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The strange occurrence of male cannibalism on adult females in snakes
Abstract
Cannibalism is widespread in the animal kingdom. The most common, well‐known cases are found in some arthropod systems where the larger females occasionally consume the smaller males before, during, or after mating (i.e., sexual cannibalism). The killing and consumption of females by males are, on the other hand, seemingly much rarer and theoretically more difficult to explain, at least among adults, because the consumption of females would result in the loss of potential mates for males. Here, we use observations submitted to a community science reporting system to describe three instances of adult males feeding on adult females in the Montpellier snake, Malpolon monspessulanus, in the south of France. We discuss our observations in the theoretical framework of cannibalism to provide potential explanations for these observations and briefly review empirical findings of cannibalism in vertebrates, which confirms that this sex‐reversed form of sexual cannibalism is rare in nature.
... During sexual cannibalism, adult individuals, typically females (but see Glaudas & Fuento, 2022), consume potential or actual mating partners; the most well-known examples being among predatory invertebrates (Elgar, 1992). Sexual cannibalism is considered a form of sexual conflict and may provide fitness benefits for the participating sex but also for preyed upon sex dependent on the timing of consumption relative to copulation (Zuk, 2016). ...
... The frog prey has been swallowed from the rear up to the middle of the body. up a small proportion of their dietary intake in terms of frequency, which could result in low detectability and thus reporting of its occurrence in the wild (Glaudas & Fuento, 2022). Another possibility is that preying on and eating conspecific adults is much more difficult and less successful compared to exploiting earlier life stages that are smaller, which could reduce its occurrence and/or detection if escape is more common. ...
Active forms of cannibalism that involve predation of live conspecifics occur widely among amphibians, most notably by tadpoles that feed on each other and adults that feed on juveniles. In contrast, cannibalism among amphibian adults (adult–adult cannibalism) is less often reported and there have been no investigations on the occurrence of sexual cannibalism in this group to date. In this study, we present an observation of potential sexual cannibalism involving an adult female green and golden bell frog, Litoria aurea, preying on a conspecific adult male during the species' breeding season. By comparing our observation to the available literature, we show that adult–adult cannibalism among amphibians is rare but tends to be committed by females against their male counterparts. We thus suggest that the occurrence of sexual cannibalism should be extended to include this group, where sexual size dimorphism occurs widely among adults that congregate spatially during breeding periods, both predictors of intra‐specific predation. We hypothesise that amphibian females may be able to exploit male advertisement calls to differentiate suitable partners from potential prey and that male individuals are vulnerable to sexual cannibalism as they must risk attracting and physically exposing themselves to females in order to reproduce. Our findings reveal the complex dynamics that exist within adult amphibian populations, suggesting that females may have a choice when deciding how to interact with and utilise their male counterparts. As our findings are preliminary, based on a small sample size of records, including several from captive individuals, we encourage authors to publish their observations of cannibalism in the field, including unsuccessful attempts, to confirm the presence of sexual cannibalism in this group.
... At least in the case of the observation in France, it would seem to be a male attempting to eat a female. In European snakes, predation by males on adult females are known in other species such as the Montpellier snake Malpolon monspessulanus and the Aesculapian snake Zamenis longissimus (Glaudas & Fuento, 2022;Major et al., 2023 ...
Zdunek, P., Meier, G., Deso, G. 2023. Attempted cannibalism by adult smooth snakes Coronella austriaca in France and Switzerland. The Herpetological Bulletin 166: 27-28.
... In fact, the presence of reproductive females is usually a limiting factor in most reproductive systems and feeding on a female could be perceived as damaging to future mating opportunities. Glaudas and Fuento (2022) highlighted the rarity of this kind of male-on-female cannibalistic event and discussed the potential ecological and evolutionary reasons behind this phenomenon. They stated that even considering this behaviour as maladaptive, predation upon a conspecific female would still provide a male with significant energy intake, especially if the female is not seen as a potential mate at the time of predation. ...
The discovery of rare cases of males cannibalising females sheds new light on the selective forces behind sexual cannibalism in the animal kingdom.
It is incredibly challenging to study the natural feeding habits of snakes. Snakes are themselves secretive and rarely observed in the wild, and they feed relatively infrequently, making observations of feeding scarce. As a result, scientific understanding of snake dietary ecology (beyond simple prey lists) remains remarkably superficial outside of a few species. In this context, our own research sets out to understand how feeding and competition for spatially‐ and temporally‐patchy resources drives interspecific competition between two species of African snakes and how those processes might change in the future. This article is protected by copyright. All rights reserved.
