Hidden social complexity behind vocal and acoustic communication in non-avian reptiles.

Social interactions are inevitable in the lives of most animals, since most essential behaviours require interaction with conspecifics, such as mating and competing for resources. Non-avian reptiles are typically viewed as solitary animals that predominantly use their vision and olfaction to communicate with conspecifics. Nevertheless, in recent years, evidence is mounting that some reptiles can produce sounds and have the potential for acoustic communication. Reptiles that can produce sound have an additional communicative channel (in addition to visual/olfactory channels), which could suggest they have a higher communicative complexity, the evolution of which is assumed to be driven by the need of social interactions. Thus, acoustic reptiles may provide an opportunity to unveil the true social complexity of reptiles that are usually thought of as solitary. This review aims to reveal the hidden social interactions behind the use of sounds in non-avian reptiles. Our review suggests that the potential of vocal and acoustic communication and the complexity of social interactions may be underestimated in non-avian reptiles, and that acoustic reptiles may provide a great opportunity to uncover the coevolution between sociality and communication in non-avian reptiles. This article is part of the theme issue 'The power of sound: unravelling how acoustic communication shapes group dynamics'.

Threats to reptiles at global and regional scales.

Reptiles are an important, yet often understudied, taxon in nature conservation. They play a significant role in ecosystems1 and can serve as indicators of environmental health, often responding more rapidly to human pressures than other vertebrate groups.2 At least 21% of reptiles are currently assessed as threatened with extinction by the IUCN.3 However, due to the lack of comprehensive global assessments until recently, they have been omitted from spatial studies addressing conservation or spatial prioritization (e.g., Rosauer et al.,4,5,6,7,8 Fritz and Rahbek,4,5,6,7,8 Farooq et al.,4,5,6,7,8 Meyer et al., 4,5,6,7,8 and Farooq et al.4,5,6,7,8). One important knowledge gap in conservation is the lack of spatially explicit information on the main threats to biodiversity,9 which significantly hampers our ability to respond effectively to the current biodiversity crisis.10,11 In this study, we calculate the probability of a reptile species in a specific location being affected by one of seven biodiversity threats-agriculture, climate change, hunting, invasive species, logging, pollution, and urbanization. We conducted the analysis at a global scale, using a 50 km × 50 km grid, and evaluated the impact of these threats by studying their relationship with the risk of extinction. We find that climate change, logging, pollution, and invasive species are most linked to extinction risk. However, we also show that there is considerable geographical variation in these results. Our study highlights the importance of going beyond measuring the intensity of threats to measuring the impact of these separately for various biogeographical regions of the world, with different historical contingencies, as opposed to a single global analysis treating all regions the same.

Poly- and perfluoroalkyl substances (PFASs) in amphibians and reptiles - exposure and health effects.

Poly- and perfluoroalkyl substances (PFASs) are commonly used in various industries and everyday products, including clothing, electronics, furniture, paints, and many others. PFASs are primarily found in aquatic environments, but also present in soil, air and plants, making them one of the most important and dangerous pollutants of the natural environment. PFASs bioaccumulate in living organisms and are especially dangerous to aquatic and semi-aquatic animals. As endocrine disruptors, PFASs affect many internal organs and systems, including reproductive, endocrine, nervous, cardiovascular, and immune systems. This manuscript represents the first comprehensive review exclusively focusing on PFASs in amphibians and reptiles. Both groups of animals are highly vulnerable to PFASs in the natural habitats. Amphibians and reptiles, renowned for their sensitivity to environmental changes, are often used as crucial bioindicators to monitor ecosystem health and environmental pollution levels. Furthermore, the decline in amphibian and reptile populations worldwide may be related to increasing environmental pollution. Therefore, studies investigating the exposure of amphibians and reptiles to PFASs, as well as their impacts on these organisms are essential in modern toxicology. Summarizing the current knowledge on PFASs in amphibians and reptiles in a single manuscript will facilitate the exploration of new research topics in this field. Such a comprehensive review will aid researchers in understanding the implications of PFASs exposure on amphibians and reptiles, guiding future investigations to mitigate their adverse effects of these vital components of ecosystems.

