Animal Behaviour 81 (2011) 749e755

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Animal Behaviour

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Sexual cannibalism in the European garden spider Araneus diadematus: the roles of female hunger and mate size dimorphism

Helma Roggenbuck a,*, Stano Pekár b,1, Jutta M. Schneider a a Department of Biology, Zoological Institute and Museum, University of Hamburg b Department of Botany and Zoology, Faculty of Sciences, Masaryk University article info Sexual cannibalism, in particular before insemination, is a long-standing evolutionary paradox because it Article history: persists despite extreme costs for the victim, usually the male. Several adaptive and nonadaptive Received 10 May 2010 hypotheses have been proposed to explain this phenomenon, but empirical studies are still scarce and Initial acceptance 7 June 2010 results are inconclusive. We studied the spider Araneus diadematus in which females may attack and kill Final acceptance 5 January 2011 potential mates at any time during courtship or mating, making the species ideal for examining the Available online 16 February 2011 causes of pre- and postinsemination sexual cannibalism. We manipulated food availability for females MS. number: 10-00323R and conducted mating trials in the laboratory to test predictions derived from two hypotheses: the adaptive female foraging (AFF) hypothesis, which views sexual cannibalism as an optimal female Keywords: behaviour in the face of a trade-off between mating and cannibalizing a courting male; and the mate size adaptive female foraging dimorphism (MSD) hypothesis, which postulates a physical advantage of larger females in subduing Araneus diadematus males. We found partial support for the AFF hypothesis, but MSD explained sexual cannibalism irre- mate choice postinsemination spective of the timing of cannibalism. Our results suggest that a complex interplay of female state, mate preinsemination choice and physical dominance is responsible for the maintenance of sexual cannibalism against male sexual size dimorphism interests. spider Ó 2011 The Association for the Study of Animal Behaviour. Published by Elsevier Ltd. All rights reserved.

Sexual cannibalism, defined as the predation of conspecifics of females may use sexual cannibalism as a mechanism to control the opposite sex at some stage during courtship and mating copulation duration (Elgar et al. 2000; Schneider et al. 2006). (reviewed in Elgar & Schneider 2004 and Wilder et al. 2009), is While postinsemination cannibalism of males may benefit both regarded as an ultimate manifestation of sexual conflict because sexes, preinsemination cannibalism can only benefit females, victims lose their entire future reproductive value while cannibals whereas for males it has high costs. Four hypotheses address the get a meal (Elgar & Schneider 2004). Costs and benefits of this phenomenon of preinsemination sexual cannibalism. (1) Mistaken behaviour to both sexes strongly depend on the timing of sexual identity hypothesis: preinsemination sexual cannibalism may be cannibalism (Elgar & Schneider 2004). Postinsemination canni- a nonadaptive by-product of mistaken identity with voracious balism of males can be adaptive for both sexes: males may benefit females failing to recognize males as prospective mates and some through paternal investment (Parker 1979; Buskirk et al. 1984), males simply being incapable of escaping from those attacks (Gould mating effort (Simmons & Parker 1989) or sperm competition 1984). (2) Aggressive-spillover hypothesis (Arnqvist & Henriksson avoidance (Andrade 1996; Prokop & Václav 2005). Females gain 1997) or genetic constraints hypothesis (Wilder et al. 2009): pre- nutrients that may increase body mass (Elgar & Nash 1988; Elgar insemination sexual cannibalism may be the result of high and 1998; Moya-Laraño et al. 2003a), body condition (Moya-Laraño indiscriminate female aggression during early life stages, spanning et al. 2003a, b; Barry et al. 2008) or fecundity (Birkhead et al. ontogenetic stages and behavioural contexts (e.g. foraging and 1988; Johnson 2001, 2005a; Barry et al. 2008). Furthermore, mating contexts). Predation of male mates before mating is inter- preted as an incidental by-product of selection on correlated traits. (3) Sexual selection: preinsemination sexual cannibalism may serve as a proper means of mate choice for females (Elgar & Nash * Correspondence: H. Roggenbuck, Department of Biology, Zoological Institute 1988; Elgar 1992; Persons & Uetz 2005; Prenter et al. 2006). and Museum, University of Hamburg, Martin-Luther-King-Platz 3, D-20146 Females’ aggression is directed towards males of inferior pheno- Hamburg, Germany. type, so that by killing unwanted courting males, females terminate E-mail address: [email protected] (H. Roggenbuck). 1 S. Pekár is at the Department of Botany and Zoology, Faculty of Sciences, further sexual harassment and allow males of preferred pheno- Masaryk University, Kotlarska 2, 611 37 Brno, Czech Republic. types to copulate and sire offspring. An alternative mechanism is

