Sexual cannibalism and population viability

Some behaviours that typically increase fitness at the individual level may reduce population persistence, particularly in the face of environmental changes. Sexual cannibalism is an extreme mating behaviour which typically involves a male being devoured by the female immediately before, during or after copulation, and is widespread amongst predatory invertebrates. Although the individual‐level effects of sexual cannibalism are reasonably well understood, very little is known about the population‐level effects. We constructed both a mathematical model and an individual‐based model to predict how sexual cannibalism might affect population growth rate and extinction risk. We found that in the absence of any cannibalism‐derived fecundity benefit, sexual cannibalism is always detrimental to population growth rate and leads to a higher population extinction risk. Increasing the fecundity benefits of sexual cannibalism leads to a consistently higher population growth rate and likely a lower extinction risk. However, even if cannibalism‐derived fecundity benefits are large, very high rates of sexual cannibalism (>70%) can still drive the population to negative growth and potential extinction. Pre‐copulatory cannibalism was particularly damaging for population growth rates and was the main predictor of growth declining below the replacement rate. Surprisingly, post‐copulatory cannibalism had a largely positive effect on population growth rate when fecundity benefits were present. This study is the first to formally estimate the population‐level effects of sexual cannibalism. We highlight the detrimental effect sexual cannibalism may have on population viability if (1) cannibalism rates become high, and/or (2) cannibalism‐derived fecundity benefits become low. Decreased food availability could plausibly both increase the frequency of cannibalism, and reduce the fecundity benefit of cannibalism, suggesting that sexual cannibalism may increase the risk of population collapse in the face of environmental change.     

Sexual cannibalism in the garden spider Araneus diadematus

In natural populations, courting males of Araneus diadematus are often consumed by females before they have successfully copulated. Despite the possible nutritional benefits of sexual cannibalism for females, the male can derive no benefit by being consumed before copulation. In this study, females that consumed a single male significantly increased their body mass, regardless of the quality of their diet. The implication is that, for A. diadematus, sexual cannibalism increases female fecundity. In experimentally controlled courtship sequences, larger males were less likely to be cannibalized than smaller males, but female size had no effect on male mating success. The mating success of males was not influenced by the age of the male, indicating that cannibalism is not the results of male senility.     

Swimming in mantids

The initiation, form of leg strokes and minimal requirements for swimming in Sphodromantis lineola are described.     

Sexual cannibalism in the fishing spider and a model for the evolution of sexual cannibalism based on genetic constraints

Several hypotheses have been proposed for the evolution of sexual cannibalism by females. Newman and Elgar (1991) suggested that sexual cannibalism prior to mating by virgin female spiders may have evolved as a result of female foraging considerations. According to this model, an adult female's decision to mate or cannibalize a courting male should be based on an assessment of the male's value as a meal versus his value as a mate. The current study provides an empirical test of the assumptions and predictions of this model in the sexually cannibalistic fishing spider. Adult females were subjected to different food treatments, and exposed to adult males in the laboratory. However, only one of the assumptions of the model and none of its five predictions were upheld. We failed to find any effects of female foraging, female mating status, female size, male size or time of the season on females' behaviour towards courting males. Females behaved stereotypically, and many females were left unmated despite numerous mating opportunities. We also demonstrate costs of sexual cannibalism in a natural population. We propose that the act of sexual cannibalism in the fishing spider is non-adaptive, and develop a model for the evolution of premating sexual cannibalism in spiders based on genetic constraints. According to this hypothesis, sexual cannibalism by adult females may have evolved as an indirect result of selection for high and non-discriminate aggression during previous ontogenetic stages. Genetic covariance between different components of aggressive behaviour may constrain the degree to which (1) juvenile and adult aggression and/or (2) aggression towards conspecifics and heterospecifics can vary independently. We briefly review the support for our model, and suggest several critical tests that may be used to assess the assumptions and predictions of the model.     

Sexual cannibalism by Octopus cyanea on a Pacific coral reef

Sexual cannibalism is rare in the animal kingdom. Although cannibalism is not uncommon in cephalopods, here we report the first documented case of sexual cannibalism. A large female Octopus cyanea was observed continuously for 2.5 days in Palau, Micronesia, when she was out of her den. On the second day, a small male followed and mated her 13 times during 3.5 h while she continued to forage over 70 m distance. After the 12th mating, she aggressively chased a different small octopus that barely escaped by jetting, inking and swimming upwards. Shortly thereafter, the original small male mated her a 13th time, but subsequently she attacked and suffocated him and spent 2 days cannibalizing him in her den. This sort of intraspecific aggression helps to explain several reports of octopuses mating out in the open, a behaviour that may serve to allow the smaller mate to escape cannibalism.     

