Intraspecific aggression in the nudibranch Chromodoris annae Bergh, 1877: novel ‘fighting’ behaviour for the Chromodorididae (Gastropoda, Opisthobranchia)

2010·1.8 MB·English

by  Willan, Richard C

B74-Willan:Basteria-2010 16/11/2010 21:00 Page 89
Intraspecific aggression in the nudibranch
Chromodoris annae Bergh, 1877: novel ‘fighting’ behaviour
for the Chromodorididae (Gastropoda, Opisthobranchia)
Richard C. Willan
MuseumandArtGalleryoftheNorthernTerritory,G.P.O.Box4646,Darwin,NorthernTerritory,Australia0801;[email protected]
beneaththemantle).MorphologicallytheChromodorididae
Thispaperdocumentsaboutofveryaggressivebehaviourbetweentwo arecharacterisedbythethinbodywall(exceptforCerato-
individualsofChromodorisannaewitnessedbytheauthorsubtidallyin soma),lackofspicularelementsintheintegument(except
Timor-LesteinAugust2010.Pugnaciousbehaviourhasbeenobserved forCadlinella;seeChangetal.,2010)resultinginaverysoft 89
andrecordedpreviouslyintwootherfamiliesofanthobranch(=dorid) anddeformablebody,possessionofrepugnatorialglandsin
nudibranchs,viz.Polyceridae(onegenusonly)andGymnodorididae themantlemargin,lackofamedialindentation(philtrum)
(twogeneraatleast),bothphanerobranchfamilieswherecannibalism intheupperlipofthefoot,andoriginofthereceptaculum
ofconspecificsisanextensionofpredationonotheranthobranch seminisdirectlyoffthedistalsectionoftheducttothebursa
dorids.Pugnaciousbehaviourhasapparentlyneverpreviouslybeen copulatrix.Theglandsinthemantlestoretoxinsderived
recordedintheChromodorididae,thelargestfamilyofcryptobranch fromspongepreyandthesetoxinsareliberatedwhenindi-
dorids.Althoughtheobservedaggressionwascertainlynotcannibalis- vidualsareirritated.Productionoftoxinsunderliesthemost
tic,itisuncertainwhetheritwasrelatedtomatingorfeeding,orhad visuallydistinctiveexternalcharacteristicstothefamily–
someotherpurpose. thoseofvividcolourandboldpatterns,characteristicstradi-
tionallyinterpretedasaposomaticbymostnudibranch
Keywords:Gastropoda,Opisthobranchia,Anthobranchia,Doridina, workers,butdisputedbysome(e.g.,Thompson,1976:52).
Chromodorididae,Chromodoris,insituobservations,conspecific- UnquestionablythefamilyChromodorididae,and
directedaggression. particularlyitslargestgenusChromodoris,attainsmaximum
globaldiversityinthetropicalwatersoftheCoralTriangle
(Willan&P.Poppe,2010).Herespeciesareextremely
Introduction diverse,andcoexistenceofsiblingspeciesandmimeticrela-
tionshipsbetweenspecies(andevenbetweenotherphylaof
Withover400describedspecies,theChromodorididaeis invertebrateswithchromodorids)arerife.
numericallythelargestfamilyofcryptobranchnudibranchs Chromodoridsareusuallyencounteredsinglyoncoral
(i.e.,nudibranchscapableofretractingthegillsintoapocket reefsduringtheday.Theyarealwaysconsidereddocileboth
Basteria74(4-6):89-94
B74-Willan:Basteria-2010 16/11/2010 21:00 Page 90
inthewildandincaptivityanduptonow,theyhavenever ofTimor-Leste(=East-Timor)(8°28.703’S,125°54.496’E),on
beenseentobehostiletoconspecificsortootherspeciesof 14August2010.Thetransectranfrom22.2mupto3min
nudibranchsunderanycircumstances.Onthecontrary depth.Thetotaldurationofthedivewas82min.Thewater
however,nudibranchsbelongingtotwoothergroupsof temperaturewas27°C.Theweatherwassunny,andthe
phaneorobranchs(i.e.,nudibranchsnotcapableofretracting waterwasveryclear(horizontalvisibilitywasestimatedat
thegillsintoapocketbeneaththemantle)thatareclosely 20m).TheparticularobservationsonChromodorisannae
relatedtoeachother,haveregularlybeenrecordedas weremadeatapprox.12.15hroncoralrubblenearthetop
aggressive;theyareGymnodorididaeandPolyceridae.The ofthesteepfringingreefslopeatadepthof6m.Bothindi-
Gymnodorididaeareallnotoriouslyaggressivetowards vidualsinvolvedinthe‘fight’(Figs1-5)wereapprox.30mm
otherdoridnudibranchsbothinthewildandincaptivity; extendedcrawlinglength.Threeadditionalindividualsof
thataggressionrelatestothefactthattheyareunselective C.annaewerealsorecordednearbyonthetransecton
carnivoreseatingotheropisthobranchs,includingcon- similarsubstrates;theyhadsimilarsizes,andtwoofthem
specifics.Indeed,somegymnodoridsapparentlyfeed werefeedingonaclumpofpaleblueencrustingdictyocer-
exclusivelyonmembersoftheirowngenus(Behrens,2005). atidspongemostprobablybelongingtothefamily
Gymnodoridseattheirpreywholeorsuckouttheviscerato Thorectidae(Fig.6).
