Search

Traits for prey acquisition form the phenotypic interface of predator-prey interactions. In venomous predators, morphological variation in venom delivery apparatus like fangs and stingers may be optimized for dispatching prey. Here, we determine how a single dimension of venom injection systems evolves in response to variation in the size, climatic conditions and dietary ecology of viperid snakes. We measured fang length in more than 1900 museum specimens representing 199 viper species (55% of recognized species). We find both phylogenetic signal and within-clade variation in relative fang length across vipers suggesting both general taxonomic trends and potential adaptive divergence in fang length. We recover positive evolutionary allometry and little static allometry in fang length. Proportionally longer fangs have evolved in larger species, which may facilitate venom injection in more voluminous prey. Finally, we leverage climatic and diet data to assess the global correlates of fang length. We find that models of fang length evolution are improved through the inclusion of both temperature and diet, particularly the extent to which diets are mammal-heavy diets. These findings demonstrate how adaptive variation can emerge among components of complex prey capture systems.

An increase in ecological opportunities, either through changes in the environment or acquisition of new traits, is frequently associated with an increase in species and morphological diversification. However, it is possible that certain ecological settings might prevent lineages from diversifying. Arboreality evolved multiple times in vipers, making them ideal organisms for exploring how potentially new ecological opportunities affect their morphology and speciation regimes. Arboreal snakes are frequently suggested to have a very specialized morphology, and being too large, too small, too heavy, or having short tails might be challenging for them. Using trait-evolution models, we show that arboreal vipers are evolving towards intermediate body sizes, with longer tails and more slender bodies than terrestrial vipers. Arboreality strongly constrains body size and circumference evolution in vipers, while terrestrial lineages are evolving towards a broader range of morphological variants. Trait-dependent diversification models, however, suggest similar speciation rates between microhabitats. Thus, we show that arboreality might constrain morphological evolution but not necessarily affect the rates at which lineages generate new species., (© 2017 The Author(s).)

Background: Covering the eye of all snakes is a transparent integumental structure known as the spectacle. In order to determine variations in spectacle thickness among species, the spectacles of 217 alcohol-preserved museum specimens of 44 species belonging to 14 different families underwent optical coherence tomography (OCT) to measure spectacular thickness. Multivariable analyses were made to determine whether family, activity period (diurnal/nocturnal) and habitat (arboreal/terrestrial/fossorial/aquatic) influenced spectacle thickness., Results: The thinnest spectacles in absolute terms were found in the Usambara bush viper (Viperidae) with a thickness of 74 ± 9 μm and the absolute thickest spectacle was found in the red-tailed pipe snake (Cylindrophiidae) which had a spectacle thickness of 244 ± 57 μm. Fossorial and aquatic snakes had significantly thicker spectacles than arboreal and terrestrial snakes. When spectacle thickness was correlated to eye size (horizontal spectacle diameter), Gray's earth snake (Uropeltidae) had the lowest ratio (1:7) and the cottonmouth (Viperidae) had the highest ratio (1:65). Multivariable and phylogenetic analyses showed that spectacular thickness could be predicted by taxonomic family and habitat, but not activity period., Conclusion: This phylogenetically broad systematic study of the thickness of the snake spectacle showed that spectacular thickness varies greatly across snake species and may reflect evolutionary adaptation and development.

The West African Gaboon viper (Bitis rhinoceros) has an extraordinary coloration of pale brown and velvety black markings. The velvety black appearance is caused by a unique hierarchical surface structures which was not found on the pale brown scales. In the present study we examined the wettability of the vipeŕs scales by measuring contact angles of water droplets. Velvet black scale surfaces had high static contact angles beyond 160° and low roll-off angles below 20° indicating an outstanding superhydrophobicity. Our calculations showed that the Cassie-Baxter model describes well wettability effects for these surfaces. Self-cleaning capabilities were determined by contaminating the scales with particles and fogging them until droplets formed. Black scales were clean after fogging, while pale scales stayed contaminated. Black scales feature multifunctional structures providing not only water-repellent but also self-cleaning properties. The pattern of nanoridges can be used as a model for surface-active technical surfaces.

