Gherardi, Francesca

Renai, B.

English

Florence Research

Biologia Ambientale - 2006, 20 (1): 183-187.Atti 10° Convegno Nazionale A.I.I.A.D., Montesilvano (PE), 2-3 aprile 2004. A.I.I.A.D.Mating and sexual selection in thethreatened crayfish, Austropotamobius italicusBarbara Renai, Francesca Gherardi*Dipartimento di Biologia Animale e Genetica “Leo Pardi”, Universitá di Firenze, Via Romana 17, 50125 Firenze, Italy* Referente per la corrispondenza (francesca.gherardi@unifi.it)AbstractMating by the threatened crayfish Austropotamobius italicus was studied in the laboratory during October-November 2002. For twohours we observed the interactions occurring in 17 groups composed of three differently-sized adult males and one receptive female andwe checked, in the subsequent three days, for spermatophore deposition by males and for spawning by females. Results showed: (1) the“reluctant” and “choosy” behaviour of the females, (2) the large-male size advantage, and (3) the occurrence of a form of “spermcompetition”. In our study, we did not find an ultimate explanation for female preference of large males. Indeed, male size is a goodpredictor of the outcome of intrasexual competition for the access of mates. If males have genes that enable them to attain the larger size,females mating with big males might produce big sons and therefore gain better reproductive success through their sons’ progeny.KEY WORDS: sexual selection / mate choice / Austropotamobius italicus / “sperm competition” / large-male size advantageComportamento riproduttivo e selezione sessuale nel gambero minacciato Austropotamobius italicusAlcuni aspetti del comportamento riproduttivo del gambero di fiume minacciato Austropotamobius italicus sono stati analizzati inlaboratorio nel periodo compreso tra ottobre e novembre 2002. Sono state osservate per due ore le interazioni di 17 gruppi composticiascuno da tre maschi adulti, di differenti dimensioni, e una femmina ricettiva. Nei tre giorni successivi sono stati eseguiti controlli perverificare l’eventuale presenza di uova nelle femmine e/o la deposizione di spermatofore da parte dei maschi. Dall’analisi dei risultati èemerso che: 1) le femmine sono generalmente “riluttanti” ed “esigenti”, 2) i maschi di maggiori dimensioni hanno più successo nellacompetizione intrasessuale e 3) anche nei gamberi è presente una forma di competizione spermatica. Non è stata trovata una spiegazionedefinitiva della preferenza della femmina per i partner “grandi”. Le dimensioni del maschio sono comunque un buon indice della riuscitanella competizione per l’accesso alla femmina. Se i maschi hanno geni che permettono loro di ottenere una taglia maggiore, le femmine chesi accoppiano con questi potranno generare individui di grandi dimensioni e ottenere un miglior successo riproduttivo attraverso la loroprogenie.PAROLE CHIAVE: selezione sessuale / scelta del partner / Austropotamobius italicus / “competizione spermatica” / vantaggio del maschiodi maggiori dimensioniINTRODUCTIONDARWIN (1871) was the first author to differentiatebetween two processes, the first favouring ‘the powerto charm the females’ (“intersexual” or “epigamic”selection; HUXLEY, 1938a,b), and the second favouring‘the power to conquer other males in battle’ (“intra-sexual” selection; HUXLEY, 1938a). Subsequent studiesshowed that intersexual and intrasexual selections of-ten act simultaneously to mould the mating behaviourof a species. However, except for a few examples(e.g. CHRISTY, 1982; FUKUI, 1995; VILLANELLI & GHE-RARDI, 1998), this issue has been neglected in thecrustacean decapod literature.The white-clawed crayfish, Austropotamobius ita-licus, is endemic to Italy (FRATINI et al., 2004). As partof the A. pallipes complex, this species is underprotection by the European Council Directive 92/43/ECC. However, the introduction of highly competitivenon-indigenous species and other factors such aspollution, diseases, over-fishing, river engineering, flo-ods, and drought are leading to the narrowing of itsRENAI e GHERARDI - Mating and sexual selection in Austropotamobius italicus184pattern of distribution.Mating in this species occurs between late Octoberand the first half of November. During this restrictedperiod, the behaviour of this species changes; locomo-tion activity and dispersal increase (GHERARDI et al.,1998), possibly augmenting the probability of a mateencounter, and males appear more aggressive, compe-ting with other males for the access of a female.Copulation is soon followed by spawning in autumnand eggs are carried through the winter and the subse-quent spring. Hatching occurs in April and May, butthe young still