leaveonlyabagofskinremaining(pers.obs.).Onespecies StandardSCUBAgearwasusedbybothmydiving
ofgymnodoridhasswitcheditsdiettofeedonthefinsof buddyandmyself.Stillphotosandshortvideosweretaken
sand-dwellinggobioidfishes(Osumi&Yamasu,1994).The withanOlympusµ760digitalcamerainsideanOlympus
Polyceridaecontainonegenus,Roboastra,thatspecialisesin PT-036housing.Twoofthevideoclipsarepostedassupple-
selectivelyeatingwholeothermembersofthesamefamily mentarymaterialontheBasteriawebsiteat
(Kerstitch,1989;Miller,1999;Behrens,2005;Willan,2003: http://www.basteria.nl/publicaties/basteria/supplements/74/
90 104showsaphotobyDianeArmstrong),particularly B74-Willan-1.aviandhttp://www.basteria.nl/publicaties/
speciesofTambja,trackingpreybyfollowingtheirmucous basteria/supplements/74/B74-Willan-2.avi.
trailsandthisbehaviouroccursbothinthewildandin
captivity.SpeciesofRoboastracertainlydocannibalisetheir
ownspecies.
Therefore,thefortuitousobservationoftwoindividuals
ofChromodorisannaeBergh,1877engagedinaprotracted
boutofextremeaggressioninthewildputstheassumed Figs1-5.Photographicdocumentationofanaggressiveencounterbe-
docilebehaviouroftheentirefamilyintoquestion.Tomy tweentwoindividualsofChromodorisannae,at6mdepth,“Bob’sRock”,
knowledgeaggressivebehaviourhasnotbeendescribed westofManatuto,northerncoastofTimor-Leste,14August2010.1,
previouslyforanymemberoftheChromodorididae,so, individualsincombat,notebothcombatantshavetheirbuccalmassfully
eventhoughonlyoneboutofaggressivebehaviourwas everted;2,onecombatantwithdrawsitsrightrhinophorefollowingan
observed,Iconsideritcertainlyofsufficientimportanceto attackbytheothercombatant;3,onecombatantwithdrawsitsgills
justifythoroughdocumentation. followinganattackbytheothercombatant;4,onecombatantthatis
upside-downrisesupanddirectsaradularstrokeverticallydownward
Methods ontotheotherindividual;5,piecesofthemantlemarginaroundthehead
(arrowed)werebittenoffeachcombatantduringtheencounter.Fig.6.
Theobservationsreportedbelowweremadeduringan TwootherindividualsofC.annaegrazingamicablyonasponge
underwatertransectperpendiculartotheshoretorecord (Dictyoceratida,probablyThorectidae)nearby.Feedingscarsonthe
opisthobranchdiversityconductedat“Bob’sRock”,westof spongeleftbytheseindividualsarearrowed.AllphotosNeilWright.
