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Cannibalism of nonviable offspring by postparturient Mexican lance-headed rattlesnakes, Crotalus polystictus

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Abstract

Female vertebrates frequently ingest undeveloped ova and stillborn offspring. Two hypotheses have been proposed to interpret this behaviour: (1) it is a form of parental care, and (2) it recycles otherwise wasted energy, facilitating maternal recovery. Our study of Mexican lance-headed rattlesnakes provides the first quantitative description of cannibalism by postparturient rattlesnakes. We collected gravid females during June–July of 2004–2007 in central México, recording 239 litters from 190 females. Production of nonviable offspring was common (48% of litters). Most females (68%) ate some or all nonviable offspring, consuming an average of 11% of postpartum mass. Females consumed undeveloped ova and stillborn neonates in similar proportions. To evaluate factors that influenced the decision to cannibalize we used logistic regression. The best model included four predictive variables: (1) parturition date; (2) proportion of nonviable offspring mass per litter; (3) maternal investment index; and (4) snout–vent length (SVL). All variables exerted a positive effect on maternal cannibalism, although SVL was only a marginally significant predictor. Consumption of nonviable offspring confers energetic benefits to emaciated postparturient females. Energetic benefits are greatest when a large proportion of a litter is nonviable, while the pressure to cannibalize is greatest when late parturition shortens the time available to forage before the next reproductive event. Our results demonstrate the importance of maternal cannibalism in rattlesnakes, and suggest stronger support for the maternal recovery hypothesis than for the parental care hypothesis.

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... Lourdais et al., 2005;Göçmen, Werner & Elbeyli, 2008;Mociño-Deloya et al., 2009) which probably reflects both its rarity and the difficulty of observing snake behaviour in the field (Mitchell, 1986). The confined and unnatural conditions under which captive snakes are kept, and where the ability of potential conspecific prey to escape is restricted, may be a factor resulting in cannibalistic behaviour. ...
... It was not possible to determine whether the female C. austriaca that ate a conspecific new-born had killed and eaten another female's live offspring (predatory cannibalism), one of its own offspring (maternal predation), or if the juvenile was already dead when eaten (carrion cannibalism). Female snakes producing young in captivity frequently ingest their own undeveloped ova and stillborn offspring e.g. the Colombian rainbow boa, Epicrates cenchria maurus (Lourdais et al., 2005) and the Mexican lance-headed rattlesnake, Crotalus polistictus (Mociño-Deloya et al., 2009). In the wild a late parturition leaves snakes, that feed infrequently when gravid (Luiselli, Capula & Shine, 1996;Reading & Davis, 1996;Reading & Jofré, 2013) a shorter time to forage before the next hibernation or reproductive event and may increase the pressure towards cannibalism (Mociño-Deloya et al., 2009). ...
... Female snakes producing young in captivity frequently ingest their own undeveloped ova and stillborn offspring e.g. the Colombian rainbow boa, Epicrates cenchria maurus (Lourdais et al., 2005) and the Mexican lance-headed rattlesnake, Crotalus polistictus (Mociño-Deloya et al., 2009). In the wild a late parturition leaves snakes, that feed infrequently when gravid (Luiselli, Capula & Shine, 1996;Reading & Davis, 1996;Reading & Jofré, 2013) a shorter time to forage before the next hibernation or reproductive event and may increase the pressure towards cannibalism (Mociño-Deloya et al., 2009). ...
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Cannibalism is a widespread behavioural trait in nature and snakes are no exception. In smooth snakes (Coronella austriaca) it has only been visibly observed in captive individuals or known from faecal/stomach content analyses. Between 2009 and 2018 one incidence of cannibalism, determined from a faecal sample, and one sighting, were recorded in wild smooth snakes in Wareham Forest plantations, UK. Analysis of faecal samples and visual encounter surveys were used to estimate its frequency. Both records occurred in early autumn and our results suggest that its incidence in wild smooth snakes in southern England is low (0.1-0.3%) and may be the result of low body condition. The circumstances resulting in cannibalism in the smooth snake may also be relevant to other animal species where cannibalism has been reported.
... The consumption of one's own offspring has often been considered a maladaptive behaviour. However, this behaviour is both taxonomically widespread and in some species is a common phenomenon (Bartlett, 1987;Clutton-Brock et al., 2001;FitzGerald, 1992;Fowler & Hohmann, 2010;Manica, 2002b;Mociño-Deloya, Setser, Pleguezuelos, Kardon, & Lazcano, 2009;Smith & Reay, 1991;Tokuyama, Moore, Graham, Lokasola, & Furuichi, 2017). Cannibalism is common because (1) eggs/offspring are small and are often similar in size to prey items taken by adults and (2) eggs have high nutritive value and are typically deposited in a single spatial location in the vicinity of nonbreeding adults (Dominey & Blumer, 1984). ...
... Although in many species, males are cannibalistic (Lavery & Keenleyside, 1990;Schwanck, 1986), it remains unclear how common female cannibalism is. Termination of parental care via cannibalism by females has also been reported in other taxa: bonobo, Pan paniscus (Fowler & Hohmann, 2010), meerkat, Suricata suricatta (Culot et al., 2011), lance-headed rattlesnake, Crotalus polystictus (Mociño-Deloya et al., 2009) and European pied flycatcher, Ficedula hypoleuca (Moreno, 2012). Female filial cannibalism is often associated with increased environmental stress or Intercept is the individual identification for each experimental pair (random effect). ...
... reduced food provisioning (Culot et al., 2011;Mociño-Deloya et al., 2009). In N. caudopunctatus, females and males defend the young and maintain the nest together. ...
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Although the consumption of one's own offspring is often viewed as maladaptive, under some circumstances this behaviour can be a beneficial way to terminate parental care. When the costs of providing care are extremely high or the benefits of performing care are especially low, parents will sometimes cannibalize their own young, which is called filial cannibalism. This behaviour enables them to cease to care while recouping lost energy. Most studies examining the link between the cost/benefit ratio of care and filial cannibalism have focused on species with male-only care. In contrast, filial cannibalism in biparental caring species has been studied only rarely. To increase our understanding of filial cannibalism in biparental species and examine the transition from cannibal to caring parent, we conducted four experiments with Neolamprologus caudopunctatus, a biparental cichlid fish from Lake Tanganyika, Africa. First, in experiment 1 we show that the establishment of a pair bond and nest construction did not inhibit cannibalism of foreign eggs. Second, in experiment 2 we removed eggs from parents for various durations and showed that the act of spawning and the presence of the parents' own brood nearly always maintained care and inhibited cannibalism. Third, parents did not discriminate between their own and foreign broods of eggs or hatched young when supplied with complete or with half-cross-fostered young (experiments 3 and 4). Atypically, across all experiments cannibalism was mostly performed by the female. Taken together, our results trace the behavioural transition from egg consumer to egg carer in this biparental species and expand our understanding of cannibalism to biparental species.
... A total of 161 (71 males, 90 females) T. scaliger and four T. scalaris were captured. Snakes were anaesthetized in the laboratory (within 20 km far from any of the study areas) with an approximate dosage of 0.8 ml/l of isoflurane as described by MOCIÑO-DELOYA et al. (2009), to obtain reliable biometric and pholidotic measurements (SETSER, 2007). Individuals were marked with a PIT tag (TX148511B model, 8.5 x 2.1 mm, 0.1 g, 134.2 kHz, Destron-Fearing, St. Paul, Minnesota, USA) as described by MOCIÑO-DELOYA et al. (2009) before release in order to avoid replication of data. ...
