Sexual Cannibalism Research Articles

Mate-finding Allee effects can be exacerbated or relieved by sexual cannibalism.

Allee effects occur when individual or population survival decreases due to populations being small or sparse. A key mechanism underlying Allee effects is difficulty in finding mates at low densities. Species may be particularly vulnerable to mate-finding Allee effects if females rely on an abundance of males to reproduce successfully. In sexually cannibalistic species, females may consume males before or after copulation, potentially reducing the supply of males to the point where a mate-finding Allee effect occurs. In this study, we investigate the extent to which sexual cannibalism can modulate mate-finding Allee effects, and the conditions under which sexual cannibalism is likely to be particularly detrimental to population viability. We created an individual-based model that tracked specific females throughout the breeding season and used extinction risk and per capita growth rate to measure the strength of the Allee effects. We varied both founder population size and mate encounter rate independently of each other to expose the mechanism driving the Allee effects. We also analysed how cannibalism-derived female fecundity benefits affected extinction risk. We found that sexual cannibalism could lead to high extinction risk, particularly when cannibalism occurred before copulation, founder population size was small and mate encounter rates were low. However, post-copulatory cannibalism reduced extinction risk, if cannibalism increased female fecundity enough. We found that there were strong threshold effects, in which small changes in encounter rate could strongly alter population extinction risk. We find that sexual cannibalism is likely to negatively impact population survival as population size and mate encounter rate decrease. This may be exacerbated if male quality declines and female hunger increases in declining populations. As many top invertebrate predators, such as spiders and mantises, are sexually cannibalistic, this may have ecosystem-wide impacts. We also suggest that other reproductive behaviours, such as rejecting all but high-quality mates or requiring multiple mates to ensure fertility, are also likely to cause mate-finding Allee effects when habitat quality degrades.

Behavioural correlations and aggression in praying mantids

Distinct behaviours can co-vary within individuals. As such, the magnitude of certain behaviours may be partly predicted by other behaviours, rather than the environment. This can constrain behaviours, potentially reducing behavioural variability. Pre-copulatory sexual cannibalism, the consumption of potential mates before copulation, can lead to females remaining unmated, particularly if males are rare. One possible explanation for the persistence of pre-copulatory cannibalism is that sexual cannibalism is correlated with high levels of aggression towards prey. Here, we test this in two species of praying mantis: the highly cannibalistic Miomantis caffra and the less cannibalistic Orthodera novaezealandiae. If cannibalism in M. caffra is linked to aggression towards prey, we predicted that (1) M. caffra would be more aggressive towards prey than O. novaezealandiae, (2) female M. caffra would be more aggressive than males, (3) aggression towards prey would be correlated across juvenile and adult instars for M. caffra but not O. novaezealandiae, and (4) aggression towards prey would be associated with a propensity for sexual cannibalism among individual M. caffra. We found evidence supporting predictions one and two, but not predictions three and four. Surprisingly, aggression was shown to be repeatable and correlated across instars for O. novaezealandiae but not M. caffra. Our results suggest sexual cannibalism is not a product of behavioural co-variation, even in clades where sexual cannibalism is common. This suggests that sexual cannibalism evolves due to the direct benefits it brings to females, rather than being a by-product of high aggression towards heterospecific prey.Significance statementIn some animals, different behaviours co-vary within individuals. This may lead to the emergence of costly behaviours and reduce behavioural plasticity. It is theorized that pre-copulatory cannibalism is a costly behavioural by-product of selection for high levels of aggression towards prey. However, there are very few studies that explicitly test this. Here, we provide a behavioural comparison between two species of praying mantis that vary in their propensity to cannibalize and tested whether general aggression is linked cannibalism. We found that aggression towards prey in adults can be linked to juvenile aggression but not a propensity for cannibalism. Although cannibalism rates were higher in the species that was more aggressive towards prey, aggression towards prey was not linked to cannibalism within individuals. This suggests that pre-copulatory cannibalism is not a behavioural by-product but a result of direct selection.