The facial pits of rattlesnakes, copperheads, lanceheads, bushmasters and other American and Asian pitvipers (Crotalinae) are highly innervated and densely vascularized infrared (IR) receptor organs. For over a century, studies have focused on a small sample of model species from North America and Asia. Based on an expanded survey of Central and South American crotalines, we report a conspicuous accessory structure composed of well-defined papillae that project from the anterior orbital adnexa. The papillae are continuous with the inner chamber of the IR receptor organ and our histological and ultrastructural data suggest that they possess a well-developed nervous network and extensive vascularization; however, they lack the characteristic IR-sensitive terminal nerve masses found in the IR-receptive pit membrane. The function of the IR receptor organ papillae is unknown.

The West African Gaboon viper (Bitis rhinoceros) is a master of camouflage due to its colouration pattern. Its skin is geometrically patterned and features black spots that purport an exceptional spatial depth due to their velvety surface texture. Our study shades light on micromorphology, optical characteristics and principles behind such a velvet black appearance. We revealed a unique hierarchical pattern of leaf-like microstructures striated with nanoridges on the snake scales that coincides with the distribution of black colouration. Velvet black sites demonstrate four times lower reflectance and higher absorbance than other scales in the UV-near IR spectral range. The combination of surface structures impeding reflectance and absorbing dark pigments, deposited in the skin material, provides reflecting less than 11% of the light reflected by a polytetrafluoroethylene diffuse reflectance standard in any direction. A view-angle independent black structural colour in snakes is reported here for the first time.

The pitviper facial pit is a pinhole camera-like sensory organ consisting of a flask-shaped cavity divided into two chambers by a suspended membrane. Neurophysiological studies and simplified optical models suggest that facial pits detect thermal radiation and form an image that is combined with visual input in the optic tectum to form a single multispectral image. External pit anatomy varies markedly among taxonomic groups. However, optical function depends on unknown internal anatomy. Therefore, we developed methods for relating anatomy to optical performance. To illustrate, we constructed detailed anatomical models of the internal anatomy of the facial pits of four individuals of four pitviper species using X-ray tomography sections of fresh material. We used these models to define the point spread function, i.e. the distribution of radiation from a point source over the pit membrane, for each species. We then used optical physics, heat transfer physics and computational image processing to define the thermal image formed on the pit membrane for each species. Our computed pit membrane images are consistent with behavioral observations if the sensitivity of membrane receptors equals the most sensitive (ca. 0.001°C) laboratory estimates. Vignetting (variation in optical aperture size with view angle) and differences between body and environmental temperatures can create temperature variation across the membrane that greatly exceeds image temperature contrasts, potentially impairing imaging. Spread functions plotted versus source point azimuth and elevation show distinct patterns that suggest new research directions into the relationships among the optical anatomy, ecology, behavior and sensory neurophysiology of pitvipers.

Both visual and infrared (IR) senses are utilized in prey targeting by pit vipers. Visual and IR inputs project to the contralateral optic tectum where they activate both multimodal and bimodal neurons. A series of ocular and pit organ occlusion experiments using the short-tailed pit viper (Gloydius brevicaudus) were conducted to investigate the role of visual and IR information during prey targeting. Compared with unoccluded controls, snakes with either both eyes or pit organs occluded performed more poorly in hunting prey although such subjects still captured prey on 75% of trials. Subjects with one eye and one pit occluded on the same side of the face performed as well as those with bilateral occlusion although these subjects showed a significant targeting angle bias toward the unoccluded side. Performance was significantly poorer when only a single eye or pit was available. Interestingly, when one eye and one pit organ were occluded on opposite sides of the face, performance was poorest, the snakes striking prey on no more than half the trials. These results indicate that, visual and infrared information are both effective in prey targeting in this species, although interference between the two modalities occurs if visual and IR information is restricted to opposite sides of the brain.