Asymmetric fin shape changes swimming dynamics of ancient marine reptiles' soft robophysical models.

Animals have evolved highly effective locomotion capabilities in terrestrial, aerial, and aquatic environments. Over life's history, mass extinctions have wiped out unique animal species with specialized adaptations, leaving paleontologists to reconstruct their locomotion through fossil analysis. Despite advancements, little is known about how extinct megafauna, such as the Ichthyosauria one of the most successful lineages of marine reptiles, utilized their varied morphologies for swimming. Traditional robotics struggle to mimic extinct locomotion effectively, but the emerging soft robotics field offers a promising alternative to overcome this challenge. This paper aims to bridge this gap by studyingMixosauruslocomotion with soft robotics, combining material modeling and biomechanics in physical experimental validation. Combining a soft body with soft pneumatic actuators, the soft robotic platform described in this study investigates the correlation between asymmetrical fins and buoyancy by recreating the pitch torque generated by extinct swimming animals. We performed a comparative analysis of thrust and torque generated byCarthorhyncus,Utatsusaurus,Mixosaurus,Guizhouichthyosaurus, andOphthalmosaurustail fins in a flow tank. Experimental results suggest that the pitch torque on the torso generated by hypocercal fin shapes such as found in model systems ofGuizhouichthyosaurus,MixosaurusandUtatsusaurusproduce distinct ventral body pitch effects able to mitigate the animal's non-neutral buoyancy. This body pitch control effect is particularly pronounced inGuizhouichthyosaurus, which results suggest would have been able to generate high ventral pitch torque on the torso to compensate for its positive buoyancy. By contrast, homocercal fin shapes may not have been conducive for such buoyancy compensation, leaving torso pitch control to pectoral fins, for example. Across the range of the actuation frequencies of the caudal fins tested, resulted in oscillatory modes arising, which in turn can affect the for-aft thrust generated.

ReptTraits: a comprehensive dataset of ecological traits in reptiles.

Trait datasets are increasingly being used in studies investigating eco-evolutionary theory and global conservation initiatives. Reptiles are emerging as a key group for studying these questions because their traits are crucial for understanding the ability of animals to cope with environmental changes and their contributions to ecosystem processes. We collected data from earlier databases, and the primary literature to create an up-to-date dataset of reptilian traits, encompassing 40 traits from 12060 species of reptiles (Archelosauria: Crocodylia and Testudines, Rhynchocephalia, and Squamata: Amphisbaenia, Sauria, and Serpentes). The data were gathered from 1288 sources published between 1820 and 2023. The dataset includes morphological, physiological, behavioral, and life history traits, as well as information on the availability of genetic data, IUCN Red List assessments, and population trends.

Understanding the role of environmental temperature on sex determination through comparative studies in reptiles and amphibians.

In vertebrates, species exhibit phenotypic plasticity of sex determination that the sex can plastically be determined by the external environmental temperature through a mechanism, temperature-dependent sex determination (TSD). Temperature exerts influence over the direction of sexual differentiation pathways, resulting in distinct primary sex ratios in a temperature-dependent manner. This review provides a summary of the thermal sensitivities associated with sex determination in reptiles and amphibians, with a focus on the pattern of TSD, gonadal differentiation, temperature sensing, and the molecular basis underlying thermal sensitivity in sex determination. Comparative studies across diverse lineages offer valuable insights into comprehending the evolution of sex determination as a phenotypic plasticity. While evidence of molecular mechanisms governing sexual differentiation pathways continues to accumulate, the intracellular signaling linking temperature sensing and sexual differentiation pathways remains elusive. We emphasize that uncovering these links is a key for understanding species-specific thermal sensitivities in TSD and will contribute to a more comprehensive understanding of ecosystem and biodiversity conservations.

Soft tissues influence nasal airflow in diapsids: Implications for dinosaurs.

