Early experience shapes the development of behavioral repertoires of hatchling snakes

Snakes are obligate predatory organisms that consume prey whole, and despite their precocious nature, snakes must develop effective feeding skills, especially when encountering large prey. I conducted two experiments that document the development of behavioral repertoires for naïve hatchling trinket snakes, Coleognathus helena. In the first experiment, I examined how experience with prey of different relative prey mass encountered at regular feeding intervals affects hatchling feeding response. I also examined whether hatchling feeding performance improved over time. Improvement was evaluated on the frequency of the most effective behavioral states such as complex prey restraint behaviors and anterior-first ingestion. In the second experiment I tested whether feeding experience with prey of a particular size influences the way hatchlings respond to a novel prey size. All hatchlings improved their predatory behavior when prey size and number of trials were controlled. Hatchlings feeding on larger prey, however, showed greater overall improvement in their feeding behavior and were quick to integrate complex prey restraint behaviors such as constriction into their feeding repertoire. Despite the fact that early experience with one prey size seemed to shape their restraint repertoire during their first four feeding events, hatchlings remained flexible and responded to prey of a novel size with size-specific prey restraint behaviors.     

Rhesus Macaques (Macaca mulatta) Use Posture to Assess Level of Threat From Snakes

Once prey animals have detected predators, they must make decisions about how to respond based on a cost‐benefit analysis of their risk level. The threat sensitivity hypothesis predicts that prey animals match their response to the level of risk, with high‐risk predator encounters eliciting stronger evasive responses than low‐risk encounters. Primates are known prey of snakes, yet they vary their responses toward snakes. We predicted that primates match their response to the threat level from snakes by assessing posture, with striking postures indicating greater risk than coiled postures and coiled postures indicating greater risk than extended sinusoidal postures. We tested this prediction in a series of experimental trials in which captive rhesus macaques (Macaca mulatta) were exposed to snake models in those postures. Results supported the predictions: macaques responded more strongly to a snake model in a striking posture than in a coiled posture and more to a snake model in a coiled posture than to an extended sinusoidal snake model. We also examined responses of macaques to a partially exposed snake model to mimic the condition of incomplete information, as snakes are often occluded by vegetation. The occluded snake model evoked a response comparable to that of the striking snake. These findings support the threat sensitivity hypothesis. Rhesus macaques use the posture of snakes as a cue in threat assessment, responding more intensely as threat increases, and they also behave as if risk is elevated when their information about snakes is incomplete.     

Predation experiments on infant spectral tarsiers (Tarsius spectrum)

In this paper, I investigate how mother and infant spectral tarsiers, Tarsius spectrum, respond to the presence of potential predators. I conducted this study at Tangkoko Nature Reserve in Sulawesi, Indonesia, from June to November 1999. I exposed 2 infants to 3 types of potential predators (large models of birds of prey, large rubber snakes and the vocalizations of large birds of prey) for a total of 18 nights. Infants moved a greater distance from their parked location when exposed to rubber snakes (1.8 m) compared to nights when they were not exposed to potential predators (0.23 m). On the other hand, when large bird of prey models were placed near the parked infant, the infant did not move from its parked locale (0.05 m). Parked infants repeatedly gave alarm calls in response to the presentation of all potential predator types. When an infant produced an alarm call following the presentation of a potential predator, the mother responded with her own alarm call approximately 88% of the time. However, when an infant produced an inappropriate alarm call, the mother responded with her own alarm call only 19% of the time. These results suggest that spectral tarsier infants use alarm calls to ask questions about the things they encounter in their environment. Infants and mothers both produced a twittering alarm call in response to the bird of prey models, whereas they both produced a harsh loud call 3 times in rapid succession in response to the presence of the rubber snakes.     

