Phylogenetic patterns in learning and decision making in pit vipers (Viperidae: Crotalinae)

Sexual size dimorphism in snakes is closely related to mating behavior and fecundity selection. It provides important information on animal morphology and evolutionary ecology because it allows us to identify key morphological and functional traits between sexes and infer intraspecific competition. In this study, we measured the morphological characters of 147 individuals of three pit viper species stored in the archive of the National Institute of Biological Resources of the Ministry of Environment and confirmed interspecific differences and sexual size dimorphism of each species. We also identified important characters affecting identification using linear discriminant analysis. The results showed that the three pit viper species differed in body and head morphology, and the number of dorsal scale rows was the most important character for species identification. It was found that female red-tongued pit vipers and short-tailed pit vipers were larger than males of each species, while male Central Asian pit vipers were larger than females. Characters related to tail length and head length were confirmed as important characters for interspecific sex discrimination. We compared characters related to head morphology between sexes to find that red-tongued pit vipers showed differences in most characters, while short-tailed pit vipers and Central Asian pit vipers did not. Therefore, short-tailed pit vipers and Central Asian pit vipers are expected to have strong intraspecific competitive pressure. In future studies, it will be necessary to conduct a detailed research on intraspecific competition of short-tailed pit vipers and Central Asian pit vipers with little morphological differences between sexes by examining resource utilization (e.g., food sources and habitats) and ecological niche.

Sexual size dimorphism in snakes is closely related to mating behavior and fecundity selection. It provides important information on animal morphology and evolutionary ecology because it allows us to identify key morphological and functional traits between sexes and infer intraspecific competition. In this study, we measured the morphological characters of 147 individuals of three pit viper species stored in the archive of the National Institute of Biological Resources of the Ministry of Environment and confirmed interspecific differences and sexual size dimorphism of each species. We also identified important characters affecting identification using linear discriminant analysis. The results showed that the three pit viper species differed in body and head morphology, and the number of dorsal scale rows was the most important character for species identification. It was found that female red-tongued pit vipers and short-tailed pit vipers were larger than males of each species, while male Central Asian pit vipers were larger than females. Characters related to tail length and head length were confirmed as important characters for interspecific sex discrimination. We compared characters related to head morphology between sexes to find that red-tongued pit vipers showed differences in most characters, while short-tailed pit vipers and Central Asian pit vipers did not. Therefore, short-tailed pit vipers and Central Asian pit vipers are expected to have strong intraspecific competitive pressure. In future studies, it will be necessary to conduct a detailed research on intraspecific competition of short-tailed pit vipers and Central Asian pit vipers with little morphological differences between sexes by examining resource utilization (e.g., food sources and habitats) and ecological niche.

The ability to discriminate among potential prey is foundational for predators making foraging decisions, as well as for the evolution of food preferences. Eastern Indigo Snakes (Drymarchon couperi; EIS) are federally threatened and considered dietary generalists, but qualitative evidence indicates that snakes are consumed more often than other prey types. In this study, we used a repeated-measures tongue-flick assay to investigate EIS response to prey scent experimentally, and made inferences about potential preferences. Hatchling EIS responded more strongly to scents from snakes as compared to their response to scents from mice or controls. Moreover, hatchling EIS discriminated between the scents of representative colubrid and crotaline snakes, exhibiting a stronger response to the latter. A follow-up experiment using scents from three different species of pit vipers indicated that hatchling EIS did not discriminate among scents from members of this snake subfamily. After a year in captivity in...

Infrared imaging in vipers: differential responses of crotaline and viperine snakes to paired thermal targets