Mating behavior of the Persian boxer mantid, Holaptilon brevipugilis (Mantodea: Mantidae)

The Persian boxer mantid,Holaptilon brevipugilis, is the mantid most recently described from Iran. Here, I present some aspects of the courtship display and mating behavior of this species. I conducted 28 mating trials, quantified the relative frequency of all mating behaviors, and estimated the pre-copulation, copulation, and post-copulation periods. I also compared the effects of frontal vs. lateral approaches of the male for mating success, since frontal approach increases the risk that the male will be seen and cannibalized by the female. In 64% of trials, the male approached the female immediately, regardless of whether the female could see him or not. Copulation was successful in 61% of trials. Male courtship consisted of dorsoventral bending of the male’s abdomen and occurred in 10% of all trials, but only when the female was facing the male. In contrast, trembling of the forelimbs was not associated with copulation, occurred in 10% of all trials, and was always followed by the male moving away from the female. I observed one female cannibalizing a male post-copulation. The Persian boxer mantid might be sexually cannibalistic, but confirming this hypothesis would require further studies, including a focus on female hunger level as a determining factor in sexual cannibalism and in male courtship behaviors.

Males sacrifice their legs to pacify aggressive females in a sexually cannibalistic spider

Monogynous male mating strategies have repeatedly evolved in spiders along with female-biased sexual size dimorphism (SSD) and extreme male mating investment. As a manifestation of sexual conflict, male African golden-silk spiders, Trichonephila fenestrata, are regularly attacked by females during copulation, and sexual cannibalism is common. Curiously, attacked males actively cast off (autotomize) their front legs and copulation continues while the female is feeding on these legs. Since the loss of legs is costly in reducing males’ ability to mate guard, it should yield significant benefits. In a series of experiments, we investigated the behavioural mechanism of male leg ejection and tested three hypotheses. First, we performed feeding experiments to test whether conspecific male legs are particularly attractive for females and act as a sensory trap. Second, we conducted mating experiments with sibling and nonsibling pairings to test whether males preferentially invest in high-quality mates. Third, by offering male legs during copulations, we tested whether male leg ejection serves to distract and pacify females. In support of the female pacifier hypothesis, our results confirm a significantly reduced probability of attacks in females that had been offered a male leg, but we found no relationship between simulated leg ejection and male survival. While there was no evidence for special properties of male legs, females accepted male legs significantly more often than insect food. The degree of male leg sacrifice did not depend on male–female relatedness, but large males lost more legs than small males, and small males achieved more copulations. However, total copulation duration was unrelated to male size. Male leg sacrifice in T. fenestrata may represent a rare example of an evolutionary transition in which the antipredation behaviour of autotomizing body parts has changed its function into a sexual context, here to pacify females and to facilitate undisturbed copulations.

The sexual behaviour of the Neotropical wolf spider Lycosa inornata (Araneae: Lycosidae), with comments on maternal behaviour

Lycosa inornata Blackwall, 1862 is a small wolf spider that inhabits open environments from Uruguay and, like other wolf spiders, little is known of their sexual behaviour, which we describe here. Male courtship behaviour includes leg rubbing, leg vibration and pedipalp drumming, as well as leg waving. Females respond to male courtship by running towards them and shoving them with her legs and body. Receptive females lower their body on the substrate and slightly raise and twist the abdomen, facilitating the mounting and subsequent pedipalp insertions. Copulation lasts less than an hour, has two behavioural copulatory patterns and one haematodochal expansion per pedipalp insertion, in turn intercalated by pedipalp chewing. Pattern I consists of several insertions with the same pedipalp before a side change. Pattern II consists of a single pedipalp insertion before a side change. Females construct a single egg sac within 40–45 days after copulation and an average of 65 spiderlings emerge after 35 days. As occurs in other species of lycosid, L. inornata presents a low rate of sexual cannibalism. This study adds to the few descriptions of sexual and reproductive behaviours in wolf spiders and we hope it will increase knowledge of this diverse family of spiders.

