Natricine Snakes Research Articles

Chemical Basis of Prey Recognition in Thamnophiine Snakes: The Unexpected New Roles of Parvalbumins

Detecting and locating prey are key to predatory success within trophic chains. Predators use various signals through specialized visual, olfactory, auditory or tactile sensory systems to pinpoint their prey. Snakes chemically sense their prey through a highly developed auxiliary olfactory sense organ, the vomeronasal organ (VNO). In natricine snakes that are able to feed on land and water, the VNO plays a critical role in predatory behavior by detecting cues, known as vomodors, which are produced by their potential prey. However, the chemical nature of these cues remains unclear. Recently, we demonstrated that specific proteins–parvalbumins–present in the cutaneous mucus of the common frog (Rana temporaria) may be natural chemoattractive proteins for these snakes. Here, we show that parvalbumins and parvalbumin-like proteins, which are mainly intracellular, are physiologically present in the epidermal mucous cells and mucus of several frog and fish genera from both fresh and salt water. These proteins are located in many tissues and function as Ca2+ buffers. In addition, we clarified the intrinsic role of parvalbumins present in the cutaneous mucus of amphibians and fishes. We demonstrate that these Ca2+-binding proteins participate in innate bacterial defense mechanisms by means of calcium chelation. We show that these parvalbumins are chemoattractive for three different thamnophiine snakes, suggesting that these chemicals play a key role in their prey-recognition mechanism. Therefore, we suggest that recognition of parvalbumin-like proteins or other calcium-binding proteins by the VNO could be a generalized prey-recognition process in snakes. Detecting innate prey defense mechanism compounds may have driven the evolution of this predator-prey interaction.

Antipredator Displays and Prey Chemical Preference of an Asian Natricine Snake,Macropisthodon rudis(Squamata: Colubridae)

Several Asian natricine snakes are known to possess special organs called nuchal glands. Extensive studies on the nuchal glands of Rhabdophis tigrinus have shown that the glands contain cardiac steroidal toxins known as bufadienolides, which are sequestered from its toad prey and are stored in the nuchal glands as defensive substances. In addition, several species of snakes with nuchal glands exhibit unique behaviors to enhance the effects of the glands (nuchal gland-related behaviors). Macropisthodon rudis is the only species that does not have the nuchal glands in the genus. We investigated its antipredator displays and chemical preference for toads to gain insight into the evolution of the nuchal glands. The results showed that M. rudis does not exhibit the nuchal gland-related behaviors such as neck arching, neck butting, and dorsal-facing posture. Additionally, this species showed high preference for toad chemicals. These results support a previous hypothesis that preference for toads predates the evolution of the nuchal glands and that the unique antipredator behaviors have evolved to enhance the defensive efficiency of the glands.

Chemosensory responses to chemical and visual stimuli in five species of colubrid snakes

Snakes utilize chemical and visual stimuli during predation, however the emphasis on these cues and which cues are used to initiate predation varies among species. For example, rattlesnakes using the ambush strategy rely on chemical cues to locate an ambush station, then visual and thermal cues to initiate envenomating strikes, then chemical cues again to track prey. By contrast, many natricine snakes use chemical cues to initiate predation, increasing the rate of tongue flicking regardless of whether visual cues are present. The present study examined the individual and interactive effects of chemical and visual stimuli of prey on the predatory behavior of five snake taxa representing three feeding guilds. Bull snakes ( Pituophis catenifer ), Eastern Corn snakes ( Pantherophis guttatus ), and Midland Rat snakes ( Scotophis spiloides ) have a diet primarily consisting of mammals; Western Fox snakes ( Mintonius vulpina ) prey primarily on bird eggs; and Common Kingsnakes ( Lampropeltis getula ) prey equally on mammals and reptiles. Three patterns of response to chemical and visual stimuli of the test prey ( Mus musculus ) were observed. Mammal specialists responded to chemical cues. Fox snakes responded to visual cues, but not to chemical cues. Kingsnakes exhibited increased rates of tongue flicking in response to both chemical and visual stimuli. This study suggests correlations between the evolution of prey preference, foraging ecology and the utilization of chemical or visual stimuli by snakes.

