoe, Tremoctoptts). Remarkabll. loss of stylets in all pelagic octopodsdid not result in transforrnationof 1s11sl1sdoenetheir musculararrangement.r'vhicl-r rally the same as in benthic Octopodidae.

ACKNOWLEDGMENTS suppofied This *ork has beeninspiredand consistentl)' by late K.N.Nesis.to nhom I am deepll grateful.I riould like to thank rerr rvarmll Ch.M. Nigmatullin. L.A. Dog u z h a e r aB . . G . I r a n o r ' . J . A . F i l i p p o v aa n d D . O . A l e r e e r tbr many I ears' useful discussion.fiiendll criticism and essentialhelp in pror iding cephalopodliteratureand rarc octopodsspecimens.I extend ml thanksto T. Kubodera. H.S. Bidrke and G.M. Vrnogradovfor their kind help in obtaining rare specimensof Vampl romorphida and Octopoda. I am deepll grateful for R.E. Young and [).1-. Donoran for proolieading the manuscript.English corrections and critical remarks. The study rvas conducted in and financed b1 \'NIRO.

References Aldred R.G.. Nixon M.. Young J.Z. 1983. Cirrothattntanurravt Chun, a finned octopod.Philosophical Transactions of the Royal Soc'ien of L o n d o n .B . 3 0 1 : 1 - 5 4 .

B a n a sR . T . . S m i t h D . E . , D . C . B i g g s . 1 9 8 2 .A n a s sociationbetweena pelagicoctopods,Argonauta sp. Linnaeus 1758.and aggregatesalps.Fishen' Bulletin L,iS.. 80: 648-650.

A l e k s e e vD . O . , B i z i k o v V . A . , K i r o m o v D . N . . P o lnozov A.A. 1989. Underuater observationson the behaviourand distributionof a gonatesquid Berryteuthis magister and other cephalopodsin the norlhu,estem PacificOcean.In: ElizarovA.A. (Ed.), Underv'ater explorations.for fisheries and bio-oceanographtcstttdies. Moscorv. VNIRO P u b l i s h i n g6: 6 - 7 7 [ I n R u s s i a n ] . Akimushkin I.l. i963. Cephalopodsof the seas o;f t h e U S S R .I z d a t e l ' s t v oA N S S S R . M o s c o u - L e ningrad.236 p. [n Russian:English translation b , v A . M e r c a d o .I P S T . J e r u s a l e m1. 9 6 5 .2 2 3 p . l

T. 1987.Phylogeneticanalysis BertholdT.. E,ngeser and systematizationof the Cephalopoda(Mollusca). Verhandlungen des naturv,rssenschaftlithen l"ereins Hambttrg, 29: 187-220.

Appellof A. 1899. Uber das Vorkommeninnerer Schalebei den achtannigenCephalopoden. Berg e n s l l l u s e u r n . l a r h o g .1 2 : 1 - 1 5 . A r k h i p k i nA . 1 . .B i z i k o v V . A . 1 9 9 1 .A c o m p a r a t i \ e anallsisof age and grorith estirnationusing statolithsand gladiusin squids.In: JerebP.. S. Ragonese.S. von Boletzlil (Eds.). Squid Age Determinution L'sing Statoliths. Proceedings of the International lllctrkshop of the Instituto di Tecnologia tlella Pesca e del Pescato.Note tecnichee Reprintsdell'lnstitutodi Tecnologiadella Pescae Via Luigi Vaecara.6l-9 1026 Madel Pescato. No. zaradel Vallo (TP). Itall . SpecialPublication. l: l9-33. B a n d e lK . . B o l e t z k yS . v . 1 9 7 9 .A c o m p a r a t i " 'set u d l of the structure.del'eloprnentand rnorphological r e l a t i o n s h i posf c h a m b e r ecde p h a l o p osdh e l l s .I e I r g e r ,2 l ( 3 ) : 3 1 3 - 3 5 . 1 . B a n d e lK . . L e i c h H . 1 9 8 6 .J u r a s s i V c amplromorpha (dibranchiatecephalopods) . .\-euesJohrbuch/iir Geolr.tgieund Paleonologie llonashefte, 3. 12914 8 .

Bizikov V.A. 1990.A new method of squid age d e t e r m i n a t i o nP. a t e n tN o . 1 5 6 5 4 , 1 0I()55 A 0 l K 6l 00. Byulleten' otkritiya i i:obretenil'a.19'. 25 !n Russianl. B i z i k o v V . A . 1 9 91 . A n e w m e t h o d o f s q u i d a g e determinationusing the gladius. ln: JerebP.. S. Ragonese.S. von Boletzky (Eds.).Squid Age Determination Using Statoliths: Proceedings of the International Ll/orkshopof the Institulo di Tecnologia della Pesca e del Pescato.Note tecniche e Reprintsdell'lnstitutodi Tecnologiadella Pesca e del Pescato,Via Luigi Vaecara.6I-91026 -Maxara del Vallo (TP), Italy. SpecialPublication No. 1: 39-51. Bizikov V.A. 1996. Atlas of morpholog, ancl anutomy of the gladius of squids. Moscov'. VNIRO P u b l i s h i n g1 : - 2 4 8 [ n R u s s i a nw i t h E n g l i s ha b stract]. B i z i k o v V . A . . A r k h i p k i nA . l . 1 9 9 7 .M o r p h o l o g la n d rnicrostructure of the gladius and statolithfrorn the borealPacificgiant squidltloroteutllisrobusta (Oegopsida:Ony'choteuthidae). .kturnul of ZooIog,.241'.415-492 Boletzky Z.v. 1992. Evolutionaryaspectsof development. life st1'le.and reproductivemode in incirrate ostopods (Mollusca. Cephalopoda). Revue suissede Zoologie, 99'. 155-110. Boletzky Z.v. 1999.Breve mise au point sur la actuels.Bulletitr classificationdes Cephalopodes