How snakes eat snakes: the biomechanical challenges of ophiophagy for the California kingsnake, Lampropeltis getula californiae (Serpentes: Colubridae)

In this study we investigated how ophiophagous snakes are able to ingest prey snakes that equal or exceed their own length. We used X-ray video, standard video, dissection, and still X-rays to document the process of ophiophagy in kingsnakes (Lampropeltis getula) feeding on corn snakes (Elaphe guttata). Most kingsnakes readily accepted the prey snakes, subdued them by constriction, and swallowed them head first. In agreement with previous observations of ophiophagy, we found that the predator snake forces the vertebral column of the prey snake to bend into waves. These waves shorten the prey's body axis and allow it to fit inside the gastrointestinal (GI) tract and body cavity of the predator. Dissection of a kingsnake immediately following ingestion revealed extensive longitudinal stretching of the anterior portion of the GI tract (oesophagus and stomach), and no visible incursion of the prey into the intestine. X-ray video of ingestion showed that the primary mechanism of prey transport was the pterygoid walk, with some contribution from concertina-like compression and extension cycles of the predator's vertebral column in two out of three observations. Complete digestion was observed in only one individual, as others regurgitated before digestion was finished. X-ray stills taken every 4 days following ingestion revealed that the corn snakes were about half digested within the first 4 days, and digestion was complete within 15 days.     

Predictors of orbital convergence in primates: a test of the snake detection hypothesis of primate evolution

Traditional explanations for the evolution of high orbital convergence and stereoscopic vision in primates have focused on how stereopsis might have aided early primates in foraging or locomoting in an arboreal environment. It has recently been suggested that predation risk by constricting snakes was the selective force that favored the evolution of orbital convergence in early primates, and that later exposure to venomous snakes favored further degrees of convergence in anthropoid primates. Our study tests this snake detection hypothesis (SDH) by examining whether orbital convergence among extant primates is indeed associated with the shared evolutionary history with snakes or the risk that snakes pose for a given species. We predicted that orbital convergence would be higher in species that: 1) have a longer history of sympatry with venomous snakes, 2) are likely to encounter snakes more frequently, 3) are less able to detect or deter snakes due to group size effects, and 4) are more likely to be preyed upon by snakes. Results based on phylogenetically independent contrasts do not support the SDH. Orbital convergence shows no relationship to the shared history with venomous snakes, likelihood of encountering snakes, or group size. Moreover, those species less likely to be targeted as prey by snakes show significantly higher values of orbital convergence. Although an improved ability to detect camouflaged snakes, along with other cryptic stimuli, is likely a consequence of increased orbital convergence, this was unlikely to have been the primary selective force favoring the evolution of stereoscopic vision in primates.     

Feeding behavior and venom toxicity of coral snake Micrurus nigrocinctus (Serpentes: Elapidae) on its natural prey in captivity

The feeding behavior and venom toxicity of the coral snake Micrurus nigrocinctus (Serpentes: Elapidae) on its natural prey in captivity were investigated. Coral snakes searched for their prey (the colubrid snake Geophis godmani) in the cages. Once their preys were located, coral snakes stroke them with a rapid forward movement, biting predominantly in the anterior region of the body. In order to assess the role of venom in prey restraint and ingestion, a group of coral snakes was 'milked' in order to drastically reduce the venom content in their glands. Significant differences were observed between snakes with venom, i.e., 'nonmilked' snakes, and 'milked' snakes regarding their behavior after the bite. The former remained hold to the prey until paralysis was achieved, whereas the latter, in the absence of paralysis, moved their head towards the head of the prey and bit the skull to achieve prey immobilization by mechanical means. There were no significant differences in the time of ingestion between these two groups of coral snakes. Susceptibility to the lethal effect of coral snake venom greatly differed in four colubrid species; G. godmani showed the highest susceptibility, followed by Geophis brachycephalus, whereas Ninia psephota and Ninia maculata were highly resistant to this venom. In addition, the blood serum of N. maculata, but not that of G. brachycephalus, prolonged the time of death of mice injected with 2 LD(50)s of M. nigrocinctus venom, when venom and blood serum were incubated before testing. Subcutaneous injection of coral snake venom in G. godmani induced neurotoxicity and myotoxicity, without causing hemorrhage and without affecting heart and lungs. It is concluded that (a) M. nigrocinctus venom plays a role in prey immobilization, (b) venom induces neurotoxic and myotoxic effects in colubrid snakes which comprise part of their natural prey, and (c) some colubrid snakes of the genus Ninia present a conspicuous resistance to the toxic action of M. nigrocinctus venom.     