Cannibalism is a relatively common trophic strategy among snakes (Polis and Myers, 1985). Many cases of cannibalism have been reported, but none of them represents a significant percentage of their diet. In the Iberian Peninsula, cases of cannibalism have been reported in Macroprotodon mauritanicus (Capellà et al., 2011), Vipera latastei (Martinez-Freiría et al., 2006), as well as in Malpolon monspessulanus (Valverde, 1967; Díaz-Paniagua, 1976; Pleguezuelos; 1998 and Recuero et al., 2010). Malpolon monspessulanus is considered an opportunistic euryphagous predator (Valverde, 1967; Pleguezuelos, 1998) whose diet composition is determined by prey availability during the anual activity period (Díaz-Paniagua, 1976; Corti et al., 2001). On 3 May 2010, we observed a roadkilled individual M. monspessulanus on an industrial area near the small village of Riudarenes, Spain (41.8107ºN, 2.7234ºE; WGS84). The specimen was sexed as a female with SVL= 1298 mm and total length= 1490 mm (Figure 1A and 1B). The snake had an open wound on the central area of body which revealed part of the stomach contents, as a result of roadkill. After emptying the stomach contents, it appeared a partially digested fragment of a colubrid snake (270 mm) (Figure 1C). This fragment was identified as part of a sub-adult of M. monspessulanus without possibility of sexing. Identification was based on color and number of dorsal scales rows and its longitudinal depression in the center. Iberian specimens invariably exhibit 19 rows in the center of the body (Pleguezuelos, 1997). The data presented here contributes to the improvement of knowledge about cannibalism in the species from a geographic area where information lacked on trophic strategy, and reports a female of exceptional large size, given that maximum size described in the Iberian Peninsula was SLV=988 mm (head and body length) (Feriche et al., 2008).
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.
Intraspecific killing has been reported among polar bears (Ursus maritimus), brown bears (U. arctos), and black bears (U. americanus). Although cannibalism is one motivation for such killings, the ecological factors mediating such events are poorly understood. Between 24 January and 10 April 2004, we confirmed three instances of intraspecific predation and cannibalism in the Beaufort Sea. One of these, the first of this type ever reported for polar bears, was a parturient female killed at her maternal den. The predating bear was hunting in a known maternal denning area and apparently discovered the den by scent. A second predation event involved an adult female and cub recently emerged from their den, and the third involved a yearling male. During 24years of research on polar bears in the southern Beaufort Sea region of northern Alaska and 34years in northwestern Canada, we have not seen other incidents of polar bears stalking, killing, and eating other polar bears. We hypothesize that nutritional stresses related to the longer ice-free seasons that have occurred in the Beaufort Sea in recent years may have led to the cannibalism incidents we observed in 2004.
Sexual cannibalism occurs in several arthropod taxa, but its evolutionary significance has long been debated. A new study shows how females that eat their mates benefit in ways that go well beyond caloric nutrition.
Here we document what we believe is an unusual incidence of leopard (Panthera pardus) cannibalism, where an adult male killed an adult female, presumably associated with a case of intraspecific food competition. Although the prey item, and adult impala (Aepyceros melampus) was a fairly large prey item we can not explain how this resource would have outweighed the value of a reproductively active female in the male's territory. No similar incidences could be found in the literature.
Numerous investigations, citing occurrences of cannibalism and/or oophagy in over 100 species of reptiles and amphibians, were reviewed with particular emphasis on predator/prey characteristics, environmental determinants, and evolutionary significance. In most species of reptiles cannibalism appears to occur opportunistically as a by-product of normal predatory behavior. Among amphibians, cannibalism is also opportunistic. However, many authors speculate that cannibalism implements particular strategies. In some cases, it is directly associated with specific behavioral, and even morphological characteristics. There is evidence that the development of cannibalistic morphotypes may be genetically and environmentally controlled.
The occurrence of cannibalism in mammals was studied during a general review of cannibalism (Polis, 1981). In total, there were 146 references documenting intraspecific predation in 75 species of mammals distributed between seven orders. Of these references, 138 refer to cannibalism whereas eight studies refer to intraspecific killing unaccompanied by cannibalism. Of the papers that specified the identity of both the predator and the prey, approximately 80% referred to infanticide (including cannibalism). It appears that infanticide often functions as part of a reproductive strategy. Juveniles and adults are occasional intraspecific prey for some species of Insectivora, Chiroptera, Primates, Lagomorpha, Rodentia, Carnivora, and Artio-dactyla. Cannibalism was best documented for the carnivores, rodents and primates. In general, cannibalism often occurs during normal predatory activities and is a function of low food availability, environmental stress, and a high density of conspecifics.
“Sexual cannibalism” refers to females killing and consuming their male partner at some stage during courtship and mating. Sexual cannibalism can occur before or during mating, which will determine potential explanations for its occurrence. This chapter discusses sexual cannibalism in the context of both sexual and natural selection. The natural history and taxonomic distribution of sexual cannibalism is discussed. Various explanations of sexual cannibalism are outlined, emphasizing how the timing of sexual cannibalism changes the costs and benefits to males and females. The evolutionary significance of sexual cannibalism depends on whether it occurs before or after insemination. Preinsemination sexual cannibalism is a nonadaptive consequence of selection on aggressive foraging in juvenile females. It is an adaptive component of female foraging, where females trade off foraging and mating requirements. It is a radical form of female mate choice. Sexual cannibalism could have evolved through the process of sexual, rather than, natural selection. It is evident that sexual cannibalism facilitates both female choice and cryptic female choice. Female foraging strategies that include sexual cannibalism are strongly opposed by counter selection on male mating success.
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