0003-3472/$38.00 Ó 2011 The Association for the Study of Animal Behaviour. Published by Elsevier Ltd. All rights reserved. doi:10.1016/j.anbehav.2011.01.005 750 H. Roggenbuck et al. / Animal Behaviour 81 (2011) 749e755 proposed by the mate size dimorphism (MSD) hypothesis (Wilder & hungry females should be more likely to attempt to cannibalize Rypstra 2008a, b), namely, females are indiscriminately aggressive, mates than sated females. (2) The female’s mating status should but whether they kill a male will depend on the female’s physical affect the probability of pre- but not postinsemination cannibalism. strength relative to the male’s ability to defend his life (see below). Virgin females should be less likely to attempt to cannibalize mates (4) Adaptive female foraging (AFF) hypothesis (Newman & Elgar prior to sperm transfer than mated females. (3) The body mass of 1991): preinsemination sexual cannibalism is regarded as an a male determines his value as a food item and thus influences the economic foraging decision of females. Model parameters predict probability of sexual cannibalism. The likelihood of sexually the occurrence of preinsemination sexual cannibalism even by cannibalistic attacks should increase with increasing male body virgin females that thereby risk remaining unmated (Elgar & mass since heavy males are more profitable as prey items than Schneider 2004). The critical assumption of this model is that lighter ones. (4) If preinsemination sexual cannibalism is an females estimate the economic value of a courting male as a sperm adaptive female foraging tactic at the cost of mating, as imple- donor versus his value as a food item. The expected encounter rate mented in the AFF model, preinsemination attacks should be more with males and the expected food intake from other prey items are successful in the sense that an attack is followed by a meal than the important factors for a female’s decision whether to kill or to postinsemination attacks (because otherwise, the most profitable mate with a male. Females are expected to perform preinsemina- tactic for a female should be to copulate to secure sperm and then tion sexual cannibalism when prey is limited and males are abun- kill the male afterwards for feeding purposes). (5) The probability dant (Newman & Elgar 1991). that a female attack ends successfully, that is, actually results in the Experimental tests of the AFF hypothesis (Newman & Elgar killing and consumption of the male, should predominantly depend 1991) are scarce. Arnqvist & Henriksson (1997) showed that on the relative size differences between the female and the male adaptive foraging is an unlikely reason for preinsemination sexual irrespective of the timing of the attack. cannibalism regularly occurring in the European fishing spider, Dolomedes fimbriatus (Pisauridae). However, partial support for the METHODS AFF hypothesis was found in another hunting spider from North America, Dolomedes triton (Johnson 2001, 2005a, b; Johnson & Sih General Protocol 2005). While female hunger may explain female aggression towards mates, the outcome of such attacks and thus the occur- Juveniles and subadults of A. diadematus were collected in June rence of sexual cannibalism was shown to be affected by sexual size and July 2005 from their orb webs in gardens and in hedges around differences: the average size difference between the sexes is meadows in a rural area of northern Germany (Tornesch, Schles- correlated with the evolution of sexual cannibalism across a broad wig-Holstein; 5341017N, 943058E). Spiders were housed individ- range of spider species (Wilder & Rypstra 2008b) and explained ually in 200 ml transparent plastic cups in our laboratory at the sexual cannibalism in two cursorial (ground-hunting) spider University of Hamburg. Small juveniles were fed a diet of Drosophila species. Experiments on the wolf spiders Hogna helluo and Schizo- twice a week and larger juveniles and adult spiders were fed two cosa ocreata (both Lycosidae), for instance, showed that in these or three Calliphora flies twice a week. Adult females were assigned species, the difference in size between mating partners (Wilder & to two different feeding regimes as described below. Spiders were Rypstra 2008b) strongly influenced the success of female attacks watered 5 days per week. After maturation, adult females were (Persons & Uetz 2005; Wilder & Rypstra 2008a, b). The MSD transferred to separate Perspex frames (36 36 cm and 6 cm deep) hypothesis provides an alternative mechanism in support of the whose rough inner surfaces allowed attachment of the orb webs. mate choice hypothesis. Mating trials were conducted in these frames. Courtship and mating behaviour of cursorial wolf spiders and of Spiders were weighed on an electronic balance (METTLER web-building species differs markedly. We studied an orb web Toledo AB54-S) to an accuracy of 0.0001 g. Males were weighed spider, Araneus diadematus, with similar sexual size dimorphism prior to mating, before potentially being mutilated or cannibalized (SSD ¼ mean difference in size between males and females for by females. To avoid