Phylogenetic correlation between male–male fighting and mode of prey subjugation in snakes

Male–male fighting (MMF) in snakes is a sexually dimorphic trait in adults that is expressed during breeding periods and confers reproductive advantages to winners. This trait, however, is not ubiquitous among the approximately 2,700 species of extant snakes, and past research shows evidence of taxonomic trends. We evaluated the phylogenetic distribution of MMF in extant snakes using two previously published estimates of snake evolutionary history. We clearly identified multiple independent gains and losses of MMF in snakes and phylogenetically important taxa for which information on MMF is lacking. We followed this with two tests of the association of MMF with mode of prey capture using the concentrated-changes test (CCT) of Maddison (1990), and a third test using the subtree decomposition method of Read and Nee (1995). In the CCT analyses, first we tested whether MMF was randomly distributed with respect to mode of prey subjugation in snake lineages. This hypothesis was rejected, with MMF being significantly more concentrated in taxa that subjugate prey by constriction and/or envenomation. Second, we tested a more temporally exact hypothesis: whether changes in state of MMF were randomly distributed with respect to occurrences of state changes in mode of prey subjugation. Results of this test depended on the exact test parameters used. In general, however, this hypothesis also was rejected, suggesting that loss of constriction and/or envenomation typically results in loss of MMF, or vice versa. Last, the subtree decomposition test indicated a significant correlation between evolution of MMF and evolution of constriction and/or envenomation as the primary mode of prey subjugation. We propose that the relationship between these states is not causal but results from both characters being independent adaptations to energy resource scarcity. Received in revised form: 20 March 2001 Electronic Publication     

How removal of cats and rats from an island allowed a native predator to threaten a native bird

The question of how to program the removal of two invasive mammals, typically cats and rats, from a marine island without increasing risk to native prey species has received two general answers based on ecological theory: removal of cats must be accompanied by control of their mesopredator prey, and risk is minimized by removing both invaders simultaneously. Nonetheless, a 31-year study showed that in a 82-ha tropical marine bird sanctuary, predation on a native prey, the blue-footed booby, by a native predator, the Atlantic Central American milk snake, apparently diminished after removal of cats then increased 11-fold after the additional removal of black rats. These novel effects are explained in terms of a hypothetical three-link trophic web in which cat removal released rats to increasingly compete with or prey on the snakes that feed on hatchling boobies, and subsequent rat removal released snakes from all remaining predation. The upshot is a disturbing scenario in which approximately 200 milk snakes currently aggregate annually in roughly 1 hectare of booby colony and predate roughly forty percent of the hatchlings. Where the lowest link of an insular trophic web is a native mesopredator that feeds on native prey, the predictions of the classic mesopredator release scenario can be inverted, and removal of invasive mammals may endanger native prey species.

     

Energetic and physiological correlates of prey handling and ingestion in lizards and snakes

In this review, we summarize the energetic and physiological correlates of prey handling and ingestion in lizards and snakes. There were marked differences in the magnitude of aerobic metabolism during prey handling and ingestion between these two groups, although they show a similar pattern of variation as a function of relative prey mass. For lizards, the magnitude of aerobic metabolism during prey handling and ingestion also varied as a function of morphological specializations for a particular habitat, prey type, and behavior. For snakes, interspecific differences in aerobic metabolism during prey handling seem to be correlated with adaptations for prey capture (venom injection vs. constriction). During ingestion by snakes, differences in aerobic metabolism might be due to differences in cranial morphology, although allometric effects might be a potentially confounded effect. Anaerobic metabolism is used for prey handling and ingestion, but its relative contribution to total ATP production seems to be more pronounced in snakes than in lizards. The energetic costs of prey handling and ingestion are trivial for both groups and cannot be used to predict patterns of prey-size selection. For lizards, it seems that morphological and ecological factors set the constraints on prey handling and ingestion. For snakes, besides these two factors, the capacity of the cardio-respiratory system may also be an important factor constraining the capacity for prey handling and ingestion.     