Density-dependent aggression, courtship, and sex ratio in a fishing spider

Sexual cannibalism is common in spiders and can be advantageous for female fitness by increasing egg production. However, it is possible that, under low mate density, females will be at risk of consuming all of the males they encounter prior to copulation. Cannibalistic females may be able to mitigate the risk of virgin death if they reduce cannibalism rates in response to low mate availability. Here, we attempted to manipulate perceived mate density and observe whether it affected female aggression towards males in the fen raft spider (Dolomedes fimbriatus). We predicted that female attack rate would increase in response to an increasing number of male encounters. We also recorded male courtship effort. Despite previous literature finding that D. fimbriatus females were highly aggressive towards conspecific males, we found that females only attacked courting males in 14% of encounters. None of these attacks resulted in cannibalism. Moreover, attacks were not associated with how many males the female had previously been exposed to. Male courtship effort decreased in response to repeated exposure to females. Some of the virgin females laid and guarded unfertilized egg cases; this made them unattractive to males, potentially reducing their reproductive lifespan prematurely.

Cannibalism

Chloe Fouilloux and colleagues introduce animal cannibalism.

Sexual Size Dimorphism: Evolution and Perils of Extreme Phenotypes in Spiders.

Sexual size dimorphism is one of the most striking animal traits, and among terrestrial animals, it is most extreme in certain spider lineages. The most extreme sexual size dimorphism (eSSD) is female biased. eSSD itself is probably an epiphenomenon of gendered evolutionary drivers whose strengths and directions are diverse. We demonstrate that eSSD spider clades are aberrant by sampling randomly across all spiders to establish overall averages for female (6.9 mm) and male (5.6 mm) size. At least 16 spider eSSD clades exist. We explore why the literature does not converge on an overall explanation for eSSD and propose an equilibrium model featuring clade- and context-specific drivers of gender size variation. eSSD affects other traits such as sexual cannibalism, genital damage, emasculation, and monogyny with terminal investment. Coevolution with these extreme sexual phenotypes is termed eSSD mating syndrome. Finally, as costs of female gigantism increase with size, eSSD may represent an evolutionary dead end.

Shape of male palpal hook affects female sexual cannibalism in Leucauge mariana (Araneae: Tetragnathidae)

In the Colombian orb-web spider Leucauge mariana (Taczanowski, 1881) (Tetragnathidae), both sexes contribute to mating plug formation. Males of this species show a conductor hook that could be involved in providing stability to the mating pair and used for mating plug removal. The aim of the study was to assess the relationship between the shape of the conductor hook in L. mariana and mating duration, the amount of sperm stored, and the occurrence of sexual cannibalism. We used geometric morphometric tools for studying the conductor hook shape. The width of the base of the conductor hook was negatively correlated with the probability of sexual cannibalism by females (PC2 = 0.017), but we did not find a significant relation with mating duration and the amount of sperm transferred. Female choice on male hook shape, or on the stability provided by the hook during the mating position, could be occurring in this species.

Male performance and associated costs in successive sexual encounters in a polygynous web wolf spider

Polygynous males increase their reproductive success by fertilizing as many females as possible. However, this strategy can lead to costs for the males. This study focused on an atypical wolf spider that lives in webs, Aglaoctenus lagotis. Previous studies report polyandrous females, but little is known about the mating strategy of males and its potential associated costs. Our goals were to determine the potential polygyny and the changes in sexual behaviour, body condition and physiology of males throughout successive matings. Males were expected to mate with multiple females; males’ body condition was expected to decrease and male mating performance, including sperm transfer, was expected to decrease over successive matings. Males were exposed to successive virgin females every 3 days until the male did not court, was cannibalized or died of natural causes. Agreeing with our predictions, males were capable of multiple matings, showing an average of 5 ± 2 matings (range 3–11). Their mating performance decreased in successive matings and, although no changes were found in the behavioural patterns during the courtship over successive matings, the number of palpal insertions decreased. Unexpectedly, overall body condition did not decrease and males did not deplete their sperm supply. We found that 44% of the males were victims of sexual cannibalism after their third mating. The females that attacked or cannibalized males had less sperm stored in their spermathecae than those that did not. We discuss hypotheses that may clarify this scenario and the role of the cryptic female choice mechanism.