damaging their webs when handling them, we a species) to the above-mentioned Lycosidae (Persons & Uetz 2005; weighed females afterwards. Spiders were preserved in 70% Wilder & Rypstra 2008b). Compared to species of other genera of ethanol after mating for morphometric measures. We measured orb web spiders, such as Nephila or Argiope, SSD is moderate in A. tibiaepatella length of the first pair of legs (and calculated the diadematus (SSD 1.89; see Wilder & Rypstra 2008b), but both mean value of the right and left legs) in both sexes using a LEICA females and males vary substantially in adult body size and mass MZ16 stereomicroscope and LEICA IM500 imaging software version (see Elgar & Nash 1988). We experimentally tested the AFF 4.0. Spider legs are sclerotized body structures that do not change hypothesis using A. diadematus as a model organism, since this is in size after the final moult; thus tibiaepatella length is a good the species that Newman & Elgar (1991) specifically had in mind proxy of body size. We used the residuals from a regression of body when they developed their model. Moreover, in this species the mass on a linear measure of body size (tibiaepatella length) as an attack of the female may occur at all stages of the mating sequence index of body condition. A spider with a positive (rather than (Elgar & Nash 1988). We conducted a large number of staged negative) residual is considered to be in better condition (see mating experiments with well-fed and food-deprived female Schulte-Hostedde et al. 2005). Age was defined as the interval A. diadematus to test for differences in their propensity to attack between final moult and date of mating. Mate size dimorphism males and to observe the consequences of such attacks. In addition (MSD) was calculated as the ratio of female to male tibiaepatella to female hunger state, we assessed the influences of female and length (female tibiaepatella length divided by male tibiaepatella male mating status and of female and male body size to evaluate length). A larger value indicates a greater size advantage of the predictions derived from the sexual selection hypothesis. female over the male. Specifically, we tested the following predictions derived from the AFF hypothesis (1e4: Newman & Elgar 1991) and from the Hunger Manipulation sexual selection hypothesis. In the context of the latter we specif- ically included predictions of the MSD hypothesis (5: Wilder & Adult females were moved to Perspex frames and randomly Rypstra 2008a, b). (1) A courting male’s value as a meal is higher assigned to one of two food availability treatments to test for the than his value as a potential mate for a starving female. Thus, effects of female hunger as a potential motivation for female H. Roggenbuck et al. / Animal Behaviour 81 (2011) 749e755 751 aggression towards mates. The diet of one group was not changed were capable of mating repeatedly (we recorded males copulating after the final moult and these females were continuously fed two or four times in succession with the same female within 20 min). In three Calliphora flies twice a week. Females in the hunger treatment this study, males were allowed to copulate maximally three times. were not fed at all after their final moult. Females stayed in the Repeated use of males and females was accounted for in statistical feeding treatments for 7e10 days between maturation and mating. analyses (see below). Females were prevented from consuming There was no difference in the mean age of fed and starved successfully captured mates. We removed these males from females at first femaleemale encounters (ManneWhitney U test: females’ webs or chelicerae, as they needed to remain intact for Z ¼0.020, Nfed ¼ 60, Nstarved ¼ 47, P ¼ 0.984; Table 1). Female body future measurement of their legs. mass at mating differed between the two treatment groups: fed We measured the duration of the palpal insertion (copulation) females were heavier than starved females (t test: t105 ¼12.393, using a digital watch. Attacks of females during courtship and mating P < 0.0001), which was also apparent in their better body condition were recorded, differentiating between failed attacks and successful (ManneWhitney U test: Z ¼8.278, Nfed ¼ 52, Nstarved ¼ 42, ones that resulted in sexual cannibalism. In relation to its timing, P < 0.0001; Table 1). Fed and starved females did not differ in sexual cannibalism was classified as pre- or postinsemination. tibiaepatella length (ManneWhitney U test: Z ¼0.041, Nfed ¼ 53, ¼ ¼ Nstarved 42, P 0.967; Table 1). We used parametric statistics (on Statistical Analyses log-transformed data if necessary) or nonparametric statistics (where the assumptions for parametric tests could not be met using We used multiple regression within generalized linear mixed- simple transformation). effects models (GLMM, Bates & Maechler 2009) with binomial error structure and logit link performed in R (R Development Core Team Mating Trials 2009) to predict pre- and postinsemination attacks and canni- balism based on male status, male age, male size, male mass, female Matings were conducted in the