The nasal passage performs multiple functions in amniotes, including olfaction and thermoregulation. These functions would have been present in extinct animals as well. However, fossils preserve only low-resolution versions of the nasal passage due to loss of soft-tissue structures after death. To test the effects of these lower resolution models on interpretations of nasal physiology, we performed a broadly comparative analysis of the nasal passages in extant diapsid representatives, e.g., alligator, turkey, ostrich, iguana, and a monitor lizard. Using computational fluid dynamics, we simulated airflow through 3D reconstructed models of the different nasal passages and compared these soft-tissue-bounded results to similar analyses of the same airways under the lower-resolution limits imposed by fossilization. Airflow patterns in these bony-bounded airways were more homogeneous and slower flowing than those of their soft-tissue counterparts. These data indicate that bony-bounded airway reconstructions of extinct animal nasal passages are far too conservative and place overly restrictive physiological limitations on extinct species. In spite of the diverse array of nasal passage shapes, distinct similarities in airflow were observed, including consistent areas of nasal passage constriction such as the junction of the olfactory region and main airway. These nasal constrictions can reasonably be inferred to have been present in extinct taxa such as dinosaurs.

Meta-analysis reveals impacts of disturbance on reptile and amphibian body condition.

Ecosystem disturbance is increasing in extent, severity and frequency across the globe. To date, research has largely focussed on the impacts of disturbance on animal population size, extinction risk and species richness. However, individual responses, such as changes in body condition, can act as more sensitive metrics and may provide early warning signs of reduced fitness and population declines. We conducted the first global systematic review and meta-analysis investigating the impacts of ecosystem disturbance on reptile and amphibian body condition. We collated 384 effect sizes representing 137 species from 133 studies. We tested how disturbance type, species traits, biome and taxon moderate the impacts of disturbance on body condition. We found an overall negative effect of disturbance on herpetofauna body condition (Hedges' g = -0.37, 95% CI: -0.57, -0.18). Disturbance type was an influential predictor of body condition response and all disturbance types had a negative mean effect. Drought, invasive species and agriculture had the largest effects. The impact of disturbance varied in strength and direction across biomes, with the largest negative effects found within Mediterranean and temperate biomes. In contrast, taxon, body size, habitat specialisation and conservation status were not influential predictors of disturbance effects. Our findings reveal the widespread effects of disturbance on herpetofauna body condition and highlight the potential role of individual-level response metrics in enhancing wildlife monitoring. The use of individual response metrics alongside population and community metrics would deepen our understanding of disturbance impacts by revealing both early impacts and chronic effects within affected populations. This could enable early and more informed conservation management.

Effects of the environment on the evolution of the vertebrate urinary tract.

Evolution of the vertebrate urinary system occurs in response to numerous selective pressures, which have been incompletely characterized. Developing research into urinary evolution led to the occurrence of clinical applications and insights in paediatric urology, reproductive medicine, urolithiasis and other domains. Each nephron segment and urinary organ has functions that can be contextualized within an evolutionary framework. For example, the structure and function of the glomerulus and proximal tubule are highly conserved, enabling blood cells and proteins to be retained, and facilitating the elimination of oceanic Ca+ and Mg+. Urea emerged as an osmotic mediator during evolution, as cells of large organisms required increased precision in the internal regulation of salinity and solutes. As the first vertebrates moved from water to land, acid-base regulation was shifted from gills to skin and kidneys in amphibians. In reptiles and birds, solute regulation no longer occurred through the skin but through nasal salt glands and post-renally, within the cloaca and the rectum. In placental mammals, nasal salt glands are absent and the rectum and urinary tracts became separate, which limited post-renal urine concentration and led to the necessity of a kidney capable of high urine concentration. Considering the evolutionary and environmental selective pressures that have contributed to renal evolution can help to gain an increased understanding of renal physiology.

Special Challenges in PET Imaging of Ectothermic Vertebrates.