... Snakes were anaesthetized in the laboratory (within 20 km far from any of the study areas) with an approximate dosage of 0.8 ml/l of isoflurane as described by MOCIÑO-DELOYA et al. (2009), to obtain reliable biometric and pholidotic measurements (SETSER, 2007). Individuals were marked with a PIT tag (TX148511B model, 8.5 x 2.1 mm, 0.1 g, 134.2 kHz, Destron-Fearing, St. Paul, Minnesota, USA) as described by MOCIÑO-DELOYA et al. (2009) before release in order to avoid replication of data. Males and non-gravid females were released within one to four days after capture, whilst gravid females were kept in the laboratory until parturition (between one and two weeks). ...
... Male snakes generally have longer tails than females (SHINE et al., 1999) because of the need to accommodate the hemipenes at the base of the tail (KING, 1989). Because of this sexual dimorphism in tail length, males also have a higher number of subcaudal scales than females and, accordingly, 94.2% (90.6-98.5%, ...
... Crotalus polystictus has a fragmented distribution throughout the southern Mexican Plateau where it occurs primarily in mid-to high-elevation grasslands and meadows (Campbell & Lamar, 2004). Recent studies of its reproductive ecology (Mociño-Deloya et al., 2009;Setser et al., 2010) have made C. polystictus among the most thoroughly studied of Mexican rattlesnakes; nevertheless, most aspects of its biology remain poorly known. Crotalus polystictus provides a unique opportunity for investigating the evolution and sexual dimorphism of head morphology because it is distinctive among rattlesnakes in having a narrow head (Klauber, 1938). ...
... Snakes used for GM analysis of head morphology were collected during June and July 2006 as part of a long-term, mark-recapture study of C. polystictus life history and ecology (Mociño-Deloya et al., 2009;Setser et al., 2010). The field site consisted of a mosaic of pasture, fallow fields, and cropland along the Rio Lerma, State of México, Mexico. ...
... After capture, snakes were transported to a nearby facility for processing and data collection before release at the site of capture. Within 6 h of capture, we anaesthetized individual snakes using isofluorane gas (Setser, 2007;Mociño-Deloya et al., 2009). As part of a series of data-collection procedures, we photographed the dorsal head aspect of anaesthetized subadult and adult snakes. ...
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Sexual dimorphism of phenotypic traits associated with resource use is common in animals, and may result from niche divergence between sexes. Snakes have become widely used in studies of the ecological basis of sexual dimorphism because they are gape‐limited predators and their head morphology is likely to be a direct indicator of the size and shape of prey consumed. We examined sexual dimorphism of body size and head morphology, as well as sexual differences in diet, in a population of Mexican lance‐headed rattlesnakes, Crotalus polystictus, from the State of México, Mexico. The maximum snout–vent length of males was greater than that of females by 21%. Males had relatively larger heads, and differed from females in head shape after removing the effects of head size. In addition, male rattlesnakes showed positive allometry in head shape: head width was amplified, whereas snout length was truncated with increased head size. By contrast, our data did not provide clear evidence of allometry in head shape of females. Adults of both males and females ate predominately mice and voles; however, males also consumed a greater proportion of larger mammalian species, and fewer small prey species. The differences in diet correspond with dimorphism in head morphology, and provide evidence of intersexual niche divergence in the study population. However, because the sexes overlapped greatly in diet, we hypothesize that diet and head dimorphisms in C. polystictus are likely related to different selection pressures in each sex arising from pre‐existing body size differences rather than from character displacement for reducing intersexual competition. © 2012 The Linnean Society of London, Biological Journal of the Linnean Society, 2012, 106, 633–640.
... Once encountered, snakes were gently captured with snake tongs, transported to a processing facility, anesthetized with isoflurane, measured from snout to vent (snout-vent length, SVL) to within 1 mm (Setser, 2007), sexed and weighed to within 0.1 g. All snakes were permanently marked with a PIT tag (c. 12 mm in length and 0.1 g in weight; Moci˜no-Deloya et al., 2009). We palpated anesthetized female snakes to determine whether gravid, and to check for the presence of food boli. ...
... We did not offer captive females food, but provided water ad lib. Gestating females held captive for longer periods were occasionally reweighed to assess changes in weight (typically due to hydration levels and defecation events; see Moci˜no-Deloya et al., 2009). In all cases, we used the mass most recently recorded before parturition in the analyses. ...
... We calculated total litter mass as the sum of all viable and non-viable offspring masses, and live litter mass as the sum of all viable offspring masses. Fourteen post-parturient females consumed some non-viable offspring before being weighed (Moci˜no-Deloya et al., 2009). In order to calculate litter masses, post-parturient masses and characteristics derived from litter and post-parturient masses for these females, we added or subtracted the summed mean masses of the appropriate number of full-term stillborn neonates (7.8 g) and/or undeveloped ova (4.3 g) to and from measured masses. ...
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Our understanding of snake biology is heavily biased towards species and populations occurring at higher latitudes. In particular, little information is available concerning the biology of the numerous species of Mexican rattlesnakes. We studied the reproductive ecology of female Mexican lance-headed rattlesnakes Crotalus polystictus in a montane (c. 2500 m a.s.l.) valley of the Rio Lerma, in the Mexican state of México. We collected data from 162 different females and 203 litters over 4 years (2004–2007). Parturition coincided with summer monsoon rains, with the majority of females giving birth in late June and early July. Larger females and females gestating larger litters typically gave birth earlier in the summer than did smaller females and females gestating smaller litters. Some females matured rapidly; 26 females reproduced as 3-year olds, 17 as 2-year olds and a single female reproduced at 1 year of age. Females commonly reproduced in consecutive years. Litter size and mean neonate size increased with maternal body length; however, the relative clutch mass did not vary with female size. The mean litter size was 7.3 neonates (range 3–15), and the mean neonate body length (snout–vent length) and mass were 198 mm and 8.7 g. Neonate size varied less than did other litter characteristics. Rapid maturity, frequent reproduction and synchronization of parturition with seasonal precipitation are consistent with previously observed patterns of snake reproduction at lower latitudes.
... On the other hand, a lot of cannibalism happens in captivity, either between neonates or between parents and their young, possibly influenced by the environmental stress to which captive snakes are subjected (Cardoso-Junior et al., 1990;Braz et al., 2006;Maia and Travaglia-Cardoso, 2017). Although cannibalism in snakes sometimes occurs between adult individuals (e.g., Capella et al., 2011), mothers are well known to ingest their non-viable eggs or neonates (Mitchell and Groves, 1993), and maternal cannibalism may be a beneficial strategy to obtain energy after the period of high reproductive demand (Lourdais et al., 2005;Mociño-Deloya et al., 2009). ...
... The event reported herein included a female P. nattereri much larger than the minimum reproductive size reported for the species (Mesquita et al., 2011) and a small juvenile (Passos et al., 2014). Likely explanations include that a larger individual simply fed on a smaller conspecific (following the general trend noted by Polis, 1981), or that this event constitutes maternal cannibalism (see Lourdais et al., 2005;Mociño-Deloya et al., 2009). However, since the relatedness of the involved individuals is unknown, it is not possible to determine the actual scenario. ...
... Maternal cannibalism involves the consumption of offspring by the female parent and can be further categorized as either the consumption of non-viable offspring (eggs, undeveloped ova or stillborn neonates) or of living offspring (Mocino-Deloya et al., 2009). Maternal cannibalism has been described from a number of animal species, including numerous reptiles (Huff, 1980;Polis and Myers, 1985;Kevles, 1986;Somma, 1989;Somma, 2003;Mitchell and Groves, 1993;Lourdais et al., 2005). ...
