A male giant squid, Architeuthis spec. (Cephalopoda, Architeuthidae) from the Fladen Ground in the northern North Sea

2006·2.8 MB·English

by  Hoving, H J T

BASTERIA,70:153-160,2006
A malegiant squid, Architeuthisspec. (Cephalopoda, Architeuthidae)
fromthe FladenGround in thenorthernNorth Sea
H.J.T. Hoving
Ocean Ecosystems, P.O.Box 14,NL 9750AAHaren,TheNetherlands;
[email protected]
J.GoudE.Gittenberger
National Museum ofNaturalHistory Naturalis,P.O.Box 9517,NL2300RALeiden,TheNetherlands;
[email protected];[email protected]
& J.J. Videler
Ocean Ecosystems, P.O.Box 14,NL9750AAHaren,The Netherlands;
[email protected]
A specimenofArchiteuthis wascaughtontheFladen Ground, c. 100miles NE. ofAberdeen
(Scotland)in1982. The animal,amalewithamantlelengthof900 mmand a minimum total
mass of18kg,wasprobablymature.Somemeasurementsaregivenand theoccurrenceofsper-
matangia(invertedspermatophores)implanted inthe ventralarms oftheanimal isdiscussed.
Keywords:Cephalopoda,Architeuthis, morphology,distribution,spermatangia,NorthSea.
INTRODUCTION
Squids arecephalopod molluscsthatoccurfromthecontinentalshelftothevery deep
partsoftheworldoceans. They competewithnektonicfishand areimportant in thediet
ofalarge varietyofmarinepredators, especially cetaceans (Clarke, 1996).
Squids rangein size from thevery smallmembers(15mmmantlelength)ofthefam-
ily Pickfordioteuthidaeto thevery large giant squids of the familiesCranchiidaeand
Architeuthidaewhosemembersexceed mantlelengths of2000 mm. Adescription of a
specimenof thelatterfamily is thesubjectof thispaper.
Althoughasmanyas21 nominalspecies havebeendescribedinArchiteuthissincethe
firstgenusand species description by Japetus Steenstrup in 1857,modernsquid taxono-
mists agreethat probably most of thesenames aresynonyms (Sweeney & Roper, 2001).
Anextensivestudy onthebeak morphology ofArchiteuthis fromtheAtlanticOcean and
NewZealandwatersdoesnot suggestmorethanonespecies (Roeleveld, 2000), i.e. A. dux
Steenstrup, 1857.Architeuthisis currentlythelargestinvertebrateoftheAnimalKingdom.
Giantsquids haveacosmopolitan distributionand informationontheirbiology and
distributionisbasedonspecimens fromthestomachs ofsperm whales, accidentaltrawl
catchesbyfishermenand specimens thatwerewashedup ontheshore.Thevertical dis-
tributionrangesprobably fromsurfacewaters to 1200m depth,butanimalsare mainly
caughtonthecontinentalslope between300-600m(Forch, 1998;Hoving etal.,2004).Only
veryrecently thefirstlive giantsquid wasphotographed byJapanese scientists atadepth
of800m (Kubodera& Mori,2005).
154 BASTERIA,Vol. 70,No.4-6, 2006
Fig.1.Overview oftheFladen Ground specimenofArchiteuthiswith theventral arms (VA) and tentacles
(T)indicated.
Hoving etah: A male giantsquidinthe northernNorthSea 155
Giant squids are predated by a wide variety ofoceanic predators during different
stagesoftheirlifecycle, e.g.juvenile giantsquids havebeenfoundinthestomachofalba-
trosses(Imber, 1992)andmature animalsareoftenfound inthestomachsofspermwhales
andsleeper sharks (Somniosusspec.) (Clarke, 1996;Cherel &Duhamel,2003). Giantsquids
ontheirturnprey onmedium-sizedprey such as crustaceans,octopus, other squids and
fishspecies such asbluewhiting(Lordan, Collins& Peralez-Raya, 1998).Interestingly, tis-
sue of Architeuthis was found in the stomachs of Australian and New Zealandgiant
squids, suggesting cannibalism(Bolstadt& O'shea, 2004;Deagle etal., 2005).
Although the numberof specimens available to science has increased in the last
decennia,mainly duetothe developmentof deep-sea fisheries,the description and docu-
mentation of individualspecimens can still contributeto abetter understanding of the
animal'sbiology, whichis stilllargely unknown.Thepresentstudy reportsanddescribes
amaleArchiteuthiscaught by Dutchfishermenin thenorthernNorthSea.Itis inthecol-
lection(public galleries) oftheNationalMuseumofNaturalHistory (Leiden).
