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Feeding in Snakes: Form, Function, and Evolution of the Feeding System
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.
... Note similarities in overall skull shape buck varying degrees of convergence amongst individual elements. Excellent reviews on the anatomy (Cundall and Irish, 2008) and function of the feeding system in snakes exist (Cundall and Greene, 2000;Moon et al., 2019), and here we will only provide a brief overview thereof. We will focus more on topics that have received relatively little attention in the literature to date such as the evolution of head shape in relation to constraints imposed by the environment (e.g., Segall et al., 2016Segall et al., , 2020. ...
... One of the main functions of the head is to allow the animal to capture and process food, and the functional morphology of feeding has been largely explored (for reviews see Cundall and Greene, 2000;Moon et al., 2019), even though some aspects of the biomechanics of feeding remain to be investigated (see Section Functional Morphology; Cundall, 2019). Yet, some snakes demonstrate a stunning exaptation of their head, and more specifically of their tongue, to attract their prey. ...
... Finally, it is crucial to consider the ecology and behavior of species at the finest possible scale (e.g., microhabitat, habitat use, diet breadth), as it provides a finer understanding of the possible adaptations and diversification of the anatomy of the head of snakes (Brecko et al., 2011;Hoso, 2017;Sherratt et al., 2018). For instance, snakes have always been considered gape limited predators that capture their prey with their mouth (Cundall and Greene, 2000;Moon et al., 2019), but some species, such as Gerarda prevostiana and Fordonia leucobalia, are able to process their prey by dismembering or chewing them (Jayne et al., 2002(Jayne et al., , 2018 and subdue their prey using their body rather than heads, such as Acrochordus (Povel and Van Der Kooij, 1997) and Cantoria violacea (Jayne et al., 2018). In conclusion, there is a need for more ecological and behavioral data to fully understand how snakes use their head and to clarify the link between its forms and functions. ...
The vertebrate head serves a diversity of functions, from energy intake to interactions with the biotic and abiotic environment. The loss of limbs in snakes placed additional selective pressures on the head as it must compensate for the functions that were fulfilled by the limbs such as manipulation, locomotion, or defense against other organisms. Rather than limiting snake diversification, selective pressures inherent to specific functions of the head allowed them to innovate, permitting the exploration of new anatomical and behavioral strategies. This chapter aims to highlight the richness in form, function, and adaptations of the head of snakes from an integrative and comparative perspective, in the light of their evolution and ecology. First, we discuss the defining features of the snake skull, followed by a review of what fossils can tell us about how snakes acquired their unique skull anatomy and the ecological origins of snakes. Next, we explore the macroevolution of skull diversity in extant snake species in the light of their ecology. From a functional perspective, * marion.segall@live.fr. § herrel@mnhn.fr. Marion Segall, Alessandro Palci, Phillip Skipwith et al. 2 we review data on the morphology and biomechanics of the head. We will then explore the relationships between external, osteological, and endocranial morphology and the sensory ecology of snakes. Finally, we will examine novel or unexplained shapes and behaviors involving the head and propose questions for future investigations.
... The evolution of venom, another novel form of subjugating prey, plays a large role in many of the more diverse snake lineages (Greene, 1997). The highly kinetic skull of snakes allows them to capture, transport, and swallow whole prey that are many times the size of the head (and in some cases, the whole snake; Kardong, 1977;Cundall and Greene, 2000;Moon et al., 2019). Several lineages have independently evolved the ability to detect and use infrared radiation as a means for finding and capturing food (de Cock Buning, 1983). ...
... With the advent of high-speed videography, the ability to finally examine the rapid snake strike revealed extremely high levels of performance. Initial descriptions of feeding strikes were primarily focused on the prey capture sequence in North American pit vipers of the genera Crotalus and Agkistrodon (Kardong, 1975;Cundall, 2002;Moon et al., 2019). Feeding on small mammals, the pit vipers exhibited stereotyped but dramatic strike performance: approximately 3 m/s velocities coupled with large gapes and rotation of the jaws allowing penetration of the fangs into the soft bodies of rodents (Kardong, 1975;Cundall, 2002). ...
... melanoleucus f behaviors and performance parameters (Figure 8): smaller approach distances (3.2 ± 2.0 cm), higher maximum velocities (2.74 ± 0.19 m/s), larger maximum gapes (84.93 ± 8.47 deg), and are most likely to make first contact with the lower jaw (MAN strikes). The species that I would classify as strikers are then Boa constrictor, Ep. cenchria, M. reticulatus (juvenile), Py. bivittatus, Py. regius (juveniles), A. contortix, as suggested by initial descriptions of strike performance in vipers (Cundall, 2002;Moon et al., 2019). However, there is room for variation in these groups, suggesting that strike performance and prey capture behavior is not as stereotyped as initial descriptions of strike performance found. ...
Integrating morphology, performance, and behavior is paramount to understanding fitness and evolution. Like many other vertebrates, snake teeth play an integral role in the capture and subjugation of prey. However, while many have investigated the shape and structure and teeth, there are few examples examining how those shape parameters of shape function during a prey capture sequence. Using a combination of high-speed video and CT scans, I integrate the shape of the teeth in 13 snake species with their function during a predatory strike. The kinematics of predatory striking add to a growing body of literature suggesting that strike performance is more variable than previously considered. Snakes fall into two broad categories of performance: high velocity, large gapes, and complex post-strike behaviors from species I am calling strikers; low velocity, small gapes, and large approach distances from species I call lungers. Tooth shape is also more variable than previously considered, with variation not only occurring amongst species, but within species and also within individual bones of a species. Most of this variation occurs at the anterior end of both jaws, where teeth may be more upright (perpendicular to the jaw), slender, and potentially
recurved. The variation in tooth shape correlates strongly with strike performance. Species in the striker category exhibit more variation in tooth shape, and are more likely to have teeth that are more upright at the anterior ends of the jaws. In some constrictors, the teeth at the anterior end of the lower jaw are upright and the teeth on the upper jaw are strongly curved posteriorly. During a strike, the upright teeth penetrate the prey and serve as a fulcrum for the rest of the skull to rotate over. The curved teeth on the upper jaw slide over the prey and ensnare it at the onset of constriction. There is also limited evidence that tooth shape changes over an ontogenetic scale, corresponding with changes in strike performance as well. There is
a clear relationship between feeding behavior and tooth morphology in snakes, and aspects of ecology, ontogeny, and evolution remain to be explored.
... Snakes are limbless animals that generally ingest prey whole using ratcheting movements of their jaws achieved by a variety of different mechanisms [1][2][3]. All are carnivorous and none uses the tongue or inertial acceleration of the whole head to move their prey through the oral cavity. ...
... Snakes turn out to be excellent examples of the diversity of evolutionary solutions to two problemscatching and subduing prey nearly as heavy as, or heavier than themselves, and then enlarging gape sufficiently to engulf the prey whole. The success of snakes in achieving both increased the diversity of prey that could be consumed and, because heavier prey provide more nutrition, decreased the time spent searching or waiting for it [3,4,11]. The evolution of macrostomy was contingent on the prior availability of larger (heavier, bulkier, or both) prey that could be caught and restrained without undue risk of severe injury. ...
... Studies of gape size and feeding performance in snakes, based on various behavioural and morphological measures, have flowered over the last 20 years and have been thoroughly reviewed [3]. Most studies have focused on caenophidian species and suggest that features of head size and shape correlate only loosely to some measures of feeding performance. ...
Snakes comprise nearly 4,000 extant species found on all major continents except Antarctica. Morphologically and ecologically diverse, they include burrowing, arboreal, and marine forms, feeding on prey ranging from insects to large mammals. Snakes are strikingly different from their closest lizard relatives, and their origins and early diversification have long challenged and enthused evolutionary biologists. The origin and early evolution of snakes is a broad, interdisciplinary topic for which experts in palaeontology, ecology, physiology, embryology, phylogenetics, and molecular biology have made important contributions. The last 25 years has seen a surge of interest, resulting partly from new fossil material, but also from new techniques in molecular and systematic biology. This volume summarises and discusses the state of our knowledge, approaches, data, and ongoing debates. It provides reviews, syntheses, new data and perspectives on a wide range of topics relevant to students and researchers in evolutionary biology, neontology, and palaeontology.
... 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). ...
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.
... 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). ...
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. ...
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.
