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This article is about arthropod behavior; for the human sexual fetish see Vorarephilia
Sexual cannibalism in praying mantises: a female biting off the head of a male
The prevalence of sexual cannibalism gives several species of Latrodectus the colorful common name "black widow spider".

Sexual cannibalism is an extreme form of sexual conflict, in which a female attacks and consumes a male of the same species before, during, or after copulation [1]1. Although uncommon, males of certain species of spiders have been known to display cannibalistic behavior [2]2. The adaptive foraging hypothesis [3]3, Aggressive spillover hypothesis [4]4, Mate choice [5]5, and Mistaken Identity [6]6 are several hypotheses that have been proposed to explain how sexual cannibalism has evolved.

Prevalence

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Sexual cannibalism is common among insects, arachnids [7], and amphipods[7] 7. There is also evidence of sexual cannibalism in gastropods and copepods [8]8. Sexual cannibalism can occur before, during or after copulation [9]9. Sexual cannibalism is common among species with prominent sexual size dimorphism (SSD), and underlines that extreme SSD has likely drove the evolution of sexual cannibalism in spiders [10]10.

Evolution and maintenance

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Female Chinese mantis eats a male copulating with her

Adaptive foraging hypothesis – The adaptive foraging hypothesis is a proposed pre-copulatory explanation in which females assess the nutritional value of a male to the male’s value as a mate[11] 11. Starving females are usually in bad physical conditions therefore they are more likely to cannibalize a male than mate with him [12]12. Cannibalism by females in the Pseudomantis albofimriata species has improved fecundity, overall growth, and body condition11. In the Dolomedes triton species, a female that was in need of additional energy and nutrients for egg development would choose the closest nutritional source, even if she will need to cannibalize the male 13. In Agelenopsis pennsylvanica and Lycosa tarantula, a significant increase in fecundity, egg cases size, hatching success, and survivorship of offspring has been observed when hungry females choose to cannibalize smaller males before copulating with larger, more genetically superior males 14,15 . This reproductive success was largely due to the increased energy uptake by cannibalizing a males and investing that additional energy (joules) in the development of egg case size and quality 14,16. In D. triton, post-copulatory sexual cannibalism was observed in the females that had a limited food source; these females would copulate with the males and then cannibalize them 13.


The adaptive foraging hypothesis has been criticized because males are considered poor meals compared with crickets, however recent findings included proteins and lipids and discovered what nutrients males of the hogna helluo species have nutrients that crickets don’t have 16,17. In H. helluo, females that cannibalize males have a higher protein diet than when they consume crickets (Acheta domesticus) 16. Further studies show that spiders (A. keyserlingi) that have high-protein/low-lipid diets, that come from sexual cannibalism, may help females produce eggs of greater egg energy density (yolk investment) 3. As a result hungry females are more likely to cannibalize a male than mate with him, because of the associated benefits of food intake to increase fecundity.


Aggressive spillover hypothesis – The aggressive spillover hypothesis suggests that female’s aggressive nature with their prey will determine the likeliness of her cannibalizing a potential mate. The more aggressive a female is with her prey the more likely she is to cannibalize a mate 13. The decision of a female to cannibalize a male is not defined by the nutritional value or genetic advantage (courtship dances, male aggressiveness, & large body size) of males, but instead depends strictly on her aggressive state 7,13. Aggression of the female is measured by latency (speed) of attack on prey. The faster the speed of attack and consumption of prey, the higher the aggressiveness level 18. Females that show aggressive characteristics tend to grow larger in size and display continuous cannibalistic behavior. Females displaying aggressive characteristics can be greatly disadvantaged because such behavior drives potential mates away and reduces her chances of mating 19. Aggressive behavior is less common in an environment that is female-biased, because there is more competition to mate with a male. Such aggressive behavior would scare off potential mates, therefore make these traits unsuccessful 15,20.


Males of the P.mirablis species use a technique called death feigning (playing dead) to avoid being cannibalized by a female. This is an all-or-nothing technique, enabling the male to sneak copulation. The female might choose to attack & cannibalize the “dead” male or just leave it 8. When males perform the death feigning technique, their success in reproduction all depends on the level of aggressiveness the female displays 8,21. Research has shown that in the Nephilengys livida species female aggressiveness state had no affect on the likelihood of her cannibalizing a potential mate. Male aggressiveness and male-male competition determined which male the female would cannibalize. Males with aggressive characteristics were favored and had more chance of mating with a female 17.