The bulk of biomedical positron emission tomography (PET)-scanning experiments are performed on mammals (ie, rodents, pigs, and dogs), and the technique is only infrequently applied to answer research questions in ectothermic vertebrates such as fish, amphibians, and reptiles. Nevertheless, many unique and interesting physiological characteristics in these ectothermic vertebrates could be addressed in detail through PET. The low metabolic rate of ectothermic animals, however, may compromise the validity of physiological and biochemical parameters derived from the images created by PET and other scanning modalities. Here, we review some of the considerations that should be taken into account when PET scanning fish, amphibians, and reptiles. We present specific results from our own experiments, many of which remain previously unpublished, and we draw on examples from the literature. We conclude that knowledge on the natural history and physiology of the species studied and an understanding of the limitations of the PET scanning techniques are necessary to avoid the design of faulty experiments and erroneous conclusions.

Puberty in a Mesozoic reptile.

The histology of bone can be preserved virtually unaltered for hundreds of millions of years in fossils from all environments and all vertebrate taxa, giving rise to the flourishing field of paleohistology.1 The shafts of long bones are formed by the apposition of periosteal bone tissue, similar to the growth of wood, and preserve, an often cyclical, record of the growth of the individual and events in its life history. One such event is sexual maturation or puberty, during which hormonal changes transform the juvenile into a sexually mature adult. Puberty has been well studied in humans and some other living vertebrates. Here, we describe puberty in Keichousaurus, a small sexually dimorphic and live-bearing marine reptile from Middle Triassic rocks of SW China, about 240 million years old. Using a combination of bone histology and morphology, we detected puberty2 as one of the four life stages (the others being fetus, juvenile, and adult). Adult Keichousaurus males have a more robust humerus than females, with pronounced muscle attachment sites and a triangular shaft cross section. Midshaft sections of the humeri of the males show the transition from the rounded juvenile cross section to the triangular adult cross section, as reflected in the contour of the growth marks. This shape change is produced by differential bone apposition of the periosteum, presumably triggered by sex hormones, as in humans,3 and influenced by changes in loading regime during puberty. This is the first report of puberty in a fossil amniote.

The evolution of sociality and the polyvagal theory.

The polyvagal theory (PT), offered by Porges (2021), proposes that the autonomic nervous system (ANS) was repurposed in mammals, via a "second vagal nerve", to suppress defensive strategies and support the expression of sociality. Three critical assumptions of this theory are that (1) the transition of the ANS was associated with the evolution of 'social' mammals from 'asocial' reptiles; (2) the transition enabled mammals, unlike their reptilian ancestors, to derive a biological benefit from social interactions; and (3) the transition forces a less parsimonious explanation (convergence) for the evolution of social behavior in birds and mammals, since birds evolved from a reptilian lineage. Two recently published reviews, however, provided compelling evidence that the social-asocial dichotomy is overly simplistic, neglects the diversity of vertebrate social systems, impedes our understanding of the evolution of social behavior, and perpetuates the erroneous belief that one group-non-avian reptiles-is incapable of complex social behavior. In the worst case, if PT depends upon a transition from 'asocial reptiles' to 'social mammals', then the ability of PT to explain the evolution of the mammalian ANS is highly questionable. A great number of social behaviors occur in both reptiles and mammals. In the best case, PT has misused the terms 'social' and 'asocial'. Even here, however, the theory would still need to identify a particular suite of behaviors found in mammals and not reptiles that could be associated with, or explain, the transition of the ANS, and then replace the 'asocial' and 'social' labels with more specific descriptors.

A review of reptile virus experimental infection studies.

Despite recent advances in molecular techniques, infection studies remain an important tool for biosecurity, veterinary and conservation medicines. Experimental infection studies are performed for many reasons: to investigate causal links between pathogens and disease, to study host species susceptibility, to study immune response to inoculation, to investigate pathogen transmission and to investigate methods for infection control. Experimental infection studies using viruses in reptiles have been conducted sporadically since at least the 1930s and this continues to be a fertile area of research. This review catalogues previously published research in the field. The key parameters of each study are tabulated, providing a summary of more than 100 experiments linked to their original publications. Common themes and trends within the data are discussed.