Shell in Varrip-vropoda de la Societe:oologie de France, 121 (3): 271278. C a r l i n iD . B . .G r a v e sJ . E . 1 9 9 9 .P h y l o g e n e t iacn a l y s i s of cyochrorne c oxydase I sequencesto determine higher-levelrelationships within the coleoid cephalopods (Mollusca:Cephalopoda). Molecular Biolog' and Evctlution,17: 1353-1310. C h u n C . l 9 l 0 - 1 9 1 5 .D i e C e p h a l o p o d eIn. . O e g o p sida. II M1'opsida.Octopoda.Wissenschaftliche Ergebnisseder DeutschenTiefsee-Expedition auf d e m d a m p f e r" V a l d i v i a " 1 8 9 8 - 1 8 9 9B. e r l i n . B d . l8: l-5-il t Arlas.1. C l a r k e M . R . 1 9 7 8 .T h e c e p h a l o p o ds t a t o l i t h- a n introduction to its form. ,Journal of illarine Bio l o g ' . l s s o c i r , t t i oLn. . K . 5 8 ( 3 ) : 7 0l - 7 0 2 . C o l l i n s M . A . . H e n r i q u e sC . 2 0 0 0 . A r e v i s i o no f the famill Stauroteuthidae(Octopoda:Cinata) rvith redescriptionsof Stauroteuthissr.r.lensrs and S. gilchristi. ./cturnalof .\lanne Biologl .,lssociatiort LiK. 80: 685-697. C o l l i n sM . A . . Y a u C . . A l l c o c k L . . M . H . T h u r s t o n . 2 0 0 1 .D i s t r i b u t i o no f d e e p - u a t ebr e n t h i ca n db e n tho-pelagiccephalopodsfront the north-eastAtlantic. Journul o/ .\[urine Biolog . ssoc'iatitttt Li(..81: l0-5-117 D o n o v a nD . T . 1 9 7 7 . E v o l u t i o no f t h e d i b r a n c h i a t e Cephalopoda. Stnposia of the Zoctlogic'ulSocieh, oJ'Londott, 38: l-s--18. D o n o v a nD . T . 1 9 8 3 . . \ l u s t i g o p l t o r O a u e n 1 8 5 6 :a little-knorin genus of Jurassiccoleoids.,\ elles .lahrhttch./iir Geologie und Pctlaontologie .4hhandlungen. 165: .18-1--195. D o n o v a nD . T . . D o s u z h a e v aL . A . . I J . M L r n e i .1 0 0 i . T u , o p a i r s o f f i n s i n t h e L a t e J u r a s s i cc o l e o i d Trachiteuthisfiorn Southem Germanr, In: Warnke. K.. Keupp. H. and S. r'on Boletzk] (eds,): Cephultytcl.s. pre.tenturtJ p,nr. B.-t.litrt P,tlcubitr logisclte.lhhutttlluttgen.B. i: 9l-99. D o y ' l eP . . D o n o v a nD . 1 . . N I . \ i r o n . 1 9 9 - 1p.h r l o e e n r and svstematics of tlre Coleoidea.l,tlt,,nrolo"gic'rtl Contributiono/' tlu L'ni.ersit.tof Kutt.sus. _\'er,Serles,5: l-l-5. E n g e s e rT . 1 9 8 6 .B e s c h r e i b u negi n e r r i e n i g b e k a n n t e n u n d e i n e r n e u e nC o l e o i d e n - A r(l V a n p r r o morphoidea.Cephalopoda)aus den Unterrothonlul.nvon Solnhofenund Eichstiitt(Ba1ern). ..1rc h a e o p t e r y x( .1 9 8 6 ) : 2 7 - 3 5 . E n g e s e rT . 1 9 8 8 .F o s s i lO c t o p o d s a c r i t i c a lr e v i e u . I n : C l a r k e . M . R . . T r u e r n a n .E . R . ( e d s . ) . The ,\lolluscct.t'ol. ll .\'eontolog,.und puleontolog; of the Cephaloporls.Academic Press.San D i e g o :8 1 - 8 7 . E n g e s e rT . . B a n d e lB . 1 9 8 8 . P h 1l o e e n e t i cc l a s s i f i c a t i o r .or f c o l e o i dc e p h a l o p o d sI n . : W i e d m a nJ . . Kullirran J. (eds.). Cephalopods- Present ctnd P a s l . S c h re i i z e r b a r l ' s c h eS.t u t t s a f t :1 0 5 -I 1 6 . F i l i p p o v aJ . A . . A l e x e e v D . O . . B i z i k o v V A . . D . N . Khromov. \99J. Conmercial and abundantcep-

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3t

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YtrLrnS R [ . . \ ' e c c h i o n e1 v l . .D . T . D o n o t a n . l c ) 9 8 . I ' h e * r r l u t r o n o f c o l e o i dc e p h a l o p o dasn d t h c i r pi.cscntdjrclsin and ecologr'.Soutlt..1fi.icun ,lcttrrrtitl t,l .\lut'tneScience,20: 393--110. Zu* G.\', 196-s.l\1ain featuresand adaptiventea n i n g o 1 -e v o l u t i o no f t h e s h e l l i n C e p h a l o p o d a . Zoolosiclteshi .fournal, 44(2): 284-286 [ln Russi a n l .

V. A. Bizikov

88

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