... Within terrestrial vertebrates, snakes are the largest group of limbless, gape-limited predators, and the ∼4000 species allow for the analysis of wide variations in morphology, behavior, and diet (Uetz et al. 2021). While some types of subduing behavior have been well studied for vertebrate prey (e.g., coiling, constriction, and envenomation), how snakes feed on other unusual or well-defended prey remains poorly known (Cundall and Greene 2000;Moon et al. 2019). For example, although feeding on invertebrates is relatively common in advanced snakes (20% of snakes in the clade Caenophidia), only a small portion of snakes consume potentially dangerous invertebrate prey such as centipedes (4%), spiders (4%), scorpions (1%), and crustaceans (1%) (SquamataBase; Grundler 2020). ...
... Although many studies have investigated the diet and morphology of snakes, very little is known about how prey choice and diet interact with the integration of behavior and skull morphology for snakes that feed on unusual prey. Snake skulls are highly modified with many kinetic bones from an ancestral static amniote skull, and the ability of snakes to swallow large prey using their mobile bones is a key feature of the radiation (Gans 1961;Cundall and Greene 2000;Moon et al. 2019). Additionally, snake skulls may also be adapted for different behaviors or specialized diets, which can include elongation of the jaws in piscivorous natricine snakes (Hampton 2011), narrowing and elongation of the skull in aquatic or fossorial snakes (Savitzky 1983;Herrel et al. 2008), and large differences in tooth shape and size associated with prey properties (i.e., prey hardness) and the snakes' foraging ecology (Savitzky 1983;Britt et al. 2009;Westeen et al. 2020;Segall et al. 2022). ...
Synopsis
Feeding is a complex process that involves an integrated response of multiple functional systems. Animals evolve phenotypic integration of complex morphological traits to covary and maximize performance of feeding behaviors. Specialization, such as feeding on dangerous prey, can further shape the integration of behavior and morphology as traits are expected to evolve and maintain function in parallel. Feeding on centipedes, with their powerful forcipules that pinch and inject venom, has evolved multiple times within snakes, including the genus Tantilla. However, the behavioral and morphological adaptations used to consume this dangerous prey are poorly understood. By studying snakes with varying degrees of dietary specialization, we can test the integration of diet, morphology, and behavior to better understand the evolution of consuming difficult prey. We studied the prey preference and feeding behavior of Tantilla using the flat-headed snake (T. gracilis) and the crowned snake (T. coronata), which differ in the percentage of centipedes in their diet. We then quantified cranial anatomy using geometric morphometric data from CT scans. To test prey preference, we offered multiple types of prey and recorded snake behavior. Both species of snakes showed interest in multiple prey types, but only struck or consumed centipedes. To subdue centipedes, crowned snakes used coiling and holding (envenomation) immediately after striking, while flat-headed snakes used the novel behavior of pausing and holding onto centipedes for a prolonged time prior to the completion of swallowing. Each skull element differed in shape after removing the effects of size, position, and orientation. The rear fang was larger in crowned snakes, but the mechanical advantage of the lower jaw was greater in flat-headed snakes. Our results suggest that the integration of behavioral and morphological adaptations is important for the success of subduing and consuming dangerous prey.
... This behavior is related to an extraordinary organization of the skull that has become highly kinetic. Indeed, snakes must coordinate the movements of eight pairs of cranial bones to catch, subdue, manipulate, and swallow their prey (Cundall & Greene, 2000;Moon et al., 2019). Despite the complexity of their feeding behavior, snakes have independently adopted a wide variety of dietary preferences (gastropods, mammals, birds, crustaceans) providing an opportunity to study possible convergences in their feeding apparatus (Rhoda et al., 2020). ...
... • Foraging substrate: Feeding on the ground provides a solid substrate for the snake to support either itself or the prey during capture, subduction, manipulation, and swallowing (Moon et al., 2019). ...
The structure, composition, and shape of teeth have been related to dietary specialization in many vertebrate species, but comparative studies on snakes' teeth are lacking. Yet, snakes have diverse dietary habits that may impact the shape of their teeth. We hypothesize that prey properties, such as hardness and shape, as well as feeding behavior, such as aquatic or arboreal predation, or holding vigorous prey, impose constraints on the evolution of tooth shape in snakes. We compared the morphology of the dentary teeth of 63 species that cover the phylogenetic and dietary diversity of snakes, using 3D geometric morphometrics and linear measurements. Our results show that prey hardness, foraging substrate, and the main feeding mechanical challenge are important drivers of tooth shape, size, and curvature. Overall, long, slender, curved teeth with a thin layer of hard tissue are observed in species that need to maintain a grip on their prey. Short, stout, less curved teeth are associated with species that undergo high or repeated loads. Our study demonstrates the diversity of tooth morphology in snakes and the need to investigate its underlying functional implications to better understand the evolution of teeth in vertebrates.
... Aquatic feeding is exhibited by many squamate clades. Snakes, in particular, are known to have secondarily evolved aquatic or semiaquatic lifestyles and aquatic food uptake (Cundall & Greene, 2000;Moon et al., 2019), but several lizards have convergently acquired semiaquatic lifestyles and are capable of aquatic feeding (Carpenter, 1966;Mayes et al., 2005;Mesquita et al., 2006;Langner, 2017). ...
... The forward acceleration of the head results from fast straightening of the curved trunk and neck, and prey is captured by the closing jaws (Drummond, 1983;Alfaro, 2003) (Fig. 7.4). Previously, it had been hypothesized that underwater strikes with open jaws may be hindered by drag and may generate bow waves that displace prey, making this method of capture more challenging (Young, 1991;Vincent et al., 2005;Moon et al., 2019). However, in silico (Van Wassenbergh et al., 2009) (Fig. 7.5b, c) and experimental studies have shown that the hydrodynamic disadvantages are limited and that the head shapes of forward-striking snakes minimize the hydrodynamic constraints. ...
The Sauropsida includes the extant crocodiles, birds, turtles, lizards and snakes. With roughly 30,000 described species, it is not only the largest phylogenetic group within Amniota, but the largest extant group within all tetrapods. Like many other tetrapod branches, sauropsids have evolved many adaptations to aquatic lifestyles: from species that occasionally feed in aquatic habitats to fully aquatic forms that only rise to the water’s surface for breathing. As amniotes, sauropsids can safely be considered primarily terrestrial vertebrates and any adaptations to aquatic life and feeding can be regarded as secondary features. Sauropsids show a very broad spectrum of convergently-evolved adaptations for aquatic feeding, from crocodylian apex predators to high-performance suspension feeding birds, suction feeding in turtles and alga-scraping in marine iguanas. Adaptations for aquatic feeding in sauropsids have evolved multiple times independently, both between and within groups. For example, suction feeding has evolved independently in turtles and birds; extremely fast forward strikes by straightening of the curved postcranial vertebral column in birds and snakes; and suspension feeding in mallards, flamingoes and sea-birds. In the following sections, we summarize the diverse adaptations to aquatic feeding in crocodylians, birds, lepidosaurs and turtles and highlight convergence and homologies where appropriate.
... Older G. stehlini attain considerable body sizes and develop particularly big heads 71 , while exhibiting aggressive antipredator responses 72 . Since snakes consume ectothermic prey alive 73 71 . Lampropeltis californiae gape size could thus allow the consumption of large females but not that of males of the same size, leading to the observed differences in SVL between sexes only in invaded sites. ...
... All of this suggests that L. californiae impact probably begins with the removal of smaller individuals with narrower heads-i.e., younger lizards, smaller males and most females. Considering G. stehlini is a long-lived lizard that lives up to 10-11 years in the wild 73 , which exceeds the time since the snake arrival in some of our study sites, persisting G. stehlini populations in the invaded areas are likely constituted by a disproportionate number of few large and old individuals, most of which are probably males-supported by our own observations in the field. Therefore, unless populations in invaded areas show strong immigration rates, which is apparently not the case, they will likely become extinct. ...
When facing novel invasive predators, native prey can either go extinct or survive through exaptation or phenotypic shifts (either plastic or adaptive). Native prey can also reflect stress-mediated responses against invasive predators, affecting their body condition. Although multiple native prey are likely to present both types of responses against a single invader, community-level studies are infrequent. The invasive California kingsnake (Lampropeltis californiae) a good example to explore invasive predators’ effects on morphology and body condition at a community level, as this invader is known to locally extinct the Gran Canaria giant lizard (Gallotia stehlini) and to notably reduce the numbers of the Gran Canaria skink (Chalcides sexlineatus) and the Boettger’s gecko (Tarentola boettgeri). By comparing a set of morphological traits and body condition (i.e. body index and ectoparasite load) between invaded and uninvaded areas for the three squamates, we found clear evidence of a link between a lack of phenotypic change and extinction, as G. stehlini was the single native prey that did not show morphological shifts. On the other side, surviving C. sexlineatus and T. boettgeri exhibited phenotypic differences in several morphological traits that could reflect plastic responses that contribute to their capacity to cope with the snake. Body condition responses varied among species, indicating the potential existence of simultaneous consumptive and non-consumptive effects at a community level. Our study further highlights the importance addressing the impact of invasive predators from a community perspective in order to gain a deeper understanding of their effect in native ecosystems.
