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An arboreal spider protects its offspring by diving into
the water of tank bromeliads
Yann Hénaut, Bruno Corbara, Frédéric Azémar, Régis Cereghino, Olivier
Dezerald, Alain Dejean
To cite this version:
Yann Hénaut, Bruno Corbara, Frédéric Azémar, Régis Cereghino, Olivier Dezerald, et al.. An arboreal
spider protects its offspring by diving into the water of tank bromeliads. Comptes Rendus Biologies,
Elsevier Masson, 2018, 341 (3), pp.196-199. �10.1016/j.crvi.2018.02.002�. �hal-02621666�
An
arboreal
spider
protects
its
offspring
by
diving
into
the
water
of
tank
bromeliads
Une
araigne´e
arboricole
utilise
les
re´servoirs
d’eau
des
brome´liace´es
pour
se
prote´ger
et
prote´ger
son
cocon
Yann
He´naut
a,*
,
Bruno
Corbara
b,
Fre´de´ric
Aze´mar
c,
Re´gis
Ce´re´ghino
c,
Olivier
De´zerald
d,
Alain
Dejean
c,ea
ElColegiodelafronterasur,UnidadChetumal,Av.Centenario,Chetumal,QuintanaRooAP424,Mexico
b
Universite´ ClermontAuvergne,CNRS,LMGE,63000Clermont-Ferrand,France
c
EcoLab,Universite´ deToulouse,CNRS,INPT,UPS,Toulouse,Toulouse,France
dLaboratoireinterdisciplinairedesenvironnementscontinentaux(LIEC)–CNRSUMR7360,Universite´ deLorraine,CampusBridoux,
57070Metz,France
e
CNRS,UMREcoFoG,AgroParisTech,Cirad,INRA,Universite´ desAntilles,Universite´ deGuyane,97310Kourou,France
ARTICLE INFO Articlehistory:
Received29November2017
Acceptedafterrevision13February2018 Availableonline9March2018
Keywords: Aechmeabracteata Cupienniussalei
Waterusedinprotectivebehavior Eggsacs
Motscle´s: Aechmeabracteata Cupienniussalei Cocons
Eauutilise´edansuncomportement protecteur
ABSTRACT
Cupienniussalei(Ctenidae)individualsfrequentlyliveinassociationwithtankbromeliads, includingAechmeabracteata,inQuintanaRoo(Mexico).WhereasC.saleifemaleswithout eggsacshuntovertheirentirehostplant,femalescarryingeggsacssettleabovetheA. bracteatareservoirstheyhavepartiallysealedwithsilk.Theretheyavoidpredatorsthat usesighttodetecttheirprey,asisknownformanybirdspecies.Furthermore,ifadangeris moreacute, thesefemalesdivewith theireggsacs intothebromeliad reservoir.An experimentshowedthatthisisnotthecaseformalesorfemaleswithouteggsacs.In additiontothelikelyabundanceofpreyfoundtherein,thepotentialofdivingintothetank toprotectoffspringmayexplainthecloseassociationofthisspiderwithbromeliads.These resultsshowthat,althougharboreal,C.saleievolvedaprotectivebehaviorusingthewater oftankbromeliadstoprotectoffspring.
C 2018Acade´miedessciences.PublishedbyElsevierMassonSAS.Allrightsreserved.
RE´ SUME´
L’araigne´eCupienniussalei(Ctenidae)vitsouventenassociationaveclabrome´liace´ea` re´servoir Aechmea bracteata. Dans le Quintana Roo (Mexique), les femelles qui transportent un cocon s’installent au-dessus d’un re´servoir d’A. bracteata qu’elles obstruentpartiellementdevoilesdesoiepoursecamouflerdespre´dateurs.Enpre´sence devibrationsimportantesetre´pe´te´es,cesfemellesplongentavecleurcocondansl’eaudu re´servoir.Notre e´tude montreque lesautres adultes(maˆleset femelles sanscocon) n’utilisentpaslesre´servoirsd’eau.Ainsi,enplusdel’abondancedeproies,lapossibilite´ de
* Correspondingauthor.