Feeding preferences in 2 disjunct populations of tiger snakes, Notechis scutatus (Elapidae)

Variations at both the genetic and phenotypic levels play animportant role in responses to food and food-related stimuli.Knowledge of such variations is crucial to understanding howpopulations adapt to changing environments. We investigatedthe dietary preferences of 2 tiger snake populations and comparedthe responses of diet-naive animals (laboratory-born neonates),diet-controlled animals (laboratory-reared juveniles), and naturaldiet–experienced animals (wild-caught adults) to visualand chemical cues from 6 prey types (mouse, skink, silver gull,chicken, shearwater, and frog). The mainland population inhabitsa swamp, feeds mostly on frogs, and suffers heavy predation.The second population inhabits a small nearby offshore islandwith no standing water (no frogs); feeds mostly on skinks, mice,and, as adults, silver gull chicks; and suffers no known predation.Although different prey are eaten in the 2 populations, adultwild-caught snakes from both populations showed a significantpreference for 3 types of prey (frog, mouse, and chick), irrespectiveof their natural diet. Neonates responded to all prey cues morethan they did to control stimuli in both populations. However,the island neonates showed significantly higher interest insilver gull chick stimuli (the main prey of the island adultsnakes) than did their mainland conspecifics. Laboratory-bredjuveniles displayed behavioral plasticity by significantly increasingtheir response to mice after being fed baby mice for 7 months.We conclude that genetic-based differences in food-related cuesare important in tiger snakes but that they are also capableof behavioral plasticity. Island adult and neonate snakes exhibitedresponses to prey types no longer consumed naturally (frog),suggesting that behavioral characters may have been retainedfor long periods under relaxed selection. Island neonates showeda strong interest in a novel prey item (silver gull). This resultcomplements previous work describing how island snakes havedeveloped the ability to swallow larger prey than usual, aswell as seemingly developing a taste for them.     

Toxic,invasive treefrog creates evolutionary trap for native gartersnakes

Possession of unique defensive toxins by nonindigenous species may increase the likelihood of creating evolutionary traps for native predators. We tested the hypothesis that nonindigenous, toxic Cuban Treefrogs (Osteopilus septentrionalis) have created an evolutionary trap for native, generalist snakes. Additionally, we explored the possibility that populations of snakes that co-occur with Cuban Treefrogs have responded in ways that allow them to escape potential trap dynamics. To evaluate a potential fitness cost of consuming Cuban Treefrogs, we monitored growth of 61 wild-caught Common Gartersnakes (Thamnophis sirtalis) fed exclusive diets of either Cuban Treefrogs, native Green Treefrogs (Hyla cinerea), or native Golden Shiners (Notemigonus crysoleucas). Snakes in the Cuban Treefrog diet treatment gained less than half the mass of those consuming native prey, and Cuban Treefrogs were significantly less digestible than native prey. There was no difference in the response of gartersnakes to prey scent cues of Cuban Treefrogs and Green Treefrogs. Our results indicate that Cuban Treefrogs likely represent an evolutionary trap for snakes because consumption of these frogs carries fitness costs, yet snakes fail to recognize this prey as being costly. We found no difference in growth or response to prey cues between snakes from invaded and non-invaded regions, suggesting snakes have not responded to escape trap dynamics. Interactions of native snakes and Cuban Treefrogs support the idea that introduced species with novel toxins may increase the likelihood of evolutionary trap formation.     

Dangerous food: lacking venom and constriction,how do snake‐like lizards (Lialis burtonis,Pygopodidae) subdue their lizard prey?