... 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). ...
... 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). ...
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.
... 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. ...
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.
... A buccal pump mechanism is used by snakes and turtles [27,[34][35][36][37][38]. Water enters the oro-pharyngeal cavity by depression cycles of the anterior tips of the mandibles and the enlargement of the oro-pharyngeal cavity produced by depression of the buccal floor (with or without lingual action in snakes). ...
Reptilia exploit a large diversity of food resources from plant materials to living mobile prey. They are among the first tetrapods that needed to drink to maintain their water homeostasis. Here were compare the feeding and drinking mechanisms in Reptilia through an empirical approach based on the available data to open perspectives in our understanding of the evolution of the various mechanisms determined in these Tetrapoda for exploiting solid and liquid food resources.
This article is part of the theme issue ‘Food processing and nutritional assimilation in animals’.
... Because limblessness and the presence of an elongated slender body have had a pervasive effect on snake biology, snakes have proved to be excellent animals for studying extreme or unusual adaptations in functional morphology (Jayne et al., 2015;Krishnan et al., 2014;Moon et al., 2019;Phadnis et al., 2019;Young et al., 2004), physiology (Goris, 2011;McCue et al., 2012;Secor, 2008;Secor & Diamond, 1998;Yoshida et al., 2020), and behavior (e.g., Catania, 2010;Jayne et al., 2002;A. K. Miller et al., 2015;Shine, 2012). ...
... This behavior is related to an 59 extraordinary organization of the skull that has become highly kinetic. Indeed, snakes must 60 coordinate the movements of eight pairs of cranial bones to catch, subdue, manipulate, and 61 swallow their prey (Cundall & Greene, 2000; Moon et al., 2019). Despite the complexity of 62 their feeding behavior, snakes have independently adopted a wide variety of dietary preferences 63 2 (gastropods, mammals, birds, crustaceans) providing an opportunity to study possible 64 convergences in their feeding apparatus (Rhoda et al., 2020). ...
1. The structure, composition, and shape of teeth have been related to dietary specialization in many vertebrate species, except snakes. Yet, snakes have diverse dietary habits that may impact the shape of their teeth. We hypothesize that prey properties, such as hardness and shape, as well as feeding behavior, such as aquatic or arboreal predation, or holding vigorous prey, impose constraints on the evolution of tooth shape in snakes. 2. We compared the morphology of the dentary teeth of 63 species that cover the phylogenetic and dietary diversity of snakes, using 3D geometric morphometrics and linear measurements. 3. Our results show that prey hardness, foraging substrate and the main mechanical challenge are important drivers of tooth shape, size, and curvature. 4. Overall, long, slender, curved teeth with a thin layer of hard tissue are observed in species that need to maintain a grip on their prey. Short, stout, less curved teeth are associated with species that undergo high or repeated loads. 5. Our study demonstrates the diversity of tooth morphology in snakes and the need to investigate its underlying functional implications to better understand the evolution of teeth in vertebrates.
... Snakes constitute a group of carnivorous tetrapods known to consume a large array of prey, including invertebrates (annelids, crustaceans, terrestrial arthropods, molluscs) and vertebrates (fish, amphibians, reptiles, birds, and mammals) (Greene, 1997). Many morphological specializations have been associated with specific types of prey, including those related to the feeding mechanisms (Cundall & Greene, 2000;Moon et al., 2019;Savitzky, 1983). Cranial adaptations to large prey size leading to increasing levels of hyperkinesis have been suggested to be present since the early evolution of Pan-Serpentes (Zaher et al., in press), whereas advanced groups of snakes present specific adaptations associated with specialized feeding mechanisms (e.g. ...
Advanced endoglyptodont snakes share a complex but homologous venom delivery system associated with the upper jaw and its dentition. Recently, a remarkable novel lower jaw venom delivery system was described for the Neotropical dipsadine radiation of goo-eating snakes. While most dipsadines are opistoglyphous and exhibit large, mainly serous venom glands associated with the upper jaw and supralabial glands, goo-eating dipsadine snakes are aglyphous and lack serous upper labial venom glands. Here, we provide new morphological and histological information on the oral glands and maxillary dentition of representatives of the major lineages of dipsadines that help trace the evolutionary steps that shaped the venom delivery system of dipsadines. We performed a maximum likelihood analysis on a molecular dataset that includes 443 terminals and seven loci. Our results show that goo-eating dipsadines form a monophyletic assemblage that includes the genus Adelphicos for the first time, along with Geophis, Atractus, Ninia, Chersodromus, Tropidodipsas, Sibon, and Dipsas. We also provide the first evidence of a complete shift from an upper jaw to a lower jaw venom delivery system associated with their specialized feeding behaviour. Unlike other dipsadines who exhibit typical endoglyptodont anteroposteriorly ridged posterior maxillary teeth, goo-eating dipsadines have uniform lateromedially ridged teeth throughout their maxilla. Our results indicate that the loss of the endoglyptodont venom delivery system occurred in the most recent common ancestor of goo-eating dipsadines, probably resulting from the loss of the embryonic posterior maxillary lamina responsible for the development of the venom delivery system.
... This behavior is related to an extraordinary organization of the skull that has become highly kinetic. Indeed, snakes must coordinate the movements of 8 pairs of cranial bones to catch, subdue, manipulate, and swallow their prey [12,13]. Despite the complexity of their feeding behavior, snakes have independently adopted a wide variety of dietary preferences (insects, mammals, birds, crustaceans) providing an opportunity to highlight convergences in their feeding apparatus [14]. ...
Teeth are one of the most studied hard tissues in vertebrates. Their structure, composition and shape are related to dietary specialization in many species. At first glance, snake teeth all look similar; conical, sharp, curved. Yet, snakes, like other vertebrates, have very diverse diets that may have affected their shape. We compared the morphology of the teeth of 63 species that cover both the phylogenetic and dietary diversity of snakes. We predicted that prey properties play a role in shaping snakes teeth along with their feeding behavior. Limblessness combined to the peculiar feeding behavior of snakes impose strong functional constraints on their teeth, especially during arboreal or aquatic feeding. Our results show that prey hardness, foraging substrate and the main feeding constraint are drivers of tooth shape, size, and curvature. We highlight two main morphotypes: long, slender, curved with a thin layer of hard tissue for snakes that need a good grip on their prey and short, stout, less curved teeth in snakes that eat hard or long prey. Our study demonstrates the diversity of tooth morphology in snakes and the need to investigate the underlying functional implications to better understand the evolution of teeth in vertebrates.
... We then performed a linear regression between body size and maximum bite force by plotting maximum bite force of individuals (SigmaPlot 11.0, Systat Software, Palo Alto, California, USA). We also investigated scaling of relevant morphometrics and bite force using standard practices in scaling literature (Herrel and O'Reilly, 2005;Penning, 2017;Moon et al., 2019) using Microsoft Excel 2012. ...
Alligator Snapping Turtles (Macrochelys temminckii) possess unique head morphology that suggests strong natural selection for bite performance, which likely influences foraging and prey selection, as well as the outcomes of intrasexual aggressive encounters, mating, and defense against predators. Therefore, bite performance has the potential to directly and indirectly impact fitness. In this study, we assessed the effects of captivity on bite force by comparing the performance of captive and reintroduced M. temminckii. On average, free-ranging M. temminckii bite with greater force than do individuals residing in captivity, and captive individuals housed under seminatural conditions in outdoor ponds outperformed those housed indoors. Further, we found that free-ranging M. temminckii released into different river systems performed comparably and required less provocation than captives to display gaping and biting behavior. It remains to be determined whether the observed performance differences were more strongly influenced by physiological limitations on muscle performance or by behavioral variation in motivation to bite with maximum force.
... 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). ...
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. ...
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
... 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]. ...