... Lourdais et al. (2005) suggested that the maternal cannibalism in Epicrates cenchria maurus of Boidae family is used to recycle wasted energy and reduce the time required for recovery from pregnancy. Mocino-Deloya et al. (2009) found that importance of maternal cannibalism in rattlesnakes, and suggest stronger support for the maternal recovery hypothesis than for the parental care hypothesis. ...
... Here, we describe formal evidence of cannibalism in the Chilean endemic P. chamissonis, with adult specimens preying on an adult (Case 1) and juvenile (Case 2) conspecific individual. Beyond the ophiophagous snakes, cannibalism can occur in females that ingest their non-viable offspring and undeveloped eggs (Lourdais et al., 2005;Mociño-Deloya et al., 2009), between neonates and juveniles (Mienis, 1986;Egler et al. 1996;Campbell and Lamar, 2004), and during opportunistic predation by adult individuals. ...
... There are two broad categories of cannibalism: filial cannibalism (consumption of close genetic relatives) and heterocannibalism (consumption of unrelated conspecifics) (Thomas & Manica, 2003;Ibáñez & Keyl, 2010). As examples of filial cannibalism, Colombian rainbow boas (Epicrates maurus) and emaciated postparturient Mexican lance-headed rattlesnakes (Crotalus polystictus) consume undeveloped eggs and non-viable offspring as a behavioural tactic to recoup energy losses (Lourdais et al., 2005;Mociño-Deloya et al., 2009). Examples of heterocannibalism are numerous, both for captive and wild snakes: Mitchell (1986) reviewed reports of cannibalism for 101 species of snakes from 1894 to 1985. ...
Article
Cannibalism is a common behaviour among snakes, but it has not yet been verified for any of the nine species of Galápagos racer (Pseudalsophis spp.), a group endemic to the Galápagos archipelago, Ecuador. Galápagos racers are opportunistic generalists feeding on a variety of vertebrate prey. There are a few anecdotal and suspected attempts of cannibalism among Galápagos racers, but it is unclear whether this behaviour occurs and if so, how frequent it is. We analysed 61 faecal samples from western Galápagos racers (Pseudalsophis occidentalis). In addition to the remains of well known prey items such as lizards, we found snake teeth and skin fragments in 11 samples. Combined with previous observations of attempted cannibalism between western Galápagos racers, our results represent evidence that this species consumes other racers as prey. Our study contributes to a growing knowledge of the natural history of Galápagos racers and highlights the role of these reptiles in complex trophic interactions in the Galápagos islands.
... Accounts from the herpetocultural community have noted that mother cordylids will consume stillborn offspring and undeveloped ova (J. Reissig, unpublished data), which aligns with published accounts from other squamates (Lourdais et al., 2005;Mocino-Deloya et al., 2009;Caldwell et al., 2018). This observation is notable since the juvenile consumed appeared alive prior to the attack, making this account more akin to what we describe about filial cannibalism in K. polyzonus. ...
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The family Cordylidae consists of 70 species of subSaharan lizard (Uetz et al., 2020) that reside across much of Africa (Reissig, 2014), from Ethiopia to South Africa (latitudinally) and Angola to Ethiopia (longitudinally). Here, we present observations of cannibalism by four species of cordylid lizard, two from free-living wild populations and another two from captive settings. Since the natural history of many cordylid species remains deficient, and several species have been observed to display reasonably high degrees of sociality, like group-living in Armadillo Lizards, Ouroborus cataphractus (Boie, 1828) (Mouton, 2011) and Sungazers, Smaug giganteus (Smith, 1844) (Parusnath, 2020), these observations provide important insights into one of the potential mechanisms shaping cordylid ecology and sociality.
... Cannibalism in reptiles occurs mostly in opportunistic foragers (Polis and Myers 1985). In snakes, besides the ophiophagous snakes, cannibalism has been documented in females that ingest their non-viable offspring and undeveloped eggs (Lourdais et al. 2005;Mociño-Deloya et al. 2009), between neonates and juveniles (Mienis 1986;Egler et al. 1996;Campbell and Lamar 2004) and in some adult individuals such as Anilius scytale, Eunectes murinus, Helicops infrataeniatus and Siphlophis compressus (Rivas and Owens 2000;Aguiar and Di-Bernardo 2004;Maschio et al. 2005;Alemu and Rowley 2008). ...
Article
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Cannibalism has been documented across many groups of snakes and the same is true for Brazilian snakes. Herein, we present the first observation of cannibalism in Thamnodynastes phoenix between two adult males from Caatinga biome of northeastern Brazil. We suggest this behavior could be influenced by a lack of resources caused by extreme abiotic conditions, as well as the opportunistic habits of this species.
... After the mother had carried the dead infant for one day, the carcass was consumed by several community members, including its mother. Maternal cannibalism, whereby a mother consumes its own offspring, occurs in various animal species, ranging from insect to mammals (e.g., Bartlett 1987;Elwood 1991;Mociño-Deloya et al. 2009). It is rare in primates, and has been attributed to high maternal stress levels (Tartabini 1991;Culot et al. 2011), or is suggested to be an aberrant behavior (Dellatore et al. 2009). ...
Article
This paper reports on the bonobos eating their newborns, a behaviour previously reportée in Lui Kotale.
... Crotalus polystictus is a medium sized viperid endemic to central Mexico (Mociño-Deloya et al., 2009;Setser et al., 2010). Individuals are commonly between 50 and 60 cm in total length, but some large individuals can reach 80 cm. ...
Article
Hertz et al. (1993) designed what is now the most widely used protocol to analyse the thermal strategies and efficiency of small squamates. Preferred temperature range (Tp) is one of the most important variables required for determining the thermal efficiency index, and is calculated by monitoring the body temperature of the individuals in an enclosure containing a thermal gradient. Although thermoregulation studies of lizards have traditionally employed thermal gradients under laboratory conditions, this approach is not suitable for snakes given that such thermal gradients do not accurately represent their natural thermal environment and thus may result in snakes selecting suboptimal temperatures. Here, we compare the results of this thermal efficiency protocol using a laboratory thermal gradient (LG) and a semi-captivity thermal gradient (SCG) in the rattlesnake Crotalus polystictus. We found traces of seasonal variation in the SCG Tp, but this could not be assessed in the LG. Tp from the LG was much higher (29 – 34.3 °C) than from the SCG (22.5-30.9 °C). Values for the accuracy of thermoregulation (db) and thermal quality of the environment (de) indices from the LG were consistently higher than from the SCG. However, the efficiency of thermoregulation (E) was higher when calculated from the SCG. Tp estimates were wider than most that have been obtained from other snake species, suggesting that C. polystictus is eurythermic. The Blowin Demers and Weatherhead index was nearly identical in both gradients. Results from the LG indicated that C. polystictus is an inaccurate and inefficient thermoregulator, due to the higher temperatures chosen in this environment. In contrast, results from the SCG suggested that it is a highly accurate and active thermoregulator. We suggest that the LG could represent a stressful environment for snakes, and, as a consequence, they might select higher temperatures to increase anti-predatory performance at the expense of less efficient thermoregulation. Generally, a thermal gradient that more accurately replicates the natural habitat of snake species should reduce stress and result in more robust estimates of thermoregulatory variables.