live attached to the female pleopodsthroughout two developmental stages, some 25 daysafter hatching (HOLDICH, 1992; GHERARDI et al., 1997).Following the rationale that informations from beha-vioural studies help define management protocols andrecovery plans for endangered species, our objectiveshere were (1) to explore the role exerted by A. italicusmate choice and male-male competition in inducingmating and (2) to investigate sperm competition andmale control over multiple matings.To these ends, we simulated in the laboratory ma-ting interactions as observed in nature, where aggre-gations composed of two-four males were seen com-bating around a female (F. Gherardi, pers. observ.).Premises of this study were the results of a prelimi-nary choice experiment in which a sex was free tochoose between tethered individuals of the other sexwith opposing phenotypic traits (VILLANELLI & GHE-RARDI, 1998). Females were found to select largermates with intact chelipeds, while males mated indi-scriminately without regard to the body size of theoffered female.MATERIAL  AND  METHODSAnimal collection and maintenanceAdult A. italicus were hand-collected in September2002 from Torrente Resco in Pian di Scò (Arezzo).Crayfish were kept isolated under a natural light-darkcycle in plastic aquaria (bottom area: 30 x 16 cm)containing 3 litres of aerated water and a 10-cm longpiece of an opaque PVC tube (diameter: 5 cm) as arefuge. They were fed twice a week on live earthwor-ms. Individuals were measured using a vernier caliperfor their cephalothorax length (CL). From their size,males were arbitrarily subdivided into three categories,small (S, CL < 29 mm), medium (M, CL 29-36 mm),and large (L, CL > 36 mm).Experimental protocolBefore our observations commenced, we formed17 groups composed of one receptive female (meanCL: 32 mm) and three differently-sized, receptivemales (one S, one M, and L male), all with intactchelae. Females were defined receptive if they showeda spermatophoric plate on the seventh and eighththoracic segments of sternites (F. Gherardi, unpubl.observ.), while male receptivity was assessed fromtheir behaviour towards a receptive female. Everygroup was placed in a 40-cm diameter aquarium andwas observed for two hours. We tape-recorded inte-ractions occurring in every group and then analysedfrom these records:1. Number of interactions. Within the female-maleinteractions, we distinguished “Mating Attempts”and “Successful Matings” (i.e. mating attempts en-ding with spermatophore deposition). Male-maleinteractions exclusively consisted of “Fights”.2. Sex of both the approaching and the retreatingindividual and, if male, its size category.3. Duration of every interaction.Crayfish were kept in the experimental aquariumfor three subsequent days and examined three timesper day for spermatophore deposition by males andfor spawning by females.Statistical analysisSince the assumptions of normality of data andhomogeneity of variance were not always met andsome data were measured on an ordinal scale, we usednonparametrical statistical techniques (SIEGEL and CA-STELLAN, 1988). Figures give median values and inter-quartile ranges (first-third quartiles). The level of si-gnificance under which the null hypothesis was rejectedis α = 0.05.RESULTSFemale-male interactionsFemales initiated interactions more often than themales (Wilcoxon signed ranks test: z=2.82, df=1,P<0.01) (Fig. 1). The number of both female and maleapproaches significantly increased with the male sizeFig. 1. Comparisons between sexes in the frequencies of appro-aches to the other sex (medians and interquartile ranges). Fema-les: N= 17; males: N= 51.RENAI e GHERARDI - Mating and sexual selection in Austropotamobius italicus 185(Spearman rank-order correlation coefficient: rs=0.416,df=49, P<0.01 and rs=0.36, df=49, P<0.01) (Fig. 2).Male-male interactionsLarge males were the initiators of male-male inte-ractions more often than the other size categories(Kruskal-Wallis: H=27.15, df=2, P<0.001) (Fig. 3).M-L pairs were engaged in more numerous fights(H=35.50, df=2, P<0.001) (Fig. 4) and combated onaverage longer (H=6.20, df=2, P<0.05) than S-M andS-L pairs. Most often, fights ended with the retreat ofthe smaller individual (G-test: G=97.95, df=2, P<0.001).Mating attempts and successful matingL males were engaged in more numerous and onaverage longer mating attempts than the other sizecategories (Friedman two-way analysis of variance byranks: Fr=13.34, df=2, P<0.05 and Fr=6, df=2, P<0.05)(Fig. 5) and arrived more often to spermatophoredeposition (G=6.094, df=2, P<0.05). However, suc-cessful matings were relatively rare. They occurredonly in 16 instances out of 224 mating attempts (7.14%), this low number being possibly the effect of therefusal by the female. In fact, mating attempts wereoften interrupted by the female retreats (z=-3.20, df=1,P<0.01) (Fig. 6). Three females were subjected to thedeposition of more than one spermatophore by theFig. 