Anthropogenic and climatic factors interact to influence reproductive timing and effort.

Reproduction, although absolutely essential to a species' persistence, is in itself challenging. As anthropogenic change increasingly affects every landscape on Earth, it is critical to understand how specific pressures impact the reproductive efforts of individuals, which directly contribute to the success or failure of populations. However, organisms rarely encounter a single burden at a time, and the interactions of environmental challenges can have compounding effects. Understanding environmental and physiological pressures is difficult because they are often context-dependent and not generalizable, but long-term monitoring across variable landscapes and weather patterns can improve our understanding of these complex interactions. We tested the effects of urbanization, climate, and individual condition on the reproductive investment of wild side-blotched lizards (Uta stansburiana) by measuring physiological/reproductive metrics from six populations in urban and rural areas over six consecutive years of variable precipitation. We observed that reproductive stage affected body condition, corticosterone concentration, and oxidative stress. We also observed that reproductive patterns differed between urban and rural populations depending on rainfall, with rural animals increasing reproductive investment during rainier years compared to urban conspecifics, and that reproductive decisions appeared to occur early in the reproductive process. These results demonstrate the plastic nature of a generalist species optimizing lifetime fitness under varying conditions.

Changes in capture availability due to infection can lead to detectable biases in population-level infectious disease parameters.

Correctly identifying the strength of selection that parasites impose on hosts is key to predicting epidemiological and evolutionary outcomes of host-parasite interactions. However, behavioral changes due to infection can alter the capture probability of infected hosts and thereby make selection difficult to estimate by standard sampling techniques. Mark-recapture approaches, which allow researchers to determine if some groups in a population are less likely to be captured than others, can be used to identify infection-driven capture biases. If a metric of interest directly compares infected and uninfected populations, calculated detection probabilities for both groups may be useful in identifying bias. Here, we use an individual-based simulation to test whether changes in capture rate due to infection can alter estimates of three key metrics: 1) reduction in the reproductive success of infected parents relative to uninfected parents, 2) the relative risk of infection for susceptible genotypes compared to resistant genotypes, and 3) changes in allele frequencies between generations. We explore the direction and underlying causes of the biases that emerge from these simulations. Finally, we argue that short series of mark-recapture sampling bouts, potentially implemented in under a week, can yield key data on detection bias due to infection while not adding a significantly higher burden to disease ecology studies.

Foraging predicts the evolution of warning coloration and mimicry in snakes.

Warning coloration and Batesian mimicry are classic examples of Darwinian evolution, but empirical evolutionary patterns are often paradoxical. We test whether foraging costs predict the evolution of striking coloration by integrating genetic and ecological data for aposematic and mimetic snakes (Elapidae and Dipsadidae). Our phylogenetic comparison on a total of 432 species demonstrated that dramatic changes in coloration were well predicted by foraging strategy. Multiple tests consistently indicated that warning coloration and conspicuous mimicry were more likely to evolve in species where foraging costs of conspicuous appearance were relaxed by poor vision of their prey, concealed habitat, or nocturnal activity. Reversion to crypsis was also well predicted by ecology for elapids but not for dipsadids. In contrast to a theoretical prediction and general trends, snakes' conspicuous coloration was correlated with secretive ecology, suggesting that a selection regime underlies evolutionary patterns. We also found evidence that mimicry of inconspicuous models (pitvipers) may have evolved in association with foraging demand for crypsis. These findings demonstrate that foraging is an important factor necessary to understand the evolution, persistence, and diversity of warning coloration and mimicry of snakes, highlighting the significance of additional selective factors in solving the warning coloration paradox.

An artificial intelligence model to identify snakes from across the world: Opportunities and challenges for global health and herpetology.

BACKGROUND: Snakebite envenoming is a neglected tropical disease that kills an estimated 81,000 to 138,000 people and disables another 400,000 globally every year. The World Health Organization aims to halve this burden by 2030. To achieve this ambitious goal, we need to close the data gap in snake ecology and snakebite epidemiology and give healthcare providers up-to-date knowledge and access to better diagnostic tools. An essential first step is to improve the capacity to identify biting snakes taxonomically. The existence of AI-based identification tools for other animals offers an innovative opportunity to apply machine learning to snake identification and snakebite envenoming, a life-threatening situation. METHODOLOGY: We developed an AI model based on Vision Transformer, a recent neural network architecture, and a comprehensive snake photo dataset of 386,006 training photos covering 198 venomous and 574 non-venomous snake species from 188 countries. We gathered photos from online biodiversity platforms (iNaturalist and HerpMapper) and a photo-sharing site (Flickr). PRINCIPAL FINDINGS: The model macro-averaged F1 score, which reflects the species-wise performance as averaging performance for each species, is 92.2%. The accuracy on a species and genus level is 96.0% and 99.0%, respectively. The average accuracy per country is 94.2%. The model accurately classifies selected venomous and non-venomous lookalike species from Southeast Asia and sub-Saharan Africa. CONCLUSIONS: To our knowledge, this model's taxonomic and geographic coverage and performance are unprecedented. This model could provide high-speed and low-cost snake identification to support snakebite victims and healthcare providers in low-resource settings, as well as zoologists, conservationists, and nature lovers from across the world.

