The shield effect: nuptial gifts protect males against pre-copulatory sexual cannibalism

Abstract

Several not mutually exclusive functions have been ascribed to nuptial gifts across different taxa. Although the idea that a nuptial prey gift may protect the male from pre-copulatory sexual cannibalism is attractive, it has previously been considered of no importance based on indirect evidence and rejected by experimental tests. We reinvestigated whether nuptial gifts may function as a shield against female attacks during mating encounters in the spider Pisaura mirabilis and whether female hunger influences the likelihood of cannibalistic attacks. The results showed that pre-copulatory sexual cannibalism was enhanced when males courted without a gift and this was independent of female hunger. We propose that the nuptial gift trait has evolved partly as a counteradaptation to female aggression in this spider species.

1. Introduction

Nuptial gift-giving behaviour has evolved independently in several forms among invertebrate and vertebrate species, but often occurs as food gifts [1–3]. Explanations for the origin and maintenance of nutritional donations differ, whether seen from the females' or the males' point of view. For females, any package of nutrients obtained without extra costs will increase their fecundity [1,4,5]. For males, nuptial gifts may function as paternal investment and/or as mating effort, depending on whether the gift contributes to female/offspring nutrition, and thus increases the number or quality of offspring, or if it serves only for the male to obtain more matings [1–3]. These hypotheses include the possibility that the male offers himself as the nuptial gift by promoting sexual cannibalism [6,7]. A third hypothesis, applying to predatory and cannibalistic species, proposes that nuptial gifts may act as physical protection against sexual cannibalism from aggressive females [8,9] but has so far received no support [10–12].

For the spider Pisaura mirabilis, Bristowe [9, p. 187] noted that ‘a male who has been put in a female's enclosure with no fly to offer her has been eaten himself’, implying that carrying the gift in his chelicerae when approaching the female might protect the male from a potentially cannibalistic attack. Such attacks are known from near-natural [10] as well as laboratory settings. Because of low frequency of sexual cannibalism (less than 5%) [11,13–15] the phenomenon was inferred to be an unimportant evolutionary force in this mating system. However, a low cannibalism frequency may be owing to effective male counteradaptations to avoid female aggression [15]. If the gift functions in the way that Bristowe [9] imagined, experimentally removing the gift should (all other things equal) expose the pre-adaptation risk of sexual cannibalism. However, experiments with no-gift males either did not find any sexual cannibalism [13] or at least reported no increased frequency [16–19].

Sexual cannibalism is a threat to males in many predatory species including much of the order of spiders [6]. Male courtship partly serves to reduce female aggression and thus the risk to the male of being cannibalized [20,21] or males may choose to mate while the female is moulting [22]. It has also been shown that the risk of sexual cannibalism in non-gift-giving species (orb-web spiders, mantids) is reduced if mating occurs while the female is feeding [23–26]. Such evidence makes the nuptial gift a likely male anti-cannibalistic strategy. In fact, Kuriwada & Kasuya [27] suggested that nuptial gifts function as a protective male strategy also in non-cannibalistic species where females are aggressive and may harm males by biting and kicking. They empirically verified that in some crickets the nuptial gift (secretions from a metanotal gland) protects the males from female aggression and suggested that the hypothesis of a protective function of the nuptial gift should be extended beyond sexual cannibalism to include any courtship situations where female aggression is costly to males. In this study, we reconsider whether male P. mirabilis benefit from nuptial gifts as shields against sexual cannibalism.

2. Methods

Spiders were collected prior to their maturity moult. When adult, the females were divided into a well-fed (W) and a poorly fed (P) group. After 7 days, females from each group were staged either with a gift-carrying (+) male or with a male with no gift (−). The numbers of females in each group were: n_W+ = 13; n_W− = 33; n_P+ = 15; n_P− = 46. We recorded the outcome as gift-stealing (i.e. females run away with the gift without mating), cannibalism, mating or male rejection. Females that did not cannibalize the male were tested again on the following days for up to 8 times. The results were analysed using survival analysis (also known as time-to-event analysis): cox proportional hazards fit. For detailed description of methods see the electronic supplementary material.

3. Results

The presence or absence of a gift was the most important factor determining whether females cannibalized the males, while feeding level had no significant influence (figure 1, table 1). Poorly fed females were nearly twice as cannibalistic as well-fed females, but this difference was not statistically significant (table 1). Females staged with no-gift males were on average more than six times as cannibalistic as females staged with gift-carrying males. Of 79 females staged with no-gift males, 15 (19%) cannibalized their partner, whereas only one of 28 females (3.6%) cannibalized gift-carrying males. All cases of sexual cannibalism committed against no-gift males were pre-copulatory, whereas the single case committed against a gift-carrying male was post-copulatory. This happened in a P+ trial in direct continuation of a seemingly normal copulation. Cannibalism occurred in 15 of 280 tests (5.4%) with no-gift males, and in 13 of 200 tests (6.5%) considering only the poorly fed females; thus the overall frequency of cannibalism per trial was 5.8%. One female in W+ performed gift-stealing twice, and eight females in P+ performed 10 cases of gift-stealing. The frequency of gift-stealing over all experiments with gift-carrying males did not differ between hungry (P+) and satiated (W+) females ( p = 0.20).