Background:
Scorpions can use their pincers and/or stingers to subdue and immobilize their prey. A scorpion can thus choose between strategies involving force or venom, or both, depending on what is required to subdue its prey. Scorpions vary greatly in the size and strength of their pincers, and in the efficacy of their venom. Whether this variability is driven by their defensive or prey incapacitation functionis unknown. In this study, we test if scorpion species with different pincer morphologies and venom efficacies use these weapons differently during prey subjugation. To that end, we observed Opisthacanthus elatus and Chactas sp. with large pincers and Centruroides edwardsii and Tityus sp. with slender pincers.
Methods:
The scorpion pinch force was measured, and behavioral experiments were performed with hard and soft prey (Blaptica dubia and Acheta domesticus). Stinger use, sting frequency and immobilization time were measured.
Results:
We found that scorpions with large pincers such as O. elatus produce more force and use the stinger less, mostly subjugating prey by crushing them with the pincers. In C. edwardsii and Tityus sp. we found they use their slender and relatively weak pincers for holding the prey, but seem to predominantly use the stinger to subjugate them. On the other hand, Chactas sp. uses both strategies although it has a high pinch force.
Conclusions:
Our results show that scorpionspecies with massive pincers and high pinch force as O. elatus use the stinger less for prey subjugation than scorpionspecies with slenderpincers.
... 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). ...
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.
... 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). ...
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.
... The mousehole snake is a colubrid endemic to Argentina and abundant in both grassland and forest plantations (Giraudo and Scrocchi 2002). It has been proposed that snakes may find nests using cues such as parental activity (Skutch 1985), chemo and/or heat reception (Marini and Melo 1998, Bonnet et al. 1999, Daghfous et al. 2012, and nestling movement and/or begging calls (Stake et al. 2005, Moon et al. 2019. Nests with nestlings may be easier to locate as they emanate more heat and scents than eggs (Bonnet et al. 1999). ...
... 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). ...
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.
... 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). ...
Feeding and breathing are two functions vital to the survival of all vertebrate species. Throughout the evolution, vertebrates living in different environments have evolved drastically different modes of feeding and breathing through utilizing diversified orofacial and pharyngeal (oropharyngeal) muscles. The oropharyngeal structures are controlled by hindbrain neural circuits. The developing hindbrain shares strikingly conserved organizations and gene expression patterns across vertebrates, thus begs the question of how a highly conserved hindbrain generates circuits subserving diverse feeding/breathing patterns. In this review, we summarize major modes of feeding and breathing and principles underlying their coordination in many vertebrate species. We provide a hypothesis for the existence of a common hindbrain circuit at the phylotypic embryonic stage controlling oropharyngeal movements that is shared across vertebrate species; and reconfiguration and repurposing of this conserved circuit give rise to more complex behaviors in adult higher vertebrates.SIGNIFICANCE STATEMENTUnderstanding how a highly conserved hindbrain generates diverse feeding/breathing patterns is important for elucidating neural mechanisms underlying the execution and coordination of these two vital behaviors. Here, we first briefly summarize key modes of vertebrates feeding/breathing, discuss main principles coordinating feeding/breathing, and provide a unifying hypothesis for the existence of a shared oropharyngeal movement control circuit across species. By synthesizing behavior, structural and neural mechanisms for feeding/breathing functions across evolution, we believe that this review and our hypothesis can open new research avenues for elucidating the precise hindbrain circuits controlling feeding, breathing and other oropharyngeal functions.
... 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. ...
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.
... 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. ...
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.
Reportamos el primer evento de depredación del Basilisco de cabeza roja (Basiliscus galeritus) por la serpiente bejuquilla (Imantodes cenchoa) en un bosque húmedo tropical en Colombia. Este nuevo registro contribuye a una mejor comprensión de la historia natural y la ecología trófica de dos especies de reptiles en su interacción depredador-presa.
Snake strikes are some of the most rapid accelerations in terrestrial vertebrates. Generating rapid body accelerations requires high ground reaction forces, but on flat surfaces snakes must rely on static friction to prevent slip. We hypothesize that snakes may be able to take advantage of structures in the environment to prevent their body from slipping, potentially allowing them to generate faster and more forceful strikes. To test this hypothesis, we captured high-speed video and forces from defensive strikes of juvenile blood pythons (Python brongersmai) on a platform that was either open on all sides or with two adjacent walls opposite the direction of the strike. Contrary to our predictions, snakes maintained high performance on open platforms by imparting rearward momentum to the posterior body and tail. This compensatory behavior increases robustness to changes in their strike conditions and could allow them to exploit variable environments.
Snakes comprise nearly 4,000 extant species found on all major continents except Antarctica. Morphologically and ecologically diverse, they include burrowing, arboreal, and marine forms, feeding on prey ranging from insects to large mammals. Snakes are strikingly different from their closest lizard relatives, and their origins and early diversification have long challenged and enthused evolutionary biologists. The origin and early evolution of snakes is a broad, interdisciplinary topic for which experts in palaeontology, ecology, physiology, embryology, phylogenetics, and molecular biology have made important contributions. The last 25 years has seen a surge of interest, resulting partly from new fossil material, but also from new techniques in molecular and systematic biology. This volume summarises and discusses the state of our knowledge, approaches, data, and ongoing debates. It provides reviews, syntheses, new data and perspectives on a wide range of topics relevant to students and researchers in evolutionary biology, neontology, and palaeontology.
The advanced snakes (Alethinophidia) include the extant snakes with a highly evolved head morphology providing increased gape and jaw flexibility. Along with other physiological and morphological adaptations, this allows them to immobilize, ingest, and transport prey that may be disproportionately large or presents danger to the predator from bites, teeth, horns, or spines. Reported incidents of snakes failing to consume prey and being injured or killed during feeding mostly reflect information in the form of natural‐history notes. Here we provide the first extensive review of such incidents, including 101 publications describing at least 143 cases of mortality (including six of ‘multiple individuals’) caused by ingestion or attempted consumption of injurious prey. We also report on 15 previously unpublished injurious feeding incidents from the USA, Austria, and Bulgaria, including mortality of five juvenile piscivorous dice snakes (Natrix tessellata) from a single location. Occurrences are spread across taxa, with mortality documented for at least 73 species from eight families and 45 genera. Incidents were generally well represented within each of three major categories: oversized prey (40.6%), potentially harmful prey (40.6%), and predator's behavioural/mechanical errors (18.9%). Reptile (33%) and fish (26%) prey caused disproportionately high mortality compared to mammals (16%). Feeding can be dangerous throughout a snake's life, with the later stages of feeding likely being more perilous. The number of reports has increased over time, and the data seem biased towards localities with a higher number of field‐working herpetologists. We propose a standardized framework, comprising a set of basic information that should ideally be collected and published, and which could be useful as a template for future data collection, reporting, and analyses. We conclude that incidents of mortality during feeding are likely to be more common than previously assumed, and this hypothesis has implications for the ecology of persistence where populations are impacted by changing trophic environments.
Snakes play a very important role in our ecosystem. They help in balancing the
food web, regulating the population of their prey, and thereby controlling pests.
They also exhibit both predator and prey characteristics and help in maintaining
biodiversity on Earth for future sustainable development. This book highlights the
extreme ecological importance of snakes with chapters on snake venom and its
therapeutic potential and the ecology of some selected snake species.
Understanding the ecology of species at risk is extremely important for their conservation and management. Due to land clearing for urban expansion, agriculture , and the import of pets, several snake species including the red-tongue viper (Gloydius ussuriensis) on Jeju Island of South Korea, have become threatened. We studied morphology, distribution, habitat characteristics, diet, and reproduction of red-tongue viper to provide a higher understanding of species ecology. This species on average reach 242-580 mm snout-vent length and is found in a wide range of habitat from mountain forest to lowland areas. Adult snakes prey almost entirely on amphibians followed by mammals and centipedes. The mating usually takes place in spring and birth takes place in autumn. This study points out the major threats and ill-information if addressed will not only contribute to the conservation efforts but also improve the negative attitudes that people hold toward these fascinating animals. The ecological data of G. ussuriensis herein provides basic information which assists in designing the management technique for conservation. Similar applications may be generalized and used to other vulnerable species to detect and quantify population ecology and risks, bolstering conservation methods that can be used to optimize the efficacy of conservation measures.