Pain Recognition in Reptiles.

Advances in reptile cognitive research would help to (1) better qualify behavioral responses to pain experiences, (2) monitor welfare impacts, and (3) model analgesic studies with ecologically relevant insight to better qualify interventional responses. The focus of future analgesic studies in reptiles require the continued elucidation of the opiate systems and the given variations across taxa in efficacy in nociceptive tests.

Divergence in rates of phenotypic plasticity among ectotherms.

An individual's fitness cost associated with environmental change likely depends on the rate of adaptive phenotypic plasticity, and yet our understanding of plasticity rates in an ecological and evolutionary context remains limited. We provide the first quantitative synthesis of existing plasticity rate data, focusing on acclimation of temperature tolerance in ectothermic animals, where we demonstrate applicability of a recently proposed analytical approach. The analyses reveal considerable variation in plasticity rates of this trait among species, with half-times (how long it takes for the initial deviation from the acclimated phenotype to be reduced by 50% when individuals are shifted to a new environment) ranging from 3.7 to 770.2 h. Furthermore, rates differ among higher taxa, being higher for amphibians and reptiles than for crustaceans and fishes, and with insects being intermediate. We argue that a more comprehensive understanding of phenotypic plasticity will be attained through increased focus on the rate parameter.

Leukocyte Concentrations Are Isometric in Reptiles Unlike in Endotherms.

AbstractHow do large and small reptiles defend against infections, given the consequences of body mass for physiology and disease transmission? Functionally equivalent mammalian and avian granulocytes increased disproportionately with body mass (i.e., scaled hypermetrically), such that large organisms had higher concentrations than expected by a prediction of proportional protection across sizes. However, as these scaling relationships were derived from endothermic animals, they do not necessarily inform the scaling of leukocyte concentration for ectothermic reptiles that have a different physiology and evolutionary history. Here, we asked whether and how lymphocyte and heterophil concentrations relate to body mass among more than 120 reptile species. We compared these relationships to those found in birds and mammals and to existing scaling frameworks (i.e., protecton, complexity, rate of metabolism, or safety factor hypotheses). Both lymphocyte and heterophil concentrations scaled almost isometrically among reptiles. In contrast, functionally equivalent granulocytes scaled hypermetrically and lymphocytes scaled isometrically in birds and mammals. Life history traits were also poor predictors of variation in reptilian heterophil and lymphocyte concentrations. Our results provide insight into differences in immune protection in birds and mammals relative to that in reptiles through a comparative lens. The shape of scaling relationships differs, which should be considered when modeling disease dynamics among these groups.

Reptilian Innate Immunology and Ecoimmunology: What Do We Know and Where Are We Going?

Reptiles, the only ectothermic amniotes, employ a wide variety of physiological adaptations to adjust to their environments but remain vastly understudied in the field of immunology and ecoimmunology in comparison to other vertebrate taxa. To address this knowledge gap, we assessed the current state of research on reptilian innate immunology by conducting an extensive literature search of peer-reviewed articles published across the four orders of Reptilia (Crocodilia, Testudines, Squamata, and Rhynchocephalia). Using our compiled dataset, we investigated common techniques, characterization of immune components, differences in findings and type of research among the four orders, and immune responses to ecological and life-history variables. We found that there are differences in the types of questions asked and approaches used for each of these reptilian orders. The different conceptual frameworks applied to each group has led to a lack of unified understanding of reptilian immunological strategies, which, in turn, have resulted in large conceptual gaps in the field of ecoimmunology as a whole. To apply ecoimmunological concepts and techniques most effectively to reptiles, we must combine traditional immunological studies with ecoimmunological studies to continue to identify, characterize, and describe the reptilian immune components and responses. This review highlights the advances and gaps that remain to help identify targeted and cohesive approaches for future research in reptilian ecoimmunological studies.

Diverse aging rates in ectothermic tetrapods provide insights for the evolution of aging and longevity.