Snakes are renowned for their ability to subdue and swallow large, often dangerous prey animals. Numerous adaptations, including constriction, venom, and a strike-and-release feeding strategy, help them avoid injury during predatory encounters. Burton's legless lizard ( Lialis burtonis Gray, Pygopodidae) has converged strongly on snakes. It is functionally limbless and feeds at infrequent intervals on relatively large prey items (other lizards) capable of inflicting a damaging bite. However, L. burtonis possesses neither venom glands, nor the ability to constrict prey. We investigated how L. burtonis subdues its prey without suffering serious retaliatory bites. Experiments showed that lizards modified their strike precision according to prey size; very large prey were always struck on the head or neck, preventing them from biting. In addition, L. burtonis delayed swallowing large lizards until they were incapacitated, whereas smaller prey were usually swallowed while still struggling. Lialis burtonis also displays morphological adaptations protecting it from prey retaliation. Its long snout prevents prey from biting, and it can retract its lidless eyes out of harm's way while holding onto a food item. The present study further clarifies the remarkable convergence between snakes and L. burtonis , and highlights the importance of prey retaliatory potential in predator evolution.  © 2007 The Linnean Society of London, Biological Journal of the Linnean Society, 2007, 91 , 719–727.     

Morphological integration and adaptation in the snake feeding system: a comparative phylogenetic study

A long-standing hypothesis for the adaptive radiation of macrostomatan snakes is that their enlarged gape--compared to both lizards and basal snakes--enables them to consume "large" prey. At first glance, this hypothesis seems plausible, or even likely, given the wealth of studies showing a tight match between maximum consumed prey mass and head size in snakes. However, this hypothesis has never been tested within a comparative framework. We address this issue here by testing this hypothesis in 12 monophyletic clades of macrostomatan snakes using recently published phylogenies, published maximum consumed prey mass data and morphological measurements taken from a large sample of museum specimens. Our nonphylogenetically corrected analysis shows that head width--independent of body size--is significantly related to mean maximum consumed prey mass among these clades, and this relationship becomes even more significant when phylogeny is taken into account. Therefore, these data do support the hypothesis that head shape is adapted to prey size in snakes. Additionally, we calculated a phylogenetically corrected morphological variance-covariance matrix to examine the role of morphological integration during head shape evolution in snakes. This matrix shows that head width strongly covaries with both jaw length and out-lever length of the lower jaw. As a result, selection on head width will likely be associated with concomitant changes in jaw length and lower jaw out-lever length in snakes.     

Apparent decoupling of prey recognition ability with prey availability in an insular snake population

Numerous studies on the feeding behavior of snakes have reported the consistency of tongue-flick responses with their natural diets. For representatives of widely distributed, dietary generalist species from particular localities, we can expect that their tongue-flick responses to potential prey unavailable in their original habitats have been reduced whereas those to prey common in the habitats have been enhanced. To test this hypothesis, intraspecific variation in tongue-flick responses to prey chemicals was examined using ingestively naive snakes (Elaphe quadrivirgata) from dietarily different populations: populations from the main Japanese island, where the snakes' diet predominantly consists of sympatric frogs, and from Mikura-jima Island, where no frogs occur and the snakes thus chiefly prey on lizards. We presented chemical stimuli from six items including those from their natural and potential prey (fish, frog, lizard, mouse, water, and cologne) to newborn snakes. Significant effects of stimuli on the tongue-flick responses were detected. On the other hand, effects of population and interaction between stimuli and population were not significant, and individual comparisons revealed no significant interlocality differences in responses to either frog or lizard chemicals. Thus, our hypothesis was not supported. However, in the Mikura-jima sample, significantly fewer snakes responded to frog chemicals than in the main island sample. The significance of the inconsistency between prey recognition ability and prey availability in the Mikura-jima population are discussed. Received: October 17, 2000 / Accepted: December 14, 2000     