E-mailaddress:yanneno@gmail.com(Y.He´naut).
ContentslistsavailableatScienceDirect
Comptes
Rendus
Biologies
ww w . sci e nc e di r e ct . com
https://doi.org/10.1016/j.crvi.2018.02.002
1. Introduction
Althoughmostspiderspeciesareterrestrial,agradient
in theirrelationshipwiththeaquaticenvironment does
exist. Theiconic exampleis seenin Argyronetaaquatica
(Cybaeidae),whoseindividualslivealmostentirelyunder
waterthankstotheabilityofhydrophobichairstoretaina
bubbleofair.Furthermore,theybuildsilkstructuresthat,
like diving bells,retain air and permit them toremain
submergedandeventodetectpreythattouchthissilknet
[1,2].Thebubbleofairretainedbythehydrophobichairs
or the silk of the diving bell allows respiration as gas
exchanges with the surrounding water occur through
differencesinthepartialpressureofoxygen andcarbon
dioxide[1,3].
Some other spider species hunt aquatic organisms,
includinginsects,tadpoles,frogs,andfishonthesurfaceof
thewater,andarethuscalledsemi-aquaticspiders.Thisis
thecasefordifferentspeciesofthePisauridaeandCtenidae
whosehuntingindividualsstayincontactwithaterrestrial
substratewhenhunting[4,5].Divingwasobservedinthe
genus Pirata(Lycosidae) when, occasionally,individuals
hunt aquatic prey such as larval mayflies and isopods
[6]. Thanks to their hydrophobic hairs, semi-aquatic
spiders most generallydive asa protectivestrategy, so
thatPirataspp.canremainunderwaterfor24hifdisturbed
[6] and Dolomedes triton (Pisauridae) for 90min [7],
whereasAncylometesrufus(Ctenidae)individualsdiveto
escape predators, but the duration of the time spent
underwaterisnotknown[4].
As noted for certain other webless, arboreal spider
species[8–10],Cupienniussalei(Ctenidae)individualsare
frequentlyassociatedwithepiphytictankbromeliadsthat
providethemwithasuitablehabitat[11].InQuintanaRoo,
Mexico,thehosttankbromeliadisAechmeabracteatathat
hasgroupsofshootsatdifferentontogeneticstages,each
forming a rosette with numerous water reservoirs or
phytotelmata [12]. Tank bromeliads shelter various
terrestrialand aquaticorganisms[12–15]; amongthem,
emergingwingedinsectsarepotentialpreyforspiders[5].
Basedon preliminaryfieldobservations,weaimedin
this study toverify if bromeliad reservoirs serve as an
aquaticrefugeforC.saleiindividuals.
2. Materialandmethods
ThisstudywasconductedinaninundatedNeotropical
forest(QuintanaRoo,Mexico;18.4267258N;88.8043608
W;120metersa.s.l.).Theidentificationofthespiderswas
basedonvoucherspecimensdepositedinthecollectionof
the‘‘MuseodeZoologı´a’’inEcosur,Chetumal,Mexico.
Cupienniussalei,calledthe‘wanderingtigerspider’due
todarkstripesonitsbodyandlegs,originatesfromCentral
America. Thisisanarboreal, weblessspecieswithlarge
individuals(10cmlegspanand3.5cminbodylengthfor
adult females, males measure up to 2.5cm in length)
[16]. Individuals are nocturnal, ambush predators that
detectpreythroughtheperceptionofvibrationsandrely
onaneurotoxicvenomtoparalyzeprey[17–20].
Adultmalesandfemales withouteggsacsaswellas
juvenileswereobservedwanderingonA.bracteataduring
thisstudy.Femaleswitheggsacsbuildathickcoatofsilk
that partially seals one reservoir (height: 6–12cm;
diameter: 5–12cm; volume of water: 110–250ml) of
thehostbromeliadandstaybehindthiscoat,carryingthe
egg sac behindtheir abdomen, 5cm above thewater
(Fig.1)[11].
