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Polyandry and Tibial Spur Chewing in the Carolina Ground Cricket (Eunemobius Carolinus)

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Polyandry and Tibial Spur Chewing in the Carolina Ground Cricket (Eunemobius Carolinus) 988 Polyandry and tibial spur chewing in the Carolina ground cricket (Eunemobius carolinus) Edyta K. Piascik, Kevin A. Judge, and Darryl T. Gwynne Abstract: During mating, the female Carolina ground cricket (Eunemobius carolinus (Scudder, 1877)) chews specialized spurs on the male’s hind tibia for access to his hemolymph. One potential benefit to spur chewing includes nutritional ac- quisition from male hemolymph. A method for testing this hypothesis is to manipulate food quality or quantity, with the prediction that mating rate will increase as food quality or quantity decreases. We manipulated diet quality in adult fe- males and provided them with four consecutive mating opportunities. We measured four aspects of mating behaviour (mating rate, latency to copulate, copulation duration, and spur chewing duration) and three of female fitness (egg number, egg-laying rate, and life span). Females of the two diet treatments did not differ significantly in any of the measured mat- ing behaviours, although females fed a low-quality diet lived longer. Male life span did not correlate with any measured variable, although males that experienced more matings and longer total times of copulation and spur chewing lost more mass. These results suggest that spur chewing may be costly for males, although we detected no evidence that this behav- iour was a benefit to the female or represented a form of male coercion. Re´sume´ : Durant l’accouplement, la femelle de la ne´mobie de Caroline (Eunemobius carolinus (Scudder, 1877)) mordille des e´perons spe´cialise´s sur les tibias poste´rieurs du maˆle pour avoir acce`sa` son he´molymphe. Un be´ne´fice potentiel de ce mordillement des e´perons est l’acquisition de nutriments de l’he´molymphe du maˆle. Un moyen de tester cette hypothe`se est de manipuler la qualite´ ou la quantite´ de la nourriture en pre´disant que le taux d’accouplement va augmenter avec la diminution de la qualite´ ou de la quantite´ de la nourriture. Nous avons manipule´ la qualite´ du re´gime alimentaire de femel- les adultes et leur avons fourni quatre occasions successives de s’accoupler. Nous avons mesure´ quatre variables du com- portement d’accouplement (taux d’accouplement, pe´riode de latence entre les accouplements, dure´e des copulations et dure´e du mordillement des e´perons) et trois de la fitness des femelles (nombre d’œufs, taux de ponte et longe´vite´). Les fe- melles des deux re´gimes alimentaires n’ont montre´ aucune diffe´rence significative dans les comportements reproducteurs observe´s, bien que les femelles nourries du re´gime infe´rieur aient ve´cu plus longtemps. Il n’y a aucune corre´lation entre la dure´e de vie des maˆles et les variables mesure´es, bien que les maˆles qui ont connu un nombre plus e´leve´ de copulations, des accouplements plus longs et des mordillements prolonge´s de leurs e´perons aient perdu plus de masse. Nos re´sultats in- diquent que le mordillement des e´perons entraıˆne un couˆt chez les maˆles, bien que nous n’ayons obtenu aucun indice qui laisse croire que ce comportement soit be´ne´fique aux femelles ou repre´sente une forme de coercition par le maˆle. [Traduit par la Re´daction] Introduction have conflicting interests in the outcome of their reproduc- tive strategies (Williams 1966; Dawkins 1976; Parker 1979; Females of many animals acquire nutrients from secre- Arnqvist and Rowe 2005). Females of many nuptial gift- tions provided by the mating male either by direct consump- giving species have evolved to mate with multiple partners tion or by absorbing them in their genital tract (Vahed 1998; at a rate beyond what is required to successfully fertilize all Gwynne 2008). These nuptial gifts include prey, seeds, glan- of their eggs (Arnqvist and Nilsson 2000). Given that mating dular products, and even body tissues of the mating male can be costly for females (Daly 1978), such polyandrous (Vahed 1998; Gwynne 2008). Nuptial gifts are commonly mating suggests that nuptial gifts benefit the female and viewed as a material benefit that increases female fitness. overcome those costs. But this has been challenged with the suggestion that gift in- There is evidence in some species that nutritious gifts pro- gredients may manipulate or coerce the female by increasing vide females with nutrients that increase the fitness of the male fitness but not hers (Arnqvist and Nilsson 2000; Vahed male’s own offspring (reviewed in Vahed 1998; Gwynne 2007). This follows from the hypothesis that the two sexes 2008), and female fitness in nuptial gift-giving insects in- Received 3 March 2010. Accepted 4 August 2010. Published on the NRC Research Press Web site at cjz.nrc.ca on 28 September 2010. E.K. Piascik1,2 and D.T. Gwynne. Department of Biology, University of Toronto Mississauga, 3359 Mississauga Road, Mississauga, ON L5L 1C6, Canada. K.A. Judge. Department of Biology, University of Toronto Mississauga, 3359 Mississauga Road, Mississauga, ON L5L 1C6, Canada; Department of Biological Sciences, University of Lethbridge, 4401 University Drive West, Lethbridge, AB T1K 3M4, Canada. 