... We must also prevent the introduction or substitution of species and pursue reforestation practices that do not involve roller chopping or agricultural burning (Mullin and Seigel 2009). Although some Crotalus species are quite tolerant or can even be beneficial to the small patches of crops, probably due to the small preys that live there (Bastos et al. 2005;Mociño-Deloya et al. 2009;Reinert et al. 2011;Wittenberg 2012;Mociño-Deloya et al. 2014), only the crops close to Abies-Pinus forests seems to be suitable habitats for C. triseriatus (Mociño-Deloya et al. 2014). Therefore, it is important to preserve the Abies-Pinus forest for several reasons, one of them is the possibility that the rattlesnakes could find a different kind of food (e.g. ...
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The isolated and fragmented populations are highly susceptible to stochastic events, increasing the extinction risk because of the decline in putative adaptive potential and individual fitness. The population has high heterozygosity values and a moderate allelic diversity, the heterozygosity values are higher than in most other Crotalus species and snake studies. Possibly these high levels of genetic diversity can be related to a large founder size, high effective population size, multiple paternity and overlapping generations. We did not find the genetic structuring but the effective number of alleles (𝑁e) was 138.1. We found evidence of bottlenecks and the majority of rattlesnakes were unrelated, despite the small sample size, endemic status, the isolated and fragmented habitat. The genetic information provided in this study can be useful as a first approach to try to make informed conservation efforts for this species and also, important to preserve the habitat of this species; the endangered Abies–Pinus forest of the Nevado the Toluca Volcano.
... However, to date, little is known of the venom ontogeny patterns among Mexican rattlesnake species. A long-term ecological study of the Mexican Lance-headed Rattlesnake (Crotalus polystictus) in Estado de México [33][34][35] afforded the opportunity to obtain venom samples from neonate, juvenile, and adult rattlesnakes. This medium-sized species averages 600-700 mm in length and occupies native and modified grasslands in central México, and is a mid-elevation species, occurring from approximately 1450-2600 m ( [4]; Figure 1). ...
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As trophic adaptations, rattlesnake venoms can vary in composition depending on several intrinsic and extrinsic factors. Ontogenetic changes in venom composition have been documented for numerous species, but little is known of the potential age-related changes in many rattlesnake species found in México. In the current study, venom samples collected from adult and neonate Crotalus polystictus from Estado de México were subjected to enzymatic and electrophoretic analyses, toxicity assays (LD50), and MALDI-TOF mass spectrometry, and a pooled sample of adult venom was analyzed by shotgun proteomics. Electrophoretic profiles of adult males and females were quite similar, and only minor sex-based variation was noted. However, distinct differences were observed between venoms from adult females and their neonate offspring. Several prominent bands, including P-I and P-III snake venom metalloproteinases (SVMPs) and disintegrins (confirmed by MS/MS) were present in adult venoms and absent/greatly reduced in neonate venoms. Age-dependent differences in SVMP, kallikrein-like, phospholipase A₂ (PLA₂), and L-amino acid oxidase (LAAO) activity levels were confirmed by enzymatic activity assays, and like many other rattlesnake species, venoms from adult snakes have higher SVMP activity than neonate venoms. Conversely, PLA₂ activity was approximately 2.5 × greater in venoms from neonates, likely contributing to the increased toxicity (neonate venom LD50 = 4.5 μg/g) towards non-Swiss albino mice when compared to adult venoms (LD50 = 5.5 μg/g). Thrombin-like (TLE) and phosphodiesterase activities did not vary significantly with age. A significant effect of sex (between adult male and adult female venoms) was also observed for SVMP, TLE, and LAAO activities. Analysis of pooled adult venom by LC-MS/MS identified 14 toxin protein families, dominated by bradykinin-inhibitory peptides, SVMPs (P-I, P-II and P-III), disintegrins, PLA₂s, C-type-lectins, CRiSPs, serine proteinases, and LAAOs (96% of total venom proteins). Neonate and adult C. polystictus in this population consume almost exclusively mammals, suggesting that age-based differences in composition are related to physical differences in prey (e.g., surface-to-volume ratio differences) rather than taxonomic differences between prey. Venoms from adult C. polystictus fit a Type I pattern (high SVMP activity, lower toxicity), which is characteristic of many larger-bodied rattlesnakes of North America.
... Tucker et al. 1998), and enhance nutrition in females that have recently given birth (e.g. Lourdais et al. 2005;Mociño-Deloya et al. 2009), cannibalism in Jackson's chameleons may simply be a hardwired adaptation driven by a selective force for indiscriminate optimization of nutrition for both males and females, rather than serving a sociobiological purpose. ...
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Various aspects of social structure can be important drivers of basic behavioral patterns, including dispersal, intraspecific niche partitioning, and resource utilization. Juvenile–adult interactions such as agonistic displays and paedophagic cannibalism can result in avoidance of adults by juveniles, and can influence community structure via shifts in ontogenetic habitat use patterns and juvenile dispersal. In this study, we examined the role of agonistic behavior in determining differences in habitat utilization between life stages in an ecologically damaging invasive lizard, Trioceros jacksonii xantholophus, in the Hawaiian Islands. We tested the hypothesis that intraspecific aggression by adults drives observed niche separation and juvenile dispersal. In the laboratory, we conducted paired conspecific trials to assess paedophagic behavior, and staged contests to assess aggression and response: 57% of adults consumed newborns when paired. In addition, juveniles fled further, faster, and more often in response to aggressive adult displays than from other juveniles. To assess the effect of antagonistic behaviors on juvenile movement and its potential role in and habitat shifts, we used radio-telemetry and exploited diet comparison to assess resource use in juveniles versus adults. Though our results suggested no significant difference in immature versus adult chameleon dispersal, juveniles were found to perch at significantly lower heights above ground, and exploited different prey types than did adults. These results suggest that resource partitioning is occurring, but the immature chameleons are sedentary as are the adults. Due to age-dependent habitat usage, our results suggest that T. j. xantholophus occupies a broader niche than previously recognized. These results highlight the importance of studies focused on patterns of behavior at different developmental stages of invasive species, which ultimately provide better information allowing prediction of ecological impacts and range expansion potential.
... Although lacking primary literature, these reports represent detailed observations from trained herpetologists and in many cases have been confirmed by subsequent studies (e.g., refs. [47][48][49] ) and were therefore retained. ...
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Identifying factors responsible for the emergence and evolution of social complexity is an outstanding challenge in evolutionary biology. Here we report results from a phylogenetic comparative analysis of over 1000 species of squamate reptile, nearly 100 of which exhibit facultative forms of group living, including prolonged parent-offspring associations. We show that the evolution of social groupings among adults and juveniles is overwhelmingly preceded by the evolution of live birth across multiple independent origins of both traits. Furthermore, the results suggest that live bearing has facilitated the emergence of social groups that remain stable across years, similar to forms of sociality observed in other vertebrates. These results suggest that live bearing has been a fundamentally important precursor in the evolutionary origins of group living in the squamates.
... Cannibalism of young by parental individuals is prevalent across a range of taxa, including teleost fishes (Hrdy 1979;Manica 2002;Mociño-Deloya et al. 2009;Culot et al. 2011;Pereira et al. 2017). Filial cannibalism or the consumption of one's own offspring has several inherent costs, such as a reduction in fitness (Smith and Reay 1991). ...