RESULTS
The specimen was caught by thebeam trawlerUrk56,operating fromIJmuiden har-
bour,in September 1982,fishingonthenorthernNorthSea,FladenGround,c.59°N0.5°E
(c. 100 milesNE. ofAberdeen,Scotland). Thefishing depthis unknownbutthe depth in
thearea rangesbetween 100 and 150m.Themantlelengthof thespecimen was 900mm
andthepreserved animalhadaminimumtotalmassof18kg.Thisis nottheoriginal total
mass since thespecimen was damaged andmostoftheviscera weregone.Additionally,
Fig.2.Anarm oftheArchiteuthisspecimenshowingthebiserial distribution ofthe suckers.
156 BASTERIA,Vol. 70,No. 4-6,2006
Fig. 3.Overview oftheremainingviscerain themantle cavityoftheFladenGround Architeuthiswiththe
gill(G),gladius(Gl), funnelretractor muscle(FRM),digestivegland(DG) andtestis (T)indicated.
Hoving etal.:A malegiantsquid inthe northernNorthSea 157
Fig. 4. Hypodermically implanted spermatangia
indicated byarrows.Coin diameter23.25 mm
thepreserved weight issignificantly lowerthanthefreshweight. Themeasurements were
takenafter almost25 years of preservation in formalin.The complete specimen is illus-
trated in fig. 1.
Thearmlengthsof arms I, II, IIIandIV(left=Landiright =R) wererespectively LI=
700+andRI=750+;LII=610+andRII=870+;LIII=980+and RIII=790+;LIV =830+and
RIV=940+ mm. Theright tentaclemeasured1040+ and theleft one810+mm. Maximum
mantlethickness was22mm. Eye diameterwas 80mm.Thediameterofthelargest suck-
ers onthearms was 15mmand thesuckers werepresentintworows onallarms (fig.2).
Gill length was 250mm and thediameterof the funnelwas 55mm. The funnellocking
cartilage was 115mm in length.
Mostoftheinternalorganswerelost.Becausetheposterior tailand finswere cutoff,
theorgansmayhavebeenwashedoutofthespecimen.However,asmall pieceoftestisis
still presentintheposterior partof themantlecavity, indicatingthatthesexofanimalis
male(fig.3). Smallfragments of thethick red-pigmented membrane, thatnormally cov-
ers theviscera, werealsopresent.
Between 180and 350 mm from thebase of theleft arm IV, spermatangia hadbeen
implanted deeply into the arm tissue (fig. 4). A spermatangium is the inverted sper-
matophore and in Architeuthis itcan beup to 300 mm long, witha maximumwidthof
approximately 1 mm, whichdecreasesorallyto0.1mm. Thespermatangium hasatight-
ly zigzag structure withanoral and aboralend(fig.5a). Theaboralend, whichis some-
timesprotruding outofthepointofentrance inthetissue,isopen.Theoralendisthepart
thathasenteredthetissuefirstduring theimplantation process. Thisend ischaracterized
by aroundto amorphous mass, whichhasa red colourafterpreservation. SEMimages
showthatthetunicthatsurroundsthespermmassofthespermatangium (theinnertunic
intheintactspermatophore) enters theamorphous oralmass(fig. 5b).
DISCUSSION
Although 115specimens ofArchiteuthishavebeen recordedintheliteraturefromthe
NorthEast Atlanticbetweentheyears 1545 to 2004(Guerraetal., 2004),thepresentspec-
imenisthefirstonecaughtbyDutchfishermen.Ithasrecently beenestablishedthatgiant
158 BASTERIA,Vol. 70,No. 4-6,2006
squidsliveandhuntat adepthof500-800m and mosttrawlrecords arefromthis depth
(Kubodera& Mori,2005).Thereforethefinding of Architeuthisonthe FladenGroundin
1982is probably anincidentratherthanasign ofnaturaloccurrenceof giantsquid atthis
depth in thisregion. Interestingly, Norwegian fishermenfishing inthe NorthAtlanticoff
Radoy nearBergen caughtanotherspecimen ofArchiteuthis(total lengthabout10mand
totalbody massabout220kg) inAugust of1982.Thisspecimen wasused forbloodanaly-
sis andBrix (1983) found a fourfolddecreaseinoxygen affinityof the squid haemocya-
nine withanincreaseoftemperaturefrom6.4eC to 15eC.Thisfindingsuggeststhatsquids
maysuffocate fromarterialdesaturationwhenthey encounterincreased temperaturesin
shallower waters. The captureof twospecimens ofArchiteuthis in more orless the same
period and relatively close toeachothermay suggestthata certainlocaloceanographic
feature or event has been responsible for these large squids to be brought to shallow
waters.TheFladenGroundisknownto trapabellofcoldwater initscentral deeperparts
dueto the stratification during the summer months. Additionally, in the period June-
August an increased influx of East ShetlandAtlantic Inflow (ESAI) is known for the
FladenGround (Witbaard, 1996). Giantsquids may have beenbrought into theregion
withthecold water of theESAI, and/orthey mayhave beentrapped in the bellof cold
water.Subsequently theymayhavebeencaughtbecauseoftheirweakenedconditiondue
tofoodshortage or dueto increasedwater temperatures.However, itis notknown how
oftengiantsquids arebeing broughtintothis region andthepresented dataaretoo mea-
gretoestablish a correlationbetween giantsquid captures and themagnitude of ESAI.