Mate choice – Females use mate choice to reject unwanted and unfit males by cannibalizing them and regulating the copulation time 5,22. Mate choice often correlates male size to their level of fitness; smaller males tend to be less aggressive and display low level of fitness, therefore smaller males are eaten more often because of their undesirable traits 5. Males perform elaborate courtship dances to display fitness and genetic advantage 23. Female orb-web spiders (Nephilengys livida) tend to cannibalize males displaying less aggressive behavior and mate with males that displaying more aggressive behavior, showing preference for this trait 17. Females favor large male body size and male aggression and would allow these males to copulate with them. Such characteristics display high male quality and genetic advantage 24,25.


Indirect mate choice can be witnessed in fishing spiders, Dolomedes fimbriatus, where females do not discriminate against smaller body size, attacking males of all sizes. Females had lower success rate cannibalizing large males because they managed to escape, where smaller males had less success escaping 4. It was shown that males with desirable traits (large body size, high aggression, and long courtship dances) would have longer copulation duration than males with undesirable traits 17,24. In A. keyserlingi and Nephila edulis females allow longer copulation duration and a second copulation for smaller males 26. The gravity hypothesis suggests that some species of spiders may favor smaller body sizes because it would enable them to climb up plants more efficiently and find a mate faster27. Also smaller males may be favored because they hatch and mature faster, giving them a direct advantage in finding and mating with a female 28. In Latrodectus revivensis females tend to limit copulation duration for small males and deny them of a second copulation, showing preference for larger body size 24. Another form of mate choice is the genetic bet-hedging hypothesis in which a female consumes males to prevent them from exploiting her 29. It is not beneficial for a female exploited by multiple males because it may result in prey theft, reduction in web, and reduced time of foraging 30. Sexual cannibalism might have promoted the evolution of some behavioral and morphological traits exhibited by spiders today 24.


Mistaken identity – Mistaken identity hypothesis suggests that sexual cannibalism occurs when females fail to identify males that try to court6. This hypothesis suggests that a cannibalistic female attacks and consumes the male without the knowledge of mate quality. In pre-copulatory sexual cannibalism, mistaken identity can be seen when a female does not allow the male to perform the courtship dance and engages in attack 13. There is no conclusive evidence for this hypothesis because scientists struggle to distinguish between mistaken identity and the other hypotheses (aggressive spillover, adaptive foraging, and mate choice) 2.

Male self-sacrifice

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In some cases, sexual cannibalism may characterize an extreme form of male monogamy, in which the male will sacrifice itself to the female. Males may gain reproductive success from being cannibalized by either providing nutrients to the female (indirectly to the offspring), or through enhancing the probability that their sperm will be used to fertilise the female's eggs.[13] Although sexual cannibalism is fairly common in spiders, male self-sacrifice has only been reported in six genera of araneoid spiders. In the most studied example, the Australian redback widow spider (Latrodectus hasselti, Theridiidae), males position their abdomen in front of the female's chelicerae in a somersault behaviour and are consumed during copulation; sexual cannibalism occurs in about 65% of matings. Relating to the adaptive self-sacrifice theory, cannibalised redback males double their paternity compared to rival males. This increase in fertilization rate is achieved by lengthening the time of copulation and decreasing the likelihood for female remating. the female starts cannibalizing the male during the sexual encounter, the distraction allows the mating period to be longer lasting. Andrade found that during pairings that resulted in the consumption of the male and a successful insemination, two thirds of the females rejected a second suitor, effectively increasing the male's paternity.[14] In addition, male orb-weaving spiders of the species Argiope aemula and Argiope aurantia, which are sexually cannibalistic, die immediately after mating, even if they are not attacked. Since they appear to expect no future mating success, they may have nothing to lose by being cannibalised, making the benefits of sexual cannibalism outweigh the costs.[15][16]

Reversed sexual cannibalism

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Reversed sexual cannibalism may transpire primarily in species in which males are larger than females. Male amphipods of the species Gammarus pulex and G. duebeni celticus may eat smaller females, especially at the moult, when they are most vulnerable. Likewise, female paddle crabs, Ovalipes catharus, are also defenseless at the moult when their shell is soft, and may be cannibalised during or after mating. In Gammarus species, sexual cannibalism would appear to be naturally opportunistic and not have any mate choice consequences.[17]