Sexual cannibalism by Octopus cyanea on a Pacific coral reef

Sexual cannibalism is rare in the animal kingdom. Although cannibalism is not uncommon in cephalopods, here we report the first documented case of sexual cannibalism. A large female Octopus cyanea was observed continuously for 2.5 days in Palau, Micronesia, when she was out of her den. On the second day, a small male followed and mated her 13 times during 3.5 h while she continued to forage over 70 m distance. After the 12th mating, she aggressively chased a different small octopus that barely escaped by jetting, inking and swimming upwards. Shortly thereafter, the original small male mated her a 13th time, but subsequently she attacked and suffocated him and spent 2 days cannibalizing him in her den. This sort of intraspecific aggression helps to explain several reports of octopuses mating out in the open, a behaviour that may serve to allow the smaller mate to escape cannibalism.     

Sexual cannibalism: high incidence in a natural population with benefits to females

Background

Sexual cannibalism may be a form of extreme sexual conflict in which females benefit more from feeding on males than mating with them, and males avoid aggressive, cannibalistic females in order to increase net fitness. A thorough understanding of the adaptive significance of sexual cannibalism is hindered by our ignorance of its prevalence in nature. Furthermore, there are serious doubts about the food value of males, probably because most studies that attempt to document benefits of sexual cannibalism to the female have been conducted in the laboratory with non-natural alternative prey. Thus, to understand more fully the ecology and evolution of sexual cannibalism, field experiments are needed to document the prevalence of sexual cannibalism and its benefits to females.

Methodology/Principal Findings

We conducted field experiments with the Mediterranean tarantula (Lycosa tarantula), a burrowing wolf spider, to address these issues. At natural rates of encounter with males, approximately a third of L. tarantula females cannibalized the male. The rate of sexual cannibalism increased with male availability, and females were more likely to kill and consume an approaching male if they had previously mated with another male. We show that females benefit from feeding on a male by breeding earlier, producing 30% more offspring per egg sac, and producing progeny of higher body condition. Offspring of sexually cannibalistic females dispersed earlier and were larger later in the season than spiderlings of non-cannibalistic females.

Conclusions/Significance

In nature a substantial fraction of female L. tarantula kill and consume approaching males instead of mating with them. This behaviour is more likely to occur if the female has mated previously. Cannibalistic females have higher rates of reproduction, and produce higher-quality offspring, than non-cannibalistic females. Our findings further suggest that female L. tarantula are nutrient-limited in nature and that males are high-quality prey. The results of these field experiments support the hypothesis that sexual cannibalism is adaptive to females.     

Sexual cannibalism in Nephila plumipes as a consequence of female life history strategies

The evolution of sexual cannibalism has been modelled as both an adaptive and nonadaptive female strategy. Recent evidence from several species suggests a connection between female foraging and sexual cannibalism, but the precise benefits for females have remained obscure. Here, we investigate the difference between cannibalistic and noncannibalistic female Nephila plumipes by removing the potential nutritional benefit of cannibalism. Courting and mating males that were killed by a female were immediately removed so that the female could not consume them. Nevertheless, cannibalistic females gained more mass from maturation to oviposition and produced larger first clutches than noncannibalistic females, although cannibalistic females matured at a smaller size and mass than noncannibalistic females. In juvenile instars, mass gain was generally smaller in females that moulted in a good condition but intermoult intervals were shorter. However, the time from maturity to oviposition was not shorter in females that matured in a good condition. Male behaviour did not differ according to the risk of cannibalism. We suggest that sexual cannibalism in N. plumipes is a side‐effect of an increased foraging vigour of females that matured at a smaller size and body mass. Selection pressure on males to avoid cannibalism may be weak because of limited mating opportunities.     

Defensive behaviour in Ghanaian praying mantids

The defensive behaviour of 25 species of praying mantids from Ghana is described. All have camouflage as the primary defence mechanism, either a general resemblance to vegetation, or a specific resemblance to bark, sticks, leaves or grass. Secondary defence mechanisms include running, flying, thanatosis, secretion of fluid from the mouth, startle display and flash colouration. The early instars of several species are ant-mimics. The female Taracbodes afzelii often guards her ootheca and also the young nymphs, and she can distinguish her nymphs from intruding ants which are attacked. Some mantids have a green/brown polymorphism and there is evidence that the frequencies of the two forms vary seasonally. Other mantids are stick, grass or bark mimics, and the possible ways in which the adaptations of these forms have evolved are outlined. The startle display is probably a bluff which protects the mantid to some extent from avian predators. It does not appear to be directed against predaceous mammals. A curious "boxing display" is described from Oxypilus, Anasigerpes and Catasigerpes. It probably functions to space out individuals, not to discourage attacks from predators. The occurrence of this display is used as taxonomic evidence for the close relationship of these three genera.     