Aldrich (1968) related the strandings of giant squids in New Foundland with the
inflowofwarm water, suggesting thatanincreased temperaturemayhavecaused their
death.
Giantsquidmalesgenerally mature atamantlelengthofapproximately 1 m(Lordan,
Collins&Peralez-Raya, 1998;Hoving etal., 2004;etc.).Thepresent specimen was amale
withanestimated ML900 mmandthereforethis specimen couldvery wellbe amature
animal.
Implanted spermatangia inmale giantsquid, as describedhere, arenotexceptional
(Hoving etal., 2004;Kjennerud, 1958;Guerraetal., 2004).Inmalesthespermatangia are
mainly foundontheventral arms while in females they are found inthe mantle, eyes,
arms andhead. In the presentspecimen thespermatangia wereembeddedbetween180
and 350mmfromthe ventral leftarm base.This is thearea where thedistalopening of
theterminalorganis situated.
The terminal organofmalesextendsfromthemantleforapproximately halfitstotal
length (totallength is c. 1 m). Pressureontheterminalorgan duringcapture in thetrawl
couldmakethe spermatophores tobecomeexpulsed fromit andunderinfluenceof sea-
water thespermatophores evaginate andimplant themselvesin thenearest tissue, inthis
case theventralarms. Although male-to-malematingisknownfromsquids (Illexcoinde-
tii(Verany, 1839);Lordan & Casey, 1997)spermatangia implants in male giantsquid are
probably self-induced.Besidesthesizeofthespecimen, thefact thattheanimalprobably
hadspermatophores initsterminalorgansupportsfurtherthattheanimalwasmature.
Although the spermatangium ofArchiteuthis has been elaborately described by
Hoving et al. (2004), a detailed illustrationof the mass at the oral end of the sper-
matangium wasnotpresented yet. The massis possibly whatthecement body is inthe
intact spermatophore, and is expelled first from the spermatophore during the sper-
matophoric reaction. Inothersquids thecement inthe spermatophores actsas a glue to
attachthespermatangium to thefemale.In Architeuthis itmay functionasananchor,to
preventthespermatangium frombeingpulled outof thetissue again(Hoving etal.,2004).
Thehypodermic implantation of spermatangia in squid is still not understood.Itis
Hoving etal:A male giant squid inthenorthernNorth Sea 159
5a
Fig.5a,b. AnatomyofspermatangiaofArchiteuthis species. 5a,aspermatangiumwith amorphousmass
(AM), unknown substance (US, probably cementbody) and aboral opening (AO) indicated (courtesy
ZoologicalSociety ofLondon);5b,SEMpicture oftheamorphousmassshowingthe tunicofthe sper-
matangiumenteringthe mass(photoM.Waldron). Note:the material forthis picture isfrom amature
male (mantlelength1280+ mm)Architeuthis spec. from South Africaaccessioned inIziko Museums of
CapeTownasSAM-S3386.
not known which process is responsible forthe actual implantation of spermatangia in
body tissue. Some authorshypothesize thatin squidspecies withalarge musculartermi-
nal organ, like Architeuthis, this organis responsible for hydraulically implanting sper-
matangia into the tissue like a stapler (Jackson & O'shea, 2003; Norman& Lu, 1997).
Otherssay thatanintrinsic mechanism,perhaps underinfluenceof proteolyticferments,
in the spermatophore allows itto implant in thetissue autonomously aftercontact with
seawater(Nesis etal., 1998).Thelatterprocess wouldbetterexplaintheself-implantation
ofspermatangia by themalein thisstudy since theimplants were exactly attheposition
wheretheterminalorganopens.
ACKNOWLEDGEMENTS
We would like to thank MirandaWaldronof the Electron Microscopy Unit of the
University ofCapeTown,SouthAfrica, forassistancewiththemaking oftheSEMpicture
and MarcLavaleije oftheNIOZ,Texel, forshowing us theWitbaard(1996) paper.