Evidence has also been found of a male eating a female in the mantid Tarachode afzeli.[18] Males of the water spider Argyronetia aquatica are larger than females, prefer to mate with larger females, and may cannibalise females that are smaller than themselves.[19] Females prefer to mate with larger males, but are more cautious of them; they flee from larger males more often than from males that are closer to their own size. The vulnerability to sexual cannibalism is a key in A. aquatica and would propose that an indirect mechanism, instead of direct mate choice, yields the size-dependent reversed sexual cannibalism that is observed. While the presence of the male-biased size dimorphism and the relative size of the female determining her vulnerability, smaller females are likely to be cannibalised. In all cases of reversed sexual cannibalism, there appears to be little hope that the female will produce viable offspring for the male, or the need for food exceeds the fitness gain that can be achieved through mating. Since most males will tend towards promiscuity in order to maximise their reproductive output, it is difficult to visualise mate choice through sexual cannibalism for males, unless the sex ratio is strongly female-biased, offering the males the opportunity to be selective or the sex roles are reversed.[17]

See also

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References

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  1. ^ Buskirk, R.E. et al. The Natural Selection of Sexual Cannibalism. The American naturalist 123, 612-625 (1984).
  2. ^ Aisenberg, A., Costa, F.G. & González, M. Male sexual cannibalism in a sand-dwelling wolf spider with sex role reversal. Biological Journal of the Linnean Society 68-75 (2011).
  3. ^ Blamires, S.J. Nutritional implications for sexual cannibalism in a sexually dimorphic orb web spider. Austral Ecology 36, 389-394 (2011).
  4. ^ Arnqvist, G. Courtship behaviour and sexual cannibalism in the semi-aquatic fishing spider, DOLOMEDES FIMBRIATUS (CLERCK) (ARANEAE: PISAURIDAE).pdf. The journal of Arachnology 20, 222-226 (1992).
  5. ^ Gatz, A.J. Non-random mating by size in American toad, Bufo americanus. Animal Behaviour 1004-1012 (1981).doi:10.1016/j.jat.2012.07.002
  6. ^ Gould, S. Only his wings remained. Natural History 93, 10-18 (1984).
  7. ^ a b Polis, G.A. The evolution and dynamics of intraspecific +4193 predation. Annual Reviews Ecological Systems 51, 225-251 (1981).
  8. ^ Bilde, T., Tuni, C., Elsayed, R., Pekár, S. & Toft, S. Death feigning in the face of sexual cannibalism. Biology letters 2, 23-5 (2006).
  9. ^ Polis, G.A. & Farley, R.D. BEHAVIOR AND ECOLOGY OF MATING IN TH E. The journal of Arachnology 33-46 (1979).
  10. ^ Wilder, S.M. & Rypstra, A.L. Sexual size dimorphism predicts the frequency of sexual cannibalism within and among species of spiders. The American naturalist 172, 431-40 (2008).
  11. ^ Barry, K.L., Holwell, G.I. & Herberstein, M.E. Female praying mantids use sexual cannibalism as a foraging strategy to increase fecundity. Behavioral Ecology 19, 710-715 (2008).
  12. ^ Andrade, M.C.B. Female hunger can explain variation in cannibalistic behavior despite male sacrifice in redback spiders. Behavioral Ecology 9, 33-42 (1988).
  13. ^ Michal Segoli, Ruthie Arieli, Petra Sierwald, Ally R. Harari & Yael Lubin (2008). "Sexual cannibalism in the brown widow spider (Latrodectus geometricus)". Ethology. 114 (3): 279–286. doi:10.1111/j.1439-0310.2007.01462.x.{{cite journal}}: CS1 maint: multiple names: authors list (link)
  14. ^ Maydianne C. B. Andrade (1996). "Sexual selection for male sacrifice in the Australian redback spider" (PDF). Science. 271 (5245): 70–72. Bibcode:1996Sci...271...70A. doi:10.1126/science.271.5245.70.
  15. ^ Matthias W. Foellmer & Daphne J. Fairbairn (2003). "Spontaneous male death during copulation in an orb-weaving spider". Proceedings of the Royal Society B. 270 (Suppl. 2): S183–S185. doi:10.1098/rsbl.2003.0042.
  16. ^ Takeshi Sasaki & Osamu Iwahashi (1995). "Sexual cannibalism in an orb-weaving spider Argiope aemula". Animal Behaviour. 49 (4): 1119–1121. doi:10.1006/anbe.1995.0140.
  17. ^ a b Cite error: The named reference Prenteretal2006 was invoked but never defined (see the help page).
  18. ^ M. Edmunds (1975). "Courtship, mating and possible sex pheromones in three species of Mantodea". Entomologist's Monthly Magazine. 111: 53–57.
  19. ^ Dolores Schütz & Michael Taborsky (2005). "Mate choice and sexual conflict in the size dimorphic water spider Argyroneta aquatica (Araneae: Argyronetidae)" (PDF). Journal of Arachnology. 33 (3): 767–775. doi:10.1636/S03-56.1.
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Category:Cannibalism Category:Carnivory Category:Mating