Female attack is not necessary for male copulatory organ breakage in the sexually cannibalistic spider Argiope argentata (Araneae: Araneidae)

2011·2.7 MB·English

by  Soledad Ghione

2011.TheJournalofArachnology39:197-200
SHORT COMMUNICATION
Female attack is not necessary for male copulatory organ breakage in the sexually cannibalistic spider
Argiope argentata (Araneae: Araneidae)
SoledadGhione'-^andFernandoG.Costa-: 'LaboratoriodeEcologiadelComportamiento,-LaboratoriodeEtologia,Ecologia
&Evolucion,InstitutedeInvestigacionesBiologicasClementeEstable,AvenidaItalia3318, 11600Montevideo,Uruguay. E-
mail: [email protected]
Abstract. Insexuallycannibalisticspiders,malesusuallyonlycopulatewithonefemale.Thisselectsformalestrategiesto
improvepaternitysuccessintheirsinglemate.Malematingstrategiescanincludegenitaldamageduringfemaleattackin
somecannibalisticorb-weavingspiders, wheremalesaredwarfand females polyandrous. Weexplored whethersexual
cannibalismisnecessaryformalegenitaldamagein thesilverspiderArgiopecirgenlata(Fabricius 1775) byperforming
matingtrialswithrecentlykilledvirginfemales.Wefoundthatmalescanbreakofftheircopulatoryorganswithoutfemale
interventionandspontaneouslydieduringcopulation. Resultssuggestthatgenitaldamageevolvedinresponsetosperm
competitioninthisspecies.
Keywords: Genitaldamage,spermcompetition,matingplug
Sexual cannibalism, defined as instances where females kill and insertion and increased copulation duration, whereas males that do
consum.e conspecific males before, during, or aftercopulation, has not break their organs are cannibalized (Schneider et al. 2001). In
beenconsidered an extremecaseofconflict ofinterest between the Argiopelohala(Pallas1772),cannibalizedmalesbreakofftheirgenital
sexes (Elgar 1992). Males benefit by fertilizing more eggs, while copulatoryorgansmorefrequently than survivingmales, suggesting
femalescan benefitby remating(Simmons2005), leadingto sexual thatsexualcannibalismfacilitatesgenitaldamage(Nessleretal.2008).
antagonisticcoevolution(Arnqvist& Rowe2005). Sexualcannibal- ThesilverspiderArgiopecirgentata(Fabricius 1775)isanaraneid
ism has been reported for a variety of invertebrates, including spider with Pan-American distribution (Levi 1968). In the field,
crustaceans, insects, and arachnids, and is particularly frequent Robinson&Robinson(1980)observedthatmalesarriveonfemales’
amongspiders(Elgar1992).Ifmalestransferspermsuccessfully,then webs,court fromtheperiphery,andafterwardsmovetothehubof
sexualcannibalismmaybepartofamalematingstrategy(Elgar& thewebwherematingusuallyoccurs,andsexualcannibalismalways
Schneider2004).Inthesecases,malesmaximizetheirpaternityinan occursduringoraftercopulation. In thelaboratory, virgin females
act ofsingle mating, becoming monogynous. Such terminal invest- areusuallyreceptivetocourtingmales,buttheyattackthemduring
mentwithoutparentalcarehasbeenshowntoevolveunderamale- thefirstinsertion,forciblydislodgingmalesfromtheirgenitaliawith
biased effective sex ratio with high risk of sperm competition theirthirdpairoflegs,resultingin70%ofthemalesdying(Ghione
(Fromhageetal.2005). 2008). Surviving males reinitiate courtship and perform a second
In a framework of high sperm competition, males will develop insertion;afterthattheyareconsumedbythefemales. Malesalways
offensiveanddefensivestrategiestoprotectpaternity, includingthe breaktheapicalregionoftheembolus,includingasingularscleriteor
use ofmating plugs. Mating plugs can be substances that become spurofunknownfunction(Levi 1968),thatremainsstuckinsidethe
hardwhileoccludinggenitalducts(Baeretal.2001;Polaketal.2001; femaleducts(Ghioneetal.2006;Ghione2008).
Aisenberg&Eberhard2009),orpartsortheentiremalecopulatory In the present study, we used freshly killed females to explore
organ, a process known as genital damage (Eberhard 1985; experimentally ifmales can break off their copulatory organs by
Kamimura 2003; Uhl et al. 2010). Genital damage is widespread themselves,oriffemalecannibalisticattackdeterminesmalegenital
