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Feeding in Snakes: Form, Function, and Evolution of the Feeding System

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Abstract

Snakes are a diverse group of squamate reptiles characterized by a unique feeding system and other traits associated with elongation and limblessness. Despite the description of transitional fossil forms, the evolution of the snake feeding system remains poorly understood, partly because only a few snakes have been studied thus far. The idea that the feeding system in most snakes is adapted for consuming relatively large prey is supported by studies on anatomy and functional morphology. Moreover, because snakes are considered to be gape-limited predators, studies of head size and shape have shed light on feeding adaptations. Studies using traditional metrics have shown differences in head size and shape between males and females in many species that are linked to differences in diet. Research that has coupled robust phylogenies with detailed morphology and morphometrics has further demonstrated the adaptive nature of head shape in snakes and revealed striking evolutionary convergences in some clades. Recent studies of snake strikes have begun to reveal surprising capacities that warrant further research. Venoms, venom glands, and venom delivery systems are proving to be more widespread and complex than previously recognized. Some venomous and many nonvenomous snakes constrict prey. Recent studies of constriction have shown previously unexpected responsiveness, strength, and the complex and diverse mechanisms that incapacitate or kill prey. Mechanisms of drinking have proven difficult to resolve, although a new mechanism was proposed recently. Finally, although considerable research has focused on the energetics of digestion, much less is known about the energetics of striking and handling prey. A wide range of research on these and other topics has shown that snakes are a rich group for studying form, function, behavior, ecology, and evolution.

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... The feeding behavior and morphology of snakes provide a unique opportunity to integrate morphology, performance, and behavior. In the last decade, there has been a resurgence of interest in snake striking and feeding (Moon et al. 2019). The primary focus of snake striking for many years was the vipers, which had been shown to strike at extremely high levels of performance (Lillywhite 2014;Moon et al. 2019). ...
... In the last decade, there has been a resurgence of interest in snake striking and feeding (Moon et al. 2019). The primary focus of snake striking for many years was the vipers, which had been shown to strike at extremely high levels of performance (Lillywhite 2014;Moon et al. 2019). Recently, broader use of high-speed videography has found that other snake species beyond the vipers can strike at similar performance levels, adults and juveniles, in defense, or feeding (Penning et al. 2016;Ryerson and Tan 2017). ...
... This axial musculature is also the primary driver in another stage used by nonvenomous snakes, constriction, where coils of the body are wrapped around a prey item, generating sufficient pressures on the internal systems to cause death (Boback et al. 2015;Penning 2017). The cranial elements of the feeding system are most explored in the swallowing stage of feeding, particularly as it relates to the maximum gape of snakes (Hampton and Moon 2013;Jayne et al. 2018;Moon et al. 2019). However, given that the skull plays a direct role in prey capture in every snake, we know little about these particular functional elements, or even how they work together (Rhoda et al. 2021). ...
Article
Synopsis Snakes, with the obvious exception of the fangs, are considered to lack the regional specialization of tooth shape and function which are exemplified by mammals. Recent work in fishes has suggested that the definition of homodont and heterodont are incomplete without a full understanding of the morphology, mechanics, and behavior of feeding. We investigated this idea further by examining changes in tooth shape along the jaw of Boa constrictor and integrating these data with the strike kinematics of boas feeding on rodent prey. We analyzed the shape of every tooth in the skull, from a combination of anesthetized individuals and CT scanned museum specimens. For strike kinematics, we filmed eight adult boas striking at previously killed rats. We determined the regions of the jaws that made first contact with the prey, and extrapolated the relative positions of those teeth at that moment. We further determined the roles of all the teeth throughout the prey capture process, from the initiation of the strike until constriction began. We found that the teeth in the anterior third of the mandible are the most upright, and that teeth become progressively more curved posteriorly. Teeth on the maxilla are more curved than on the mandible, and the anterior teeth are more linear or recurved than the posterior teeth. In a majority of strikes, boas primarily made contact with the anterior third of the mandible first. The momentum from the strike caused the upper jaws and skull to rotate over the rat. The more curved teeth of the upper jaw slid over the rat unimpeded until the snake began to close its jaws. In the remaining strikes, boas made contact with the posterior third of both jaws simultaneously, driving through the prey and quickly retracting, ensnaring the prey on the curved posterior teeth of both jaws. The curved teeth of the palatine and pterygoid bones assist in the process of swallowing.
... Snakes are limbless tetrapods that forage almost exclusively using their heads (Cundall and Greene 2000;Moon et al. 2019). The hyperkinetic skulls of snakes are composed of over 20 bones articulated but unfused with one another, eight of which are directly involved in feeding (Fig. 1A). ...
... The feeding bones are developmentally modular at least insofar that the different bones are ultimately the results of spatially separated developing cellular populations (i.e., the ossification centers of each bone do not meet to fuse together during development, but see Discussion; Raff 1996;Boughner et al. 2007;Polachowski and Werneburg 2013). Alternatively, the movements of these spatially separated bones must act in concert to successfully forage; snakes must capture, manipulate, and ingest prey exclusively using their head and anterior trunk (Cundall and Greene 2000; Moon et al. 2019). The feeding sequence of snakes can be divided into several segments: prey capture, prey manipulation and repositioning, and swallowing that includes the highly conserved "pterygoid walk" where the teeth of the palatine and pterygoid grasp and hold onto prey, whereas the braincase advances over it (Boltt and Ewer 1964;Cundall and Greene 2000;Moon et al. 2019). ...