laboratory in August and status, female age, female feeding status, size ratio, encounter September 2005. Females were mated to randomly selected males. number and copulation duration (this variable was not used in the Matings were initiated by carefully placing a male with a paint- models for preinsemination attacks and cannibalism). This method brush on top of a female’s Perspex frame. Experiments were was chosen to account for repeated use of some males and females abandoned if males did not display any courtship behaviour within in the experiment. Therefore, female identity was used as a random 1 h of introduction. effect in the model. For the GLMM analysis we excluded all cases Araneus diadematus males typically commence courtship by (approximately 36%) with missing size measurements. The constructing a mating thread from the female’s web to the maximal model included all two-way interactions between fixed surrounding vegetation (see Elgar & Nash 1988). The male charac- variables, but these were generally found to be nonsignificant at the teristically plucks the mating thread with his outstretched forelegs 5% level. Therefore, only the model with main effects was further (vibratory courtship; see Elgar 1991) to lure the female out of the simplified using stepwise selection of significant terms based on web’s central hub onto the thread, where copulation takes place. the likelihood ratio test (Zuur et al. 2009). After the female has adopted the typical mating posture, hanging from the mating thread by her third and fourth pairs of legs, with RESULTS forelegs closely drawn towards the body to allow access to the paired genital openings on the ventral opisthosoma, the male tries to insert Preinsemination Attacks one of his secondary genital organs (pedipalps). In general, several attempts are necessary before the male succeeds in inserting his The frequency of female attacks prior to copulation was 42.9% pedipalp. After successful copulation, males usually initiate another (76/177 cases). Female age, encounter number, male mass, male courtship sequence to achieve an additional insertion. Adult females size and male age did not significantly affect the attack probability may attack males at any point during this mating sequence. Detailed (Table 2). However, female mating status, female/male size ratio, descriptions of courtship and mating in A. diadematus are given in male mating status and female feeding status had significant Elgar & Nash (1988) and in Newman & Elgar (1991). (additive) effects on the likelihood of attack. Starved females were We staged 223 mating trials in total, using 107 females and 122 males. An overview of phenotypic traits (body size, body mass, Table 2 condition) and age of study animals is given in Table 1. We limited Summary list of results of GLMM analyses with 10 explanatory variables and their the femaleemale encounter rate to a maximum of three encounters effects on pre- and postinsemination attacks and cannibalism per female. Females were allowed to copulate with either one male ¼ ¼ ¼ Explanatory Preinsemination Postinsemination repeatedly (N 63) or with a second (N 39) or third (N 5) male, variables which was introduced after removal of the previous one(s). Indi- Attacks Cannibalism Attacks Cannibalism 2 2 2 2 vidual males were repeatedly used for trials (up to four times), as c1 P c1 P c1 P c1 P (1) encounters with females did not always result in copulations Encounter number 0.3 0.60 1.1 0.32 2.0 0.16 0.15 0.70 and (2) preceding personal observations had shown that males Copulation ee 2.2 0.14 2.2 0.15 duration Male body mass 0.4 0.51 0.2 0.68 4.8 0.028 3.3 0.07 Table 1 Male body size 1.8 0.18 1.6 0.21 3.3 0.07 1.5 0.22 Body mass, body size (mean tibiaepatella length), condition and age of A. dia- Male age 1.5 0.23 1.2 0.30 0.06 0.81 1.4 0.24 dematus females and males used in this study Male mating status 9.1 0.003 3.5 0.06 0.05 0.84 3.0 0.08 Female/male size 6.1 0.014 23.2 <0.0001 16.8 <0.0001 22.6 <0.0001 \\ \\ __ Fed Starved ratio Body mass (mg) 152.295.50 (58) 69.234.00 (47) 31.70.69 (120) Female age 1.5 0.22 0.1 0.75 1.8 0.19 0.2 0.66 Size (mm) 5.220.07 (53) 5.250.11 (42) 4.990.04 (91) Female mating 4.2 0.04 0.9 0.35 2.1 0.15 0.9 0.35 Condition 35.924.80 (52) 44.471.64 (42) 00.50 (90) status Age (days) 9.070.13 (60) 9.020.17 (47) 16.580.75 (122) Female feeding 20.8 <0.0001 5.9 0.015 0.04 0.84 12.0 <0.001 status Sample sizes are given in parentheses and vary because not all data were available for each animal. Mean SE is shown for each trait. Significant effects are shown in bold. 752 H. Roggenbuck et al. / Animal Behaviour 81 (2011) 749e755 more likely than fed females to attack a male and mated females 1 attacked more often than virgins (Fig. 1a, b). Virgin males were more often attacked than mated males. Female aggression Fed increased with increasing female/male size ratio (Fig. 1a, b). In Starved 0.8 other words, female aggression was most likely if a relatively small, inexperienced male encountered a starved, mated female and least likely if a relatively large, mated male encountered a fed, virgin 0.6 female (Fig. 1a, b).