Optimal ultra-short copulation duration in a sexually cannibalistic spider

Sexual conflict has been shown to shape many behaviors in the reproductive context, such as the duration of copulation, across a broad taxonomic range. In spiders, copulation duration is one of the most variable reproductive traits, ranging from seconds to hours. Some species in the araneid genus Argiope exhibit very short copulations of a few seconds per pedipalp insertion. This has been hypothesized to be the result of cannibalistic females imposing selection on males to escape the attack by reducing insertion duration to a minimum. However, copulation duration is positively correlated with the number of sperm transferred and fertilization success in many species. Thus, given the tradeoff between sperm transfer and the risk of being cannibalized, males may optimize the duration of copulation to maximize lifetime reproductive success. Here we test whether males in the orb-weaver Argiope aurantia, which exhibits the shortest copulation in any spider and rivals the honey bee for shortest copulation reported for any arthropod with internal genital coupling, are optimizing the insertion duration of the first pedipalp to maximize the number of sperm transferred and eggs fertilized. We analyzed total sperm transferred to the female, and male fertilization success as a function of the first insertion’s duration, using data collected in previous staged-mating experiments and determined optimal copulations of 3–4 s, which is close to the averages of the source populations. Thus, we present evidence for sexual cannibalism as a driver of the extremely short copulations in A. aurantia. Females and males often conflict over mating frequency. In spiders, both sexes have paired reproductive organs and can remain half virgin if only one of the two possible copulations are completed. In the orb-weaver Argiope aurantia, males place mating plugs and females almost always immediately attack males in copula, probably to prevent them from achieving both copulations and to be able to upgrade to a second mate. We find an optimal duration of 3–4 s for males to terminate copulation, which reduces the risk of being killed, while at the same time maximizing sperm transfer and fertilization success because copulation duration is positively related to the number of sperm transferred and allows males to achieve the second copulation. The optimal duration detected here is very close to average copulation durations in nature. Hence, we document the adaptive value of the shortest copulation known for any spider.

Females of a cannibalistic spider control mutilation of their genitalia by males

AbstractWhen females can mate multiply, the interests of both sexes over female remating may not coincide, leading to selection for adaptations and counteradaptations in males and females. In several orb-weaving spiders, males damage external structures of the female genitalia during copulation, which hinders the female from remating. We investigated whether females have control over the mutilation of their genitalia in the orb-weaving spider Larinia jeskovi. We found that female sexual cannibalism during copulation reduced the number of insertions a male was able to perform and hence limited the probability of genital mutilation by the male. Genital mutilation did not differ between treatments in which females experienced different availabilities of other males before the mating trial: males absent, males near the female (“vicinity group”), and males in the female’s web (“web group”). However, traits of the mating male (size, condition) were significantly correlated with the occurrence of cannibalism during mating in “web” and “vicinity” treatments. These results suggest that females have control over mutilation by an early termination of mating, can respond to the availability of potential mates and can alter the probability of mutilation according to certain male traits. Female sexual cannibalism may represent a counteradaptation to genital mutilation allowing females to mate multiply.

ROV Observations on Reproduction by Deep-Sea Cephalopods in the Central Pacific Ocean

Telepresence-enabled operations by remotely operated vehicles (ROVs) allow many researchers a unique perspective on morphology, behavior, and small-scale distributions of deep-sea animals. I present some examples of cephalopod natural history from recent ROV dives in the central Pacific Ocean. These examples include clues to reproductive behavior of deep-sea squids and cirrate “dumbo” octopods. During 7-12 March 2017, the ROV Deep Discoverer (D2) operating from NOAA Ship Okeanos Explorer recorded high-definition video of several squid in the genus Chiroteuthis. These included a mature male, a mature female, and a moribund squid identifiable as C. picteti. The female had obviously mated, with spermatangia implanted in many locations, and was holding in its arms another squid that appeared to be another Chiroteuthis. Considered together, these observations may indicate a deep-sea spawning aggregation and, possibly, sexual cannibalism. Another series of observations by D2 revealed eggs of cirrate octopods attached to octocorals. The remarkable thing about these observations was that in two of them (18 March and 4 May) the egg chorion had swollen and burst the external egg capsule. This may explain how the hatching embryo is able to escape from the tough protective coating secreted by the oviducal gland of cirrates but not secreted by the better-known incirrate octopods.