Propagule size and sex ratio influence colonisation dynamics after introduction of a non-native lizard.

The composition of founding populations plays an important role in colonisation dynamics and can influence population growth during early stages of biological invasion. Specifically, founding populations with small propagules (i.e. low number of founders) are vulnerable to the Allee effect and have reduced likelihood of establishment compared to those with large propagules. The founding sex ratio can also impact establishment via its influence on mating success and offspring production. Our goal was to test the effects of propagule size and sex ratio on offspring production and annual population growth following introductions of a non-native lizard species (Anolis sagrei). We manipulated propagule composition on nine small islands, then examined offspring production, population growth and survival rate of founders and their descendants encompassing three generations. By the third reproductive season, per capita offspring production was higher on islands seeded with a relatively large propagule size, but population growth was not associated with propagule size. Propagule sex ratio did not affect offspring production, but populations with a female-biased propagule had positive growth, whereas those with a male-biased propagule had negative growth in the first year. Populations were not affected by propagule sex ratio in subsequent years, possibly due to rapid shifts towards balanced (or slightly female biased) population sex ratios. Overall, we show that different components of population fitness have different responses to propagule size and sex ratio in ways that could affect early stages of biological invasion. Despite these effects, the short life span and high fecundity of A. sagrei likely helped small populations to overcome Allee effects and enabled all populations to successfully establish. Our rare experimental manipulation of propagule size and sex ratio can inform predictions of colonisation dynamics in response to different compositions of founding populations, which is critical in the context of population ecology and invasion dynamics.

Citizen science and online data: Opportunities and challenges for snake ecology and action against snakebite.

The secretive behavior and life history of snakes makes studying their biology, distribution, and the epidemiology of venomous snakebite challenging. One of the most useful, most versatile, and easiest to collect types of biological data are photographs, particularly those that are connected with geographic location and date-time metadata. Photos verify occurrence records, provide data on phenotypes and ecology, and are often used to illustrate new species descriptions, field guides and identification keys, as well as in training humans and computer vision algorithms to identify snakes. We scoured eleven online and two offline sources of snake photos in an attempt to collect as many photos of as many snake species as possible, and attempt to explain some of the inter-species variation in photograph quantity among global regions and taxonomic groups, and with regard to medical importance, human population density, and range size. We collected a total of 725,565 photos-between 1 and 48,696 photos of 3098 of the world's 3879 snake species (79.9%), leaving 781 "most wanted" species with no photos (20.1% of all currently-described species as of the December 2020 release of The Reptile Database). We provide a list of most wanted species sortable by family, continent, authority, and medical importance, and encourage snake photographers worldwide to submit photos and associated metadata, particularly of "missing" species, to the most permanent and useful online archives: The Reptile Database, iNaturalist, and HerpMapper.

Supervised Learning Computer Vision Benchmark for Snake Species Identification From Photographs: Implications for Herpetology and Global Health.

We trained a computer vision algorithm to identify 45 species of snakes from photos and compared its performance to that of humans. Both human and algorithm performance is substantially better than randomly guessing (null probability of guessing correctly given 45 classes = 2.2%). Some species (e.g., Boa constrictor) are routinely identified with ease by both algorithm and humans, whereas other groups of species (e.g., uniform green snakes, blotched brown snakes) are routinely confused. A species complex with largely molecular species delimitation (North American ratsnakes) was the most challenging for computer vision. Humans had an edge at identifying images of poor quality or with visual artifacts. With future improvement, computer vision could play a larger role in snakebite epidemiology, particularly when combined with information about geographic location and input from human experts.

Ectoparasite Load Is Reduced in Side-Blotched Lizards (Uta stansburiana) at Wind Farms: Implications for Oxidative Stress.