Preinsemination Cannibalism 0.4

The frequency of preinsemination cannibalism (i.e. trials in which females attacked males prior to copulation and succeeded in Probability of cannibalism 0.2 killing) was 15.8% and hence relatively low (12/76 cases). Female age, male age, male size, encounter number, male mass, female mating status and male mating status failed to show significant 0 effects on the probability of cannibalism (Table 2). However, female feeding status and size ratio were significant predictors of canni- 0.8 1 1.2 1.4 1.6 balism. The probability of a deadly attack was much higher when Female/Male size ratio a male encountered a fed female (Fig. 2). Fed females cannibalized Figure 2. Model of the relationship between the probability of preinsemination males with more than 50% probability if they were at least 23% cannibalism and the female/male size ratio for both fed and starved A. diadematus females. N ¼ 122.

1 larger than the male, that is, at a female/male ratio of 1.23. In (a) M-virgin,F-mated contrast, attacks by starved females were followed by cannibalism M-virgin,F-virgin only if the females had a much more pronounced size advantage M-mated,F-mated 0.8 over the male. Indeed, starved females cannibalized males with M-mated,F-virgin a 17.7-times lower odds ratio than fed females (Fig. 2).

0.6 Postinsemination Attacks

The frequency of postinsemination attacks was 35.3% (55/156 0.4 cases). Female age, male mating status, female feeding status, male age, copulation duration, male size, encounter number and female mating status did not have significant effects on the probability of 0.2 postinsemination attacks (Table 2). Only two variables, male mass and female/male size ratio, were significant. Similar to preinsemi- nation attacks, the probability of attacks after mating increased 0 strongly with the size ratio. However, it decreased slightly with male mass: a size difference of 4% was sufficient to predict a 50% attack 0.8 1 1.2 1.4 1.6 probability against relatively lighter males (mean ¼ 17 mg). 1 However, a 32% size difference was required if a relatively heavy male (b) (mean ¼ 57 mg) was to be attacked with the same probability (Fig. 3). Attack probability

0.8 Postinsemination Cannibalism

The frequency of postinsemination cannibalism (i.e. trials in 0.6 which females attacked males after copulation and succeeded in killing) was 52.7% (29/55 cases) and higher than before mating. Female mating status, male age, male mass, male mating status, 0.4 encounter number, female age, male size and copulation duration did not have significant effects (Table 2). Only female feeding status fi M-virgin,F-mated and female/male size ratio had a signi cant effect. The risk of being 0.2 M-virgin,F-virgin killed after copulation was much higher for a male that mated with M-mated,F-mated a fed female: fed females cannibalized males with more than 50% M-mated,F-virgin probability if females were more than 14% larger than males, that is, 0 at a female/male size ratio of 1.14. Consistent with premating 0.8 1 1.2 1.4 1.6 cannibalism, starved females cannibalized males with an 8.9-times lower odds ratio than fed females (Fig. 4). Female/Male size ratio