Comparative studies of mortality in the wild are necessary to understand the evolution of aging; yet, ectothermic tetrapods are underrepresented in this comparative landscape, despite their suitability for testing evolutionary hypotheses. We present a study of aging rates and longevity across wild tetrapod ectotherms, using data from 107 populations (77 species) of nonavian reptiles and amphibians. We test hypotheses of how thermoregulatory mode, environmental temperature, protective phenotypes, and pace of life history contribute to demographic aging. Controlling for phylogeny and body size, ectotherms display a higher diversity of aging rates compared with endotherms and include phylogenetically widespread evidence of negligible aging. Protective phenotypes and life-history strategies further explain macroevolutionary patterns of aging. Analyzing ectothermic tetrapods in a comparative context enhances our understanding of the evolution of aging.

Invited review: Thermal effects on oxidative stress in vertebrate ectotherms.

Human-induced climate change is occurring rapidly. Ectothermic organisms are particularly vulnerable to these temperature changes due to their reliance on environmental temperature. The extent of ectothermic thermal adaptation and plasticity in the literature is well documented; however, the role of oxidative stress in these processes needs more attention. Oxidative stress occurs when reactive oxygen species, generated mainly through aerobic respiration, overwhelm antioxidant defences and damage crucial biomolecules. The effects of oxidative damage include the alteration of life-history traits and reductions in whole-organism fitness. Here we review the literature addressing experimental temperature effects on oxidative stress in vertebrate ectotherms. Acute and acclimation temperature treatments produce distinctly different results and highlight the role of phylogeny and thermal adaptation in shaping oxidative stress responses. Acute treatments on organisms adapted to stable environments generally produced significant oxidative stress responses, whilst organisms adapted to variable conditions exhibited capacity to cope with temperature changes and mitigate oxidative stress. In acclimation treatments, the temperature treatments higher than optimal temperatures tended to produce significantly less oxidative stress than lower temperatures in reptiles, whilst in some eurythermal fish species, no oxidative stress response was observed. These results highlight the importance of phylogeny and adaptation to past environmental conditions for temperature-dependent oxidative stress responses. We conclude with recommendations on experimental procedures to investigate these phenomena with reference to thermal plasticity, adaptation and biogeographic variation that provide the most significant benefits to adaptable populations. These results have potential conservation ramifications as they may shed light on the physiological effects of temperature alterations in some vertebrate ectotherms.

VTMaxHerp: A data set of voluntary thermal maximum temperatures of amphibians and reptiles from two Brazilian hotspots.

Amphibians and reptiles are ectothermic animals and therefore depend on environmental temperatures to maintain their physiological functions. Despite being poorly documented, data on thermal behavioral thresholds to avoid overheating in their habitats are essential to improve the understanding of their thermal ecology and physiology. Here we provide a data set of 312 individual voluntary thermal maximum (VTMax ) values, the maximum temperature tolerated by individuals before actively moving to a colder place, for 53 species of amphibians and reptiles of the Atlantic Forest and Cerrado savannas of southeastern South America. Voluntary thermal maximum values were recorded as the body temperature at which the individuals exited a heating box experimental setup. This data set comprises 25 species of 15 genera and eight families of amphibians and 28 species of 24 genera and 12 families of reptiles. Of the total number of individual records, 67.9% derived from the Cerrado and 32.0% derived from the Atlantic Forest ecoregions. Overall, lizards had higher VTMax than amphibians and snakes, and individuals in the Atlantic Forest had overall higher VTMax values than the ones in Cerrado. This data set is the first to compile VTMax values for South American herpetofauna, along with detailed experimental information such as heating rates and time to reach VTMax . This data set provides a baseline for understanding thermal tolerances and requirements of Neotropical ectothermic vertebrate species, which might be useful for future research on the impact of climate change and to test novel ecological hypotheses. There are no copyright or proprietary restrictions except that this data paper should be cited when data are used for publications. In addition, the authors would appreciated being informed of research projects or teaching purposes when these data are used.