Prior to both offensive and defensive striking, snakes can display notable differences in prestrike behaviors between offensive and defensive contexts. However, few studies have investigated strike movements during the different scenarios with which snakes are faced. To better understand how snakes strike, we measured the strikes of Western Ratsnakes (Pantherophis obsoletus; N = 11) presented with two different targets: one simulated predator (a gloved human hand) and one prey (pre-killed mice). For each strike, we recorded strike distance, duration, velocity (average and peak), acceleration (average and peak), and time to start mouth gape. In both encounters, ratsnakes displayed similar time to the initiation of a mouth gape while all peak performances were significantly different between strike types with performances being higher in defensive strikes. Defensive strikes took longer (mean = 122 ± 13 ms), reached greater distances (mean = 15.1 ± 1.7 cm), had higher maximum velocities (mean = 1.80 ± 0.11 ms⁻¹), and maximum accelerations (mean = 101.4 ± 15.2 ms⁻²). Offensive strikes had much shorter durations (mean = 49 ± 5 ms), distances (mean = 4.3 ± 0.6 cm), maximum velocities (mean = 1.06 ± 0.10 ms⁻¹), and maximum accelerations (mean = 81.4 ± 18.9 ms⁻²). The results for average performance measurements are similar to those for the maximum performance comparisons. Our results show that snakes can recognize and differentiate prey from threats and respond differently in each situation. Our results also show that predatory and defensive strikes are quantitatively and situationally distinct, should be treated as separate behaviors, and therefore should be evaluated and analyzed separately from one another.
The outcomes of predator-prey interactions between endotherms and ectotherms can be heavily influenced by environmental temperature, owing to the difference in how body temperature affects locomotor performance. However, as elastic energy storage mechanisms can allow ectotherms to maintain high levels of performance at cooler body temperatures, detailed analyses of kinematics are necessary to fully understand how changes in temperature might alter endotherm-ectotherm predator-prey interactions. Viperid snakes are widely distributed ectothermic mesopredators that interact with endotherms both as predator and prey. Although there are numerous studies on the kinematics of viper strikes, surprisingly few have analyzed how this rapid movement is affected by temperature. Here we studied the effects of temperature on the predatory strike performance of rattlesnakes (Crotalus spp.), abundant new world vipers, using both field and captive experimental contexts. We found that the effects of temperature on predatory strike performance are limited, with warmer snakes achieving slightly higher maximum strike acceleration, but similar maximum velocity. Our results suggest that, unlike defensive strikes to predators, rattlesnakes may not attempt to maximize strike speed when attacking prey, and thus the outcomes of predatory strikes may not be heavily influenced by changes in temperature.
As body size strongly determines the biology of an organism at all levels, it can be expected that miniaturization comes with substantial structural and functional constraints. Dwarf snakes of the genus Eirenis are derived from big, surface‐dwelling ancestors, considered to be similar to those of the sister genus Dolichophis. To better understand the structural implications of miniaturization on the feeding apparatus in Eirenis, the morphology of the cranial musculoskeletal system of Dolichophis schmidti was compared with that of the miniature Eirenis punctatolineatus and E. persicus using high‐resolution µCT data. The gape index was compared between D. schmidti and 14 Eirenis species. Our results show a relatively increased neurocranium size and decreased maximal jaw muscle force in E. persicus, compared with the D. schmidti, and an intermediate situation in E. punctatolineatus. A significant negative allometry in gape index relative to body size is observed across the transition from the Dolichophis to Pediophis and Eirenis subgenera. However, the gape index relative to head size showed a significant negative allometry only across the transition from the Dolichophis to Pseudocyclophis subgenus. In Dolichophis–Eirenis dwarfing lineages, different structural patterns are observed through miniaturization, indicating that overcoming the challenge of miniaturization has achieved via different adaptations. Dwarf snakes of the genus Eirenis are derived from big, surface dwelling ancestors, considered to be similar to the genus Dolichophis. In Dolichophis–Eirenis dwarfing lineages, different structural implications of miniaturization on the feeding apparatus are observed, indicating that overcoming the challenge of miniaturization has achieved via different adaptations.
Phenotypic diversity, or disparity, can be explained by simple genetic drift or, if functional constraints are strong, by selection for ecologically relevant phenotypes. We here studied phenotypic disparity in head shape in aquatic snakes. We investigated whether conflicting selective pressures related to different functions have driven shape diversity and explore whether similar phenotypes may give rise to the same functional output (i.e., many‐to‐one mapping of form to function). We focused on the head shape of aquatically foraging snakes as they fulfill several fitness‐relevant functions and show a large amount of morphological variability. We used 3D surface scanning and 3D geometric morphometrics to compare the head shape of 62 species in a phylogenetic context. We first tested whether diet specialization and size are drivers of head shape diversification. Next, we tested for many‐to‐one mapping by comparing the hydrodynamic efficiency of head shape characteristic of the main axes of variation in the dataset. We 3D printed these shapes and measured the forces at play during a frontal strike. Our results show that diet and size explain only a small amount of shape variation. Shapes did not fully functionally converge as more specialized aquatic species evolved a more efficient head shape than others. The shape disparity observed could thus reflect a process of niche specialization.
Phenotypic diversity, or disparity, can be explained by simple genetic drift or, if functional constraints are strong, by selection for ecologically relevant phenotypes. We here studied phenotypic disparity in head shape in aquatic snakes. We investigated whether conflicting selective pressures related to different functions have driven shape diversity and explore whether similar phenotypes may give rise to the same functional output (i.e. many-to-one mapping of form to function). We focused on the head shape of aquatically foraging snakes as they fulfil several fitness-relevant functions and show a large amount of morphological variability. We used 3D surface scanning and 3D geometric-morphometrics to compare the head shape of 62 species in a phylogenetic context. We first tested whether diet specialization and size are drivers of head shape diversification. Next, we tested for many-to-one mapping by comparing the hydrodynamic efficiency of head shapes characteristic of the main axis of variation in the dataset. We 3D printed these shapes and measured the forces at play during a frontal strike. Our results show that diet and size explain only a small amount of shape variation. Shapes did not functionally converge as more specialized aquatic species evolved a more efficient head shape than others. The shape disparity observed could thus reflect a process of niche specialization under a stabilizing selective regime.
The ecological origin of snakes remains amongst the most controversial topics in evolution, with three competing hypotheses: fossorial; marine; or terrestrial. Here we use a geometric morphometric approach integrating ecological, phylogenetic, paleontological, and developmental data for building models of skull shape and size evolution and developmental rate changes in squamates. Our large-scale data reveal that whereas the most recent common ancestor of crown snakes had a small skull with a shape undeniably adapted for fossoriality, all snakes plus their sister group derive from a surface-terrestrial form with non-fossorial behavior, thus redirecting the debate toward an underexplored evolutionary scenario. Our comprehensive heterochrony analyses further indicate that snakes later evolved novel craniofacial specializations through global acceleration of skull development. These results highlight the importance of the interplay between natural selection and developmental processes in snake origin and diversification, leading first to invasion of a new habitat and then to subsequent ecological radiations.
Across ecosystems and trophic levels, predators are usually larger than their prey, and when trophic morphology converges, predators typically avoid predation on intraguild competitors unless the prey is notably smaller in size. However, a currently unexplained exception occurs in kingsnakes in the genus Lampropeltis. Kingsnakes are able to capture, constrict and consume other snakes that are not only larger than themselves but that are also powerful constrictors (such as ratsnakes in the genus Pantherophis). Their mechanisms of success as intraguild predators on other constrictors remain unknown. To begin addressing these mechanisms, we studied the scaling of muscle cross-sectional area, pulling force and constriction pressure across the ontogeny of six species of snakes (Lampropeltis californiae, L. getula, L. holbrooki, Pantherophis alleghaniensis, P. guttatus and P. obsoletus). Muscle cross-sectional area is an indicator of potential force production, pulling force is an indicator of escape performance, and constriction pressure is a measure of prey-handling performance. Muscle cross-sectional area scaled similarly for all snakes, and there was no significant difference in maximumpulling force among species. However, kingsnakes exerted significantly higher pressures on their prey than ratsnakes. The similar escape performance among species indicates that kingsnakes win in predatory encounters because of their superior constriction performance, not because ratsnakes have inferior escape performance. The superior constriction performance by kingsnakes results from their consistent and distinctive coil posture and perhaps from additional aspects of muscle structure and function that need to be tested in future research.