Manatuto,approx.40kmeastofDili,onthenortherncoast
Basteria74(4-6)
B74-Willan:Basteria-2010 16/11/2010 21:00 Page 91
91
Willan,R.C.–Aggressivebehaviourinachromodoridnudibranch
B74-Willan:Basteria-2010 16/11/2010 21:00 Page 92
Observations Discussion
Whenfirstseen,thetwoChromodorisannaeindividualswere AllmembersofthefamilyChromodorididaehavehitherto
entwinedtogetherhead-to-headwithoneontopandthe beenconsideredasdocileandnon-aggressivebymolluscan
otherunderneathinavigorous‘fight’inthemannerof specialistsandamateurdiversinterestedinnudibranchs
courtinglandslugsLimaxmaximusLinnaeus,1758(Janus, alike.Nowadaysobviousbehavioursofmantleflappingand
1982;Rowson,2005).However,bothindividualswere trailing,whichtypifysomespeciesofchromodorids,and
horizontal,alwaysretainingsomepartoftheirfoot,albeit whichIfirstwitnessedinVanuatuin1972,arewellknown
small,attachedtothesubstratum.Theirbodiesweregently andwidelyreported(e.g.,Behrens,2005).However,no
waftingtoandfrowiththesurge.Bothindividualswere aggressivebehaviourtowardsconspecificslikethatunder-
makingrepeatedlungesattheother(Figs1-5).Thebuccal takenbythefamilyGymnodorididae(i.e.,opportunistic
massofeachindividualwasprotrudedforaboutaminuteat predationonothernudibranchs)orbythegenusRoboastra
atimeaccompaniedbyraspingcyclesbytheradulalasting (i.e.,deliberatecannibalism)haseverbeenreportedinthe
approximatelytwoseconds.Iestimatethat20ofthese Chromodorididaetomyknowledge.MycolleagueScott
radularraspingcyclestookplacebeforethebuccalmasswas Johnson,whohasbeenstudyingandobservingnudibranchs
retracted.Bothindividualswereraspingateachothersimul- subtidallyintheMarshallIslandsfor25years,hasnever
taneously(Fig.1).Soextremeweretheseraspingcycles,that seenanyaggressivebehaviourbychromodorids.According
Icouldeasilymakeouttheradularribbonatthetipofthe tohimChromodorisannaeisrareintheMarshallIslands.
evertedprobosciswithmynakedeye. ThecausefortheaggressivebehaviourwhichIobserved
Afterapproximatelytwominutesofhead-to-head wasnotobvious.Itwascertainlyaneventinvolvingtwo
combat,theindividualscrawledroundandroundeach conspecificindividualsofmatchedsize.Icandefinitely
92 otherwhileremaininginclosecontactandtheattacks eliminatethepossibilitythattwoindividualsofdifferent
continuedundiminishedinadifferentorientation.Atone (i.e.,sibling)specieswereinvolved.Eventhoughadozen
point,oneoftheanimalsrearedupabovetheotherlikea speciesofthe‘black-lined’groupofChromodorisspeciesare
cobra,exposeditsoraltube(Fig.4),anddirectedaradular knowntooccurinIndonesianwaters,thesetwoindividuals
biteattheotherindividualinconjunctionwithadownward weredefinitelybothC.annae.Iamsufficientlyfamiliarwith
lungeontopofit.Duringthebout,radularraspingwas otherverysimilarlooking(i.e.,pheneticallysimilar)‘black-
directedatthehead,themantlemargin,therhinophores lined’speciesthatoccurinthispartofsoutheastAsia–
andthegills.Noraspingattacksweredirectedtowardsthe C.michaeliGosliner&Behrens,1998,C.dianaeGosliner&
genitalarea.Clearlytheseattackswerepainfulaseach Behrens,1998,C.elisabethinaBergh,1877,C.magnifica(Quoy
individualretractedthatpartofthebodyfollowingabite, &Gaimard,1832),C.cf.africanaEliot,1904,C.strigataRud-
andtherhinophores(Fig.2)andthegills(Fig.3)were man,1982,C.colemaniRudman,1982,C.lochiRudman,1982,
instantaneouslyretractedwhentheywerebeingbitten. C.willaniRudman,1982,C.joshiGosliner&Behrens,1998
Duringthe‘fight’bothindividualssustainedsomedamage andsomeundescribedspecies(Kodiat,2010a)–toconfirm
tothemantlebrim(Fig.5arrow)astheresultofradular thattheywerenotinvolvedandthusbecertainthetwo
rasping. individualsbelongedtothesamespecies.
The‘fight’lastedfor12minutes,afterwhichtimeboth IdonotthinkwhatIobservedwasacourtshipritual(i.e.,
individualsbecamequiescentandmotionless,andmoved aggressiveforeplay)becausethegenitalaperture/organs
outofcontact. wereneverprotractedineitherindividualandthebiting
Atnotimeduringthe‘fight’couldIobservetheexpul- wasneverdirectedtowardthegenitalregion.However,
sionofanyrepugnatoryfluidfromthemantleofeither bothindividualswouldhavebeensexuallymatureandthey
individual,soIassumenonewasbeingproduced. couldhavematedjustbeforethis‘fight’,soitcouldhave
Basteria74(4-6)
B74-Willan:Basteria-2010 16/11/2010 21:00 Page 93
beenroughafterplay.Nospawnbelongingtothisspecies(a References
whiteflattenedopencoil,asfiguredbyBehrens,2005:119
andbyCobb,2009)wasinthevicinityandChromodoris Behrens,D.W.,2005.Nudibranchbehavior:1-176.NewWorld
annaedoesnotbrooditsspawn,soitisunlikelyoneanimal PublicationsInc.,Jacksonville,Florida,U.S.A.
wasdefendingitsspawnastheaeolidnudibranch Cobb,G.,2009.ChromodoriaannaefoundsthnQueensland.–TheSea
PteraeolidiaianthinaAngas,1864does(Willan,1990). SlugForumhttp://www.seaslugforum.net/message/23001.Last
Asnonudibranchisknowntobeterritorial[exceptfor accessed19August2010.