... Alternatively, the movements of these spatially separated bones must act in concert to successfully forage; snakes must capture, manipulate, and ingest prey exclusively using their head and anterior trunk (Cundall and Greene 2000; Moon et al. 2019). The feeding sequence of snakes can be divided into several segments: prey capture, prey manipulation and repositioning, and swallowing that includes the highly conserved "pterygoid walk" where the teeth of the palatine and pterygoid grasp and hold onto prey, whereas the braincase advances over it (Boltt and Ewer 1964;Cundall and Greene 2000;Moon et al. 2019). The coordinated movement of different groups of bones is required to perform these different functions, forming functional modules. ...
Article
The kinetic skull is a key innovation that allowed snakes to capture, manipulate, and swallow prey exclusively using their heads using the coordinated movement of 8 bones. Despite these unique feeding behaviors, patterns of evolutionary integration and modularity within the feeding bones of snakes in a phylogenetic framework have yet to be addressed. Here, we use a dataset of 60 µCT scanned skulls and high-density geometric morphometric methods to address the origin and patterns of variation and integration in the feeding bones of aquatic-foraging snakes. By comparing alternate superimposition protocols allowing us to analyze the entire kinetic feeding system simultaneously, we find that the feeding bones are highly integrated, driven predominantly by functional selective pressures. The most supported pattern of modularity contains four modules, each associated with distinct functional roles: the mandible, the palatopterygoid arch, the maxilla, and the suspensorium. Further, the morphological disparity of each bone is not linked to its This article is protected by copyright. All rights reserved. 2 magnitude of integration, indicating that integration within the feeding system does not strongly constrain morphological evolution, and that adequate biomechanical solutions to a wide range of feeding ecologies and behaviors are readily evolvable within the constraint due to integration in the snake feeding system.
... Snakes are limbless tetrapods that forage almost exclusively using their heads (Cundall and Greene 2000;Moon et al. 2019). The hyperkinetic skulls of snakes are composed of over 20 bones articulated but unfused with one another, eight of which are directly involved in feeding (Fig. 1A). ...
... The feeding bones are developmentally modular at least insofar that the different bones are ultimately the results of spatially separated developing cellular populations (i.e., the ossification centers of each bone do not meet to fuse together during development, but see Discussion; Raff 1996;Boughner et al. 2007;Polachowski and Werneburg 2013). Alternatively, the movements of these spatially separated bones must act in concert to successfully forage; snakes must capture, manipulate, and ingest prey exclusively using their head and anterior trunk (Cundall and Greene 2000; Moon et al. 2019). The feeding sequence of snakes can be divided into several segments: prey capture, prey manipulation and repositioning, and swallowing that includes the highly conserved "pterygoid walk" where the teeth of the palatine and pterygoid grasp and hold onto prey, whereas the braincase advances over it (Boltt and Ewer 1964; Cundall and Greene 2000; Moon et al. 2019). ...
... Alternatively, the movements of these spatially separated bones must act in concert to successfully forage; snakes must capture, manipulate, and ingest prey exclusively using their head and anterior trunk (Cundall and Greene 2000; Moon et al. 2019). The feeding sequence of snakes can be divided into several segments: prey capture, prey manipulation and repositioning, and swallowing that includes the highly conserved "pterygoid walk" where the teeth of the palatine and pterygoid grasp and hold onto prey, whereas the braincase advances over it (Boltt and Ewer 1964; Cundall and Greene 2000; Moon et al. 2019). The coordinated movement of different groups of bones is required to perform these different functions, forming functional modules. ...
... Snakes are restricted in terms of the prey that they can consume as they are unable to mechanically reduce the sizes and process their captured prey (Greene, 1997;Mori & Vincent, 2008), thereby making them gape-limited predators. As such, snake gape size, and therefore head size, can be directly linked to the range of prey that snakes consume (Arnold, 1993;Cundall & Greene, 2000;Cundall, 2019), thus allowing for the inference of direct relationships between changes in the functional morphology of snake feeding apparatus and the consumption of specific prey (Rodríguez-Robles, Bell & Greene, 1999;Vincent et al., 2006;Moon et al., 2019). For example, North American natricine snakes that feed exclusively on fish have longer quadrate bones and increased swallowing performance of large fish prey to congeneric generalists (Vincent et al., 2009). ...
... Snakes that consume large prey are typically able to do so because they possess specialized adaptive morphology, or, are simply large-bodied and have large heads (Cundall & Greene, 2000;Moon et al., 2019). Generally, snake species with larger heads can consume a broader range of prey than those with smaller heads (Arnold, 1993;Greene, 1997;Cundall & Greene, 2000). ...
... Generally, snake species with larger heads can consume a broader range of prey than those with smaller heads (Arnold, 1993;Greene, 1997;Cundall & Greene, 2000). As a result, large-bodied snakes are predicted to have a wide dietary niche (Shine, 1991;Arnold, 1993;Luiselli, 2006;Moon et al., 2019) and generalist diets. Conversely, dietary specialists that only consume a limited number of prey types should showcase predictable phenotypical adaptations in their head elements that facilitate the ingestion of their preferred prey (Mori & Vincent, 2008). ...