Figure 1. Models of the relationship between the probability of preinsemination Evaluation of AFF and MSD Hypotheses attack and the female/male size ratio for (a) fed and (b) starved A. diadematus females. Within each plot logit models for combinations of levels of two other explanatory variables are displayed: female status (virgin, mated) and male status (virgin, mated). Prediction 1: our results do support this prediction since starved N ¼ 111. females were more likely to attack males before copulation even if H. Roggenbuck et al. / Animal Behaviour 81 (2011) 749e755 753

preinsemination attacks was significantly lower (15.8%) than that of 2 postinsemination attacks (52.7%; c1 ¼ 16.2, P < 0.0001). Prediction 5: in accordance with this prediction, MSD affected 1 both the probability and the success of female attacks irrespective of their timing. 0.8 DISCUSSION 0.6 Our experiments confirmed that both satiation and mating 0.4 status affected female aggressiveness in the direction predicted by the AFF hypothesis (Newman & Elgar 1991): males were most likely

Attack probability Attack 0.2 to be attacked by a starved and mated female. However, contrary to the prediction of the AFF hypothesis, the presumed trade-off 0 between foraging and mating was not mediated by a higher capture 50 success prior to mating in comparison to after mating. On the Male mass (mg) 1.4 contrary, we found that preinsemination capture success was much 40 1.2 lower than postinsemination success since only 15.8% of pre- 30 insemination attacks versus 52.7% of postmating attacks ended in 1 the death of the male. Furthermore, male size was not related to its 20 0.8 le/Male size ratio value as a prey, but was relevant through the mechanism predicted Fema by the MSD hypothesis as both female attacks and the capture success increased with increasing size differences between the Figure 3. Model of the relationship between the probability of postinsemination attack, the female/male size ratio and male mass. N ¼ 98. sexes. Hence, it was the smaller males not the larger ones that were more likely to be attacked and cannibalized. The AFF hypothesis (Newman & Elgar 1991) deals with the they were virgin (Fig. 1a, b) while starvation had no effect on likelihood of state-dependent decisions of females, that is, condi- postinsemination attacks (Table 2). However, fed females were tions under which females should either mate with or eat a male. more successful in capturing males that they attacked than starved Predictions concerning the outcome of female attacks are not females (Figs 2, 4). included in the model, but were found to be crucial since female Prediction 2: our results do support this prediction since mated attacks very often did not lead to male death and sexual canni- females were more likely than virgin females to attack a male balism. Wilder et al. (2009) emphasized that sexual cannibalism before copulation (Fig. 1a, b). However, female mating status did must be viewed as a double-stage event that includes (1) the female not affect the probability of either pre- or postinsemination attack and (2) the successful act of killing. They proposed an inter- cannibalism (Table 2). action between female hunger and size differences between mating Prediction 3: the energetic value of a male, measured as body partners, that is, MSD as a determinant of the occurrence of attacks mass, affected neither the probability of attacks before copulation nor and sexual cannibalism declines in importance with increasing the probability of sexual cannibalism before or after copulation, but female hunger level. Our results provide partial support for this had a significant effect on postinsemination attacks (Table 2, Fig. 3). interaction: in premating attacks, starved A. diadematus females Prediction 4: our results do not support this prediction. Although were more aggressive than fed ones, irrespective of the size ratio the proportion of premating attacks was higher than that of post- (high attack probability despite size ratio values < 1, i.e. male size 2 mating attacks (c1 ¼ 0.65, P ¼ 0.42), the actual capture success of advantage; Fig. 1a, b). However, the pattern was different in the following stage, namely the actual capture (Fig. 2). The aggressive- ness of starved virgin females was rarely followed by cannibalism of 1 the males. In contrast, Wilder & Rypstra (2008a) found that both female hunger level and relative size differences are predictors of Fed the occurrence of sexual cannibalism in the wolf spider H. helluo.In fi 0.8 Starved contrast to our ndings, experimentally starved female wolf spiders cannibalized males more frequently than fed females. Moreover, starved females engaged in pre- and postcopulatory sexual canni- 0.6 balism, whereas fed females exclusively cannibalized after copula- tion (Wilder & Rypstra 2008a). These findings support a trade-off between foraging and mating and make sense under the assump- 0.4 tion that a male is a safer meal before than after mating: an assumption that is contradicted by our results. Starved virgin