Dietary Correlates of the Origin and Radiation of Snakes

Stomach analyses of living families and of a fossil containingprey were used to address possible dietary correlates of thehistory of snakes. Aniliids, morphologically primitive amongliving snakes, feed on relatively heavy, elongate vertebrates.Large aniliids eat larger prey than do small individuals but,as in advanced snakes, they also take small items. Living boids,structurally intermediate between aniliids and advanced snakes,feed on relatively heavy prey of a much greater variety of shapesthan do aniliids. An Eocene fossil that might be a boid containsa relatively large crocodilian in its gut. These findings, previousstudies, and morphological considerations suggest that veryearly snakes used constriction and powerful jaws to feed onelongate, heavy prey. This would have permitted a shift fromfeeding often on small items to feeding rarely on heavy items,without initially requiring major changes in jaw structure relativeto a lizard-like ancestor. Subsequent morphological changescould then have allowed boids to utilize a broad range of preytypes, including many of those currently eaten by advanced snakes.More recent dietary themes include the consumption of even heavierprey by highly venomous elapids and viperids, and frequent feedingon relatively small items by some other advanced snakes.     

Snake phylogeny based on osteology,soft anatomy and ecology

Relationships between the major lineages of snakes are assessed based on a phylogenetic analysis of the most extensive phenotypic data set to date (212 osteological, 48 soft anatomical, and three ecological characters). The marine, limbed Cretaceous snakes Pachyrhachis and Haasiophis emerge as the most primitive snakes: characters proposed to unite them with advanced snakes (macrostomatans) are based on unlikely interpretations of contentious elements or are highly variable within snakes. Other basal snakes include madtsoiids and Dinilysia--both large, presumably non-burrowing forms. The inferred relationships within extant snakes are broadly similar to currently accepted views, with scolecophidians (blindsnakes) being the most basal living forms, followed by anilioids (pipesnakes), booids and booid-like groups, acrochordids (filesnakes), and finally colubroids. Important new conclusions include strong support for the monophyly of large constricting snakes (erycines, boines. pythonines), and moderate support for the non-monophyly of the trophidophiids' (dwarf boas). These phylogenetic results are obtained whether varanoid lizards, or amphisbaenians and dibamids, are assumed to be the nearest relatives (outgroups) of snakes, and whether multistate characters are treated as ordered or unordered. Identification of large marine forms, and large surface-active terrestrial forms, as the most primitive snakes contradicts with the widespread view that snakes arose via minute, burrowing ancestors. Furthermore, these basal fossil snakes all have long flexible jaw elements adapted for ingesting large prey ('macrostomy'), suggesting that large gape was primitive for snakes and secondarily reduced in the most basal living foms (scolecophidians and anilioids) in connection with burrowing. This challenges the widespread view that snake evolution has involved progressive, directional elaboration of the jaw apparatus to feed on larger prey.     

Aerobic metabolism during predation by a boid snake

We quantified the oxygen uptake rates (VO(2)) and time spent, during the constriction, inspection, and ingestion of prey of different relative sizes, by the prey-constricting boid snake Boa constrictor amarali. Time spent in prey constriction varied from 7.6 to 16.3 min, and VO(2) during prey constriction increased 6.8-fold above resting values. This was the most energy expensive predation phase but neither time spent nor metabolic rate during this phase were correlated with prey size. Similarly, prey size did not affect the VO(2) or duration of prey inspection. Prey ingestion time, on the other hand, increased linearly with prey size although VO(2) during this phase, which increased 4.9-fold above resting levels, was not affected by prey size. The increase in mechanical difficulty of ingesting larger prey, therefore, was associated with longer ingestion times rather than proportional increases in the level of metabolic effort. The data indicate that prey constriction and ingestion are largely sustained by glycolysis and the intervening phase of prey inspection may allow recovery between these two predatory phases with high metabolic demands. The total amount of energy spent by B. c. amarali to constrict, inspect, and ingest prey of sizes varying from 5 to 40% of snake body mass varied inversely from 0.21 to 0.11% of the energy assimilated from the prey, respectively. Thus, prey size was not limited by the energetic cost of predation. On the contrary, snakes feeding on larger prey were rewarded with larger energetic returns, in accordance with explanations of the evolution of snake feeding specializations.     