Article
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Interspecific competition for limited resources should theoretically occur between species that are morphologically similar to each other. Consequently, species that reduce competition by adapting to specialize on a specific resource should be morphologically disparate to sympatric contemporaries and show evidence of phenotypic specialization. However, few studies have compared the morphologies of specialist and generalist competitors. In this context, we compare the feeding morphology and diet of an obligate, specialist, bird‐egg‐eating snake to three sympatric generalists that only facultatively consume bird eggs. We measured and compared body and head morphology of preserved museum specimens of each of four, syntopic snake species from southern Africa: the obligate bird‐egg‐eating rhombic egg‐eater (Dasypeltis scabra), and the facultative bird‐egg‐eating boomslang (Dispholidus typus), cape cobra (Naja nivea) and mole snake (Pseudaspis cana). Given the physical challenges of consuming bird eggs in snakes, we predicted that consumption of bird eggs would be facilitated by the evolution of relatively larger heads in the smaller‐bodied Dasypeltis. We found that head size was not phylogenetically conserved in the clades of these taxa and that contrary to our expectations, the specialist egg‐eaters evolved to possess significantly smaller heads relative to body size than their competitors. We found a positive relationship between dietary niche breadth and head size within these species and their close relatives. Thus, relatively large‐headed species have evolved diverse diets that overlap with the restricted diets of the small‐headed specialist thereby producing this atypical competitive interaction. Our findings suggest that specialized adaptations can decouple typical body‐size‐constrained competition dynamics between sympatric snake species and highlight the complexity of the origins of dietary specialization. African egg‐eating snakes have smaller‐sized heads, both in absolutely terms and relative to body size, than other bird‐egg‐eating snakes. As a result, these snakes must compete with morphologically dissimilar species to themselves, a pattern that is typically unusual in snakes.
... For snakes, all locomotor and striking movements are produced by complex axial musculature (Gasc, 1981;Jayne, 1982;Moon, 2000;Mosauer, 1935), including striking behaviors. Striking behaviors are used in important ecological contexts such as predation and defense (LaDuc, 2002;Moon, Penning, Segall, & Herrel, 2019). However, ontogenetic changes in morphology and performance are largely unexplored (but see Herrel et al., 2011;Jayne & Riley, 2007;Penning & Moon, 2017), particularly in one of the largest adaptive radiations of snakes, the family Colubridae (Alfaro, 2002;Greenwald, 1974Greenwald, , 1978Penning, Sawvel, & Moon, 2016). ...
... However, ontogenetic changes in morphology and performance are largely unexplored (but see Herrel et al., 2011;Jayne & Riley, 2007;Penning & Moon, 2017), particularly in one of the largest adaptive radiations of snakes, the family Colubridae (Alfaro, 2002;Greenwald, 1974Greenwald, , 1978Penning, Sawvel, & Moon, 2016). Snakes are obligate carnivores that use a variety of predation modes that can change in response to changes in body and prey size (Andrade & Abe, 1999;Lind & Welsch, 1994;Moon et al., 2019). With so few snakes having been investigated, we are currently unable to describe general patterns of performance, especially across ontogeny. ...
Article
In many organisms, juveniles have performance capabilities that partly offset their disadvantageous sizes. Using high-speed video recordings and imaging software, we measured the scaling of head morphology, axial morphology, and defensive strike performance of Pantherophis obsoletus across their ontogeny to understand how size and morphology affect performance. Head measurements were negatively allometric whereas the cross-sectional area (CSA) of epaxial muscles displayed positive allometry. The greater relative muscle CSA of larger ratsnakes allows them to produce higher forces relative to their mass, and those forces act on a relatively smaller head mass when it is thrust forward during striking. Maximum strike accelerations of 70-273.8 ms-2 and velocities of 1.08-3.39 ms-1 scaled positively with body mass but differed from the geometric predictions. Velocity scaled with mass0.15 and acceleration scaled with mass0.17 . Larger snakes struck from greater distances (range = 4.1-26 cm), but all snakes covered the strike distances with similarly short durations (84 ± 3 ms). The negatively allometric head size, isometry of anterior mass, and positively allometric muscle CSA enable larger P. obsoletus to strike with higher velocities and accelerations than smaller individuals. Our results contrast with the scaling of strike performance in an arboreal viper, whose strike distance and velocity were independent of body mass. When strike distance is modulated, all other performance capacities are affected because of the interdependence of acceleration, velocity, duration, and distance.
... In the absence of discrete push points, snakes are able to generate static contact zones by coiling with their ventrum against the branch-like object to periodically grip a surface through medial force exertion Jayne 2007, 2009). These kinematics are remarkably similar to those of constriction, although constriction coils are applied with ventral and lateral body walls, dependent upon species and number of loops (Mehta 2005;Mehta and Burghardt 2008;Moon et al. 2019). As the slope of the incline increases, the animal's mass contributes less to the production of normal forces and contact becomes more reliant on muscular effort and friction, the latter aided by the l t and l b of the scales. ...
... disrupting the prey's cardiovascular blood flow, and inducing death likely via cardiac arrest (Boback et al. 2015;Moon et al. 2019). Although this clearly involves tremendous force, this behavior does not substantially pressurize the systemic blood pressure of the snake exerting the force; systemic blood pressures reach higher levels throughout hissing and prey ingestion than during constriction (Wang et al. 2001). ...