AbstractWind-generated power is one of the fastest growing alternative energy strategies worldwide and will likely account for 20% of US energy production by 2030. The installation and maintenance of wind farms are associated with increased human activity and can generate noise pollution, disturb and fragment habitat, and even alter community composition and structure. These environmental and ecological changes can increase physiological stress for vertebrates and affect important life-history attributes, such as immune function. However, little is known about how wind farms influence physiology and disease or parasite resistance in nonvolant wildlife. Here, we test the notion that renewable wind farms increase physiological stress and correlated aspects of disease resistance (parasite load) in a common desert vertebrate, the side-blotched lizard (Uta stansburiana). We captured lizards from three wind farms and three undisturbed reference sites in the San Gorgonio Pass wind resource area in the Mojave Desert, California. We quantified individual external parasite loads and measured plasma antioxidant capacity and concentrations of reactive oxygen metabolites as a combined metric of oxidative stress. Contrary to our expectations, individuals at wind farm sites had significantly fewer external parasites than at undeveloped sites. Additionally, we found a slight positive correlation between parasite load and oxidative stress for individuals at wind farm sites but not at reference sites. Our results demonstrate a complex, potentially context-dependent relationship between stress physiology and disease resistance for lizards in anthropogenically disturbed environments. Understanding how wind farms affect the physiology and ecoimmunology of terrestrial fauna is necessary to mitigate the ecological costs of alternative energy development.

Citizen science and online data: opportunities and challenges for snake ecology and action against snakebite

The secretive behavior and life history of snakes makes studying their biology, distribution, and the epidemiology of venomous snakebite challenging. One of the most useful, most versatile, and easiest to collect types of biological data are photographs, particularly those that are connected with geographic location and date-time metadata. Photos verify occurrence records, provide data on phenotypes and ecology, and are often used to illustrate new species descriptions, field guides and identification keys, as well as in training humans and computer vision algorithms to identify snakes. We scoured eleven online and two offline sources of snake photos in an attempt to collect as many photos of as many snake species as possible, and attempt to explain some of the inter-species variation in photograph quantity among global regions and taxonomic groups, and with regard to medical importance, human population density, and range size. We collected a total of 725,565 photos—between 1 and 48,696 photos of 3098 of the world's 3879 snake species (79.9%), leaving 781 “most wanted” species with no photos (20.1% of all currently-described species as of the December 2020 release of The Reptile Database). We provide a list of most wanted species sortable by family, continent, authority, and medical importance, and encourage snake photographers worldwide to submit photos and associated metadata, particularly of “missing” species, to the most permanent and useful online archives: The Reptile Database, iNaturalist, and HerpMapper.

What makes a fang? Phylogenetic and ecological controls on tooth evolution in rear-fanged snakes.

BACKGROUND: Fangs are a putative key innovation that revolutionized prey capture and feeding in snakes, and - along with their associated venom phenotypes - have made snakes perhaps the most medically-significant vertebrate animals. Three snake clades are known for their forward-positioned fangs, and these clades (Elapidae, Viperidae, and Atractaspidinae) contain the majority of snakes that are traditionally considered venomous. However, many other snakes are "rear-fanged": they possess potentially venom-delivering teeth situated at the rear end of the upper jaw. Quantification of fang phenotypes - and especially those of rear-fanged species - has proved challenging or impossible owing to the small size and relative rarity of many such snakes. Consequently, it has been difficult to understand the evolutionary history of both venom and prey-capture strategies across extant snakes. We quantified variation in the dentition of 145 colubriform ("advanced") snake species using microCT scanning and compared dental characters with ecological data on species' diet and prey capture method(s) to understand broader patterns in snake fang evolution. RESULTS: Dental traits such as maxilla length, tooth number, and fang size show strong phylogenetic signal across Colubriformes. We find extreme heterogeneity and evolutionary lability in the rear-fanged phenotype in colubrid (colubrine, dipsadine, and natricine lineages) and lamprophiid snakes, in contrast to relative uniformity in the front fanged phenotypes of other groups (vipers and, to a lesser extent, elapids). Fang size and position are correlated with venom-use in vipers, elapids, and colubrid snakes, with the latter group shifting fangs anteriorly by shortening the entire maxillary bone. We find that maxilla length and tooth number may also be correlated with the evolution of dietary specialization. Finally, an ancestral state reconstruction suggests that fang loss is a recurring phenomenon in colubrid snakes, likely accompanied by shifts in diet and prey capture mode. CONCLUSIONS: Our study provides a framework for quantifying the complex morphologies associated with venom use in snakes. Our results suggest that fang phenotypes, and particularly the rear-fanged phenotype, in snakes are both diverse and labile, facilitating a wide range of ecological strategies and contributing to spectacular radiations of these organisms in tropical and subtropical biomes worldwide.