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Adult animals of many species often behave in a cannibalistic manner when encountering conspecific offspring. Kin discrimination is critical for avoiding the consumption of one’s own offspring or filial cannibalism. Some fishes cannibalize embryos when other nutritional sources are unavailable. We tested the hypotheses that (1) adult mangrove rivulus, Kryptolebias marmoratus, cannibalize conspecific offspring; (2) cannibalism of unrelated conspecifics is more prevalent than filial cannibalism and (3) the drive to cannibalize embryos is associated with nutritional status (‘energy-based hypothesis’). We examined cannibalistic behaviours of the self-fertilizing amphibious K. marmoratus in the laboratory using two isogenic strains. Adults recognized kinship of single embryos, cannibalizing unrelated embryos (28% of the time) but not their own. The ability to recognize kin differed between isogenic strains. Thus, genetic differences significantly influenced behaviour. Fasting had no significant effect on cannibalistic behaviours and thus nutritional state is not an important factor driving cannibalism in this species under these conditions. This is the first documented evidence that a fish species can recognize the kinship of an individual embryo. Significance statement Across the animal world, there are many examples of animals that eat their own offspring (filial cannibalism), but the outcome of such behaviour may be reproductively costly. Other animals may consume offspring belonging to other parents (non-kin cannibalism). The trick is to recognize the difference between your own versus someone else’s offspring to optimize reproductive success. Previous studies on fish have shown that parents can assess the relative ratio of kin to non-kin embryos in an entire nest, but the ability to recognize single embryos has not been demonstrated. We have shown that when a self-fertilizing mangrove fish was presented with a single embryo, it never ate its own but consumed unrelated embryos, suggesting that they have the ability to recognize solo relatives at very early stages of development.
... After the mother had carried the dead infant for one day, the carcass was consumed by several community members, including its mother. Maternal cannibalism, whereby a mother consumes its own offspring, occurs in various animal species, ranging from insect to mammals (e.g., Bartlett 1987;Elwood 1991;Mociño-Deloya et al. 2009). It is rare in primates, and has been attributed to high maternal stress levels (Tartabini 1991;Culot et al. 2011), or is suggested to be an aberrant behavior (Dellatore et al. 2009). ...
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Maternal cannibalism, whereby a mother consumes her own offspring, occurs in various animal taxa and is commonly explained by nutritional stress or environmental pressures. It is rare in nonhuman primates and is considered an aberrant behavior only observed under high-stress conditions. It was therefore surprising when, in the first reported case of cannibalism in wild bonobos, a mother consumed part of the dead infant at LuiKotale. Here we report two more cases of maternal cannibalism by wild bonobos at two different study sites, Wamba and Kokolopori. The dead infants’ mothers participated in the cannibalism in both cases. At Kokolopori, although the mother did consume part of the carcass, it was held and shared by another dominant female. At Wamba, the mother was a dominant female within the community and was the primary consumer of the carcass. In both cases, cannibalism resembled other meat-eating events, with the dominant female controlling meat consumption. Infanticide was not observed in either case, but its occurrence could not be ruled out. Although rare, the occurrence of maternal cannibalism at three different study sites suggests that this may represent part of the behavioral repertoire of bonobos, rather than an aberrant behavior.
... However, previous dietary studies have shown that G. caesaris is mainly herbivorous (consuming leaves and seeds), a general trend in island lizards (Cooper and Vitt, 2002;Pérez-Mellado and Corti, 1993), secondarily consuming insects (beetles, ants, and flies), vertebrates being minor prey, with no record of predation on conspecifics (Barahona, 1998;Martin et al., 2005). Yet, the presence of conspecifics in prey remains is frequently found at a low rate, because cannibalism tends to be constrained to the largest individuals (Polis, 1988), to only one sex (e.g., females; Mociño-Deloya et al., 2009), or to short periods of the year (Fox, 1975). Large sample sizes spanning all periods of the activity cycle of the organism are hence required to detect such usually hidden behavior (Engeman et al., 1996). ...
Article
Cannibalism is not rare among animals, and particularly in reptiles it is favored by a strong ontogenetic shift in body size and generalized carnivore habits. We looked for evidence of this behavior in a medium-sized lizard, endemic of oceanic islands (Canary Islands), with a high prevalence of a parasite transmitted by cannibalism. Conspecific predation appeared in this lizard, with a rather low incidence (0.76% of fecal pellets included conspecifics), although the analysis of a very large sample (n = 11,651 pellets) indicated ontogenetic, sexual, and seasonal patterns of such predation. Only the largest individuals were cannibal, invariably males, which only depredated immature individuals, almost exclusively during the post-hatching period (summer and autumn). Together with other natural-history traits already known for the species (e.g., high density, low breeding output, large offspring), cannibalism adds further evidence that this lizard fits the island syndrome.
... It is a wireless sensor technology, based on the detection of electromagnetic signals emitted by a tag. It can be used to detect tags through a variety of habitats, e.g., a layer of soil (Mociño-Deloya et al. 2009). This method allows tracking organisms regularly in time and with limited disturbance of their behaviour, keeping the individual information of movements. ...
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The PhD work aims at detecting and understanding factors and mechanisms explaining the spatial heterogeneity of banana black weevils' (Cosmopolites sordidus) populations in order to control them. Two approaches are commonly considered to understand the spatial heterogeneity of populations: statistics applied to spatial data and mechanistic modelling. My PhD work considers the interest of combining those approaches to understand the movement processes of insect adults and the interaction between life traits and spatial dynamics of a population. Understanding movement processes requires collecting spatial data at the individual level. By combining a statistical approach by maximum likelihood estimation and a mechanistic individual-based model, I showed a high dependence of movement versus habitat matrix. I showed also that perception of space is less important for a weevil located on a banana plant or on crop residues than for a weevil located on bare soil or ditch. An individual-based model (COSMOS) was developed to simulate the spatial dispersion and infestation of C. sordidus in interaction with different elements of the cropping system. The model was successfully tested at the plot scale, by comparing infestation statistics between observed and simulated values. The emerging properties of the model were tested by simulating different spatial arrangements of banana plants. For instance, the model showed that the time to colonize a plot is longer when the plot is planted regularly than when it is planted in patches. The model revealed the importance of the interface between banana area and fallow for locating weevils' trap.
... Ambush-foraging species in particular may not suffer detrimental effects of viviparity on either predation or foraging success (Schuett et al., 2013). Viviparous reptiles can also cannibalize non-viable offspring to quickly recoup energy after reproduction (Lourdais et al., 2005;Mocino-Deloya et al., 2009;Van Dyke et al., 2014b). Finally, even oviparous species face effects of locomotor impairment throughout the active season due to factors other than reproduction, including cool temperatures, large meals, and tail autotomy (Shine, 2003). ...
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To understand evolutionary transformations it is necessary to identify the character states of extinct ancestors. Ancestral character state reconstruction is inherently difficult because it requires an accurate phylogeny, character state data, and a statistical model of transition rates and is fundamentally constrained by missing data such as extinct taxa. We argue that model based ancestral character state reconstruction should be used to generate hypotheses but should not be considered an analytical endpoint. Using the evolution of viviparity and reversals to oviparity in squamates as a case study, we show how anatomical, physiological, and ecological data can be used to evaluate hypotheses about evolutionary transitions. The evolution of squamate viviparity requires changes to the timing of reproductive events and the successive loss of features responsible for building an eggshell. A reversal to oviparity requires that those lost traits re-evolve. We argue that the re-evolution of oviparity is inherently more difficult than the reverse. We outline how the inviability of intermediate phenotypes might present physiological barriers to reversals from viviparity to oviparity. Finally, we show that ecological data supports an oviparous ancestral state for squamates and multiple transitions to viviparity. In summary, we conclude that the first squamates were oviparous, that frequent transitions to viviparity have occurred, and that reversals to oviparity in viviparous lineages either have not occurred or are exceedingly rare. As this evidence supports conclusions that differ from previous ancestral state reconstructions, our paper highlights the importance of incorporating biological evidence to evaluate model-generated hypotheses. J. Exp. Zool. (Mol. Dev. Evol.) 00B: 1-11, 2015. © 2015 Wiley Periodicals, Inc. © 2015 Wiley Periodicals, Inc.