Out of Asia: Natricine snakes support the Cenozoic Beringian Dispersal Hypothesis

Based on a combination of six mitochondrial gene fragments (12S RNA, cyt b, ND1, ND2, ND4 and CO1) and one nuclear gene (c-mos) from 22 genera we infer phylogenetic relationships among natricine snakes and examine the date and area of origin of these snakes. Our phylogenetic results indicate: (1) the subfamily Natricinae is strongly supported as monophyletic including a majority of extant genera, and a poorly known and previously unassigned species Trachischium monticola, (2) two main clades are inferred within Natricinae, one containing solely taxa from the Old World (OW) and the other comprising taxa from a monophyletic New World (NW) group with a small number of OW relatives. Within the first clade, the genera Xenochrophis and Amphiesma are apparently not monophyletic. Divergence dating and ancestral area estimation indicate that the natricines originated in tropical Asia during the later Eocene or the Oligocene. We recover two major dispersals events out of Asia, the first to Africa in the Oligocene (28Ma) and the second to the Western Palearctic and the New World at 27Ma. This date is consistent with the dispersal of numerous other OW groups into the NW.

Comparison of cranial form and function in association with diet in natricine snakes

The skull of squamates has many functions, with food acquisition and ingestion being paramount. Snakes vary interspecifically in the frequency, size, and types of prey that are consumed. Natural selection should favor phenotypes that minimize the costs of energy acquisition; therefore, trophic morphology should reflect a snake's primary prey type to enhance some aspect of feeding performance. I measured 19 cranial variables for six natricine species that vary in the frequency with which they consume frogs and fish. Both conventional and phylogenetically corrected analyses indicated that fish-eating snakes have relatively longer upper and lower jaw elements than frog-eating snakes, which tended to have broader skull components. I also compared the ratio of the in-lever to the out-lever lengths of the jaw-closing mechanism [jaw mechanical advantage (MA)] among species. Fish-eating snakes had significantly lower MAs in the jaws than did the frog-eating snakes. This result suggests that piscivores have faster closing jaws and that the jaws of frog-eating snakes have higher closing forces. Cranial morphology and the functional demands of prey capture and ingestion appear to be associated with primary prey type in natricine snakes.

Behavioural correlates with hemipenis morphology in New World natricine snakes

Copulatory organs (hemipenes) of male snakes vary markedly among species in shape and ornamentation. We suggest that sexual conflict over copulation duration may have shaped the evolution of hemipenis morphology, favouring more elaborate organs in species in which a long duration of copulation is especially beneficial to males, despite the associated costs to females. To test this proposition, we compare mating behaviour between two species of gartersnakes differing in hemipenis morphology. In addition, we review data on copulation duration and hemipenis morphology and relate hemipenis morphology to phylogeny among of New World natricines. As predicted, copulation duration was significantly shorter in the common gartersnake (Thamnophis sirtalis), a species with simple subcylindrical hemipenes, than in the plains gartersnake (Thamnophis radix), a species with more complex, bilobed organs. Furthermore, female T. radix frequently exhibited vigorous body rolls during copulation, a behaviour associated with copulation termination, whereas female T. sirtalis never exhibited this behaviour. Copulations were of shorter duration when female T. radix (but not T. sirtalis) more greatly exceeded males in body size, suggesting that females can more easily disengage from small males. Our review of New World natricines provides only weak evidence for an association between copulation duration and hemipenis morphology. Our mapping of hemipenis morphology onto the New World natricine phylogeny suggests that hemipenis morphology is evolutionarily plastic; both simple and bilobed hemipenes occur in all three major natricine clades, as well as in two of three gartersnake subclades and several sister-species pairs.

Convergence in trophic morphology and feeding performance among piscivorous natricine snakes

Piscivory has independently evolved numerous times amongst snakes, and therefore these animals provide a powerful opportunity to test for convergent evolution in a vertebrate feeding system. In this study, we integrate performance trials with comparative methods to test the hypothesis that piscivory drives convergence in trophic morphology and feeding performance among natricine snakes. Within and across species, increasing the relative length of the quadrate bone in the skull is positively and strongly linked to a reduction in the time needed to swallow large fish prey. Thus, our feeding experiments suggest that a longer quadrate bone enables snakes to better conform their head shape to the shape of the prey during swallowing. Ancestral diet reconstructions and phylogenetically corrected multiple regression analyses further reveal that evolutionary increases in piscivory are coupled to the evolution of relatively longer quadrates, and hence improved feeding performance on fish prey in these animals. The exploitation of similar dietary niches drives the evolution of convergent trophic morphologies and feeding performances in natricine snakes.