The rapid and accurate recognition of dangerously venomous snakes following bites is crucial to making appropriate decisions regarding first aid, evacuation, and treatment. Past recommendations for identification of dangerous North American pit vipers have often required subjective determinations of head shape or relied on traits shared with some nondangerous species (elliptical pupils and undivided subcaudal scales). Heat-sensitive facial pits are diagnostic but require close examination of the dangerous head, and cephalic traits are useless when working with a decapitated carcass. Exclusive of cephalic traits, pit vipers north of Mexico can be recognized by the combination of keeled middorsal scales and undivided subcaudal scales. The order of colored rings is usually suggested to identify coral snakes in the United States, yet extension of the colored rings across the ventral scales must be added as an essential identifying factor to ensure elimination of all harmless look-alikes. A novel 3-step flow chart is presented that allows dangerous snakes in the United States and Canada to be recognized quickly and dependably without relying on cephalic traits. This process cannot be used in other countries, however, due to greater variability of these characteristics in snakes from other parts of the world. Finally, close examination of potentially venomous snakes is extraordinarily dangerous and steps to safeguard those making such observations are discussed., (Copyright © 2011 Wilderness Medical Society. Published by Elsevier Inc. All rights reserved.)

Most research into the adaptive significance of warning signals has focused on the colouration and patterns of prey animals. However, behaviour, odour and body shape can also have signal functions and thereby reduce predators' willingness to attack defended prey. European vipers all have a distinctive triangular head shape; and they are all venomous. Several non-venomous snakes, including the subfamily Natricinae, commonly flatten their heads (also known as head triangulation) when disturbed. The adaptive significance of this potential behavioural mimicry has never been investigated.We experimentally tested if the triangular head shape typical of vipers offers protection against predation. We compared the predation pressure of free-ranging predators on artificial snakes with triangular-shaped heads against the pressure on replicas with narrow heads. Snakes of both head types had either zigzag patterned bodies, typical of European vipers, or plain (patternless) bodies. Plain snakes with narrower Colubrid-like heads suffered significantly higher predation by raptors than snakes with triangular-shaped heads. Head shape did not, however, have an additive effect on survival in zigzag-patterned snakes, suggesting that species which differ from vipers in colouration and pattern would benefit most from behavioural mimicry. Our results demonstrate that the triangular head shape typical of vipers can act as a warning signal to predators. We suggest that head-shape mimicry may be a more common phenomenon among more diverse taxa than is currently recognised.

When environmental conditions exert sex-specific selection on offspring, mothers should benefit from biasing their sex allocation towards the sex with the highest fitness in a given environment. Yet, studies show mixed support for such adaptive strategies in vertebrates, which may be due to mechanistic constraints and/or weak selection on facultative sex allocation. In an attempt to disentangle these alternatives, we quantified sex-specific fitness returns and sex allocation (sex ratio and sex-specific mass at birth) according to maternal factors (body size, age, birth date, and litter size), habitat, and year in a viviparous snake with genotypic sex determination. We used data on 106 litters from 19 years of field survey in two nearby habitats occupied by the meadow viper Vipera ursinii ursinii in south-eastern France. Maternal reproductive investment and habitat quality had no differential effects on the growth and survival of sons and daughters. Sex ratio at birth was balanced despite a slight female-biased mortality before birth. No sexual mass dimorphism between offspring was evident. Sex allocation was almost random apart for a trend towards more male-biased litters as females grew older, which could be explained by an inbreeding avoidance strategy. Thus, a weak selection for facultative sex allocation seems sufficient to explain the almost equal sex allocation in the meadow viper.