Sexual dimorphism in leg length among orb-weaving spiders: a possible role for sexual cannibalism

The degree and direction of sexual dimorphism across different species is commonly attributed to differences in the selection pressures acting on males and females. The extent of these differences is especially apparent in species that practise sexual cannibalism, where the female attempts to capture and eat a courting male. Here, we investigate the relationship between sexual dimorphism in size and leg length, sexual cannibalism and courtship behaviour in three taxonomic groups of orb-weaving spiders, using morphological data from 249 species in 36 genera. Females are larger than males in all three taxonomic groups, and males have relatively longer legs than females in both the Araneinae and Tetragnathidae. Across genera within each taxonomic group, male body size is positively correlated with both female body size and male leg length, and female body size is positively correlated with female leg length. Sexual size dimorphism is negatively correlated with relative male leg length within the Araneinae, but not within either the Tetragnathidae or the Gasteracanthinae. There was no negative correlation between sexual size dimorphism and relative female leg length in any taxonomic group. We argue that the relationship between sexual size dimorphism and relative male leg length within the Araneinae may be the result of selection imposed by sexual cannibalism by females.     

Sexual size dimorphism predicts the frequency of sexual cannibalism within and among species of spiders

Sexual cannibalism varies widely among spiders, but no general evolutionary hypothesis has emerged to explain its distribution across taxa. Sexual size dimorphism (SSD) also varies widely among spiders and could affect the vulnerability of males to cannibalistic attacks by females. We tested for a relationship between SSD and sexual cannibalism within and among species of spiders, using a broad taxonomic data set. For most species, cannibalism was more likely when males were much smaller than females. In addition, using phylogenetically controlled and uncontrolled analyses, there was a strong positive relationship between average SSD of a species and the frequency of sexual cannibalism. This is the first evidence that the degree of size difference between males and females is related to the phylogenetic distribution of sexual cannibalism among a broad range of spiders.     

Contrasting scales of oviposition and parasitism in praying mantids

We report on spatial patterns of parasitism of oothecae (egg cases) of praying mantises (Stagmomantis limbata) by torymid wasps, Podagrion spp. Using collections of mapped mantid oothecae from Riparian sites in the Sonoran desert and Grassland sites in the Chiricahua Mountains (both in Arizona, USA), we characterized the spatial distributions of oothecae and parasitism. The likelihood of an egg case suffering some parasitism was higher at Grassland sites, which had high oothecal densities, than at low-density Riparian sites. However, experimental isolation of Grassland oothecae to densities comparable to Riparian sites reduced parasitism rates. At Riparian sites, parasitized oothecae exhibited on average the same extent of parasitism as parasitized oothecae at high densities but with much greater variation. Indeed, large fractions of Riparian oothecae suffered both severe (>50%) and light (<20%) parasitism, whereas most parasitized Grassland oothecae suffered intermediate levels of parasitism. Analysis of first nearest neighbor distances indicated that the parasite load of an ootheca did not depend on its immediate isolation. However, extending the analysis to include subsequent nearest neighbors (using a technique from spatial statistics called the R(K) function), we found that even though oothecae of S. limbata were spatially clustered, some oothecae in a (statistically defined) cluster escaped parasitism when overall oothecal densities were low. This pattern suggests that when oothecae are sparsely distributed, Podagrion wasps exploit only a fraction of the oothecae available locally, even though the oothecae are strongly aggregated relative to their overall density. We suggest this lack of congruency in the scales of oothecal deposition and parasitism at low densities (which is absent when oothecae are at high densities) may be explained in part by behavioral aspects of the parasite's reproduction, including increased host fidelity by relatively sedentary female parasites. Received: June 13, 2000 / Accepted: October 16, 2000     

Geographic variation in genital morphology of Ciulfina praying mantids

Geographic variation in morphological traits is widespread and important to our current understanding of evolutionary processes. Although male genitalia are perhaps the most divergent morphological traits in animals, geographic variation in genital traits has received little attention and the mechanism driving such variation is unclear. The species isolation hypothesis of genital evolution makes explicit predictions about geographic variation in genitalia predicting patterns of genital divergence that reflect the risk of mating with related but incompatible species. The sexual selection and pleiotropy hypotheses, however, predict general levels of geographic variation that reflect divergent sexual selection pressures or genetic drift. To test these predictions, we investigated geographic variation in genital morphology in the praying mantid genus Ciulfina (Mantodea: Liturgusidae) using elliptic Fourier analysis. We found significant levels of geographic variation in the genital morphology of four Ciulfina species irrespective of the relative proximity of different populations to contact zones with other species. These results reject the species isolation hypothesis, and instead support either the sexual selection or pleiotropy hypotheses to explain patterns of genital evolution in this genus.