Article
Full-text available
Locomotion in most tetrapods involves coordinated efforts between appendicular and axial musculoskeletal systems, where interactions between the limbs and the ground generate vertical (GV), horizontal (GH), and mediolateral (GML) ground-reaction forces that are transmitted to the axial system. Snakes have a complete absence of external limbs and represent a fundamental shift from this perspective. The axial musculoskeletal system of snakes is their primary structure to exert, transmit, and resist all motive and reaction forces for propulsion. Their lack of limbs makes them particularly dependent on the mechanical interactions between their bodies and the environment to generate the net GH they need for forward locomotion. As organisms that locomote on their bellies, the forces that enable the various modes of snake locomotion involve two important structures: the integument and the ribs. Snakes use the integument to contact the substrate and produce a friction-reservoir that exceeds their muscle-induced propulsive forces through modulation of scale stiffness and orientation, enabling propulsion through variable environments. XROMM work and previous studies suggest that the serially repeated ribs of snakes change their cross-sectional body shape, deform to environmental irregularities, provide synergistic stabilization for other muscles, and differentially exert and transmit forces to control propulsion. The costovertebral joints of snakes have a biarticular morphology, relative to the unicapitate costovertebral joints of other squamates, that appears derived and not homologous with the ancestral bicapitate ribs of Amniota. Evidence suggests that the biarticular joints of snakes may function to buttress locomotor forces, similar to other amniotes, and provide a passive mechanism for resisting reaction forces during snake locomotion. Future comparisons with other limbless lizard taxa are necessary to tease apart the mechanics and mechanisms that produced the locomotor versatility observed within Serpentes.
... Vipers will strike and release, allowing venom to disable and kill their prey, which they will subsequently track down and ingest (Greene, 1997;Kardong, 1998;Lillywhite, 2014). Many elapids, also with significantly potent venom, will bite and hold onto their prey, preventing their escape while the venom acts (Lillywhite, 2014;Moon et al., 2019). Constriction, a behavior exhibited by several different families (Boidae, Pythonidae, Colubridae), is a behavior that is used in both the killing and subsequent prey-handling. ...
... How snakes decide where to begin transport is still unclear. With few exceptions, snakes primarily swallow their food headfirst (de Quieroz and de Quieroz, 1987;Cundall and Greene, 2000;Moon et al., 2019), which reduces total swallowing time (Diefenbach and Emsilie, 1971). Once transport/ swallowing begins, the coils relax and the prey is drawn in through a process known as pterygoid walking (Cundall and Greene, 2000;Lillywhite;2014). ...
... Aunque las investigaciones acerca de la energía usada en la digestión de las serpientes han sido numerosas, se sabe poco sobre la energía y procesos de captura, manejo y engullimiento de las presas [11]. Nosotros describimos el comportamiento predatorio y las adaptaciones de ingestión y deglución de Chironius monticola, donde se destaca la ayuda con rocas para empujar a su presa capturada y engullirla rápidamente; en contraste con no poseer un apoyo físico, es probable que el proceso podría durar varios minutos más. ...
Article
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We report two cases of predatory behavior of Chironius monticola on Pristimantis w-nigrum, which occurred in the province of El Oro, southwest of Ecuador. In the first case a juvenile male Chironius monticola was observed in the process of swallowing a Pristimantis w-nigrum, the event lasted at least ten minutes in which the snake did not consume the frog in its entirety. The second event describes how Chironius monticola held with its mouth the head of a Pristimantis w-nigrum, then apparently makes use of stones around it to push its prey and swallow it completely. This case was videotaped for 3 min 16 s. This event is the first known record of external resource use for this species. Both records suggest the preference for anurans by Chironius monticola, although more data are needed to assert this since their diet depends of the availability of prey as well as their age.
... Defensive striking may also be performed to reduce the likelihood that a predator or dangerous animal (e.g. large mammal) approaches (Moon et al., 2019). Defensive strikes that do not result in snakes contacting the putative target can function as a warning or bluff, meant to increase the distance between the snake and the perceived threat. ...
Article
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Movements of ectotherms are constrained by their body temperature due to the effects of temperature on muscle physiology. As physical performance often affects the outcome of predator-prey interactions, environmental temperature can influence the ability of ectotherms to capture prey and/or defend themselves against predators. However, previous research on the kinematics of ectotherms suggests that some species may use elastic storage mechanisms when attacking or defending, thereby mitigating the effects of sub-optimal temperature. Rattlesnakes (Crotalus) are a speciose group of ectothermic viperid snakes that rely on crypsis, rattling, and striking to deter predators. We examined the influence of body temperature on the behavior and kinematics of two rattlesnake species (C. oreganus helleri and C. scutulatus) when defensively striking towards a threatening stimulus. We recorded defensive strikes at body temperatures ranging from 15°C-35°C. We found that strike speed and speed of mouth gaping during the strike were positively correlated with temperature. We also found a marginal effect of temperature on the probability of striking, latency to strike, and strike outcome. Overall, warmer snakes are more likely to strike, strike faster, open their mouth faster, and reach maximum gape earlier than colder snakes. However, the effects of temperature were less than would be expected for purely muscle-driven movements. Our results suggest that, although rattlesnakes are at a greater risk of predation at colder body temperatures, their decrease in strike performance may be mitigated to some extent by employing mechanisms in addition to skeletal muscle contraction (e.g. elastic energy storage) to power strikes.
... Snakes are a highly diverse group of predator reptiles, characterized by a unique gap-limited feeding system, adapted to consume large and entire prey (Moon et al., 2019). They employ a variety of strategies (i.e., ambush predators vs actively searchers) and traits (e.g., constriction, envenomation) to localise and subdue prey, which primarily determine their trophic niche (Glaudas et al., 2019;Lyons et al., 2020), and subsequently influence other ecological features as habitat selection, movement patterns or thermoregulatory activity (e.g., Blouin-Demers and Weatherhead, 2001;Wasko and Sasa, 2012). ...