Wetestedthereactionsofadultmalesandfemaleswith
orwithoutaneggsacbyhavingoneexperimenterrapidly,
but lightlytapa 20-cm-longwoodenstickon theplant
withaforcecorrespondingtoknockingonadoor(15cm
fromthespiders;5timesduring2srepeatedevery10s,
untilthespidersreactedbyfleeing).Wenotedthebehavior
ofthesemaleandfemalespiders(seeTable1).Forfemales
carryingan eggsac,priortothisexperiment,we gently
openedthecoatofsilktoobservetheirbehaviorand,after
1min, as they seemed unalarmed, we used the same
procedure asfor themalesand otherfemales. Thislast
experimentwasconductedthreetimesseparatedby2h
topermitthespiderstocalmdown.
Two females that had remained underwater during
morethan30minwiththeireggsacwerecollected,taken
tothelaboratoryandinstalledinaterrariumwithashoot
ofA.bracteatatoverifyiftheyandtheirbroodsurvivedthis
longimmersion.
3. Resultsanddiscussion
In theexperimental situation, all C. salei males and
femalesdevoidofaneggsacmovedbehindtheshootto
hide. When the tapping continued, they fled the host
bromeliadtoseekanotherhidingplace(seeTable1forthe
numberofobservations). In twocases,theyraisedtheir
forelegsandopenedtheircheliceraebeforefleeing.
Whenconfrontedwiththedisturbances,allsixfemales
witheggsacsfirstopenedtheircheliceraeandraisedtheir
forelegs in a posture of intimidation. When disturbed
again,theychangedthepositionoftheireggsacs,initially
situated behind their body, grasping them with their
forelegs to place them in front of the cephalothorax
(Fig.2A),anddivedintothewaterwiththeeggsac(Fig.2B
andC;Table1). Allsixfemales stayedunderwaterfrom
30to90min.Lateron,afterthesefemalesleftthewaterof
thetankof thebromeliadsand returned totheir initial
position,thesameexperimentwasconducted,resultingin
thesameresult.Whenthisexperimentwasconductedfor
pouvoirplongerpourprote´gerladescendancepourraitexpliquerl’associationentre cette espe`ced’araigne´e et les brome´liace´es. Nosexpe´riences montrent que les femellesporteusesd’uncoconmanifestentunestrate´giedeprotectionvis-a`-visdes coconsetd’elles-meˆmesens’immergeantdurant30,voire90minutes.
C2018Acade´miedessciences.Publie´ parElsevierMassonSAS.Tousdroitsre´serve´s.
thethirdtime,thefemalespidersquicklyjumpedoutof
thetankcarryingtheireggsacs,movedbehindtheshootof
thehostbromeliadandjumpedontoanotherplantasdid
spiderswithouteggsacs.
Thetwofemales bredinthelaboratorycontinuedto
carry their egg sacs; after 4 and 5 days, respectively,
spiderlingsemerged.Theyremainedontheexternalpartof
thebromeliad,thefemalealwaysremainingclosetothem
inadefensiveposture.Therefore,asforthedivingbellsof
Argyroneta,thesilkoftheeggsacslikelyretainsairthrough
surfacetensionstrengths.
Although terrestrial (i.e. neither aquatic nor
semi-aquatic), C. salei females have adapted to diving, but,
because in this experiment they dove only when they
carriedeggsacs,thisbehaviorisspecificallyrelatedtotheir
fitness (i.e. offspring protection). Indeed, wandering
Ctenidaearehighlysusceptibletobeingpreyeduponby
birdsinforestcanopiesandfemalesaremoreattractiveto
visualhuntingpredatorswhencarryinganeggsacwhose
colorcontrastswiththespiderbody[21].