What do stable isotopes tell us about the trophic ecology of Thamnodynastes hypoconia (Serpentes: Dipsadidae) in southern Brazil?

Snakes are a useful model for ecological studies because they are gape-limited predators that may undergo ontogenetic changes in diet. We analyzed carbon and nitrogen stable isotope ratios to estimate percent contributions of different prey to snake biomass, trophic positions and isotopic niche width of juveniles and adults of the snake Thamnodynastes hypoconia. We also estimated the isotopic niche overlap between the two age categories. During eight intervals over a two-year period, we collected samples of whole blood and scales at a site in southern Brazil. Isotopic ratios of carbon and nitrogen did not differ between juveniles and adults for either tissue type, nor did mean trophic positions of juveniles and adults differ. The percent contribution of prey categories to snake biomass differed to a limited extent between the two years, with Hylidae being the most important anuran group assimilated during the first year and Leptodactylidae during the second year, for both ages. The isotopic niche occupied by adult snakes was slightly larger than that of juveniles when the analysis was based on data from whole blood samples, as expected because snakes are gape-limited. We found a reverse pattern when the analysis was based on scales, which may indicate that adult snakes have a smaller niche over the long term as they become selective foragers in certain prey. Isotopic overlap between juveniles and adults occurred during the two years, but it was bigger during the second year. We infer that, despite differences in gape size, juvenile and adult snakes in the study area exploit similar prey, with the degree of trophic similarity varying interannually.

Identifying the snake: First scoping review on practices of communities and healthcare providers confronted with snakebite across the world.

BACKGROUND: Snakebite envenoming is a major global health problem that kills or disables half a million people in the world's poorest countries. Biting snake identification is key to understanding snakebite eco-epidemiology and optimizing its clinical management. The role of snakebite victims and healthcare providers in biting snake identification has not been studied globally. OBJECTIVE: This scoping review aims to identify and characterize the practices in biting snake identification across the globe. METHODS: Epidemiological studies of snakebite in humans that provide information on biting snake identification were systematically searched in Web of Science and Pubmed from inception to 2nd February 2019. This search was further extended by snowball search, hand searching literature reviews, and using Google Scholar. Two independent reviewers screened publications and charted the data. RESULTS: We analysed 150 publications reporting 33,827 snakebite cases across 35 countries. On average 70% of victims/bystanders spotted the snake responsible for the bite and 38% captured/killed it and brought it to the healthcare facility. This practice occurred in 30 countries with both fast-moving, active-foraging as well as more secretive snake species. Methods for identifying biting snakes included snake body examination, victim/bystander biting snake description, interpretation of clinical features, and laboratory tests. In nine publications, a picture of the biting snake was taken and examined by snake experts. Snakes were identified at the species/genus level in only 18,065/33,827 (53%) snakebite cases. 106 misidentifications led to inadequate victim management. The 8,885 biting snakes captured and identified were from 149 species including 71 (48%) non-venomous species. CONCLUSION: Snakebite victims and healthcare providers can play a central role in biting snake identification and novel approaches (e.g. photographing the snake, crowdsourcing) could help increase biting snake taxonomy collection to better understand snake ecology and snakebite epidemiology and ultimately improve snakebite management.

Stoichiometric and stable isotope ratios of wild lizards in an urban landscape vary with reproduction, physiology, space and time.

Spatial and temporal variation in stoichiometric and stable isotope ratios of animals contains ecological information that we are just beginning to understand. In both field and lab studies, stoichiometric or isotopic ratios are related to physiological mechanisms underlying nutrition or stress. Conservation and ecosystem ecology may be informed by isotopic data that can be rapidly and non-lethally collected from wild animals, especially where human activity leaves an isotopic signature (e.g. via introduction of chemical fertilizers, ornamental or other non-native plants or organic detritus). We examined spatial and temporal variation in stoichiometric and stable isotope ratios of the toes of Uta stansburiana (side-blotched lizards) living in urban and rural areas in and around St. George, Utah. We found substantial spatial and temporal variation as well as context-dependent co-variation with reproductive physiological parameters, although certain key predictions such as the relationship between δ15N and body condition were not supported. We suggest that landscape change through urbanization can have profound effects on wild animal physiology and that stoichiometric and stable isotope ratios can provide unique insights into the mechanisms underlying these processes.

Long-term monitoring of two snake species reveals immune-endocrine interactions and the importance of ecological context.