Article
Numerous dietary studies have shown that European vipers (genus Vipera ) present low feeding frequency and a specialist diet, which is characterised by a marked ontogenetic shift. However, how eco-geographic factors shape species’ feeding ecology remains scarcely addressed. We investigated the feeding ecology of the Iberian adder, Vipera seoanei , examining 402 specimens distributed across its distributional range and addressing how biological, temporal and eco-geographic factors relate to the species feeding activity and dietary consumption. Our results indicated a low feeding frequency in the species, higher in juveniles than in adults. Adult females showed higher rates of prey consumption than adult males, which match to the distinct reproductive demands of both sexes, although no differences between reproductive and non-reproductive females were found. V. seoanei preyed on a varied taxa spectrum, but showed a rather specialist diet based on small mammals. Amphibians and reptiles were also an important part of its diet, particularly in the juveniles. Body size was found as the single biological trait related to the consumption of major prey groups, supporting the occurrence of an ontogenetic shift in the diet. Two habitat and two climatic factors correlated to the consumption of major prey groups, reflecting the ecological requirements of prey across the viper’s range. Overall, this study extends the existing knowledge on the feeding ecology of European vipers, signalling how energy intake and allometric constraints shape the feeding activity and dietary consumption of the species across the geography, leading to distinct feeding strategies in juveniles and adults.
... In research, captive snakes were fed with rats and mice, but live prey can possibly injure snakes if not eaten right away and vertebrate prey options tend to be more calorically-rich and may cause the problem of obese snakes. (Moon et al., 2019). In an experimental trial, a sausage diet was formulated by using BSF larvae and was fed to juvenile corn snakes (Pantherophis guttatus) at the rate of 15% of their body weight. ...
Article
For the past few decades, attentiveness has been progressive in the arcade of insect production for human food and animal feeds. The husbandry of edible insects has arisen as an auspicious unconventional approach for making protein-enriched feed ingredients. The industrialisation of insect-based protein is going to be more lucrative, dynamic, and well-organised in the future for livestock agribusiness and aquaculture, and consequently, it lowers environmental hazards by decreasing the accumulation of greenhouse gases in the atmosphere. Black soldier flies (BSF) are commercially utilised for the biodegradation of biological wastes at a large scale. BSF larvae’s propensity to ingest rotten vegetables, fruits, livestock faeces, and cadavers has empowered their advancement in waste removal services. Although these bio-wastes contain efficient nutrients, there are also colonies of many microbes in these biological trashes. The larvae of Hermetia illucens produce a large number of antimicrobial peptides to protect themselves against microbial invasion. The immune system of these insects is being potentiated by the genome of their innate gut microbes that helps to avoid the settlement of pathogens to which larvae are vulnerable from the feeding substrates. Insects have a strong innate defence system that figures out the production of a wide-ranging variety of antimicrobial peptides. The usage of antibiotics in livestock husbandry has been documented as the leading problem for antibiotic resistance against many pathogens in animals and humans consuming adulterated food products with antibiotic residues. Until this time many types of research have been done about the use of BSF insects in poultry and aquaculture but very few studies have been done on lab animals like rats, rabbits, and reptiles
... In birds, diet and brain regions are also related, but whereas in fish this seems to be based on perception/detection of a prey, in birds it is more related to the complexity of the food manipulation (Gutiérrez-Ibáñez et al. 2010). Snakes not only have a very diverse dietary range, but they also use their head to manipulate and swallow their prey (Moon et al. 2019). Some crustacean-eating snakes such as Fordonia leucobalia, Cantoria violacea and Gerarda prevostiana even show complex manipulation behavior (Jayne et al. 2018). ...
Article
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Environmental properties, and the behavioral habits of species impact sensory cues available for foraging, predator avoidance and inter/intraspecific communication. Consequently, relationships have been discovered between the sensory ecology and brain morphology in many groups of vertebrates. However, these types of studies have remained scare on snake. Here, we investigate the link between endocranial shape and the sensory-related ecology of snakes by comparing 36 species of snakes for which we gathered six sensory-ecology characteristics. We use µCT scanning and 3D geometric morphometrics to compare their endocranium in a phylogenetically informed context. Our results demonstrate that size is a major driver of endocranial shape, with smaller species tending to maximize endocranial volume using a more bulbous shape, while larger species share an elongate endocranial morphology. Phylogeny plays a secondary role with more derived snakes diverging the most in endocranial shape, compared to other species. The activity period influences the shape of the olfactory and optic tract, while the foraging habitat impacts the shape of the cerebellum and cranial nerve regions: structures involved in orientation, equilibrium, and sensory information. However, we found that endocranial morphology alone is not sufficient to predict the activity period of a species without prior knowledge of its phylogenetic relationship. Our results thus demonstrate the value of utilizing endocranial shape as complementary information to size and volume in neurobiological studies.
... The same is true for many, if not most, snake lineages who can coil their bodies to perform a variety of functions, but do not necessarily demonstrate coiling around their prey during feeding, let alone constriction (e.g. Bealor & Saviola 2007;Moon et al. 2019). True constriction of the kind alluded to in the generalization given by Martill et al. (2015) is largely restricted to snakes that also demonstrate extreme macrostomy (see Caldwell 2019). ...