Morphological convergence as a consequence of extreme functional demands: examples from the feeding system of natricine snakes

Despite repeated acquisitions of aquatic or semi-aquatic lifestyles revolving around piscivory, snakes have not evolved suction feeding. Instead, snakes use frontally or laterally directed strikes to capture prey under water. If the aquatic medium constrains strike performance because of its physical properties, we predict morphological and functional convergence in snakes that use similar strike behaviours. Here we use natricine snakes to test for such patterns of convergence in morphology and function. Our data show that frontal strikers have converged on a similar morphology characterized by narrow elongate heads with a reduced projected frontal surface area. Moreover, simple computational fluid dynamics models show that the observed morphological differences are likely biologically relevant as they affect the flow of water around the head. In general, our data suggest that the direction of evolution may be predictable if constraints are strong and evolutionary solutions limited.

Aquatic versus terrestrial locomotion: comparative performance of two ecologically contrasting species of European natricine snakes

AbstractOne indicator of ecological differences between species is differential locomotory performance in different media. In this study, we compare locomotory speed of two species of natricine snakes on land and in water at a range of temperatures in the laboratory. As expected, both species moved more quickly at higher temperatures and both swam faster than they moved on land. However, the difference between aquatic and terrestrial speed was much greater for the aquatic species, Natrix maura, than for the semi‐aquatic Natrix natrix. Furthermore, although N. maura was significantly faster than N. natrix in water, the opposite was true on land. In fact, N. maura was reluctant to move very far on land at all and would not complete a 2 m terrestrial course. Although we found no evidence of a negative correlation between the aquatic and terrestrial speeds of individual N. natrix, this interspecific comparison is consistent with the notion of a tradeoff between performance abilities on land and in water.

Comparative experimental tests of natricine antipredator displays, with special reference to the apparently unique displays in the Asian genus, Rhabdophis

Nuchal glands are unique organs known in only twelve Old World natricine species (three genera) including Rhabdophis tigrinus tigrinus. The glands of R. t. tigrinus contain a toxic secretion that may be derived from its toxic toad diet. A series of peculiar antipredator behaviors, for example neck arch, neck butt, and dorsal-facing posture, are exhibited by R. t. tigrinus, and a functional association between this behavior and the nuchal glands has been suggested. To investigate the ubiquitousness of these putatively unique displays among snakes, antipredator responses of 27 taxa of natricine snakes, both with and without nuchal glands, were studied using a common testing procedure. Three of four taxa with nuchal glands exhibited neck arch, neck butt, and dorsal-facing posture. None of the remaining 23 taxa, which do not possess the glands, showed neck arch and neck butt. Principal-components analysis indicated the association of the above three displays along with the behaviors termed neck flatten and head elevation, confirming the presence of a series of nuchal gland-related behaviors. These results support the assumption that the suite of peculiar displays is associated with the deterrent effects of the nuchal gland secretion.

Like mother, like daughter: inheritance of nest-site location in snakes

A trait can be passed from parents to offspring even if it has no genetic basis. For example, if daughters return to reproduce at the same sites where they were hatched themselves, nest-site location is consistent within matrilineages. Most cases of natal homing (nest-site philopatry) across generations have been inferred from molecular evidence rather than directly demonstrated, and involve species with low dispersal abilities. However, some animals disperse long distances but then return to their own place of birth to reproduce, based on cues imprinted early in their own development. Our field studies on tropical natricine snakes (Tropidonophis mairii, Colubridae) show that when they are ready to nest, females return to the sites where their mothers were captured pre-nesting, and where they themselves were released as hatchlings.

HEADSTARTING AS A MANAGEMENT TOOL: A CASE STUDY OF THE PLAINS GARTERSNAKE

The use of headstarting and related techniques as management tools for threatened and endangered species remains controversial, due in part to a lack of empirical data on their effectiveness. Here, we present data on pre-natal mortality, growth, and survival during headstarting as well as growth, survival, and reproduction following release for an unprotected population of plains gartersnakes. We combine these data with data on growth and survival of comparably sized wild-caught snakes to provide an overall evaluation of the potential effectiveness of headstarting. Depending on rearing conditions, proportions of live births varied from 0.79 (‘worst-case’) to 0.94 (‘best-case’), survival during headstarting ranged from 0.74 (‘worst-case’) to 0.88 (‘best-case’), and second-year survival following release ranged from 0.11 (‘worst-case’) to 0.40 (‘best-case’). In comparison, survival of free-ranging snakes was 0.16 in their first year and 0.40 in their second year. Assuming the proportion of live births in nature is close to 1, expected survival to reproductive maturity among free-ranging snakes is 0.06, whereas that for headstarted snakes ranges from 0.07 (‘worst-case’) to 0.33 (‘best-case’). The growth rate of headstarted snakes following release was similar to that of similar-sized free-ranging snakes, and headstarted snakes were successful at reproduction. Together, these results suggest that, if carefully implemented, headstarting may be an effective management tool for endangered plains gartersnake populations in Ohio and for other natricine snakes with similar demographic characteristics.