Constriction is an evolutionarily and functionally important behavior that many snakes use to subdue a variety of prey. However, little work has examined the effects of prey size on constriction performance. Furthermore, many snakes are known to feed even while previously consumed prey remain in the stomach. This temporary increase in mass may place constraints on subsequent performance. To test these effects, I investigated constriction performance in eastern kingsnakes Lampropeltis getula handling different sizes and quantities of rodent prey in two experiments by measuring coil length and peak constriction pressure. In the first experiment, constriction coil length and peak constriction pressure did not differ significantly between snakes feeding on either ‘small’ (5% relative prey mass, RPM) or ‘large’ (15% RPM) rodent prey. However, there was a significant interaction between prey size and repeated feeding. Snakes that had previously consumed large meals had significantly shorter coil lengths and lower peak constriction pressures when fed for a second time (reductions of 60 and 51%, respectively). In Experiment 2, snakes offered five sequential, similarly sized prey (@ 7% RPM), showed a regular decrease in coil length and peak constriction pressure across sequential feeding trials. During the final (fifth) trials, snakes used 45.7% shorter coils and exerted 50.1% lower peak constriction pressures. Thus, prey size alone did not affect constriction performance, but predation performance was significantly affected by the prior consumption of prey ≥7% RPM, and performance was further reduced during additional feeding trials.
Predation plays a central role in the lives of most organisms. Predators must find and subdue prey to
survive and reproduce, whereas prey must avoid predators to do the same. The resultant antagonistic
coevolution often leads to extreme adaptations in both parties. Few examples capture the imagination
like a rapid strike from a venomous snake. However, almost nothing is known about strike performance
of viperid snakes under natural conditions. We obtained high-speed (500 fps) three-dimensional video
in the field (at night using infrared lights) of Mohave rattlesnakes (Crotalus scutulatus) attempting to
capture Merriam’s kangaroo rats (Dipodomys merriami). Strikes occurred from a range of distances
(4.6 to 20.6 cm), and rattlesnake performance was highly variable. Missed capture attempts resulted
from both rapid escape maneuvers and poor strike accuracy. Maximum velocity and acceleration of
some rattlesnake strikes fell within the range of reported laboratory values, but some far exceeded
most observations. Thus, quantifying rapid predator-prey interactions in the wild will propel our
understanding of animal performance.
Macrostomy is the anatomical feature present in macrostomatan snakes that permits the ingestion of entire prey with high cross-sectional area. It depends on several anatomical traits in the skeleton and soft tissues, of which the elongation of gnathic complex and backward rotation of the quadrate represent crucial skeletal requirements. Here, the relevance of postnatal development of these skull structures and their relationship with macrohabitat and diet are explored. Contrary to the condition present in lizards and basal snakes that occupy underground macrohabitats, elements of the gnathic complex of most macrostomatan snakes that exploit surface macrohabitats display conspicuous elongation during postnatal growth, relative to the rest of the skull, as well as further backward rotation of the quadrate bone. Remarkably, several clades of small cryptozoic macrostomatans reverse these postnatal transformations and return to a diet based on prey with low cross-sectional area such as annelids, insects or elongated vertebrates, thus resembling the condition present in underground basal snakes. Dietary ontogenetic shift observed in most macrostomatan snakes is directly linked with this ontogenetic trajectory, indicating that this shift is acquired progressively as the gnathic complex elongates and the quadrate rotates backward during postnatal ontogeny. The numerous independent events of reversion in the gnathic complex and prey type choice observed in underground macrostomatans and the presence of skeletal requirements for macrostomy in extinct non-macrostomatan species reinforce the possibility that basal snakes represent underground survivors of clades that had the skeletal requirements for macrostomy. Taken together, the data presented here suggest that macrostomy has been shaped during multiple episodes of occupation of underground and surface macrohabitats throughout the evolution of snakes.
Snake venoms represent an adaptive trophic response to the challenges confronting a limbless predator for overcoming combative prey, and this chemical means of subduing prey shows several dominant phenotypes. Many front-fanged snakes, particularly vipers, feed on various vertebrate and invertebrate prey species, and some of their venom components (e.g., metalloproteinases, cobratoxin) appear to have been selected for "broad-brush" incapacitation of different prey taxa. Using proteomic and genomic techniques, the compositional diversity of front-fanged snakes is becoming well characterized; however, this is not the case for most rear-fanged colubroid snakes. Because these species consume a high diversity of prey, and because venoms are primarily a trophic adaptation, important clues for understanding specific selective pressures favoring venom component composition will be found among rear-fanged snake venoms. Rear-fanged snakes typically (but not always) produce venoms with lower complexity than front-fanged snakes, and there are even fewer dominant (and, arguably, biologically most relevant) venom protein families. We have demonstrated taxon-specific toxic effects, where lizards and birds show high susceptibility while mammals are largely unaffected, for both Old World and New World rear-fanged snakes, strongly indicating a causal link between toxin evolution and prey preference. New data are presented on myotoxin a, showing that the extremely rapid paralysis induced by this rattlesnake toxin is specific for rodents, and that myotoxin a is ineffectual against lizards. Relatively few rear-fanged snake venoms have been characterized, and basic natural history data are largely lacking, but directed sampling of specialized species indicates that novel compounds are likely among these specialists, particularly among those species feeding on invertebrate prey such as scorpions and centipedes. Because many of the more than 2200 species of colubroid snakes are rear-fanged, and many possess a Duvernoy's venom gland, understanding the nature of their venoms is foundational to understanding venom evolution in advanced snakes.
Background:
With over 3,500 species encompassing a diverse range of morphologies and ecologies, snakes make up 36% of squamate diversity. Despite several attempts at estimating higher-level snake relationships and numerous assessments of generic- or species-level phylogenies, a large-scale species-level phylogeny solely focusing on snakes has not been completed. Here, we provide the largest-yet estimate of the snake tree of life using maximum likelihood on a supermatrix of 1745 taxa (1652 snake species + 7 outgroup taxa) and 9,523 base pairs from 10 loci (5 nuclear, 5 mitochondrial), including previously unsequenced genera (2) and species (61).
Results:
Increased taxon sampling resulted in a phylogeny with a new higher-level topology and corroborate many lower-level relationships, strengthened by high nodal support values (> 85%) down to the species level (73.69% of nodes). Although the majority of families and subfamilies were strongly supported as monophyletic with > 88% support values, some families and numerous genera were paraphyletic, primarily due to limited taxon and loci sampling leading to a sparse supermatrix and minimal sequence overlap between some closely-related taxa. With all rogue taxa and incertae sedis species eliminated, higher-level relationships and support values remained relatively unchanged, except in five problematic clades.
Conclusion:
Our analyses resulted in new topologies at higher- and lower-levels; resolved several previous topological issues; established novel paraphyletic affiliations; designated a new subfamily, Ahaetuliinae, for the genera Ahaetulla, Chrysopelea, Dendrelaphis, and Dryophiops; and appointed Hemerophis (Coluber) zebrinus to a new genus, Mopanveldophis. Although we provide insight into some distinguished problematic nodes, at the deeper phylogenetic scale, resolution of these nodes may require sampling of more slowly-evolving nuclear genes.
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.
This study aimed at evaluating the energetic return and feeding time on Philodryas nattereri kept in captivity. Snakes were fed biweekly for 60 days (four feeding trials), in two different feeding treatments (single and multiple prey items). The energetic return revealed no significant difference between the feeding treatments; however, we found a negative relationship between snake size and prey handling time during a feed using multiple prey items. In P. nattereri, when large preys are as easy to find as small ones, there seems to be no difference in energetic return.
To accommodate the pronounced metabolic response to digestion, pythons increase heart rate and elevate stroke volume, where the latter has been ascribed to a massive and fast cardiac hypertrophy. However, numerous recent studies show that heart mass rarely increases, even upon ingestion of large meals, and we therefore explored the possibility that a rise in mean circulatory filling pressure (MCFP) serves to elevate venous pressure and cardiac filling during digestion. To this end, we measured blood flows and pressures in anaesthetized Python regius. The anaesthetized snakes exhibited the archetypal tachycardia as well as a rise in both venous pressure and MCFP that fully account for the approximate doubling of stroke volume. There was no rise in blood volume and the elevated MCFP must therefore stem from increased vascular tone, possibly by means of increased sympathetic tone on the veins. Furthermore, although both venous pressure and MCFP increased during volume loading, there was no evidence that postprandial hearts were endowed with an additional capacity to elevate stroke volume. In vitro measurements of force development of paced ventricular strips also failed to reveal signs of increased contractility, but the postprandial hearts had higher activities of cytochrome oxidase and pyruvate kinase, which probably serves to sustain the rise in cardiac work during digestion.