Article
The origin of snakes remains one of the most contentious evolutionary transitions in vertebrate evolution. The discovery of snake fossils with well-formed hind limbs provided new insights into the phylogenetic and ecological origin of snakes. In 2015, a fossil from the Early Cretaceous Crato Formation of Brazil was described as the first known snake with fore- and hind limbs (Tetrapodophis amplectus), and was proposed to be fossorial, to exhibit large gape feeding adaptations (macrostomy) and to possess morphologies suggesting constriction behaviours. First-hand examination of T. amplectus, including its undescribed counterpart, provides new evidence refuting it as a snake. We find: a long rostrum; straight mandible; teeth not hooked zygosphenes/zygantra absent; neural arch and spines present and tall with apical epiphyses; rib heads not tubercular; synapophyses simple; and lymphapophyses absent. Claimed traits not preserved include: braincase/descensus parietalis; ‘L’-shaped nasals; intramandibular joint; replacement tooth crowns; haemal keels; tracheal rings; and large ventral scales. New observations include: elongate retroarticular process; apex of splenial terminating below posterior extent of tooth row; >10 cervicals with hypapophyses and articulating intercentra; haemapophyses with articulating arches; reduced articular surfaces on appendicular elements; rows of small body scales; and reduced mesopodial ossification. The axial skeleton is uniquely elongate and the tail with >100 vertebrae is not short as previously claimed, although overall the animal is small (∼195 mm total length). We assessed the relationships of Tetrapodophis using a revised version of the original morphological dataset, an independent morphological dataset, and these two datasets combined with molecular data. All four were analysed under parsimony and Bayesian inference and unambiguously recover Tetrapodophis as a dolichosaur. We find that Tetrapodophis shows aquatic adaptations and there is no evidence to support constricting behaviour or macrostomy.
... All prey subjugation modes, including complex constriction coils or variable body pinning techniques, engage the cranial one-to two-thirds of the snake's body, a pattern that is consistent throughout the multiple acquisitions of constriction within the clade (Bealor and Saviola, 2007;Boback et al., 2015;Greene and Burghardt, 1978;Mehta and Burghardt, 2008;Moon, 2000). Moreover, this mode of prey subjugation uses the rib cage of the snake to pressurize the rib cage of the prey, with less variable and higher mass-specific forces correlated with more consistent, uniform coil postures, that are presumably more efficient and safer for the snake (Boback et al., 2015;Moon et al., 2019). The LC has also been suggested to be an integral contributor to such behaviors in constricting colubrids, as a result of its control over the ribs in contact with the prey and large physiological cross-sectional area (PCSA), nearly or more than double the PCSA of the other epaxial muscles typically associated with constriction force production (Capano, 2020;Moon, 2000;Penning, 2018). ...
Article
The evolution of constriction and of large prey ingestion within snakes are key innovations that may explain the remarkable diversity, distribution and ecological scope of this clade, relative to other elongate vertebrates. However, these behaviors may have simultaneously hindered lung ventilation such that early snakes may have had to circumvent these mechanical constraints before those behaviors could evolve. Here, we demonstrate that Boa constrictor can modulate which specific segments of ribs are used to ventilate the lung in response to physically hindered body wall motions. We show that the modular actuation of specific segments of ribs likely results from active recruitment or quiescence of derived accessory musculature. We hypothesize that constriction and large prey ingestion were unlikely to have evolved without modular lung ventilation because of their interference with lung ventilation, high metabolic demands and reliance on sustained lung convection. This study provides a new perspective on snake evolution and suggests that modular lung ventilation evolved during or prior to constriction and large prey ingestion, facilitating snakes' remarkable radiation relative to other elongate vertebrates.
... This suggests that by using venom and/or chelae, incapacitation performance was similar between these species. A similar trend has been observed in some snakes where constriction might be equally or more effective than the use of toxins when subduing prey, underlining the importance of mechanical strategies during prey incapacitation [42,43]. ...
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... Using highly kinetic joints, snakes can achieve extremely large gap and cranial kinesis, providing substantial degree of freedom to the upper jaw to move relatively independently of the head. Therefore, jaws of the snake can be opened and advanced unilaterally in an alternating pattern of protraction of the upper and lower jaw on either side, functioning as the primary vector of transportation/swallowing (Moon et al., 2019). This motion is aptly termed the "pterygoid walk," since the snake basically "walks over" the prey through a combination of ratchet-like jaw movements and concertinalike body undulation (Boltt and Ewer, 1964;Kley and Brainerd, 2002). ...
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Evolutionary trajectories are often biased by developmental and historical factors. However, environmental factors can also impose constraints on the evolutionary trajectories of organisms leading to convergence of morphology in similar ecological contexts. The physical properties of water impose strong constraints on aquatic feeding animals by generating pressure waves that can alert prey and potentially push them away from the mouth. These hydrodynamic constraints have resulted in the independent evolution of suction feeding in most groups of secondarily aquatic tetrapods. Despite the fact that snakes cannot use suction, they have invaded the aquatic milieu many times independently. Here, we test whether the aquatic environment has constrained head shape evolution in snakes and whether shape converges on that predicted by biomechanical models. To do so, we used three-dimensional geometric morphometrics and comparative, phylogenetically informed analyses on a large sample of aquatic snake species. Our results show that aquatic snakes partially conform to our predictions and have a narrower anterior part of the head and dorsally positioned eyes and nostrils. This morphology is observed, irrespective of the phylogenetic relationships among species, suggesting that the aquatic environment does indeed drive the evolution of head shape in snakes, thus biasing the evolutionary trajectory of this group of animals.