Influence of body size on swimming performance of four species of neonatal natricine snakes acutely exposed to a cholinesterase‐inhibiting pesticide

Locomotor performance is an important fitness-related trait in reptiles because of its potential influence on prey capture and predator avoidance. Because cholinesterase-inhibiting pesticides disrupt neuromuscular signaling, reduction in performance seems to be a logical translation of this biochemical disruption to the organism level. In the present study, we compared the swimming performance of four species of natricine snakes acutely exposed to a formulation of carbaryl to determine whether neonatal body size or skin permeability influences responsiveness. Exposure to high concentrations of carbaryl (2.5-5.0 mg/L) resulted in reduced swimming performance in all four species of snakes, and species responded similarly to the pesticide once body size was accounted for allometrically. Using traditional methods in physiological ecology to estimate skin permeability (a parameter that influences the dose of contaminant absorbed), we found that water flux across the integument also scaled allometrically with body surface area and, therefore, was similar among species after controlling for this relationship. We suggest that future studies examining the effects of repeated low-dose exposure to cholinesterase inhibitors on performance parameters will be useful in assessing the ecological significance of our findings.

Correlated evolution of aquatic prey-capture strategies in European and American natricine snakes

The evolution of aquatic prey-capture strategies in snakes has been suggested as a model system for the study of convergence. However, hypotheses of correlated evolution of prey-capture strategy with different aspects of foraging niche have never been tested quantitatively. Whereas a considerable amount of data is available for North American species, data for European species are scarce. In this study we combine original data on prey-capture strategies and strike velocities for European natricines with data for North American Natricinae obtained from the literature. We did not find any evidence for correlated evolution between prey-capture strategy and strike velocity with diet, but there was a significant correlation with prey density. Thus, our study suggests that prey density, rather than diet, played an important role in the evolution of the different prey-capture strategies and strike velocities of natricine snakes.

Morphological and ecological convergence in two natricine snakes

Similar morphologies between species may be due to shared ancestry or convergent evolution . Understanding instances of morphological and ecological convergence is central to evolutionary ecology because they help us understand the fit between organism and environment. Two species of stream-dwelling natricine snakes, Thamnophis rufipunctatus and Nerodia harteri present a model system for studying ecological and morphological convergence and adaptation. The species are allopatric and both live in shallow riffles in streams and forage visually for fish. We studied morphological similarity, trait evolution and functional significance of ecologically relevant traits in these and related species, and used mitochondrial DNA sequences for the ND4 gene to estimate their phylogenetic relationships. Character mapping of head length and head width supported the hypothesis of independent evolution of head shape in T . rufipunctatus and N . harteri . The elongate snout is a derived trait in these two taxa that is associated with reduced hydrodynamic drag on the snakes’ heads when in a swift current, compared to other species with the ancestral blunt snout. We hypothesize that lower hydrodynamic drag facilitates prey capture success in these species that are known to forage by holding their position in currents and striking at fish prey. The elongate snout morphology has also resulted in a diminished binocular vision field in these snakes, contrary to the hypothesis that visually orientated snakes should exhibit relatively greater binocular vision. Convergent evolution of the long snout and reduced hydrodynamic drag in T. rufipunctatus and N. harteri are consistent with the hypothesis that the long snout is an adaptation to foraging in a swift current. © 2005 The Linnean Society of London, Biological Journal of the Linnean Society , 2005, 85 , 363‐371. ADDITIONAL KEYWORDS: adaptation - binocular vision field - convergent evolution - hydrodynamic drag - Nerodia - Thamnophis - whole organism performance.

Differential swimming performance of two natricine snakes exposed to a cholinesterase-inhibiting pesticide

Environmental contaminants have direct effects on organisms at the molecular, cellular, and tissue levels, but the net results of these sub-organismal effects are only consequential to exposed populations if they alter organism-level traits that ultimately influence fitness (e.g., growth, locomotor performance, reproduction, and survival). Here, we explore the possibility that the swimming performance of neonate black swamp snakes ( Seminatrix pygaea) and diamondback water snakes ( Nerodia rhombifer) may be affected by exposure to carbaryl (2.5 and 5.0 mg/L). The highest concentration of carbaryl caused greater reductions in swim velocity in S. pygaea than in N. rhombifer. Most individuals recovered from the effects of carbaryl on swimming performance within 96 h, but recovery was significantly slower in S. pygaea than in N. rhombifer. We hypothesize that the sensitivity of S. pygaea may arise from its highly permeable integument compared to other natricines. Our findings suggest that performance can serve as an ecologically relevant response to contaminant exposure in reptiles and warrants further study.