Figure 1.

Time-to-event curve showing the cumulative proportion of females that had cannibalized a male partner during subsequent mating trials. Treatments: W+, well-fed females staged with gift-carrying males; P+, poorly fed females staged with gift-carrying males; W−, well-fed females staged with no-gift males; P−, poorly fed females staged with no-gift males. All cases of sexual cannibalism in W− and P− treatments were pre-copulatory, whereas the single one in P+ was post-copulatory. Statistical analysis in table 1.

Table 1.

Cox proportional hazards test (likelihood ratio test) of cannibalistic events (n = 107 females, 17 cannibalistic events, 90 censored values). The dependent variable is the number of mating trials until the first cannibalistic event of each female. W, well-fed females; P, poorly fed females.

	risk ratio	95% CI	d.f.	χ2	p-value
feeding condition (P/W)	1.91	0.67–6.79	1	1.31	0.25
gift (−/+)	6.42	1.32–115.8	1	5.47	0.0193
feeding condition × gift			1	0.54	0.46

4. Discussion

The results confirmed the hypothesis that the nuptial gift in P. mirabilis protects the male against pre-copulatory cannibalism. Possibly, our experimental design was more sensitive for analysing infrequent events than that used in previous studies. With the low frequency of cannibalism in all treatments, a very large sample size would be needed to demonstrate a significant effect without repeated testing. We believe this is the first experimental demonstration of an anti-cannibalistic effect of a nuptial gift. We do not see this as an alternative explanation for the evolution of gift-giving behaviour. Each of the mechanisms involved, i.e. parental investment, mating effort and avoidance of sexual cannibalism, may have enhanced the others synergistically during the evolutionary process.

Most females of P. mirabilis were rather unaggressive towards no-gift males even if they had starved for one or even two weeks. Even after eight trials, only 30% of the poorly fed females had cannibalized a no-gift suitor and well-fed females even fewer (figure 1). The frequency of cannibalism against no-gift males was slightly elevated compared with previous laboratory studies with gift-carrying males. Precautions against a potentially lethal attack must be important for males as soon as the risk is non-zero. Therefore, a multitude of behavioural and morphological adaptations have evolved to reduce this risk [25,26,28]. Sexual cannibalism can be considered the ultimate form of female mate choice [6]. An elaborate courtship that informs the female about the quality of the male [29] should also reduce the likelihood of a potentially cannibalistic attack. In many spiders, particular courtship signals (visual, auditive, vibrational) may serve this function [20,21]. In P. mirabilis, females trade matings for food [30], and the presence of a nuptial gift is the essential part of the courtship promoting female acceptance [13] even though it is not used by the female as an indicator of male quality [31]. The use of fake gifts by males may thus be a way to get access to receptive females [18], but considering the results of the present paper it may also serve to reduce the risk of a cannibalistic attack.

Pre-copulatory cannibalism against gift-carrying males was not observed in this study but has been observed previously [13–15,30]. Gift-stealing from these males was observed, however. Like cannibalism, gift-stealing occurred at low frequency and independently of female hunger. In previous studies, we noted that gift-stealing and pre-copulatory cannibalism are often performed by the same few females [30]. Our present results suggest that gift-stealing is the most likely outcome of successful female aggression if the male has a gift, while the risk of cannibalism is enhanced if he has no gift.

Observations indicate that the nuptial gift is not the only anti-cannibalism adaptation of the males. During fights the males' strong forelegs seemed to serve the purpose of keeping the female's chelicerae away from his body. With a gift in his chelicerae he seemed to use the legs to direct the female's body and chelicerae towards the gift. A seemingly aggressive attack thus ended in gift acceptance and mating rather than in cannibalism, a behaviour also described from another nuptial gift-giving spider [32]. The role of male front legs in avoiding sexual cannibalism has been proposed and/or confirmed for several groups of spiders [33,34].

We conclude that pre-copulatory cannibalism and gift-stealing are alternative behavioural options for aggressive females, with gift-stealing being the most likely outcome if the male has a gift, cannibalism if he has not. The low level of sexual cannibalism in previous studies (and probably in nature) is thus partly a result of low aggression in a majority of the females, partly owing to male traits that may have evolved as counteradaptations to female aggression. The nuptial gift is one such counteradaptation, and we hypothesize that low sexual size dimorphism and strong forelegs in males are others.

Ethics

The work conducted complies with the ethical regulations in Denmark.

Data accessibility

The dataset supporting this article has been deposited in Dryad: http://dx.doi.org/10.5061/dryad.q5m84.

Authors' contributions

S.T. conceived, designed and performed the laboratory experiments, analysed the data and wrote the manuscript draft. M.J.A. participated in the conception/design of the study and in writing the manuscript. Both authors approved the final version and agree to be accountable for all aspects of the work.

Competing interests

We have no competing interests.

Funding

S.T. was supported by a grant from the Carlsberg Foundation. M.J.A. was supported by ANII (SNI), Uruguay.