Observations on the mating behavior of a dryinid and first record of sexual cannibalism in the hymenoptera

Sexual cannibalism is a phenomenon that has been reported in a wide variety of invertebrate predators. In arthropods, it has been documented mostly in arachnids. The Dryinidae, a small cosmopolitan family of aculeate hymenopterans, are exclusively parasitic of the hemipteran suborders Cicadomorpha and Fulgoromorpha. They include some species that have been successfully employed in biological control programs. The ecology and biology of the Dryinidae is generally little known. In this short communication, studying biological traits of Gonatopus chilensis, a parasitoid of planthoppers, we report two novel facts for dryinid species: occasionally virgin females were re-mated by the same male, and after mating, occasionally young females caught the male and devoured its gaster. This is the first record of sexual cannibalism for the family Dryinidae and, to our knowledge, for the order Hymenoptera.

Bringing down the house: male widow spiders reduce the webs of aggressive females more

Theory suggests that males should adjust courtship in response to a variety of factors, including female quality, the risk of male-male competition, and often in spiders, the risk of sexual cannibalism. Male black widow spiders demonstrate a behavior during courtship whereby they tear down and bundle a female’s web in addition to providing other vibratory and contact sexual signals. This web reduction has been hypothesized to play a role in all three factors (sexual signaling, competition reduction, and cannibalism reduction), but rarely are these tested together. Here, we test these hypotheses by conducting mating trials using the western black widow (Latrodectus hesperus) and measuring both male and female quality and behavior. Our results indicate that amount of web reduction is best predicted by female aggression, and not aspects of either male or female quality (e.g., body mass), or by the potential for the web to attract other males (e.g., web mass). Yet, actual mating success was best predicted by the proportion of web reduced. Furthermore, there was no consistent among-individual variation in either reduction behavior or male success, indicating that all variation in both measures was due to plasticity and/or other unaccounted-for male or female traits. Collectively, we conclude that the primary function of web reduction behavior is to reduce female aggression and thus the risk of sexual cannibalism, and that any other functions such as signaling and reducing male-male competition have relatively lower importance. Male widow spiders must account for female aggression, quality, and male-male competition when courting females. During courtship, males will reduce a female’s web by tearing it down and bundling the silk, which may aid in all three of these issues. Our results demonstrate that males reduce the webs of aggressive females more, and less so to potentially reduce competition from other males or in response to female quality. Ultimate mating success was dictated by how much a male reduced the web of a given female. Finally, males showed no among-individual variation in reduction behavior, indicating that the extensive variation in this behavior is due solely to plasticity in response to the female.

Sex or food? Effects of starvation, size and diet on sexual cannibalism in the amphipod crustacean Gammarus zaddachi

Cannibalism of females by males before, during or immediately following sex has been attributed to misidentification of females, rejection of females as mates and prioritisation of feeding over reproduction. In the gammarid amphipod Gammarus zaddachi, males demonstrate that they have identified a female and accepted her as a suitable mate by engaging in precopula pairing behaviour. However, a male may later decide to eat the female after pairing with her. Laboratory experiments were performed in which survival of females in precopula pairs of G. zaddachi was monitored after their male partners had been subjected to starvation, herbivorous diets or diets containing animal matter. These indicate that the female is less likely to survive when she is abnormally small relative to the male, when the male is at risk of death by starvation or when the male’s diet has lacked animal content. Decisions by males to forgo reproductive opportunities in favour of cannibalism, even after engaging in costly mate-guarding behaviour, emphasise the importance of carnivory in the trophic ecology of Gammarus species.