Sexual Dimorphism and Allometric Size Variation in a Population of Grass Snakes (Natrix natrix) in Southern England

Sexual dimorphism is widespread in animals, either because of sexual selection or ecological divergence between the sexes. In natricine snakes, for example, females are usually larger than males and have larger heads and shorter tails relative to body length. Grass Snakes (Natrix natrix) near Canterbury, U.K., generally proved to be typical natricines in these respects. Most differences between the sexes were apparent at hatching, rather than being confined to adults, but there was no evidence that the sexes differed in allometry. Despite high r2-values, allometry of relationships of body mass, head width, and tail length with body length were not satisfactorily explained by linear regressions (using log-transformed data). Rather, both polynomial and piecewise regressions provided better fits, suggesting that allometric coefficients were not constant but varied with body size. Nonetheless, all analyses were in agreement that small snakes had relatively heavier bodies and wider heads than large snakes. How general such patterns are, and their ecological significance, remain to be determined.

Research Article: Foraging and prey handling behaviors of the generalist Thamnophis hammondii offered various prey types

Foraging success is critical to the survival of any predator. When encountering introduced prey species, predatory generalists often adapt more readily to the prey than do predatory specialists. The foraging and prey handling behaviors of Thamnophis hammondii offered three different prey types (Lepomis spp., larval Rana catesbeiana, and juvenile X. laevis) were examined. Durations of foraging and prey handling behaviors were analyzed to determine if these behaviors varied by snake gender, collection locality, or prey type. Differences in behavior type and duration as a function of gender or location were not detected. Snake behaviors varied between prey types, with differences in the duration of the following behaviors: time overland, cruising, margin wandering, midwater diving, prey-orienting underwater, and ingesting. Snakes successfully captured all prey types, with the highest attack and success rates when foraging for R. catesbeiana. The results indicate that T. hammondii exhibits a variable repertoire of foraging behaviors when presented various prey types. The generalist nature of this species may allow it to forage effectively for prey types that may be unavailable to other natricine snakes.

Predicted and observed maximum prey size – snake size allometry

Summary For gape‐limited predators such as snakes, it should be possible to predict the relationship between maximum prey size and body size from the relationship between maximum prey size and gape size and between gape size and body size. Such predictions were generated for Water Snakes, Nerodia sipedon L., using a data subset and then tested with a larger data set. Gape size was computed based on jaw length and width and cyclical regression was used to identify prey of maximum size for snakes of a given gape or mass. Predicted and observed maximum prey cross‐section–snake mass allometry were in good agreement. Predicted maximum prey mass–snake mass allometry somewhat exceeded observed allometry which did not differ from 1. Observed minimum prey size–snake size allometry was significantly greater than 0, indicating that larger snakes drop small prey from their diets. Gape size–body size allometry in two other natricine snakes (Thamnophis sirtalis, Storeria dekayi) suggest that patterns of ontogenetic change in prey size should differ among species in predictable ways. Sex differences in gape size–snake size allometry suggest that sex differences in maximum prey size should increase with increasing snake size, even when linear measures of head dimensions do not.

Heterologous amplification of microsatellite markers from colubroid snakes in European natricines (serpentes: natricinae).

Eighteen microsatellite loci developed for a range of snake species (New World natricines, elapids, crotalids) were tested against European natricines (Natrix natrix, N. maura, and N. tessellata) in cross-species amplification experiments. Five loci were polymorphic (average expected heterozygosity 0.749 for a population of N. natrix in Amsterdam, mean sample size 47.8) and three loci were monomorphic. The remainder could not be consistently scored or failed to amplify. Further tests on single individuals of a diverse set of eight species of colubroid snakes showed that 15 of the 18 loci could be cross-amplified in at least one of these species. We conclude that our results show promise for the utilization of these markers for experimental assessments of genetic variation in the phylogenetically closely related group of European natricine snakes with emphasis on N. natrix. The full suite of microsatellite markers now available for snakes may show additional potential for subsequent investigation across a broader range of colubroid snakes.