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Scale sensilla are small tactile mechanosensory organs located on the head scales of many squamate reptiles (lizards and snakes). In sea snakes and sea kraits (Elapidae: Hydrophiinae), these scale organs are presumptive scale sensilla that purportedly function as both tactile mechanoreceptors and potentially as hydrodynamic receptors capable of sensing the displacement of water. We combined scanning electron microscopy, silicone casting of the skin and quadrate sampling with a phylogenetic analysis to assess morphological variation in sensilla on the postocular head scale(s) across four terrestrial, 13 fully aquatic and two semi-aquatic species of elapids. Substantial variation exists in the overall coverage of sensilla (0.8–6.5%) among the species sampled and is broadly overlapping in aquatic and terrestrial lineages. However, two observations suggest a divergent, possibly hydrodynamic sensory role of sensilla in sea snake and sea krait species. First, scale sensilla are more protruding (dome-shaped) in aquatic species than in their terrestrial counterparts. Second, exceptionally high overall coverage of sensilla is found only in the fully aquatic sea snakes, and this attribute appears to have evolved multiple times within this group. Our quantification of coverage as a proxy for relative ‘sensitivity’ represents the first analysis of the evolution of sensilla in the transition from terrestrial to marine habitats. However, evidence from physiological and behavioural studies is needed to confirm the functional role of scale sensilla in sea snakes and sea kraits.
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Across the diversity of vertebrates, bite force has been studied and suggested to have important ecological and evolutionary consequences. However, there is a notable lineage of vertebrates that use this performance trait yet are missing from the bite-force literature: the snakes. Snakes often rely on biting during prey subjugation and handling. Many snakes bite and hold prey while a constriction coil is formed or while venom is being delivered, or both. Others use biting exclusively without employing any additional prey-handling behaviors. In addition to biting, constriction is an important predation mechanism. Here, I quantify bite force and constriction pressure in kingsnakes (Lampropeltis getula). Furthermore, I explore the proximate determinants of bite force as well as the relationship between biting and constriction performance. Bite force increased linearly with all head and body measures. Of these, head height was the best predictor of bite force. Bite force in kingsnakes was within the range of values reported for lizards, but their relative performance was lower for their head size compared to lizards. Peak constriction pressure also increased with all body measures. Biting and constricting use 2 different parts of the musculoskeletal system and are positively and significantly correlated with one another. Future work targeting a greater diversity of snakes that rely more heavily on biting may reveal a greater range of bite performance in this diverse and successful vertebrate group. © 2016 International Society of Zoological Sciences, Institute of Zoology/Chinese Academy of Sciences and John Wiley & Sons Australia, Ltd
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To survive, organisms must avoid predation and acquire nutrients and energy. Sensory systems must correctly differentiate between potential predators and prey, and elicit behaviours that adjust distances accordingly. For snakes, strikes can serve both purposes. Vipers are thought to have the fastest strikes among snakes. However, strike performance has been measured in very few species, especially non-vipers. We measured defensive strike performance in harmless Texas ratsnakes and two species of vipers, western cottonmouths and western diamond-backed rattlesnakes, using high-speed video recordings. We show that ratsnake strike performance matches or exceeds that of vipers. In contrast with the literature over the past century, vipers do not represent the pinnacle of strike performance in snakes. Both harmless and venomous snakes can strike with very high accelerations that have two key consequences: the accelerations exceed values that can cause loss of consciousness in other animals, such as the accelerations experienced by jet pilots during extreme manoeuvres, and they make the strikes faster than the sensory and motor responses of mammalian prey and predators. Both harmless and venomous snakes can strike faster than the blink of an eye and often reach a target before it can move. © 2016 The Author(s) Published by the Royal Society. All rights reserved.
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Constriction is a prey-immobilization technique used by many snakes and is hypothesized to have been important to the evolution and diversification of snakes. However, very few studies have examined the factors that affect constriction performance. We investigated constriction performance in ball pythons (Python regius) by evaluating how peak constriction pressure is affected by snake size, sex, and experience. In one experiment, we tested the ontogenetic scaling of constriction performance and found that snake diameter was the only significant factor determining peak constriction pressure. The number of loops applied in a coil and its interaction with snake diameter did not significantly affect constriction performance. Constriction performance in ball pythons scaled differently than in other snakes that have been studied, and medium to large ball pythons are capable of exerting significantly higher pressures than those shown to cause circulatory arrest in prey. In a second experiment, we tested the effects of experience on constriction performance in hatchling ball pythons over 10 feeding events. By allowing snakes in one test group to gain constriction experience, and manually feeding snakes under sedation in another test group, we showed that experience did not affect constriction performance. During their final (10th) feedings, all pythons constricted similarly and with sufficiently high pressures to kill prey rapidly. At the end of the 10 feeding trials, snakes that were allowed to constrict were significantly smaller than their non-constricting counterparts. J. Exp. Zool. 9999A:XX-XX, 2016. © 2016 Wiley Periodicals, Inc.
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Mate, prey, and predator recognition often depend on the integration of information from multiple sensory modalities including visual, auditory, and/or olfactory inputs. In Crotalinae, the eyes sense visible light while the pit organs detect infrared (IR) radiation. Previous studies indicate that there is significant overlap between the eye and pit sensory fields and that both senses are involved in recognition processes. This study investigated the relationships between eye and pit sizes in this taxonomic group as a function of phylogeny and habitat. In view of the fact that pit orientation depends largely on snout shape, pit vipers were grouped as follows: 1) arboreal, 2) terrestrial with rounded snout, and 3) terrestrial with pointed snout. The pit orientations and habitant patterns were fully independent of the Crotalinae phylogenetic tree. The phylogenetic generalized least squares model showed that both eye and pit areas were not of significantly phylogenetic relatedness, implying alternatively a strong effect of adaptation on eye and pit sizes. Negative correlations between relative eye and pit areas in terrestrial (both pointed and rounded snouts) and arboreal species were statistically significant. Our results suggest that the eyes and pits function in a complementary fashion such that selection for IR-perception relaxes selection pressures on the visual system and selection for visual discrimination relaxes selection pressures acting on the IR-system. J. Morphol., 2015. © 2015 Wiley Periodicals, Inc.