... Another case of cannibalism is oophagy (Elgar & Crespi 1992). Consumption of eggs by females is common in reptiles (Huang 2008;Mociño-Deloya et al. 2009). Female P. gaigeae might eat eggs of conspecifics, but we have no direct evidence that they do. ...
Article
Island populations may evolve distinct behavioral repertoires as a response to the conditions of insular life. Strong intraspecific competition is typical in insular lizards and may include cannibalism. In this study, we investigated sexual and age patterns of aggression in two populations of the Skyros wall lizard (Podarcis gaigeae), one from the main island of Skyros (Aegean Sea, Greece) and another from the satellite islet Diavates. The latter is terrestrial predator-free biotope, hosting a dense population of large-bodied lizards that have been reported to exert cannibalism. In staged encounters, we examined the aggressive propensities of adult male and female lizards against their age-peers and juveniles. Males from both populations were much more aggressive than females toward juveniles and other adults. Males from Diavates were more frequently aggressive to juveniles and other male lizards than males from Skyros. Diavates cannibals also captured their targets at shorter latency. We ascribe this distinct behavioral pattern to the high population density. Infanticide and intramale aggressiveness confer two great advantages to cannibals: food and elimination of future rivals.
... The cannibalism is a reported phenomenon for snakes of the families Colubridae, Elapidae and Viperidae (Polis and Myers 1985, Engeman et al. 1996, Krysko 2002, Martínez et al. 2006, Mociño-Deloya et al. 2008, Capellà et al. 2010. It is considered a relatively common trophic behavior among snakes, which is important in the ecology of many species (Polis and Myers 1985). ...
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This note describes the observation of a specimen of the colubrid snake Liophis lineatus that swallowed a co-specific individual after trying to obtain the same frog prey (Leptodactylus sp.). The serpentes were seen among construction debris in a farm near the town of La Fría , in Táchira state, Venezuela, in august 2008. Although there is little information on the natural history of Liophis lineatus, the reported predator behavior of this species suggests this is a case of accidental cannibalism. RESUMEN: M. Escalona. "Canibalismo de Liophis lineatus (Linnaeus)(Serpentes: Colubridae) en condiciones naturales". En esta nota reportamos la observación de un evento de canibalismo en el colúbrido Liophis lineatus, luego de que dos serpientes de esta especie intentaran alimentarse de la misma presa de rana (Leptodactylus sp.). Las serpientes fueron observadas entre escombros en una finca cerca del pueblo La Fría, en el estado Táchira, Venezuela, en agosto de 2008. Aunque se conoce poco sobre la historia natural de Liophis lineatus, el comportamiento depredador reportado para esta especie sugiere que este es un caso de canibalismo accidental.
... Animals were anaesthetized during measurement to improve precision using an approximate dosage of 0.8 mL of isoflurane per litre of the container (Setser 2007). Most adult snakes were permanently marked with passive integrated transponders (PIT; model TX148511B, 8.5 mm × 2.1 mm dimensions, 0.1 g mass, 134.2 kHz emis-sion frequency; detailed procedures in Mociño-Deloya et al. 2009b). We determined sex by inspecting tail width near the vent or by evaginating hemipenes. ...
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Optimal diet theory predicts that predators optimize energy intake by balancing costs and benefits of foraging. One extreme strategy of snake foraging ecology is shown by specialist species that forage on low-energy prey, such as Thamnophis scaliger (Jan, 1863) which feeds almost exclusively on earthworms. Compared with other prey types such as small mammals, lizards, or arthropods, earthworms are low-energy prey because of their small size and high water content. Given the importance of energy acquisition for fueling snake reproduction, we expect that a low-energy dietary specialist such as T. scaliger needs to forage frequently to store enough fat to reproduce. The high frequency of snakes containing prey, the presence of multiple earthworms in snakes, and the fact that females continue to feed when gravid suggest that T. scaliger is a voracious consumer of earthworms. Despite these foraging behaviours, females did not reproduce in sequential years, suggesting constraints in energy input to reproduce more frequently. A meta-analysis of the diet, body size, and reproductive frequency of some species of the genus Thamnophis Fitzinger, 1843 confirms that consumption of invertebrate prey is associated with small snake size, but not with biennial reproductive frequency within the genus.
... It is a wireless sensor technology, based on the detection of electromagnetic signals emitted by a tag. It can be used to detect tags through a variety of habitats, for example a layer of soil (Mociño-Deloya et al. 2009). This method allows researchers to track organisms regularly in time and with limited disturbance of their behaviour, keeping the individual information of movements. ...
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The study of movements of individual organisms in heterogeneous environments is of primary importance for understanding the effect of habitat composition on population patterns. We developed a new experimental methodology to measure individual movements of walking insects, based on radiotracking. Our aims were to understand the link between habitat heterogeneity and moving patterns, and to characterize the movements with dynamic models of diffusion. We tracked individual movements of adults of Cosmopolites sordidus (Coleoptera: Curculionidae) with passive radio frequency identification (RFID) tags under different field management practices. Diffusion models based on recapture data indicated a subdiffusive movement of this species. Substantial variation was found between individual paths, but this variation was not sex dependent. Movement of released C. sordidus was affected by banana planting pattern and the presence/absence of crop residues but not by the presence of a cover crop between rows of bananas or by banana variety. These results show that the RFID technology is useful for evaluating the dispersal parameters of cryptic insects in heterogeneous environments.
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CONTRIBUTIONS TO THE KNOWLEDGE OF THE DIET OF Cerrophidion petlalcalensis (Marco Antonio López Luna, Richard C. Vogt, Miguel Ángel De la Torre Loranca, 1999) ) (VIPERIDAE). Abstract.— Novel data about the consumption of reptiles as a part of the diet of Cerrophidion petlalcalensis is provided. Keywords.— Feeding, Montane pitviper, Natural history, Petlalcala montane pitviper, Viper. Resumen.— Se aportan datos novedosos acerca del consumo de reptiles como parte de la dieta de Cerrophidion petlalcalensis. Palabras clave.— Alimentación, Historia natural, Nauyaca de frío, Nauyaca del cerro Petlalcala, Vipérido.
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Crotalus polystictus es Una serpiente de cascabel endémica de México. Se considera bajo protección especial de acuerdo a la NOM-059-2010-SEMARNAT. Crotalus polystictus fue registrada por primera vez en el área Natural protegida Sierra de Quila, Jalisco. Este registro se encuentra a por lo mneos 31 km al noroeste del punto más cercano de su distribución conocida.
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Crotalus polystictus is a Mexican endemic rattlesnake. It is considered under special protection status according to NOM-059-2010-SEMARNAT. Crotalus polystictus was recorded for the first time, along with its ecological distribution within the natural protected area Sierra de Quila, Jalisco. This record is at least 31 km northwest from its closest known geographic distribution.
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Crotalus polystictus is a Mexican endemic rattlesnake. It is considered under special protection status according to NOM-059- 2010-SEMARNAT. Crotalus polystictus was recorded for the first time, along with its ecological distribution within the natural protected area Sierra de Quila, Jalisco. This record is at least 31 km northwest from its closest known geographic distribution.