amongsexuallycannibalisticspiders,wheremales usuallybreakoff damage.Wehypothesizethatthefemale’sattackhasadirectimpact
parts or the entire copulatory organ during copulation (Andrade onthecopulatoryoutcome,bothintheremovalofthemaleandthe
1996;Andrade& Banta2002; Elgar&Schneider2004; Foellmer& breakingoffoftheinsertedcopulatoryorgan.
Fairbairn 2004; Miller 2007; Nessler et al. 2008). Male spiders’ We collected nine subadult males, 11 subadult females, and 18
copulatory organs are paired (palpal bulbs) and the intromittant adultmalesofA.cirgentatabetweenSeptembertoMarch(springand
features, the emboli, are introduced into the paired female genital summer of2005-2006 and 2006-2007), in meadows at Piedras de
openingsduringmating,usuallyoneatatime.Inspiders,allknown Afilar, Canelones, Uruguay (34°45'42.5"S and ’55°33'10.8"W), a
cases ofgenital damage occur in entelegyne spiders in which the temperate region. We housed spiders individually in 500-ml glass
genitaliaaresclerotizedandtheovipositoryductisindependentfrom containers,providingwaterdaily,and Tenebriosp.larvae(Tenebrio-
the copulatory ducts, and therefore not occluded by mating plugs nidae)twiceperweek.
(Uhletal.2010). In order to determine ifthe male can break offhis copulatory
Inspiders,paternitysuccessisusuallylinkedtocopulationduration organsbyhimselforifitisthefemalethatbreaksthemoffwhenshe
andspermtransfer(Elgar1995).Schneideretal.(2006)andNessleret abruptly removes the male from her genitalia, we carried out
al.(2006)suggestedtheoccurrenceofasexualconflictovercopulation experiments with recently killed virgin females. We killed them by
duration in the orb-web spider Argiope hruennichi (Scopoli 1772), means of hypothermia, placing them at a low temperature for
wherefemaleattackoccurspreciselywhenthemaledislodgestheused 20minutes. Afterwards, dead femaleswerecarefullyattached “face
copulatory organ and tries to insert theotherone (Schneideret al. down”(typical“sitandwait”andmatingposture)totheirownweb’s
2006).Intheorb-webspiderNephikipliimipes(Latreille 1804),palpal radii,fixedbyaddingmeltedparaffinontoeachoftheireightlegtarsi.
organ breakage increases male survivorship, allowing a second Once females were fixed to the web in the proper position, we
197
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Figure 1. a)DeadmaleattachedtofemalegenitaliainArgiopeargeiitcitcr,b)thesamemaleinsertingtherightpalpalorganandshowingthe
leftonewiththebrokenembolustip(arrow).
carefullyremovedsilkwithforcepsfromtheirspinneretsandaddedit fromtheperipherybutdidnotmovetothehubwithinonehour,ora
tothehuborcenteroftheweb,asnaturallyoccurswhenfemalesare maleinitiatedcourtshipbutdidnotproceed tocopulationoverthe
positionedintheweb. courseoftwohours.Thisexchangeofunsuccessfulmalescontinued
Foreachtrial,twoadultmaleswerecarefullyplacedequidistantly until eithercopulation occurred ora total of5 hours had elapsed,
fromthemarginoftheorb-webofarecentlyattachedkilledfemale. limitedbytherapiddecayofthedeadfemaleinwarmexperimental
We placed two males to increase the likelihood ofcopulation. We conditions.Whenonemaleachievedcopulation,theothermalewas
simulated female behaviors observed in a sexual context (Ghione, immediately(butcarefully)removedfromthewebinordertoavoid
pers. obs.) by softly shaking the web, using a pencil to prod the male-maleinterferences.
female’s corpse, in response to male courtship. We replaced males We performed a total of 11 trials and obtained four successful
when a maledid notcourtduringa 15-min period,a malecourted copulations.Theoccurrenceofcopulationswashighlyunpredictable
GHIONE&COSTA—MALEGENITALDAMAGEINARGIOPEARGENTATA 199
anddifficult.Malegenitaldamagewasdeterminedunderadissecting reviewer for carefully reading the manuscript and improving the
microscope. Wedeposited voucherspecimens in thearachnological English.
collectionofFacultaddeCiencias,Montevideo,Uruguay.
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