The role of vision in the predatory behaviour of natricine snakes

Early workers concluded that ingestively naive garter snakes (Thamnophis) recognize chemical cues from their normal prey, and that such cues are sufficient to elicit prey attack, whereas visual prey cues are not sufficient. In the light of recent observations on how garter and water snakes (Nerodia) forage, new tests were made of the role of visual stimuli in the aquatic predation of several natricine species. Both experienced and ingestively naive snakes oriented to and attacked a fish model in plain water, although they made more orientations and attacks when diffuse fish odour was present in the water. Fish odour in water also elicited increased aquatic searching behaviour. Early views on the role of vision in the predation of newborn natricine snakes require modification, and there is a need for investigation of the properties of effective visual stimuli and the ontogeny of responsiveness to them.     

Wait Until Dark? Daily Activity Patterns and Nest Predation by Snakes

Predation involves costs and benefits, so predators should employ tactics that reduce their risk of injury or death and that increase their success at capturing prey. One potential way that predators could decrease risk and increase benefits is by attacking prey at night when risks may be reduced and prey more vulnerable. Because some snakes are facultatively nocturnal and prey on bird nests during the day and night, they are ideal for assessing the costs and benefits of diurnal vs. nocturnal predation. We used automated radiotelemetry and cameras to investigate predation on nesting birds by two species of snakes, one diurnal and the other facultatively nocturnal. We predicted that snakes preying on nests at night should experience less parental nest defence and capture more adults and nestlings. Rat snakes (Pantherophis obsoletus) were relatively inactive at night (23–36% activity) but nearly always preyed on nests after dark (80% of nest predations). Conversely, racers (Coluber constrictor) were exclusively diurnal and preyed on nests during the times of day they were most active. These results are consistent with rat snakes strategically using their capacity for facultative nocturnal activity to prey on nests at night. The likely benefit is reduced nest defence because birds defended their nests less vigourously at night. Consistent with nocturnal predation being safer, rat snake predation events lasted three times longer at night than during the day (26 vs. 8 min). Nocturnal nest predation did not make nests more profitable by increasing the likelihood of capturing adults or removing premature fledging of nestlings. The disconnect between rat snake activity and timing of nest predation seems most consistent with rat snakes locating prey during the day using visual cues but waiting until dark to prey on nests when predation is safer, although designing a direct test of this hypothesis will be challenging.     

Ecological and phylogenetic variability in the spinalis muscle of snakes

Understanding the origin and maintenance of functionally important subordinate traits is a major goal of evolutionary physiologists and ecomorphologists. Within the confines of a limbless body plan, snakes are diverse in terms of body size and ecology, but we know little about the functional traits that underlie this diversity. We used a phylogenetically diverse group of 131 snake species to examine associations between habitat use, sidewinding locomotion and constriction behaviour with the number of body vertebrae spanned by a single segment of the spinalis muscle, with total numbers of body vertebrae used as a covariate in statistical analyses. We compared models with combinations of these predictors to determine which best fit the data among all species and for the advanced snakes only (N = 114). We used both ordinary least‐squares models and phylogenetic models in which the residuals were modelled as evolving by the Ornstein–Uhlenbeck process. Snakes with greater numbers of vertebrae tended to have spinalis muscles that spanned more vertebrae. Habitat effects dominated models for analyses of all species and advanced snakes only, with the spinalis length spanning more vertebrae in arboreal species and fewer vertebrae in aquatic and burrowing species. Sidewinding specialists had shorter muscle lengths than nonspecialists. The relationship between prey constriction and spinalis length was less clear. Differences among clades were also strong when considering all species, but not for advanced snakes alone. Overall, these results suggest that muscle morphology may have played a key role in the adaptive radiation of snakes.