We studied the effects of relative prey mass and experience on prey-handling behaviors of 16 ingestively naïve Corn Snakes (Pantherophis guttatus) feeding on different categorical sizes of live House Mice (Mus musculus) over 11 feeding trials. We randomly assigned hatchlings to two categories of prey mass, relative to snake mass (small = 20–40% and large = 41–60%), and analyzed the effects of prey mass on capture position, prey-handling method, time to subdue prey, condition of prey at ingestion, direction of ingestion, and duration of ingestion. Prey mass significantly affected prey-handling behaviors. As snakes experienced larger prey, they used more complex prey-handling behaviors (hairpin loops and constriction). Snakes that had prior large-prey experience maintained constant subduing times across feeding trials, whereas snakes that had prior experience with small prey showed an increase in subduing time across trials. Snakes feeding on large prey took longer to ingest prey than snakes feeding on small prey; however, as snakes gained feeding experience, they maintained relatively constant ingestion times across trials. All snakes employed complex prey-handling behaviors prior to the point at which the prey could vigorously defend themselves, suggesting an advantage to employing complex behaviors before they are necessary. When prey reached a certain absolute size, all were constricted and killed, regardless of prior experience or relative prey size.
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.
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
We investigated the gross anatomy, histology and ultrastructure of Duvernoy's glands and scanning electron microscopy of maxillary teeth of Helicops modestus, as well as its prey-handling behavior in laboratory. We later compared this histology with other species of Hydropsini. Duvernoy's glands are located in the post-ocular region, immediately behind the supralabial gland. Each gland is connected to a pair of ungrooved rear fangs by a vestibule from which the secretion is drained. Histological analysis showed that the gland is wrapped by a layer of connective tissue and consists of a glandular body formed by prismatic cells organized in acini and a duct lined with columnar cells. The prismatic cells are positive to PAS and bromophenol blue, indicating glycoprotein content, whereas the columnar ductal cells are positive to PAS and alcian blue pH 2.5, indicating the presence of acid mucous. Transmission electron microscopy showed electron-dense, heterogeneous granules in the prismatic cells, whereas the granules of the columnar cells were electron-luscent and homogeneous. The Duvernoy's glands of H. modestus are more similar to those of H. angulatus than any other species analyzed. Observations of prey-handling behavior showed that H. modestus strikes and holds fish in its mouth while repeatedly carrying out bilateral raking motions with both maxillae. Ingestion starts headfirst. We observed only a single episode of constriction. Snakes usually swallowed fish alive but clearly immobilized, suggesting that the primary function of the Duvernoy's secretion is associated with the quiescence/immobilization of the fish prey.
The use of high-speed puncture mechanics for prey capture has been documented across a wide range of organisms, including vertebrates, arthropods, molluscs and cnidarians. These examples span four phyla and seven orders of magnitude difference in size. The commonality of these puncture systems offers an opportunity to explore how organisms at different scales and with different materials, morphologies and kinematics perform the same basic function. However, there is currently no framework for combining kinematic performance with cutting mechanics in biological puncture systems. Our aim here is to establish this framework by examining the effects of size and velocity in a series of controlled ballistic puncture experiments. Arrows of identical shape but varying in mass and speed were shot into cubes of ballistic gelatine. Results fromhigh-speed videography showthat projectile velocity can alter how the target gel responds to cutting. Mixed models comparing kinematic variables and puncture patterns indicate that the kinetic energy of a projectile is a better predictor of penetration than either momentum or velocity. These results form a foundation for studying the effects of impact on biological puncture, opening the door for future work to explore the influence of morphology and material organization on high-speed cutting dynamics. © 2016 The Author(s) Published by the Royal Society. All rights reserved.
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.
Snakes are a highly successful group of vertebrates, within great diversity in habitat, diet, and morphology. The unique adaptations for the snake skull for ingesting large prey in more primitive macrostomatan snakes have been well documented. However, subsequent diversification in snake cranial shape in relation to dietary specializations has rarely been studied (e.g. piscivory in natricine snakes). Here we examine a large clade of snakes with a broad spectrum of diet preferences to test if diet preferences are correlated to shape variation in snake skulls. Specifically, we studied the Xenodontinae snakes, a speciose clade of South American snakes, which show a broad range of diets including invertebrates, amphibians, snakes, lizards, and small mammals. We characterized the skull morphology of 19 species of xenodontine snakes using geometric morphometric techniques, and used phylogenetic comparative methods to test the association between diet and skull morphology. Using phylogenetic partial least squares analysis (PPLS) we show that skull morphology is highly associated with diet preferences in xenodontine snakes.
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.
We examined morphological differences in cranium size and shape between closely related snake species, Natrix natrix and Natrix tessellata (Natricinae, Colubroidea), as well as variation within species. These two snake species have similar ecology and habitat preferences but differ in feeding strategies. Our hypothesis was that divergence in size and shape of cranial elements between species depends on their functional role and anatomical relationships. To analyse complex, kinetic crania, we applied computed microtomography and 3D geometric morphometrics. We analysed size and shape of six cranial elements separately. We selected two “non-trophic” structures (akinetic braincase and mobile nasals) and four movable “trophic” skeletal elements (maxillae, quadrates, pterygoids and compound bones) which are involved in prey capture and swallowing. Our results showed that N. natrix and N. tessellata significantly differ in size and shape of all analysed cranial elements. In both species, cranium is significantly larger in females than in males. To account for possible differences in shape due to differences in size, we estimated allometric and non-allometric component of shape variation. For all elements, except nasals, allometry accounted for a significant proportion of the variance in shape. The analysis of non-allometric component of shape variation revealed significant dimorphism in shape of the braincase and maxilla between N. tessellata females and males, and marginally significant sexual dimorphism in shape of maxilla in N. natrix. These results indicated that sexual dimorphism in skull shape is species specific and not entirely caused by selection for larger size in females.
Allometric growth is one of the dominant factors of morphological variation, although this issue is still poorly explored. Using geometric morphometrics, we evaluated and described the ontogenetic allometry in the skull of the snake Hydrodynastes gigas. Furthermore, we described the skull morphology of the species and compared it with its congener, H. bicinctus. We found that 46.91 % of shape variation was explained by allometry: smaller centroid sizes were mostly correlated to short postorbital process, medial region of frontals elongated, shortened nasals and elongated parietal, and shortened/oblique supratemporals in relation to the anteroposterior axis of the skull; larger centroid sizes point mainly to postorbital process elongated, elongated nasals and shortened parietals, posterior region of parietal strongly tapered, and elongated/parallel supratemporals in relation to the anteroposterior axis of the skull. In general aspect, the skull of H. gigas differs from the skull of H. bicinctus by being less dorsoventrally compressed. Comparisons between our results and the results of other studies which considered allometry in specific bones of snakes’ skull showed some common patterns, although we found a different correlation between parietal and skull length. These results reinforce the importance of further studies to evaluate the existence of recurrent patterns of allometric growth in the skull of other representatives of this group of snakes. Moreover, the analyses presented herein revealed a significant ontogenetic allometry in the skull of H. gigas and represent the first approach of geometric morphometrics with this goal for snakes.
Low temperature reduces the performance of muscle-powered movements, but in movements powered by elastic-recoil mechanisms, this effect can be mitigated and performance can be increased. To better understand the morphological basis of high performance and thermal robustness of elastically powered movements, we compared feeding dynamics at a range of temperatures (5-25°C) in two species of terrestrial plethodontid salamanders, Plethodon metcalfi and Ensatina eschscholtzii, which differ in tongue muscle architecture and the mechanism of tongue projection. We found that Ensatina is capable of ballistic projection with a mean muscle-mass-specific power of 2100 W kg(-1), revealing an elastic mechanism. Plethodon, in contrast, projected its tongue non-ballistically with a mean power of only 18 W kg(-1), indicating it is muscle-powered. Ensatina projected the tongue significantly farther than Plethodon and with dynamics that had significantly lower thermal sensitivity at temperatures below 15°C. These performance differences were correlated with morphological differences, namely elongated collagenous aponeuroses in the projector muscle of Ensatina as compared to Plethodon which are likely the site of energy storage, and the absence in Ensatina of projector muscle fibers attaching to the tongue skeleton that allows projection to be truly ballistic. These findings demonstrate that, in these otherwise similar species, the presence in one species of elaborated connective tissue in series with myofibers confers not only 10-fold greater absolute performance but also greater thermal robustness of performance. We conclude that changes in muscle and connective-tissue architecture are sufficient to alter significantly the mechanics, performance and thermal robustness of musculoskeletal systems.