Pteraeolidiaianthina(Angas,1864)duringtheincubationof Kodiat,E.,2010a.Chromodorissp.–NudiPixel
itseggs;seeabove],itishighlyimprobablethatthetwo http://www.nudipixel.net/species/chromodoris_sp/.Lastaccessed
Chromodorisannaewerefightingoverterritory.However, 19August2010.
theycouldhavebeenfightingoveratinypieceoffoodthat Kerstitch,A.1989.SeaofCortezmarineinvertebrates:aguideforthe
wasinvisibletome.Butthenalargeclumpoftheir PacificCoast,MexicotoEcuador:1-113.SeaChallengers,Monterey,
dictyoceratid(probablyfamilyThorectidae)spongefood California,U.S.A.
waspresentnearby.Ithadalreadybeendiscoveredbytwo Janus,H.,1982.Theillustratedguidetomolluscs[ExpandedEnglish
otherindividualsanditwouldhavebeenproducingstrong edition]:1-180.BurkePublishingCo.Ltd,London,U.K.
pheromones,sothesetwoindividualscouldhavecrawled Miller,M.,1999.Roboastratigrisupdate.–TheSlugSite
overtoeatitratherthanfightoveratinymorsel. http://slugsite.us/bow/roboastra/robo_la.htmLastaccessed
Despitetheinabilitytoidentifyareasonforthis 22August2010.
aggressivebehaviour,itsexistenceprovidesanexplanation Osumi,D.&Yamasu,T.,1994.ThenudibranchGymnodorisnigricolor
fortheobservationthatadultchromodorids,particularly Baba,parasiticwithmarinegobies.–ZoologicalScience11
membersofthe‘black-lined’speciesgroup,sometimeshave (Supplement:Proceedingsofthe65thAnnualMeetingofthe
tatteredmantles(e.g.,Willan,2005:fig.12;Willan& ZoologicalSocietyofJapan):54. 93
P.Poppe,2010).Perhapssuchdamageresultsnotfrom Rowson,B.&R.,2005.Happyslappingslugs.–MolluscWorld9:11,
attemptsatpredationbyfishesand/orcrustaceans,butfrom figonp.9.
numerousaggressiveencounterswithconspecificslikethe Scott,J.,2010b.Chromodorisannae.–NudiPixel
oneIwasfortunatetohavewitnessedinTimor-Leste? http://www.nudipixel.net/photo/00025986/.Lastaccessed
19August2010.
Acknowledgements Thompson,T.E.,1976.Biologyofopisthobranchmolluscs1:1-205.
TheRaySociety,London,U.K.
IthankmydivingbuddyNeilWrightfordrawingmy Willan,R.C.,1990.Fieldobservationsonfeedingandantagonistic
attentiontothisextraordinaryeventandfortakingthe behaviorbyPteraeolidiaianthina(Nudibranchia:Aeolidoidea).–
photosthatshowitsowell.GaryCobb(SunshineCoast, TheVeliger32(2):228-229.
Queensland)composedtheplate.GaryCobb,ScottJohnson Willan,R.C.,2003.Chapter12Nudibranchs.In:Andrew,N.
(MarshallIslands)andYen-WeiChang(Kaohsiung,Taiwan) &Francis,M.(eds),2003:100-107.Thelivingreef:theecologyof
confirmedtheyhadneverwitnessedaggressivebehaviour NewZealand’srockyreefs.CraigPottonPublishing,
bychromodoridsintheirmanyhoursofobserving Nelson,NewZealand.
nudibranchsunderwater.Divinggearandsupportforthe
surveyinTimor-LestewasprovidedbyDiveTimorLorosae.
Willan,R.C.–Aggressivebehaviourinachromodoridnudibranch
B74-Willan:Basteria-2010 16/11/2010 21:00 Page 94
Willan,R.C.,2005.Themolluscanfaunafromtheemergentreefsofthe Willan,R.C.&PoppeP.,2010.Chromodorididae.In:Poppe,G.T.,2010,
northernmostSahulShelf,TimorSea–Ashmore,Cartierand Philippinemarinemolluscs3:190-272.ConchBooks,Hackenheim,
HiberniaReefs;biodiversityandzoogeography.–TheBeagle, Germany.
RecordsoftheMuseumsandArtgalleriesoftheNorthernTerritory
2005,Supplement1:51-81.
94
Basteria74(4-6)