2. The size of males plotted against (A) the number of female approaches to them and (B) the number of male approaches (B) toa female. N = 51Fig. 3. Comparison among male size categories for the frequen-cies of their approaches in male-male interactions (medians andinterquartile ranges). N= 51.Fig. 4. Comparisons among pairs composed of differently-sizedmales for the frequency of fights (medians and interquartile ran-ges). SM= small-medium pair, SG= small-large pair and MG=medium-large pair. N= 51.Fig. 5. Comparison among male size categories for the frequency (A) and mean duration (B) of mating attempts (medians and interquartileranges). N= 51.RENAI e GHERARDI - Mating and sexual selection in Austropotamobius italicus186same or by a different male. Before attaching the newspermatophore, the male always removed the old oneby feeding on it.DISCUSSIONOur study clearly indicates that A. italicus femalesare both “reluctant” and “choosy” in their matingbehaviour. On the one hand, they often interruptedmating attempts and also showed a form of “passive”resistance to the males by keeping their abdomencurled and therefore by impeding spermatophore de-position by males (BERRILL & ARSENAULT, 1984). Onthe other, they seemed to prefer males of bigger size.In fact, we found that females most often approa-ched large, rather than medium or small, males. Asimilar female preference for large males was obser-ved in other crustacean decapods studied so far (e.g.crabs, GREENSPAN, 1980; shrimp, RAHMAN et al.,2002; crayfish, VILLANELLI & GHERARDI, 1998; FUR-RER, 2004). Reluctance and choosiness of A. italicusfemales can be justified by their large investment intooffspring (see, also, A. pallipes, WOODLOCK & REY-NOLDS, 1988 and the grapsid crab Gaetice depressus,FUKUI, 1995).On the contrary, males seem to be undiscriminatingin their choice of mates, probably because they have alittle chance of encountering receptive females. Infact, (1) mating in A. italicus takes place over a shortperiod of time, (2) females are a rare resource in spaceand time (BREWIS & BOWLER, 1985), and (3) theoperational sex ratio (i.e. the ratio of one sex to theother among individuals ready to mate, ANDERSSON,1994) becomes heavily skewed towards males as themating season progresses (SNEDDEN, 1990).The effects of mate choice by females on A. itali-cus mating are difficult to isolate from the directinfluence of intrasexual competition. As expected in aspecies like A. italicus where receptive females arelimited in space and time, male-male competition isparticularly intense and is dominated by large males.Male-male combats may passively lead females tomate with a successfully competing male, which isusually the bigger individual in arthropods (BERRILL &ARSENAULT, 1984; WOODLOCK & REYNOLDS, 1988; GHE-RARDI, 2001). We found that large males were engagedin more numerous and longer mating attempts than thesmaller size categories and more likely arrived at depo-siting spermatophores than the other males, notwith-standing that this event was relatively rare in thelaboratory and in the taxon of study (see also FURRER,2004).In A. italicus, where any form of mate guarding isabsent and male-male conflict for access to females iscombined with external fertilisation, there is a particu-larly good opportunity for sperm competition (i.e. “thecompetition between ejaculates of two or more malesfor the fertilisation of the eggs of a single female”;PARKER, 1970). Indeed, the occurrence of sperm com-petition leading to the last-male advantage is confirmedby this and previous studies in A. italicus (VILLANELLI& GHERARDI, 1998) and other Astacidae (Astacus asta-cus and A. leptodactylus; FURRER, 2004). Males feedon the previously deposited spermatophore before co-pulating, being however unable to recognise their ownspermatophores. This apparently primitive form ofsperm competition was previously found in pseudo-scorpions (WEYGOLDT, 1969), millipedes, and collem-bolans (SCHALLER, 1971), in which, however, sperma-thophores are deposited on the substratum and notattached onto the female abdomen.CONCLUSIONSMating in A. italicus is best explained by the large-male size advantage resulting from an active matechoice of females for large partners. The considerableinvestment of energy in offspring justifies female cho-osiness, whereas the restricted mating period