A. diadematus females attacked males but rarely ended up with a meal. Failed preinsemination attacks imply ener- Probability of cannibalism 0.2 getic costs to a female. Thus, if females perform preinsemination sexual cannibalism for feeding purposes, energetic costs of attacks fi 0 should be outweighed by energetic bene ts of successful attacks, that is, females should attack only if the expected energy balance is 0.8 0.9 1 1.1 1.2 1.3 1.4 positive. Hence, optimal foraging is unlikely to maintain such Female/Male size ratio a wasteful effort. A similar relationship is found when mating status is considered: although previously mated females were more Figure 4. Model of the relationship between the probability of postinsemination cannibalism and the female/male size ratio for both fed and starved A. diadematus inclined to attack before copulation, they were not more likely to females. N ¼ 136. kill the male. Our experiments rather suggest that a female’s 754 H. Roggenbuck et al. / Animal Behaviour 81 (2011) 749e755 hunger and mating status affect her motivation for aggressive because one crucial assumption of a trade-off between mating and behaviour, while the occurrence of pre- and postinsemination foraging for virgin females is not met. A model that would explain sexual cannibalism is driven by size differences between the sexual cannibalism in A. diadematus would have to include the mating partners, a finding that strengthens the MSD hypothesis female’s physical predominance and the male’s ability to resist proposed by Wilder & Rypstra (2008b). In agreement with other (Wilder & Rypstra 2008a, b). In accordance with studies on curso- studies using sexually cannibalistic insects and spiders (Birkhead rial spiders, our results suggest that a complex interplay of female et al. 1988; Andrade 1998; Maxwell 1998; Herberstein et al. state, mate choice and physical dominance is responsible for the 2002; Lelito & Brown 2006; Barry et al. 2008), our results suggest maintenance of sexual cannibalism against male interests. that females clearly match their needs to forage and to mate, rather than trading the two options off. Acknowledgments Size differences between mating partners (MSD) have a strong influence on the frequency of sexual cannibalism by affecting male We are very grateful to Mark Briffa, Matthias W. Foellmer, Lutz vulnerability to female aggression (Wilder & Rypstra 2008a). It is Fromhage and two anonymous referees for helpful comments on plausible that the relative sizes of sexual partners crucially affect the manuscript. the likelihood of female cannibalistic attacks since the females’ physical requirements needed to overwhelm courting males and the males’ competence at avoiding such attacks increase with References increasing body size. Evidence for size-related precopulatory sexual Andrade, M. C. B. 1996. Sexual selection for male sacrifice in the Australian redback cannibalism in spiders (reviewed in Prenter et al. 2006) has been spider. Science, 271,70e72. presented for A. diadematus (Elgar & Nash 1988), D. fimbriatus Andrade, M. C. B. 1998. Female hunger can explain variation in cannibalistic (Arnqvist 1992; Arnqvist & Henriksson 1997), D. triton (Johnson behavior despite male sacrifice in redback spiders. Behavioral Ecology, 9,33e42. Arnqvist, G. 1992. Courtship behavior and sexual cannibalism in the semi-aquatic 2005b), Meta segmentata (Rubenstein 1987) and S. ocreata fishing spider, Dolomedes fimbriatus (Clerck) (Araneae: Pisauridae). Journal of (Persons & Uetz 2005). Similarly, our results suggest that MSD is an Arachnology, 20, 222e226. important parameter for the occurrence of preinsemination sexual Arnqvist, G. & Henriksson, S. 1997. Sexual cannibalism in the fishing spider and cannibalism in A. diadematus, since both the probability of attacks a model for the evolution of sexual cannibalism based on genetic constraints. Evolutionary Ecology, 11, 255e273. and the probability of cannibalism prior to copulation increased Barry, K. L., Holwell, G. I. & Herberstein, M. E. 2008. Female praying mantids use with increasing female/male size ratio. sexual cannibalism as a foraging strategy to increase fecundity. Behavioral e Elgar & Nash (1988) found that sexual cannibalism in A. dia- Ecology, 19,710 715. Bates, D. & Maechler, M. 2009. lme4: Linear Mixed-effects Models using S4 classes. R dematus was determined by male body size, whereas female body package version 0.999375-31. Vienna: R Foundation for Statistical Computing. size had no influence on sexual cannibalism. However, the size ratio http://CRAN.R-project.org/package¼lme4. of mating partners (MSD) was not considered. Although females Bel-Venner, M. C., Dray, S., Allainé, D., Menu, F. & Venner, S. 2008. Unexpected male choosiness for mates in a spider. Proceedings of the Royal Society B, 275, attacked males of different sizes at the same frequency, smaller 77e82. males were more likely to be killed before getting a chance to mate Birkhead, T. R., Lee, K. E. & Young, P. 1988. 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