Rapid evolution caused by human exploitation of wildlife is not usually addressed in studies of the impacts of such exploitation despite its direct relevance to population persistence. Japanese mamushi (Gloydius blomhoffii), an endemic venomous snake of the Japanese archipelago, has been heavily hunted by humans, and many populations appear to be declining or are already extirpated. We compared local populations that have been hunted regularly with populations that have not been hunted. Mamushi in hunted populations were smaller, had fewer vertebrae, produced more and smaller offspring, had increased reproductive effort among smaller females, and in nature fled at greater distances from an approaching human and were less defensive than mamushi in unhunted populations, as predicted from life-history theory. Heritability estimates for body size, number of vertebrae, and antipredator behavior were statistically significant, and neonates from hunted sites showed the same distribution of altered characters (compared with those from unhunted sites) as adults. Thus, distribution of the divergent trait between hunted and unhunted sites appeared in part to be genetically based, which suggests rapid evolution to human predation pressures. Trait distributions in hunted populations probably deviate from naturally (as opposed to anthropogenically) selected optima and, therefore, may have long-term negative repercussions on population persistence. Because rapid evolution affects a suite of parameters that characterize exploited populations, accurate understanding of the impacts of exploitation and effective resource management and conservation can only be achieved if evolutionary consequences are considered explicitly.

Envenoming by Protobothrops mucrosquamatus and Viridovipera stejnegeri accounts for the majority of venomous snakebites in Taiwan. We conducted a retrospective study to systematically examine the clinical manifestations and responses to antivenom therapy after P. mucrosquamatus and V. stejnegeri envenoming. Information on demographic characteristics, treatments, and systemic/local complications were abstracted from medical charts between 1991 and 2006. One hundred forty-nine patients with P. mucrosquamatus envenoming and 51 with V. stejnegeri envenoming were eligible for the final analysis, and they differed in terms of patient age, bite site, local bruising, proportion of patients needing >/= 3 vials of antivenom, and mean hospital stay. Univariate analysis revealed that P. mucrosquamatus envenoming had a higher risk of developing rhabdomyolysis, cellulitis, necrosis, and skin graft. Our findings suggested that P. mucrosquamatus envenoming was associated with a greater risk of severe clinical events, and monitoring for major clinical complications would be recommended.

The fangs of vipers are extremely long, rotating, hollow teeth. Analysis of video records of more than 750 strikes recorded at 60 or 250 frames per second for 285 individuals representing 86 species in 31 genera shows that vipers reposition fangs after initial contact with prey in more than a third of the strikes. Repositioning resulted when fangs missed prey entirely or hit prey regions that did not permit adequate penetration. The prevalence of repositioning, even among species that normally release prey, suggests strong selective pressure for rapid neuromotor response to fang placement error. The rapidity of repositioning suggests the existence of (a) fine-scale sensory detection of fang penetration depth, (b) rapid modulation of contraction of antagonistic muscles, and (c) possibly neurological modifications to shorten transmission time between sensory input and motor output. Extreme fang length has apparently coevolved with extreme functions.

It is commonly assumed that the facial pit of pitvipers forms relatively sharp images and can detect small differences in environmental surface temperatures. We have visualized the temperature contrast images formed on the facial pit membrane using a detailed optical and heat transfer analysis, which includes heat transfer through the air in the pit chambers as well as via thermal infrared radiation. We find the image on the membrane to be poorly focused and of very low temperature contrast. Heat flow through the air in the pit chambers severely limits sensitivity, particularly for small animals with small facial pit chambers. The aperture of the facial pit appears to be larger than is optimal for detecting small targets such as prey at 0.5 m. Angular resolution (i.e. sharpness) and image strength and contrast vary complexly with the size of the pit opening. As a result, the patterns of natural background temperatures obscure prey items and other environmental features, creating false patterns. Consequently, snakes cannot simply target the strongest signal to strike prey. To account for observed behavioral capabilities, the sensory endings on the pit membrane apparently must respond to temperature contrasts of 0.001 degrees C or less. While neural image sharpening likely enhances imaging performance, it appears important for foraging snakes to select ambush sites offering uniform backgrounds and strong thermal contrasts. As the ancestral facial pit was likely less sensitive than the current organ, objects with strong thermal signals, such as habitat features, were needed to drive the evolution of this remarkable sense.