You have accessMoreSectionsView PDF ToolsAdd to favoritesDownload CitationsTrack Citations ShareShare onFacebookTwitterLinked InRedditEmail Cite this article Roth Timothy C., Brodin Anders, Smulders Tom V., LaDage Lara D. and Pravosudov Vladimir V. 2010Is bigger always better? A critical appraisal of the use of volumetric analysis in the study of the hippocampusPhil. Trans. R. Soc. B3652423http://doi.org/10.1098/rstb.2010.0163SectionYou have accessCorrectionsIs bigger always better? A critical appraisal of the use of volumetric analysis in the study of the hippocampus Timothy C. Roth Timothy C. Roth Google Scholar Find this author on PubMed Search for more papers by this author , Anders Brodin Anders Brodin Google Scholar Find this author on PubMed Search for more papers by this author , Tom V. Smulders Tom V. Smulders Google Scholar Find this author on PubMed Search for more papers by this author , Lara D. LaDage Lara D. LaDage Google Scholar Find this author on PubMed Search for more papers by this author and Vladimir V. Pravosudov Vladimir V. Pravosudov Google Scholar Find this author on PubMed Search for more papers by this author Timothy C. Roth Timothy C. Roth Google Scholar Find this author on PubMed Search for more papers by this author , Anders Brodin Anders Brodin Google Scholar Find this author on PubMed Search for more papers by this author , Tom V. Smulders Tom V. Smulders Google Scholar Find this author on PubMed Search for more papers by this author , Lara D. LaDage Lara D. LaDage Google Scholar Find this author on PubMed Search for more papers by this author and Vladimir V. Pravosudov Vladimir V. Pravosudov Google Scholar Find this author on PubMed Search for more papers by this author Published:12 August 2010https://doi.org/10.1098/rstb.2010.0163This article corrects the followingReview ArticleIs bigger always better? A critical appraisal of the use of volumetric analysis in the study of the hippocampushttps://doi.org/10.1098/rstb.2009.0208 Timothy C. Roth, Anders Brodin, Tom V. Smulders, Lara D. LaDage and Vladimir V. Pravosudov volume 365issue 1542Philosophical Transactions of the Royal Society B: Biological Sciences27 March 2010There was an error in figure 2. The corrected figure is as shown below. Download figureOpen in new tabDownload PowerPoint Previous Article VIEW FULL TEXT DOWNLOAD PDF FiguresRelatedReferencesDetailsCited by Krochmal A, Place A, LaDuc T and Roth T (2018) Phylogenetic patterns in learning and decision making in pit vipers (Viperidae: Crotalinae), Animal Behaviour, 10.1016/j.anbehav.2018.09.016, 145, (117-123), Online publication date: 1-Nov-2018. Striedter G (2015) Evolution of the hippocampus in reptiles and birds, Journal of Comparative Neurology, 10.1002/cne.23803, 524:3, (496-517), Online publication date: 15-Feb-2016. Related articlesIs bigger always better? A critical appraisal of the use of volumetric analysis in the study of the hippocampus27 March 2010Philosophical Transactions of the Royal Society B: Biological Sciences This Issue12 August 2010Volume 365Issue 1551Theme Issue 'Neuronal network analyses: progress, problems, and uncertainties' compiled and edited by David Parker Article InformationDOI:https://doi.org/10.1098/rstb.2010.0163Published by:Royal SocietyPrint ISSN:0962-8436Online ISSN:1471-2970History: Published online12/08/2010Published in print12/08/2010 License:© 2010 The Royal Society Citations and impact Subjectsbehaviourcognitionneuroscience

Background/Objectives: Pit vipers (subfamily Crotalinae) are responsible for a large proportion of snakebite envenoming cases in Southeast Asia. Envenomation by these snakes commonly causes hematotoxic effects, including platelet dysfunction and coagulation disturbances. Although antivenom remains the mainstay of treatment, species-specific antivenoms are not available for several regional pit viper species. This study evaluated the hematotoxic activities of selected Southeast Asian pit viper venoms and the cross-neutralizing capacity of commercially available antivenoms. Methods: Venoms from five medically important pit viper species-Calloselasma rhodostoma, Trimeresurus albolabris, T. hageni, T. purpureomaculatus, and Tropidolaemus wagleri-were tested. Washed platelets and platelet-poor plasma obtained from healthy individuals (n = 10) were used to assess venom-induced platelet aggregation and coagulation, respectively. The neutralizing effects of three antivenoms including hemato polyvalent antivenom (HPAV), T. albolabris antivenom (TAAV), and C. rhodostoma antivenom (CRAV)-were examined in vitro. Results: All tested venoms induced in vitro platelet aggregation (%Max > 50%) and promoted plasma coagulation. At the manufacturer-recommended concentration, TAAV significantly cross-neutralized the hematotoxic effects of T. purpureomaculatus and T. hageni venoms (p < 0.0001) but failed to neutralize coagulation induced by T. wagleri. CRAV showed no cross-neutralization against arboreal pit viper venoms. In contrast, HPAV strongly inhibited platelet aggregation and coagulation induced by all tested venoms (p < 0.0001). Conclusions: These findings highlight the limited cross-neutralization capacity of monovalent antivenoms against arboreal pit viper hematotoxicity. In contrast, HPAV demonstrated broad cross-neutralizing activity and may represent a practical therapeutic option for Southeast Asian pit viper envenoming when species-specific antivenoms are unavailable.

In vivo diminution by chelators of snake venom-provoked hemorrhage and in vitro inhibition of proteolytic activity

Melanin deposits in the heads of both true vipers (Viperinae) and pit vipers (Crotalinae) are concentrated over the dorsal and dorsolateral aspects of the venom glands. This pigment may occur in any or all of six sites which include the epidermis, dermis, tissues covering the venom glands, and the interior of the glands themselves. The extreme localization of these melanin deposits suggests that they shield the venom glands from light. Calculations indicate that without such shielding the light energy penetrating the venom glands in the visible and ultraviolet portions of the solar spectrum would damage the venom‐synthesizing apparatus and detoxify stored venom.Elapid and hydrophiid snakes have less dense pigment over the venom gland than vipers. Literature reports indicate that elapid venom is less sensitive to photodetoxification than is venom from vipers. Most colubrid snakes, including several with protein‐secreting Duvernoy's glands, have little or no melanin associated with the glands. Venomous colubrids in the genera Ahaetulla, Dryophis, Leptophis, and Oxybelis have pigment over the glands as dense as that seen in vipers.Iridophores probably also shield venom glands from radiation. In puff adders and Gaboon vipers (Bitis) there appears to be an ontogenetic change in the shielding of the venom glands from melanocytes in young individuals to iridophores in adults.