The previous known cases of spiders able to dive
correspondtotheaquaticArgyronetathatuseadivingbell
andsemi-aquaticspidersthatdivetoavoidpredation(and
onlyoccasionallytohunt)[1,4,6,7].Thepresentstudyadds
thecaseofterrestrialfemalespidersdivingwiththeiregg
Fig.2.Behaviorofthespiderswhencarryingeggs.Movingtheeggsacs, initiallysituatedbehindthespider,infrontofthecephalothorax(A). Holdingtheeggsac,usingthefirstlegs(B),anddivingintothewater(C). Thewhitescalesrepresent1cm.
Fig.1. ShootofAechmeabracteatawiththecoatofsilk(A),thespiderand behind,itseggsac(B).Thewhitescalesrepresent5cm.
Table1
BehaviorofCupienniussaleiindividualsnotedonAechmeabracteata.Comparisonsoftheirreactionswhenleftaloneorwhendisturbed(seetext).Statistical comparisonofthereactionofdisturbedfemaleswithorwithoutaneggsac;Fisher’sexact-test(Pastsoftware):P=4.34106
.
Cupienniussaleiindividualsnotedontankbromeliads Naturalsituation Afterbeingdisturbed Hunt Buildawebaboveawell Escape Dive
Juveniles 15 0 – –
Adultmales 15 0 15 0
Adultfemales 20 0 20 0
sacstoprotect their offspring frompredatorsthanksto
theirassociationwithtankbromeliads.Becauseusingthe
reservoirsofa tankbromeliadallowsC.salei femalesto
protecttheiroffspringbeyondthelimitsoftheirphysical
capacities(e.g.,chelicera,legs),thisusecanbeconsidered
an‘extendedphenotype’[22,23].
Inconclusion,therelationshipbetweenC.saleiandtank
bromeliadsismuchmorecomplexthanpreviouslyknown,
the benefit for the spider being related both to prey
availability[5]anditsfitness(thisstudy).Indeed,C.salei
females bearingeggsacsprotecttheir offspringthrough
camouflage by purposely constructing a web above a
reservoirofatankbromeliadandescapethreatsbydiving
intothatreservoir.
Disclosureofinterest
The authors declare that they have no competing
interest.
Acknowledgments
We are gratefulto Andrea Yockey-Dejean for
proof-reading themanuscript. Financialsupportfor thisstudy
was provided by the French ‘Centre national de la
recherchescientifique’(CNRS;project2ID)andaninternal
fundofElColegiodelaFronteraSur(ECOSUR),Mexico.
References
[1]D.Schu¨tz,M.Taborsky,Adaptationstoanaquaticlifemaybe respon-sibleforthereversedsexualsizedimorphisminthewaterspider, Argyronetaaquatica,Evol.Ecol.Res.5(2003)105–117.
[2]M.R. Flynn,J.W.M.Bush,Underwaterbreathing: themechanicsof plastronrespiration,J.FluidMech.608(2008)275–296.
[3]R.S.Seymour,S.K.Hetz,Thedivingbellandthespider:thephysicalgill ofArgyronetaaquatica,J.Exp.Biol.214(2011)2175–2181.
[4]M.Ribeiro-Moura,L.Pimenta-Azevedo,Observationofpredationofthe giantfishingspiderAncylometesrufus(Walckenaer,1837)(Araneae, Ctenidae)onDendropsophusmelanargyreusCope,1877(Anura, Hyli-dae),BiotaNeotrop.11(2011)349–351.
[5]M.Nyffeler,B.J.Pusey,Fishpredationbysemi-aquaticspiders:aglobal pattern,PLoSONE9(2014)e99459.
[6]W.Gettmann,UntersuchungenzumNahrungsspektrumvon Wolfspin-nen(Lycosiden)derGattungPirata,Mitt.Dt.Ges.Allg.Angew.Ent.1 (1978)63–66.
[7]J.C.Johnson,A.Sih,Fear,food,sexandparentalcare:asyndromeof boldnessinthefishingspiderDolomedestriton,Anim.Behav.74(2007) 1131–1138.