1Corresponding author (e-mail: [email protected]). 2Present address: Department of Zoology, The University of British Columbia, Vancouver, BC V6T 1Z4, Canada. Can. J. Zool. 88: 988–994 (2010) doi:10.1139/Z10-065 Published by NRC Research Press Piascik et al. 989 creased monotonically with increasing mating rate (Arnqvist Materials and methods and Nilsson 2000). However, nuptial gifts provided by males are also likely selected for their ability to manipulate the fe- Study animals male’s mating rate (Arnqvist and Nilsson 2000; Vahed In September 2008, we collected adult E. carolinus from 2007). In support of the coercion hypothesis, at least one the campus of the University of Toronto Mississauga study concludes that substances in the gift decrease female (43832’58@N, 79839’57@W). We used the first generation off- receptivity to additional matings (Sakaluk et al. 2006). spring of collected adults in the experimental trials. The ex- Effects of nuptial gifts on paternal investment and male perimental population was kept in a controlled environment relative mating success are not necessarily mutually exclu- room (25 8C, 70% relative humidity, 12 h light : 12 h dark sive, and in addition to selective advantages to males, it is photoperiod). We isolated the nymphs into individual plastic important to study the effects of nuptial gifts on females containers (9 cm diameter, 4.5 cm height) on the day that (Vahed 1998; Arnqvist and Nilsson 2000; Gwynne 2008). they hatched and weighed each to the nearest 0.1 mg (Met- If nuptial gifts provide direct benefits available from other tler AE50 electronic balance) on the following day, hereafter sources (e.g., nutrients and (or) water), then there should be termed moult mass. Each container had one vial of water a negative correlation between female mating rate and direct plugged with cotton for moisture and a piece of egg carton benefit received from other sources (Boggs 1990). A general for shelter. We fed the nymphs ground rabbit chow (Little method of testing this hypothesis involves manipulating the Friends Rabbit Food, Martin Mills Inc.) for the first 2 weeks, putative material benefit that the female receives from the after which they were fed whole pellets. Each day, we nuptial gift (Gwynne 2008). Under the material benefits hy- checked the nymphs for eclosion to adulthood and weighed pothesis, resource-deprived females are predicted to increase any new adults. their mating rate, decrease their latency to copulate, increase their copulation duration, and (or) increase their gift con- Female diet manipulation sumption. For example, poorly nourished female katydids Upon adult eclosion, we randomly assigned adult females (Kawanaphila nartee Rentz, 1993) increase their refractory to one of two diet treatments. The low-diet treatment con- period only when allowed to consume the spermatophylax sisted of 67% rabbit chow and 33% cellulose powder donated by the mating male (Simmons and Gwynne 1991). (Keycel 200-CT; Canada Colours and Chemicals Limited, In another example, Ursprung et al. (2009) showed that fe- Brampton, Ontario, Canada), whereas the high-diet treat- male seed beetles (Callosobruchus maculatus (Fabricius, ment consisted of 99% rabbit chow and 1% cellulose pow- 1775)) with access to nutrients and water increase their mat- der. Cellulose contains no nutritional material and its use in ing frequency only in response to water deprivation (see also the high-diet treatment was to control for any effects of the Edvardsson 2007; Fox and Moya-Laran˜o 2009). This study substance on the females. The proportion of cellulose pow- suggests that polyandry in this beetle species provides mate- der in our low-quality diet followed the methods of Wagner rial benefits to females that may offset some of the costs of and Hoback (1999) who reported a diet effect on male call- associating or mating with males (den Hollander and ing effort in the field cricket Gryllus lineaticeps Sta˚l, 1861 Gwynne 2009). Finally, in a nursery web spider (Pisaura (see also Wagner and Harper 2003). We fed adult males the mirabilis Clerck, 1757) that uses nuptial prey, starved fe- nymphal diet of 100% rabbit chow pellets. males accepted more copulations than fed individuals (Prokop and Maxwell 2009). Mating trials Males of some ground crickets (Orthoptera: Gryllidae, For the mating trials, we used male crickets between 4- Nemobiinae) donate hemolymph to their mates by allowing and 11-days postadult eclosion and females between 5- and the copulating female to chew on specialized spurs on his 12-days postadult eclosion. We systematically paired a fe- hind legs (Mays 1971). Female nemobiine crickets will male with a different male each day. Each female was given mate with more than one male and females of the southern an opportunity to mate with one male once a day for four ground cricket (Allonemobius socius (Scudder, 1877)) gain consecutive days.
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