Fifty shades of silk: sexual behavior and bridal veil deposition in the spider Ctenus longipes

Males of some spider species lay silk threads on the female’s body during courtship and/or copulation. There are several hypotheses trying to explain the function of this behavior, known as bridal veil deposition. One of them proposes that bridal veils could occur to immobilize females and prevent sexual cannibalism when females are larger than males, or that they could inhibit female aggressive behavior. Ctenus longipes is a wandering and nocturnal spider that inhabits ravine forests in South America. The aim of this work was to describe in detail courtship and copulatory behaviors in C. longipes and confirm the occurrence of a bridal veil, discussing its possible functions in this species. For that purpose, we exposed 13 virgin male-female pairs at laboratory conditions and recorded courtship, copulation, and post-copulation behaviors. We also measured body and leg size of all individuals to estimate sexual size dimorphism. In all the cases, the male deposited silk on top of the female’s body in the form of a bridal veil, covering the anterior carapace and forelegs. The data did not support the hypothesis that bridal veil deposition is related to sexual cannibalism avoidance because females were not immobilized during mating, larger females did not present longer silk bindings, and we did not observe aggressions in any case. Future studies where males are prevented from producing silk will allow a better understanding of whether or not the veil is involved in avoiding cannibalism in C. longipes.

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.

Female nursery web spiders (Pisaurina mira) benefit from consuming their mate

AbstractThe often coincidental involvement of cooperation and conflict in animal reproduction is epitomized by sexual cannibalism, which can lead to obvious male costs while simultaneously providing direct benefits to developing offspring. Male nursery web spiders (Pisaurina mira) avoid postcopulatory sexual cannibalism by wrapping females with silk. Here, we test the hypothesis that this silk wrapping results in a loss of consumption cost for females. In specific, we hypothesize that females lose out on potential fitness benefits associated with cannibalizing their mating partners. To test this, we paired females with males that were experimentally manipulated to prevent the silk wrapping of females, thereby increasing the likelihood of sexual cannibalism. Females either did not kill their mate, and thus consumed nothing, or did kill their mate. If females killed their mating partner, we allowed them to consume the male, consume nothing, or consume a cricket. We found no effect of female or male body sizes on the likelihood of females killing their mate. While our treatments did not affect the number of offspring females produced, females that consumed either a male or a cricket produced egg sacs faster than females that consumed nothing, suggesting a benefit of increased postcopulatory food consumption. Further, only females that ate a male had heavier and longer lived offspring, suggesting a benefit of sexual cannibalism specifically. Our results support the hypothesis that females can receive fitness benefits associated with sexual cannibalism.

Population Structure, Movement Patterns, and Frequency of Multiple Matings in Tenodera sinensis (Mantodea: Mantidae).

Models of the evolution of sexual cannibalism show that the frequency of male mating opportunities has significant impact on male choice and male risk aversion. In this study, we examined ecological components that should affect opportunities for multiple mating in wild populations of the Chinese mantid (Tenodera sinensis Saussure). While conducting mark-recapture studies of two field populations over the course of two seasons, along with Global Positioning System data on locations of individuals, we collected data on population densities, movement patterns, and individual ranges to estimate the overlap of adult males and female mantids. Our results show that local populations of mantids range from 89 to 161 individuals and occur at densities ranging from 10 to 39 mantids per 1,000 m2. Males move greater distances daily compared with females, giving males larger home range sizes. The ranges of male mantids overlapped with multiple females, thus offering the potential for multiple mating by males. We directly observed 11 encounters between male and female T. sinensis, including one multiple mating by an individual male. The overall mate encounter rate for males was 12.5%. We also provide additional observations of interspecific sexual attraction between T. sinensis and Mantis religiosa Linne (Mantodea: Mantidae). Mantids were most commonly found within the top 20% of two flowering plants, goldenrod (Solidago Linnaeus spp. (Asterales: Asteraceae)) and mugwort (Artemisia vulgaris Linnaeus (Asterales: Asteraceae)), which should place them in prime locations for capturing flying pollinators.