[8]S.Calac¸a-Dias,A.Domingos-Brescovit,Microhabitatselectionand co-occurrenceofPachistopelmarufonigrumPocock(Araneae, Theraphosi-dae) and Nothroctenus fuxicosp. nov.(Araneae,Ctenidae) intank bromeliadsfromSerradeItabaiana,Sergipe,Brazil,Rev.Bras.Zool. 21(2004)789–796.
[9]G.Q. Romero,J. Vasconcellos-Neto,Spatialdistribution patternsof jumpingspidersassociatedwithterrestrialbromeliads,Biotropica36 (2004)596–601.
[10]J.A.Santos,G.Q.Romero,Anewbromeliad-dwellingjumpingspider (Araneae,Salticidae)fromBrazil,J.Arachnol.32(2004)188–190.
[11]Y.He´naut,B.Corbara,L.Pe´lozue´lo,F.Aze´mar,R.Ce´re´ghino,B.He´rault, A.Dejean,Atankbromeliadfavorsspiderpresenceinaneotropical inundatedforest,PLOSONE9(2014)e114592.
[12]A.Dejean,I.Olmsted,EcologicalstudiesonAechmeabracteata(Swartz) (Bromeliaceae),J.Nat.Hist.31(1997)1313–1334.
[13]J.H.Frank,L.P.Lounibos,Insectsandalliesassociatedwithbromeliads: areview,Terr.Arthropod.Rev.1(2009)25–153.
[14]S.Talaga,O.De´zerald,A.Carteron,F.Petitclerc,C.Leroy,R.Ce´re´ghino,A. Dejean,Tankbromeliadsasnaturalmicrocosms:afacultative associa-tionwithantsinfluencestheaquaticinvertebratecommunity struc-ture,C.R.Biol.338(2015)696–700.
[15]A.Dejean,F.Petitclerc,F.Aze´mar,L.Pe´lozue´lo,S.Talaga,M.Leponce,A. Compin,AquaticlifeinNeotropicalrainforestcanopies:techniques usingartificialphytotelmatatostudytheinvertebratecommunities inhabitingtherein,C.R.Biol.(2017)20–27.
[16]T.Tomasinelli,Cupienniussalei,Br.TarantulaSoc.J.15(1999), http:// www.thebts.co.uk/media/Cupiennius%20salei.pdf.
[17]E.A.Seyfarth,Dailypatternsoflocomotoractivityinawandering spider,Physiol.Entomol.5(1980)199–206.
[18]F.G.Barth,H.Bleckmann,J.Bohnenberger,E.A.Seyfarth,Spidersofthe genusCupienniusSimon1891(Araneae,Ctenidae).II.Onthevibratory environmentofawanderingspider,Oecologia77(1988)194–201.
[19]L. Kuhn-Nentwig, I.M. Fedorova, B.P.Lu¨scher, L.S. Kopp, C. Trachsel, J. Schaller, X.L.Vu,T.Seebeck,K.Streitberger,W.Nentwig,E.Sigel,L.G.Magazanik,A venom-derivedneurotoxin,CsTx-1,fromthespiderCupienniussaleiexhibits cytolyticactivities,J.Biol.Chem.287(2012)25640–25649.
[20]C.Trachsel,D.Siegemund,U.Ka¨mpfer,L.S.Kopp,C.Bu¨hr,J.Grossmann, C.Lu¨thi,M.Cunningham,W.Nentwig,L.Kuhn-Nentwig,S.Schu¨rch,J. Schaller,Multicomponent venom ofthe spider Cupienniussalei: a bioanalyticalinvestigationapplyingdifferentstrategies,FEBSJ.279 (2012)2683–2694.
[21]B.Gunnarsson,K.Wiklander,Foragingmodeofspidersaffectsriskof predationbybirds,Biol.J.Linn.Soc.115(2015)58–68.
[22]R.Dawkins,TheExtendedPhenotype.TheLongReachoftheGene, OxfordUniversityPress,Oxford,UK,1982.
[23]P.Hunter,Extendedphenotyperedux.Howfarcanthereachofgenes extendinmanipulatingtheenvironmentofanorganism?EMBORep. 10(2009)212–215.