While there is huge promise in monitoring physiological parameters in free-living organisms, we also find high amounts of variability over time and space. This variation requires us to capitalize on long-term physiological monitoring to adequately address questions of population health, conservation status, or evolutionary trends as long-term sampling can examine ecoimmunological and endocrine interactions in wild populations while accounting for the variation that often makes ecophysiological field studies difficult to compare. In this study, we tested how immune efficacy and endocrinology interact while accounting for ecological context and environmental conditions in two snake species. Specifically, we measured bacterial killing ability, steroid hormones, and morphological characteristics in multiple populations of the Western Terrestrial Gartersnake (Thamnophis elegans) and Common Gartersnake (T. sirtalis) for multiple seasons over 6 years. Leveraging this long-term dataset, we tested how a broad immune measure and endocrine endpoints interact while accounting for individual traits, sampling date, and environmental conditions. Across both species, we found bacterial killing ability to be directly related to corticosterone (CORT) and temperature and greater overall in the spring compared to the fall. We found CORT and testosterone yielded relationships with individual sex, sampling temperature, and time of year. Wild populations can exhibit high amounts of variation in commonly collected physiological endpoints, highlighting the complexity and difficulty inherent in interpreting single endpoints without taking ecological and environmental conditions into account. Our study emphasizes the importance of reporting the environmental conditions under which the sampling occurred to allow for better contextualization and comparison between studies.

Investment of both essential fatty and amino acids to immunity varies depending on reproductive stage.

Trade-offs among the key life-history traits of reproduction and immunity have been widely documented. However, the currency in use is not well-understood. We investigated how reproducing female side-blotched lizards, Uta stansburiana, allocate lipids versus proteins when given an immune challenge. We tested whether lizards would invest more in reproduction or immunity depending on reproductive stage. Females were given stable isotopes (15 N-leucine and 13 C-1-palmitic acid), maintained on a regular diet and given either a cutaneous biopsy or a sham biopsy (control). Stable isotopes were monitored and analyzed in feces and uric acid, skin biopsies, eggs, and toe clips. We found that lizards deposited both proteins and lipids into their healing wounds (immune-challenged), skin (control), and eggs (all) and that catabolism of proteins exceeded incorporation into tissue during wound-healing. Specifically, we found that healed biopsies of wounded animals had more leucine and palmitic acid than the nonregrown skin biopsies taken from unwounded control animals. Earlier in reproduction, lizards invested relatively more labeled proteins into healing their wound tissue, but not into unwounded skin of control animals. Thus, reproduction is sometimes favored over self-maintenance, but only in later reproductive stages. Finally, we documented positive relationships among the amount of palmitic acid deposited in the eggs, the amount of food eaten, and the amount of palmitic acid excreted, suggesting higher turnover rates of lipids in lizards investing highly in their eggs.

Physiological Correlates of Multiple Parasitic Infections in Side-Blotched Lizards.

We investigated the presence of ectoparasites and hemoparasites in side-blotched lizards (Uta stansburiana) across a large part of their range and measured how parasitic infection related to several key physiological indicators of health. Blood samples were collected from 132 lizards from central Arizona, southern Utah, and eastern Oregon. Hemoparasites were found in 22 individuals (3.2% prevalence in Arizona, 19.1% in Utah, and 6.3% in Oregon), and ectoparasites were found on 51 individuals (56.3% prevalence in Arizona, 56.1% in Utah, and 6.7% in Oregon), with 11 individuals infected with both. Hemoparasites and ectoparasites were found in all three states. Immunocompetence was higher in individuals infected with both hemoparasites and ectoparasites. Body condition, glucocorticoid levels, and reproductive investment were not related to infection status. Our study provides evidence that parasitic infection is associated with an active immune system in wild reptiles but may not impose other costs usually associated with parasites.

Ontogenetic shifts in the diet of plains hog-nosed snakes (Heterodon nasicus) revealed by stable isotope analysis.

Wild snake diets are difficult to study using traditional methods, but stable isotopes offer several advantages, including integrating dietary information over time, providing data from individuals that have not fed recently, and avoiding bias towards slowly-digesting prey items. We used stable isotope signatures of carbon and nitrogen from scale tissue, red blood cells, and blood plasma to assess the diet of wild plains hog-nosed snakes (Heterodon nasicus) in Illinois. We developed Bayesian mixing models which, taken together, predicted that H. nasicus shifted from a juvenile diet predominantly (31-63%) composed of six-lined racerunners (Aspidoscelis sexlineatus) and their eggs to an adult diet predominantly (44-56%) composed of eggs of the aquatic turtles Chrysemys picta and Chelydra serpentina, with a contribution from toads (Anaxyrus sp.; 6-27%) during their adolescent years. These results agreed with sparse data from gut contents. Combining traditional and isotopic techniques for studying the diets of wild snakes can increase the utility of both types of data.