Pitvipers (Viperidae: Crotalinae) possess thermal radiation receptors, the facial pits, which allow them to detect modest temperature fluctuations within their environments. It was previously thought that these organs were used solely to aid in prey acquisition, but recent findings demonstrated that western diamondback rattlesnakes (Crotalus atrox) use them to direct behavioral thermoregulation, suggesting that facial pits might be general purpose organs used to drive a suite of behaviors. To investigate this further, we conducted a phylogenetic survey of viperine thermoregulatory behavior cued by thermal radiation. We assessed this behavior in 12 pitviper species, representing key nodes in the evolution of pitvipers and a broad range of thermal environments, and a single species of true viper (Viperidae: Viperinae), a closely related subfamily of snakes that lack facial pits but possess a putative thermal radiation receptor. All pitviper species were able to rely on their facial pits to direct thermoregulatory movements, while the true viper was unable to do so. Our results suggest that thermoregulatory behavior cued by thermal radiation is a universal role of facial pits and probably represents an ancestral trait among pitvipers. Further, they establish behavioral thermoregulation as a plausible hypothesis explaining the evolutionary origin of the facial pit.

A new species of terrestrial pitviper, Porthidium porrasi, is described from mesophytic forests of the Península de Osa and surrounding area of the Pacific versant of southwestern Costa Rica. It is most similar to P. nasutum and is characterized by a pattern of bands, persistence of the juvenile tail color in adults, and a high number of dorsal scales. Analysis of mtDNA sequences confirms its distinction from P. nasutum. The existence of this species reinforces the notion of elevated herpetofaunal endemism in southwestern Costa Rica.

Snakes from temperate climates are often made to hibernate in zoos to stimulate reproduction. Unfortunately, deaths have occurred during and after hibernation. This study evaluated the health status, pre- and posthibernation, of 31 adult viperid snakes. It included morphometric measurements, hematology, and blood chemistry. No differences were seen in body weights and weight to length ratios between pre- and posthibernation examinations, suggesting that the overall condition of the snakes did not change. No differences were seen in hematologic and blood chemistry parameters, except that bile acids (3alpha-hydroxybile acids) decreased, the implications of which are unknown. Three individuals had markedly high plasma uric acid levels posthibernation; of these, two individuals died from extensive visceral gout and one recovered with fluid therapy. Viperid snakes should be clinically healthy, well hydrated, and in good body condition when they are put into hibernation. They should be maintained in an environment with sufficient humidity and should have access to water. Blood samples should be collected on arousal for measuring plasma uric acid levels. Changes in morphometry, hematology, and blood chemistry appear to be abnormal and should be investigated thoroughly.

A new species of green, prehensile-tailed pitviper of the genus Bothriechis is described from the Atlantic slopes of eastern Guatemala and western Honduras. This species appears to be most closely related to B. bicolor of the Pacific versant of Chiapas (Mexico) and Guatemala. Several other species of Bothriechis occur on the Atlantic versant of northern Central America, including two montane species, B. aurifer and B. marchi but, with one possible exception, these are not known to be sympatric with the new species and occur in different mountain ranges. The widespread B. schlegelii occurs up to at least 900 m on the Sierra de Caral, where the lowest elevation recorded for the new species is 885 m.

The macroecological relationship between geographic range size and body size has been described recently as an envelope region defined in bivariate space and limited by ecological and physical constraints. These constraints can be explained by selective processes acting at different levels and theories for an optimal body size. However, since data are obtained for different species in a large taxonomic group, at continental scales, it is possible that these variables may be strongly affected by spatial and phylogenetic autocorrelations. In this paper, we analyzed data on geographic range size (GRS) and body size (BS) for 36 species of Viperid snakes from South America, searching for spatial trends that could affect the shape of the macroecological constraint space. Data were analyzed using spatial autocorrelation and trend surface analyses, detecting a significant spatial pattern for GRS, fitted by a quadratic trend (R2 = 0.665; P < 0.001). After removing this effect, the relationship between trend residuals for GRS and BS still forms a constraint space, in such a way that results for South American Viperid snakes support both the shape of constraint space previously observed in other taxonomic groups and the ecological and evolutionary processes developed to explain it.