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L'objectif de cette thèse est d'identifier et de comprendre les processus liant un ravageur à son habitat afin de limiter la population de ce ravageur. Deux approches peuvent permettre d'étudier l'hétérogénéité spatiale des populations d'une espèce: les statistiques appliquées à des données spatialisées et la modélisation mécaniste. Mon travail de thèse montre l'intérêt de combiner ces deux approches afin de comprendre l'interaction entre traits de vie et dynamique spatiale d'une population. Comprendre les comportements de dispersion nécessite de collecter des données spatiales à l'échelle de l'individu. En combinant une approche statistique par maximum de vraisemblance et un modèle mécaniste sur des données spatialisées que j'ai récoltées sur l'insecte par télémétrie RFID (Radio Frequency IDentification), j'ai montré une forte dépendance du déplacement vis-à-vis des éléments du paysage. Un modèle stochastique individu-centré (COSMOS) a été développé afin de simuler la propagation spatiale et les attaques du charançon en interaction avec les différents éléments du système de culture. Le modèle a été confronté avec succès à des données d'infestation réelles à l'échelle d'une parcelle de bananiers, en comparant les données d'infestation observées aux données simulées. Les propriétés émergentes du modèle ont été explorées en simulant des assemblages spatiaux de bananiers. Par exemple, le modèle a montré que la vitesse de colonisation d'une parcelle est plus importante lorsqu'elle est plantée de manière régulière plutôt qu'en groupes de bananiers. Le modèle a révélé l'importance de la zone de transition entre la bananeraie et la jachère pour l'optimisation du piégeage.
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This study reports results of a 14-month live-trap study of small-rodent communities in 2 habitats, cloud forest and disturbed areas, at Las Joyas Scientific Station of the Sierra de Manantlán Biosphere Reserve, western Mexico. Seven taxa of 2 families (Muridae, Het-eromyidae) of small rodents were captured (Hodomys alleni, Liomys pictus, Oryzomys couesi, Peromyscus aztecus, Reithrodontomys fulvescens, R. sumichrasti, and Sigmodon alleni). Information about age structure, population dynamics, biomass, and reproduction were obtained with mark–recapture techniques for the most abundant species (P. aztecus and R. fulvescens) in both habitats. These species comprised 80.3% of the 707 captures in the cloud forest (P. aztecus, 51.2%; R. fulvescens, 29.1%), whereas, in the disturbed areas, R. fulvescens represented 81.7% of the 916 captures. Species varied in population density, relative abundance, and timing of reproduction, which was seasonal. Reproductive activity for P. aztecus peaked in the middle of the wet season (September 1995) in the cloud forest and in the wet season and middle of the dry-cold season (January 1996) in the disturbed areas. R. fulvescens showed reproductive activity in the wet season (July–October 1995) in both habitats. Density fluctuated annually for P. aztecus in both habitats, with a peak in January and February 1996; R. fulvescens showed the same patterns of density in both habitats with the highest values at the end of the wet season.
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The aim of this chapter is to encourage additional studies of prey size-snake size relations. The fascinating evolutionary vistas sketched by Green (1983), Mushinsky (1987), Pough and Groves (1983), and Voris and Voris (1983) have not been explored as assiduously as they might. In this chapter I focus on one tantalizing result from the recent literature on snake diets in the hope of encouraging more work. The result is that in many of the snake species studied so far, larger snakes drop small prey items out of their diet. The implication is that snakes pass over, perhaps even avoid, some of the smallest prey items they encounter. Foraging theory is used to devise some hypotheses to explain this apparently enigmatic result. In trying to use foraging theory to this end, I was constantly plagued by the lack of relevant data. However, the lack of data is undoubtedly a reflection of our failure to adapt theory to snake biology. Perhaps even a provisional application of theory to the problem will help break the logjam.
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Foraging behaviour is influenced by an animal's level of hunger, and may reflect a trade-off between optimizing food acquisition and avoiding predation. Young tiger snakes were raised either on a high or low food diet and exposed to a predation threat while foraging. Under these circumstances, lower condition snakes (low food diet) were prone to take additional feeding/foraging risks: food was accepted at a much higher rate compared with the higher condition animals (high food diet) that were less inclined to risk feeding under a predation threat. This study provides the first direct example of predation risk-associated foraging decisions in snakes.
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In August and September of 1991 we observed three groups of neonatal prairie rattlesnakes (Crotalus viridis viridis) near a prairie dog town in the Sand Hills (Cherry County, Nebraska). One of these groups included at least 31 neonates and 2 postpartum females. In addition to spatio-temporal association of neonates and putative mothers, we observed a radio-tagged male prairie rattlesnake consecutively visit two natal sites, just before and just after parturition. Mean mass of neonates in two groups was below the range previously reported for this subspecies. Young-of-the-year (YOY) captured during ingress were longer and weighed more than neonates captured at birth. Feces collected from nine YOY captured at hibernacula contained pocket mouse (Perognathus spp.) remains. In contrast to other intensively studied populations, most YOY in the Sand Hills appear to feed and grow before first hibernation.
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Eleven years of data on a small population of adders (Vipera berus) in southern Sweden provide quantitative information on the nature and degree of costs faced by reproducing animals. Reproduction imposes both an energy cost (measured by loss in body mass) and a mortality cost on adders of both sexes. The extent of the energy cost is broadly independent of levels of reproductive activity in males, but mortality costs are highest for large males, perhaps because they are more obvious to predators. In females, energy costs include a high ‘fixed’ (fecundity-independent) component, such that a large litter may cost little more to produce than would a small litter. Energy costs and mortality costs are separate in males, but inter-related in females. Mortality of reproducing females is high (40% per year), primarily because post-parturient females are emaciated and must forage actively, hence increasing their vulnerability to predators. Females producing relatively large litters (high Relative Clutch Mass) lose more body mass, and are less likely to survive after reproducing. The observed low reproductive frequencies of female adders may result from the presence of high fecundity-independent costs of reproduction.
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Before we can quantify the degree to which reproductive activities constitute a cost (i.e., depress an organism's probable future reproductive output), we need to determine the timescale over which such costs are paid. This is straightforward for species that acquire and expend resources simultaneously (income breeders), but more problematical for organisms that gather resources over a long period and then expend them in a brief reproductive phase (capital breeders). Most snakes are capital breeders; for example, female aspic vipers (Vipera aspis) in central western France exhibit a 2- to 3-year reproductive cycle, with females amassing energy reserves for one or more years prior to the year in which they become pregnant. We use long-term mark-recapture data on free-living vipers to quantify the appropriate timescale for studies of reproductive costs. Annual survival rates of female vipers varied significantly during their cycle, such that estimates of survival costs based only on years when the females were ‘reproductive’ (i.e., produced offspring) substantially underestimated the true costs of reproduction. High mortality in the year after reproducing was apparently linked to reproductive output; low energy reserves (poor body condition) after parturition were associated with low survival rates in the following year. Thus, measures of cost need to consider the timescale over which resources are gathered as well as that over which they are expended in reproductive activities. Also, the timescale of measurement needs to continue long enough into the post-reproductive period to detect delayed effects of reproductive ‘decisions’.
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In many species the high energetic demands of reproduction induce a negative energy balance, and thus females must rely on tissue catabolism to complete the reproductive process. Previous works have shown that both fat and protein are energy resources during prolonged fasting in vertebrates. While many ecological studies on energy costs of reproduction have focused on variations in fat stores, the impact of protein investment on the female has not been thoroughly investigated. Notably, as there is no specialized storage form for proteins, intense catabolism is likely to entail structural (musculature) loss that may compromise maternal physical performance after reproduction. Measurements on captive rainbow boas ( Epicrates cenchria maurus) confirm that reproducing females undergo significant protein catabolism (as indicated by elevated plasma uric acid levels) and show considerable musculature loss during gestation (as detected by reduced width of the epaxial muscles). Protein mobilization entailed a significant functional loss that was illustrated by decrements in tests of strength and constriction after parturition. In wild situations, such effects are likely to decrease the snakes' ability to forage and apprehend prey. Hence, the time period needed to recover from reproduction can be extended not only because the female must compensate losses of both fat stores and functional muscle, but also because the ability to do so may be compromised. Performance alteration is likely to be of equal or greater importance than reduced energy stores in the physiological mediation of elevated post-reproduction mortality rates and infrequent reproductive bouts (e.g. biannual or triannual), two common ecological traits of female snakes.