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Almost all snakes swallow their prey whole. However, a few species are known as exceptions. Two species of Asian crab-eating snakes tear off crab legs and ingest them one at a time to eat prey that is otherwise too large. Two species of leptotyphlopid blindsnakes break off the head of termites or suck abdominal contents of termites, discarding remains of termites. Here, we show that a typhlopid blindsnake Indotyphlops braminus decapitates its termite prey and consumes only the thorax and abdomen. In our feeding trials, I. braminus decapitated a median of 47% of termites they eat, while swallowing the remaining termites whole. Decapitation did not affect ingestion speed, and therefore, it is unlikely that decapitation assists for fast ingestion. Ingested termite heads often remain undigested in the feces, implying that the decapitation functions to remove an indigestible part of termites. Decapitation might also be related to circumvention of chemical defenses of termites because termite heads often contain toxic compounds. These observations showed unusual feeding behavior used by a basal snake, which could be associated with removal of indigestible and/or toxic parts of prey items.
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The predatory behavior of rattlesnakes includes many distinctive preparatory phases leading to an extremely rapid strike, during which venom is injected. The rodent prey is then rapidly released, removing the snake's head from retaliation by the prey. The quick action of the venom makes possible the recovery of the dispatched prey during the ensuing poststrike period. The strike is usually completed in less than 0.5 s, placing a premium on an accurate strike that produces no significant errors in fang placement that could result in poor envenomation and subsequent loss of the prey. To clarify the basis for effective strike performance, we examined the basic kinematics of the rapid strike using high-speed film analysis. We scored numerous strike variables. Four major results were obtained. (1) Neurosensory control of the strike is based primarily upon sensory inputs via the eyes and facial pits to launch the strike, and upon tactile stimuli after contact. Correction for errors in targeting occurs not by a change in strike trajectory, but by fang repositioning after the jaws have made contact with the prey. (2) The rattlesnake strike is based upon great versatility and variation in recruitment of body segments and body postures. (3) Forces generated during acceleration of the head are transferred to posterior body sections to decelerate the head before contact with the prey, thereby reducing impact forces upon the snake's jaws. (4) Body acceleration is based on two patterns of body displacement, one in which acute sections of the body open like a gate, the other in which body segments flow around postural curves similar to movements seen during locomotion. There is one major implication of these results: recruitment of body segments, launch postures and kinematic features of the strike may be quite varied from strike to strike, but the overall predatory success of each strike by a rattlesnake is very consistent.
Chapter
Body elongation and limblessness have evolved significantly within Tetrapoda, typically associated with aquatic, fossorial, crevice dwelling, or grass-swimming lifestyles. Some lineages of secondarily elongate vertebrates (for example, limbless skinks) have solved the concomitant problem of reduction in size of the feeding apparatus by eating many tiny items, whereas others (for example, some caecilians) shear ingestible chunks out of large prey. Many advanced snakes achieved a third solution by radically restructuring their heads and feeding infrequently on large items; perhaps not coincidentally. Among limbless squamate reptiles, only Serpentes has achieved substantial adaptive radiation and high species richness. More than 2,500 species of living snakes inhabit most temperate and tropical land masses, and they often are prominent predators in terrestrial, arboreal, fossorial, aquatic, and even marine faunas. Snakes eat prey as different as onycophorans, fish eggs, centipedes, cormorants, and porcupines; many species commonly consume individual items weighing 20% of their own mass, and some venomous species occasionally subdue and eat prey that exceed their own mass by as much as 50%. This chapter first briefly surveys snake diversity and then examines in detail the functional and morphological aspects of capturing, swallowing, and processing prey that generally characterize relatively derived subgroups. It only touches on sensory aspects of feeding.
Chapter
The problem of the origin of snakes has been a central issue in herpetology ever since the innovative work of Cope (1869). Although the riddle appears to be rather easily solved if looked at from a somewhat superficial prespective, it must be admitted that an acceptable solution is no closer than at the beginning of this century, and while faith in the promise for progress of a purely observational approach vanishes, conceptual issues are more and more thrown into focus.
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Prey capture behavior between cottonmouths (Agkistrodon piscivorus) and Egyptian cobras (Naja haje) differ fundamentally in response to proximate factors. Cottonmouths, when presented with several mice in close succession, tended to release the first mice but hold on to later mice. Cottonmouths, too, were more deliberate in establishing coils from which to strike than the cobra. In the Egyptian cobra, there was no appreciable change in hold/release behavior through a sequence of up to 4 mice. More important was the retaliation of the mouse when struck. Egyptian cobras usually held a struck mouse, regardless of its position in the sequence, unless bitten by the mouse. Mice which bit the cobra were usually released. Cobra struck mice died more quickly if held in the jaws and the range of death rates was less than for mice released. In both species prey size was a generally important factor influencing behavior, although more so in cottonmouths. Thus, cottonmouths and Egyptian cobras share with the Palaestinian viper (Vipera palaestinae) a tendency to change hold/release behavior in response to prey size. The site along the body where a mouse was struck affected the severity of envenomation.