Protein expression level is one of the strongest predictors of protein sequence evolutionary rate, with high-expression protein sequences evolving at slower rates than low-expression protein sequences largely because of constraints on protein folding and function. Expression evolutionary rates also have been shown to be negatively correlated with expression level across human and mouse orthologs over relatively long divergence times (i.e., ∼100 million years). Long-term evolutionary patterns, however, often cannot be extrapolated to microevolutionary processes (and vice versa), and whether this relationship holds for traits evolving under directional selection within a single species over ecological timescales (i.e., <5000 years) is unknown and not necessarily expected. Expression is a metabolically costly process, and the expression level of a particular protein is predicted to be a tradeoff between the benefit of its function and the costs of its expression. Selection should drive the expression level of all proteins close to values that maximize fitness, particularly for high-expression proteins because of the increased energetic cost of production. Therefore, stabilizing selection may reduce the amount of standing expression variation for high-expression proteins, and in combination with physiological constraints that may place an upper bound on the range of beneficial expression variation, these constraints could severely limit the availability of beneficial expression variants. To determine whether rapid-expression evolution was restricted to low-expression proteins owing to these constraints on highly expressed proteins over ecological timescales, we compared venom protein expression levels across mainland and island populations for three species of pit vipers. We detected significant differentiation in protein expression levels in two of the three species and found that rapid-expression differentiation was restricted to low-expression proteins. Our results suggest that various constraints on high-expression proteins reduce the availability of beneficial expression variants relative to low-expression proteins, enabling low-expression proteins to evolve and potentially lead to more rapid adaptation.

It is known that striking rodent prey induces a sustained, high rate of tongue flicking in rattlesnakes. The present study shows this phenomenon (called strike-induced chemosensory searching, SICS) to occur in species of rattlesnakes not previously investigated and in two species ofAgkistrodon. SICS occurs in Old World vipers (Eristocophis, Vipera, Bitis), including species which normally hold their prey after striking. A hypothesis is offered which (1) accounts for the occurrence of SICS in these latter species and (2) suggests that SICS in some viperids may have arisen through paedomorphic evolution. More generally, it is concluded that SICS is probably a homologous trait in vipers and pit vipers and that the trait may have first appeared in elapid ancestors of the viperidae.

It has been suggested that true vipers (Viperidae: Viperinae) possess the ability to detect temperature differences between objects despite the lack of an apparent infrared radiation sensor. We tested the ability to distinguish between heated and unheated targets in three species of pitvipers (Viperidae: Crotalinae), four species of true vipers, two species of colubrids (Colubridae: Natricinae, Colubrinae) and Azemiops feae (Viperidae: Azemiopinae). All species of pitvipers tested could distinguish between the warm and cool targets, while no tested species of true viper, colubrid or Azemiops demonstrated this ability. In addition, pitvipers exhibited behaviors that true vipers or Azemiops did not exhibit. Our results suggest that the tested species of true vipers, Azemiops and colubrids may not posses the ability to sense infrared radiation or do not use it in a defensive context, and suggest that some defensive behaviors are associated with the pit organ in pitvipers.

The hemipenes of four species of Chinese pit vipers, Trimeresurus albolabris, T. medoensis, T. stejnegeri, T. xiangchengensis, were described and illustrated. The results showed that the four species are notably different in hemipenial structures, and the hemipenes of four species can be clustered into three types. Furthermore, a comparison with the hemipenes of related species in the genus was conducted.

Diversification in vipers: Phylogenetic relationships, time of divergence and shifts in speciation rates

A novel 25 kDa protein from the venom of Bitis arietans with similarity to C-type lectins causes fibrinogen-dependent platelet agglutination

Context. Therapy for snakebites relies on the application of antivenoms, which may be produced with different immunogenic mixtures of venom and possess different pharmaceutical characteristics. For these reasons, immunological cross-reactivity and heterologous neutralization were analyzed relative to the protein content of three antivenoms used in the Americas. Methods. The antivenoms studied were composed of equine F(ab’)2 fragments from animals immunized with Crotalinae venoms. The antivenoms were tested against venoms of seven pit viper species from Argentina, seven from Mexico, one from Costa Rica, and one from Colombia. Results. Immunoblotting showed high cross-reactivity of all major protein bands with all the antivenoms tested. ELISA results also showed high cross-reactivity among the different venoms and antivenoms, and a high heterologous neutralization was observed. The results can be interpreted in different ways depending on whether the reactivity is considered in terms of the volume of antivenom used or by the amount of protein contained in this volume of antivenom. The antivenoms with high immunochemical reactivity and neutralizing capacity were those with higher protein content per vial; but when doses were adjusted by protein content, antivenoms of apparently lower neutralizing capacity and immunochemical reactivity showed at least similar potency and reactivity although volumetrically at higher doses. Conclusion. Protein content relative to neutralization potency of different products must be taken into account when antivenoms are compared, in addition to the volume required for therapeutic effect. These results show the importance of obtaining high-affinity and high-avidity antibodies to achieve good neutralization using low protein concentration and low-volume antivenoms.