and thelow number of receptive females make, first, malesrelatively undiscriminating in their mate choice and,second, intrasexual competition over females (also inthe form of sperm competition) particularly intense. Inour study, we did not find an ultimate explanation forfemale preference of large males. Indeed, male size isa good predictor of the outcome of intrasexual compe-tition for the access of mates. If males have genes thatenable them to attain the larger size, females matingwith big males might produce big sons and thereforegain better reproductive success through their sons’progeny.AcknowledgementsThis work was made possible by funds from Un.D.A.Felix.Fig. 6. Comparisons between sexes in the frequencies of theirretreats from the other sex (medians and interquartile ranges).Females: N = 17, males: N = 51.RENAI e GHERARDI - Mating and sexual selection in Austropotamobius italicus 187REFERENCESGREENSPAN B. N., 1980. Male size and reproductive success inthe communal courtship system of the fiddler crab Ucarapaz. Animal Behaviour, 28: 387-392.HOLDICH D. M., 1992. Crayfish nomenclature and terminology.Finnish Fisheries Research, 14: 157-159.HUXLEY, J. S., 1938a. The present standing of the theory of sexualselection. In: G.R. de Beer (ed.), Evolution: essays on aspectsof evolutionary biology presented to Professor E.S., Goorichon his seventieth birthday, pp. 11-42. Clarendon Press,Oxford. Viii + 350 pp.HUXLEY J. S., 1938b. Darwin’s theory of sexual selection and thedata subsumed by it, in the light of recent research. AmericanNaturalist, 72: 416-433.PARKER G.A., 1970. Sperm competition and its evolutionaryconsequences in the insects. Biological Review, 45: 525-567.RAHMAN N., DUNHAM D. W., GOVIND C. K., 2002. Size-assorta-tive pairing in the big-clawed Snapping shrimp, Alpheusheterochelis. Behaviour, 139: 1443-1468.SCHALLER R., 1971. Indirect sperm transfer by soil arthropods.Annual Review of Entomology, 16: 407-446.SIEGEL S., CASTELLAN N. J. Jr., 1988. Nonparametric statistics forthe behavioural sciences. McGraw-Hill, New York.SNEDDEN W. A., 1990. Determinants of male mating success inthe temperate crayfish Orconectes rusticus: chela size andsperm competition. Behaviour, 115 (1-2): 100-113.VILLANELLI F., GHERARDI F., 1998. Breeding in the crayfish,Austropotamobius pallipes: mating patterns, mate choiceand intermale competition. Freshwater Biology, 40: 305-315.WEYGOLDT P., 1969. The Biology of Pseudoscorpions. HarvardUniversity Press, Cambridge, Massachusetts.WOODLOCK B., REYNOLDS J. D., 1988. Laboratory breedingstudies of freshwater crayfish, Austropotamobius pallipes(Lereboullet). Freshwater Biology, 19: 71-78.ANDERSSON M., 1994. Sexual selection. Princeton UniversityPress, Princeton, NJ.BERRILL M., ARSENAULT M. R., 1984. The breeding behaviour ofa northern temperate Orconectid crayfish, Orconectes rusti-cus. Animal Behaviour, 32: 333-339.BREWIS J. M., BOWLER K., 1985. A study of reproductive femalesof the freshwater crayfish Austropotamobius pallipes. Hydro-biologia, 121: 145-149.CHRISTY J. H., 1982. Burrow structure and use in the sand fiddlercrab, Uca pugilator (Bosc). Animal Behaviour, 30: 687-694.DARWIN C., 1871. The Descent of Man, and Selection in Relationto Sex. London, John Murray.FRATINI S., ZACCARA S., BARBARESI S., GRANDJEAN F., SOUTYGROSSETC., CROSA G., GHERARDI F., 2004. Phylogeography of thethreatened crayfish (genus Austropotamobius) in Italy: impli-cations for its conservation. Heredity, 94: 108-118.FUKUI Y., 1995. The effects of Body Size on Mate Choice in aGrapsid Crab, Gaetice depressus (Crustacea, Decapoda).Journal of Ethology, 13: 1-8.FURRER S. C., 2004. Untersuchungen zur Partnerwahl und derenAuswirkungen auf die Reproduktion bei den FlusskrebsenAstacus astacus und Astacus leptodactylus sowie Untersu-chumgen zur Life History beim Steinkrebs Austropotamo-bius torrentium. PhD Thesis dissertation.GHERARDI F., 2001. Behaviour. In: Biology of freshwater cray-fish. (D. M. Holdich ed.), Blackwell Science Ltd., Oxford:258-290.GHERARDI F., BARBARESI S., VILLANELLI, F. 1998. Movementpatterns in the white-clawed crayfish Austropotamobiuspallipes in a Tuscan stream. Journal of Freshwater Ecology,13: 413-424.GHERARDI F., VILLANELLI F., DARDI, P., 1997. Behavioral ecologyof the white-clawed crayfish Austropotamobius pallipes in aTuscan stream: preliminary results. Freshwater crayfish, 11:182-193.

Mating and sexual selection in the threatened crayfish, Austropotamobius italicus.

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Mating and sexual selection in the threatened crayfish, Austropotamobius italicus.

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