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Snakes are often regarded as the least social of all vertebrate groups, but this assumption stems from the fact that they are secretive and difficult to observe in nature, rather than direct evidence. Recent studies have revealed a surprising degree of social complexity in snakes. Here, I examine the ability of captive-raised timber rattlesnakes (Crotalus horridus) to recognize siblings by measuring the mean separation distance and frequency of contact between pairs of individuals housed together. The results show that female siblings associate more closely with each other than nonsibling pairs. Previous studies have shown that timber rattlesnakes occupying the same hibernacula have higher relatedness than snakes using neighbouring hibernacula, and frequently form social aggregations. Rattlesnakes exhibit other characteristics consistent with advanced sociality, including group defence, conspecific alarm signals and maternal defence of young. These findings reinforce the notion that, rather than being solitary and asocial, some snake species may form family groups.
Book
1. Introduction 2. Estimation 3. Hypothesis testing 4. Graphical exploration of data 5. Correlation and regression 6. Multiple regression and correlation 7. Design and power analysis 8. Comparing groups or treatments - analysis of variance 9. Multifactor analysis of variance 10. Randomized blocks and simple repeated measures: unreplicated two-factor designs 11. Split plot and repeated measures designs: partly nested anovas 12. Analysis of covariance 13. Generalized linear models and logistic regression 14. Analyzing frequencies 15. Introduction to multivariate analyses 16. Multivariate analysis of variance and discriminant analysis 17. Principal components and correspondence analysis 18. Multidimensional scaling and cluster analysis 19. Presentation of results.
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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.
Article
Summary 1. The ways that fluctuations in prey abundance and weather conditions can affect reproductive output in a 'capital breeding' ectotherm, the aspic viper (Vipera aspis) were examined. 2. Our longitudinal study confirms that female aspic vipers adjust reproductive invest- ment by integrating allocations of energy from stores ('capital') and facultative feeding ('income'). Thus, long-term energy storage enabled females to reproduce successfully even in years when prey were scarce. 3. Not surprisingly, temporal changes in body reserves of female vipers preparing for reproduction depended upon current feeding rates. However, the mean environmental temperature during the active season also affected mass gain. 4. Allometric patterns suggest that reproductive output was limited by energy avail- ability in 8 out of the 9 years of our study. In the other year, high prey availability in the preceding season meant that reproductive output was maximized within the constraints set by maternal body size (and thus, abdominal volume). 5. High summer temperatures increased basking opportunities of gravid vipers and thus accelerated gestation. However, maternal metabolic costs also increased in such situations, resulting in low postpartum body condition.
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Climatic conditions during embryonic development can exert profound and long-term effects on many types of organisms, but most previous research on this topic has focussed on endothermic vertebrates (birds and mammals). Although viviparity in ectothermic taxa allows the reproducing female to buffer ambient thermal variation for her developing offspring, even an actively thermoregulating female may be unable to provide optimal incubation regimes in severe weather conditions. We examined the extent to which fluctuations in natural thermal conditions during pregnancy affect reproduction in a temperate viviparous snake, the aspic viper (Vipera aspis). Data gathered from a long term field study demonstrated that ambient thermal conditions influenced (1) female body temperatures and (2) gestation length, embryo viability, and offspring phenotypes. Interestingly, thermal conditions during each of the three months of gestation affected different aspects of reproduction. Hotter weather early in gestation (June) increased ventral scale counts (=number of body segments) of neonates; hotter weather mid-gestation (July) hastened development and thus the date of parturition; and hotter weather late in gestation (August) reduced the incidence of stillborn neonates. The population that we studied is close to the northern limit of the species’ range, and embryonic thermal requirements may prevent Vipera aspis from extending into cooler conditions further north.
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In many animal species, mothers that produce stillborn offspring or undeveloped ova immediately ingest them. This cannibalism has been interpreted in two ways: (1) as a form of parental care (to prevent disease spreading to healthy littermates, and eliminate predator-attracting scent cues); or (2) to recycle otherwise wasted energy, thus facilitating maternal recovery. Our experimental study on captive Colombian rainbow boas (Epicrates cenchria maurus) provides the first quantitative support for this latter hypothesis. We show that by eating their non-viable offspring and undeveloped eggs, female boas can rapidly recycle a significant component of their otherwise wasted reproductive investment. Female boas that ingested non-viable progeny equivalent to half their litter mass exhibited rapid recovery of dorsal musculature and hence were able to constrict prey items more forcefully than were unfed females when tested 2 weeks after parturition. The consequent enhancement of constricting ability may influence maternal survival and foraging success. Thus, maternal cannibalism may be an effective tactic to avoid wasting reproductive resources, and to shorten the period required for recovery from pregnancy. © 2005 The Linnean Society of London, Biological Journal of the Linnean Society, 2005, 84, 767–774.
Article
Cannibalism is uncommon in most species despite being taxonomically widespread. This rarity is surprising, because cannibalism can confer important nutritional and competitive advantages to the cannibal. A general, but untested, explanation for why cannibalism is rare is that cannibals may be especially likely to acquire pathogens from conspecifics, owing to greater genetic similarity among conspecifics and selection for host specificity and resistance to host immune defences among pathogens. We tested this hypothesis by contrasting the fitness consequences of intra- versus interspecific predation of diseased and non-diseased prey. We fed cannibalistic tiger salamander (Ambystoma tigrinum) larvae diseased conspecifics, healthy conspecifics, diseased heterospecifics (a sympatric congener, small-mouthed salamanders, A. texanum), or healthy heterospecifics. Cannibals that ate diseased conspecifics were significantly less likely to survive to metamorphosis and grew significantly less than those that ate diseased heterospecifics, but none of the other groups differed. Tiger salamander larvae also preferentially preyed on heterospecifics when given a choice between healthy conspecifics and heterospecifics. These results suggest that pathogen transmission is an important cost of cannibalism and provide a general explanation for why cannibalism is infrequent in most species. Copyright 1998 The Association for the Study of Animal Behaviour Copyright 1998 The Association for the Study of Animal Behaviour.
Article
Spontaneous anorexia has been documented in various animal species and is usually associated with activities competing with food intake. In natural conditions, most female aspic vipers (Vipera aspis) stop feeding during the two months of pregnancy. We carried out a simple experiment on 40 pregnant females to determine whether anorexia was obligatory or facultative, and to investigate the energetic consequence of fasting on post-partum body condition and litter traits. Three diet treatments were applied during gestation: no food, one feeding occasion, and two feeding occasions. Twelve nonpregnant, unfed females were used as a control group. Most gravid females accepted captive mice during gestation, suggesting that anorexia reported in the field was a side effect of the tremendous changes in activity pattern associated with pregnancy. Mass loss was high for unfed reproductive females, indicating high energy expenditure associated with embryo maintenance. Prey consumption allowed compensation for metabolic expenditure and enhanced post-partum female body condition, but had no effects on litter characteristics. The magnitude of the metabolic expenditure during gestation appeared to be independent of fecundity.
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