LITERATURE
ALDRICH, F.A., 1968. The distribution ofgiantsquids (Cephalopoda:Architeuthidae)in the north
Atlanticandparticularly abouttheshores ofNewfoundland.— Sarsia34:393-398.
BOLSTAD, K.S., & S.O'SHEA, 2004.Gut contents of a giantsquid Architeuthis dux (Cephalopoda,
Oegopsida)from NewZealand waters. — New Zealand JournalofZoology31:15-21.
160 BASTERIA,Vol. 70,No. 4-6,2006
BRIX,O., 1983. Giantsquidsmay die whenexposedtowarmwatercurrents. — Nature 303(2): 422-423.
CHEREL, Y., & G. DUHAMEL, 2003. Antarctic jaws: trophic relationships between sharks and
cephalopods,includinggiantsquids,inKerguelenwaters.Symposium:Biology,recruitment&cul-
tureofcephalopods.Phuket,Thailand,17-21February2003.Programme and abstracts: 17.
CLARKE, M.R., 1996. Cephalopods as prey. III. Cetaceans. In: M.R. CLARKE, ed., The role of
cephalopodsinthe World'soceans.—PhilosophicalTransactionsoftheRoyalSocietyofLondon,B.
SpecialVolume 351:1053-1065.
DEAGLE, B.E.,S.N.JARMAN,D.PEMBERTON&N.J. GALES, 2005.Geneticscreeningforprey onthe
gutcontentsfromagiantsquid(Architeuthissp.). —JournalofHeredity96:417-423.
FORCH,E.C., 1998. The marinefaunaofNewZealand: Cephalopoda:Oegopsida:Architeuthidae (Giant
Squid).—NIWABiodiversity Memoir110:1-113.
GUERRA,A., A.F.GONZALEZ, E.G.DAWE &F. ROCHA, 2004.Records ofgiantsquidinthe north-
easternAtlantic,and tworecords ofmaleArchiteuthissp. offthe IberianPeninsula. —Journalofthe
MarineBiological Associationofthe United Kingdom84: 427-431.
HOVING, H.J.T., M.A.C.ROELEVELD, M.R.LIPINSKI&Y.MELO, 2004.Reproductive system ofthe
giantsquidArchiteuthisin South Africanwaters. —JournalofZoology264:153-169.
IMBER,M.J.,1992.Cephalopodseatenbywanderingalbatrosses (Diomedea exulansL.)breedingatsixcir-
cumpolarlocalities. — JournaloftheRoyalSociety ofNewZealand 22:243-263.
JACKSON,G.D., & S.O'SHEA, 2003. Uniquehooks inthe male scaledsquidLepidoteuthisgrimaldii.—
JournaloftheMarineBiologicalAssociation ofthe United Kingdom83:1099-1100.
KJENNERUD, J.,1958.Descriptionofagiantsquid,Architeuthis,stranded onthe westcoastofNorway.
- UniversitetetiBergen,Arbok,naturvitenkapeligrekke 9:1-14.
KUBODERA, T., & K. MORI, 2005. First-ever observations of a live giant squid in the wild. —
ProceedingsoftheRoyal Society,Biological Sciences(B)272:2583-2586.
LORDAN, C.,& J.CASEY, 1997. The firstrecord of'accidental' copulationbetween male squidofthe
genusIllex. — JournalofMolluscan Studies63:556-558.
LORDAN, C.,M.A.COLLINS & C.PERALES-RAYA,1998.Observationsonmorphology,ageand dietof
threeArchiteuthis caughtoffthe westcoast ofIreland in1995. — Journalofthe MarineBiological
Associationofthe UnitedKingdom78:903-917.
NESIS, K.N., CH.M. NIGMATULLIN & I.V. NIKITINA, 1998. Spent females of deepwatersquid
Galiteuthis glacialisunder theiceatthe surface ofthe WeddellSea (Antarctic).— JournalofZoology
244:185-200.
NORMAN, M.D.,& C.C.LU, 1997.Sex ingiantsquid. — Nature389: 683-684.
ROELEVELD,M.A.C.,2000. Giantsquidbeaks: implications for systematics. — Journalofthe Marine
BiologicalAssociationoftheUnited Kingdom80:185-187.
SWEENEY, M. J., & C.F.E. ROPER, 2001. Records ofArchiteuthis specimens from published reports.
National MuseumofNaturalHistory,Smithsonian Institution.http://www.mnh.si.edu/cephs/archirec.pdf.
WITBAARD,R. 1996.Growth variationsinArcticaislandica L. (Mollusca):areflection ofhydrography-
related food supply.— ICESJournalofMarineScience,53: 981-987