Modern snakes probably originated as habitat specialists, but it controversial unclear whether they were ancestrally terrestrial burrowers or marine swimmers. We used x-ray virtual models of the inner ear to predict the habit of Dinilysia patagonica, a stem snake closely related to the origin of modern snakes. Previous work has shown that modern snakes perceive substrate vibrations via their inner ear. Our data show that D. patagonica and modern burrowing squamates share a unique spherical vestibule in the inner ear, as compared with swimmers and habitat generalists. We built predictive models for snake habit based on their vestibular shape, which estimated D. patagonica and the hypothetical ancestor of crown snakes as burrowers with high probabilities. This study provides an extensive comparative data set to test fossoriality quantitatively in stem snakes, and it shows that burrowing was predominant in the lineages leading to modern crown snakes.
Snakes are important predators that have radiated throughout many ecosystems, and constriction was important in their radiation. Constrictors immobilize and kill prey by using body loops to exert pressure on their prey. Despite its importance, little is known about constriction performance or its full effects on prey. We studied the scaling of constriction performance in two species of giant pythons (Python reticulatus Schneider 1801 and Python molurus bivittatus Kuhl 1820) and propose a new mechanism of prey death by constriction. In both species, peak constriction pressure increased significantly with snake diameter. These and other constrictors can exert pressures dramatically higher than their prey's blood pressure, suggesting that constriction can stop circulatory function and perhaps kill prey rapidly by over-pressurizing the brain and disrupting neural function. We propose the latter "red-out effect" as another possible mechanism of prey death from constriction. These effects may be important to recognize and treat properly in rare cases when constrictors injure humans.
As legless predators, snakes are unique in their ability to immobilize and kill their prey through the process of constriction, and yet how this pressure incapacitates and ultimately kills the prey remains unknown. In this study, we examined the cardiovascular function of anesthetized rats before, during and after being constricted by boas (Boa constrictor) to examine the effect of constriction on the prey's circulatory function. The results demonstrate that within 6 s of being constricted, peripheral arterial blood pressure (PBP) at the femoral artery dropped to 1/2 of baseline values while central venous pressure (CVP) increased 6-fold from baseline during the same time. Electrocardiographic recordings from the anesthetized rat's heart revealed profound bradycardia as heart rate (fH) dropped to nearly half of baseline within 60 s of being constricted, and QRS duration nearly doubled over the same time period. By the end of constriction (mean 6.5±1 min), rat PBP dropped 2.9-fold, fH dropped 3.9-fold, systemic perfusion pressure (SPP=PBP-CVP) dropped 5.7-fold, and 91% of rats (10 of 11) had evidence of cardiac electrical dysfunction. Blood drawn immediately after constriction revealed that, relative to baseline, rats were hyperkalemic (serum potassium levels nearly doubled) and acidotic (blood pH dropped from 7.4 to 7.0). These results are the first to document the physiological response of prey to constriction and support the hypothesis that snake constriction induces rapid prey death due to circulatory arrest.
© 2015. Published by The Company of Biologists Ltd.
Snakes are a remarkably diverse and successful group today, but their evolutionary origins are obscure. The discovery of snakes with two legs has shed light on the transition from lizards to snakes, but no snake has been described with four limbs, and the ecology of early snakes is poorly known. We describe a four-limbed snake from the Early Cretaceous (Aptian) Crato Formation of Brazil. The snake has a serpentiform body plan with an elongate trunk, short tail, and large ventral scales suggesting characteristic serpentine locomotion, yet retains small prehensile limbs. Skull and body proportions as well as reduced neural spines indicate fossorial adaptation, suggesting that snakes evolved from burrowing rather than marine ancestors. Hooked teeth, an intramandibular joint, a flexible spine capable of constricting prey, and the presence of vertebrate remains in the guts indicate that this species preyed on vertebrates and that snakes made the transition to carnivory early in their history. The structure of the limbs suggests that they were adapted for grasping, either to seize prey or as claspers during mating. Together with a diverse fauna of basal snakes from the Cretaceous of South America, Africa, and India, this snake suggests that crown Serpentes originated in Gondwana.
Copyright © 2015, American Association for the Advancement of Science.
Neotropical “goo-eating” dipsadine snakes display a set of morphological and histo-chemical adaptations linked to the capture of their soft-bodied, viscous invertebrate prey. Within this group, species from the genus Sibynomorphus feed chiefly on snails and slugs. Here, we analyzed a series of skull and mandible characters in S. mikanii, S. neuwiedi and S. turgidus using geometric morphometrics, with the aim of assessing morphological adaptations related to slug- and snail-feeding in that genus. We further compared the results with Leptodeira annulata, a species that feeds on vertebrates. To evaluate shape differences of the skull and mandible between species we performed a multivariate analysis of variance and a linear discriminant analysis. Our results show that the narrow, elongate skull in S. mikanii may help with slug ingestion, while asymmetry in teeth number and mandibular shape in S. neuwiedi and S. turgidus are likely related to snail feeding.
We compared the head skeleton (skull and lower jaw) of juvenile and adult specimens of five snake species [Anilios (=Ramphotyphlops) bicolor, Cylindrophis ruffus, Aspidites melanocephalus, Acrochordus arafurae, and Notechis scutatus] and two lizard outgroups (Ctenophorus decresii, Varanus gilleni). All major ontogenetic changes observed were documented both qualitatively and quantitatively. Qualitative comparisons were based on high-resolution micro-CT scanning of the specimens, and detailed quantitative analyses were performed using three-dimensional geometric morphometrics. Two sets of landmarks were used, one for accurate representation of the intraspecific transformations of each skull and jaw configuration, and the other for comparison between taxa. Our results document the ontogenetic elaboration of crests and processes for muscle attachment (especially for cervical and adductor muscles); negative allometry in the braincase of all taxa; approximately isometric growth of the snout of all taxa except Varanus and Anilios (positively allometric); and positive allometry in the quadrates of the macrostomatan snakes Aspidites, Acrochordus and Notechis, but also, surprisingly, in the iguanian lizard Ctenophorus. Ontogenetic trajectories from principal component analysis provide evidence for paedomorphosis in Anilios and peramorphosis in Acrochordus. Some primitive (lizard-like) features are described for the first time in the juvenile Cylindrophis. Two distinct developmental trajectories for the achievement of the macrostomatan (large-gaped) condition in adult snakes are documented, driven either by positive allometry of supratemporal and quadrate (in pythons), or of quadrate alone (in sampled caenophidians); this is consistent with hypothesised homoplasy in this adaptive complex. Certain traits (e.g. shape of coronoid process, marginal tooth counts) are more stable throughout postnatal ontogeny than others (e.g. basisphenoid keel), with implications for their reliability as phylogenetic characters.
We examined the divergence in pileus shape and ontogenetic allometric changes in pileus shape in two closely related species of snakes - Natrix natrix and N. tessellata. These two species have similar ecology, but different microhabitat and diet preferences. We analysed the ontogenetic series from hatchlings to adults. Hatchlings of two species significantly diverged in pileus size and shape. At the adult stage, significant sexual dimorphism in pileus size and shape was found within both species. Adults of N. natrix and N. tessellata (females and males) diverged in pileus shape, but not in size. Allometric shape changes accounted for significant amount of variance in pileus shape among different age classes, and appear to be species- and sex-specific. Our results suggested that allometries of pileus shape are highly evolvable traits, which may result from natural selection for functional optimisation of head shape in Natricine species.
An organism’s morphology is driven by selection on function while being constrained by phylogenetic and developmental factors as well as functional trade-offs. If selection on function is strong and solutions limited, then convergence is expected. In this paper we quantify head shape in a group of ecologically diverse snakes (homalopsid snakes) differing in habitat use and diet using three-dimensional geometric morphometric approaches. Using data on head shape we explore whether snakes eating different prey show different morphologies. Moreover, we test whether head shape is constrained by other factors such as habitat use, burrow use, or activity pattern. Our results demonstrate similar head shapes in species consuming similar prey. Snakes that capture elusive prey under water differ from those that capture and swallow prey like frogs or crustaceans. Moreover, habitat use, the use of burrows, and activity pattern also significantly impact head shape in this group of snakes. However, this signal appears to be partly confounded by the diet signal. For axes discriminating specifically between habitat use groups or animals that use burrows vs. those that do not shapes were in accordance with our predictions. Our results suggests an adaptive signal in the evolution of head shape in homalopsid snakes with diet, habitat use and the use of burrows all influencing the evolution of head shape in
the group.
