Effects of temperature on growth, development, and survival of amphibian larvae: macroecological and evolutionary patterns.

Temperature affects the rate of biochemical and physiological processes in amphibians, influencing metamorphic traits. Temperature patterns, as those observed in latitudinal and altitudinal clines, may impose different challenges on amphibians depending on how species are geographically distributed. Moreover, species' response to environmental temperatures may also be phylogenetically constrained. Here, we explore the effects of acclimation to higher temperatures on tadpole survival, development, and growth, using a meta-analytical approach. We also evaluate whether the latitude and climatic variables at each collection site can explain differences in species' response to increasing temperature and whether these responses are phylogenetically conserved. Our results show that species that develop at relatively higher temperatures reach metamorphosis faster. Furthermore, absolute latitude at each collection site may partially explain heterogeneity in larval growth rate. Phylogenetic signal of traits in response to temperature indicates a non-random process in which related species resemble each other less than expected under Brownian motion evolution (BM) in all traits, except survival. The integration of studies in a meta-analytic framework allowed us to explore macroecological and macroevolutionary patterns and provided a better understanding of the effects of climate change on amphibians.

Using the dead to infer about the living: Amphibian roadkill spatiotemporal dynamics suggest local populations' reduction.

Roads represent one of the main sources of wildlife mortality, population decline, and isolation, especially for low-vagility animal groups. It is still not clearly understood how wildlife populations respond to these negative effects over space and time. Most studies on wildlife road mortality do not consider the spatial and temporal components simultaneously, or the imperfect roadkill detection, both of which could lead to inaccurate assumptions and unreliable mitigation actions. In this study, we applied a multi-season occupancy model to a 14-year amphibian mortality dataset collected along 120 km of roads, combined with freely available landscape and remote sensing metrics, to identify the spatiotemporal patterns of amphibian roadkill in a Mediterranean landscape in Southern Portugal. Our models showed an explicit general decrease in amphibian roadkill. The Iberian painted frog (Discoglossus galganoi) experienced roadkill declines over time of ∼70 %, while the spiny common toad (Bufo spinosus) and the fire salamander (Salamandra salamandra) had a loss of nearly 50 %, and the Southern marbled newt (Triturus pygmaeus) had 40 %. Despite the decreasing trend in roadkill, spatial patterns seem to be rather stable from year to year. Multi-season occupancy models, when combined with relevant landscape and remote sensing predictors, as well as long-term monitoring data, can describe dynamic changes in roadkill over space and time. These patterns are valuable tools for understanding roadkill patterns and drivers in Mediterranean landscapes, enabling the differentiation of road sections with varying roadkill over time. Ultimately, this information may contribute to the development of effective conservation measures.

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.

Circadian rhythm and surface activity in soil-dwelling caecilians (Amphibia: Gymnophiona).

The degree to which burrowing, soil-dwelling caecilian amphibians spend time on the surface is little studied, and circadian rhythm has not been investigated in multiple species of this order or by manipulating light-dark cycles. We studied surface-activity rhythm of the Indian caecilians Ichthyophis cf. longicephalus and Uraeotyphlus cf. oxyurus (Ichthyophiidae) and Gegeneophis tejaswini (Grandisoniidae), under LD, DD and DL cycles. We examined daily surface activity and the role of light-dark cycles as a zeitgeber. All three species were strictly nocturnal and G. tejaswini displayed the least surface activity. Four out of thirteen individuals, two I. cf. longicephalus, one G. tejaswini and one U. cf. oxyurus, displayed a more or less distinct surface-activity rhythm in all three cycles, and for the nine other animals the activity patterns were not evident. An approximately 24 h free-run period was observed in the three species. When the light-dark cycle was inverted, surface activity in the three species shifted to the dark phase. The findings of this study suggest that caecilians have a weak circadian surface-activity rhythm, and that the absence of light can act as a prominent zeitgeber in these burrowing, limbless amphibians.

Milk provisioning in oviparous caecilian amphibians.

Among vertebrates, the yolk is commonly the only form of nutritional investment offered by the female to the embryo. Some species, however, have developed parental care behaviors associated with specialized food provisioning essential for offspring survival, such as the production of lipidic-rich parental milk in mammals. Here, we show that females of the egg-laying caecilian amphibian Siphonops annulatus provide similarly lipid-rich milk to altricial hatchlings during parental care. We observed that for 2 months, S. annulatus babies ingested milk released through the maternal vent seemingly in response to tactile and acoustic stimulation by the babies. The milk, composed mainly of lipids and carbohydrates, originates from the maternal oviduct epithelium's hypertrophied glands. Our data suggest lactation in this oviparous nonmammalian species and expand the knowledge of parental care and communication in caecilians.

Endocrine disruption in teleosts and amphibians is mediated by anthropogenic and natural environmental factors: implications for risk assessment.

Environmental variation in the Anthropocene involves several factors that interfere with endocrine systems of wildlife and humans, presenting a planetary boundary of still unknown dimensions. Here, we focus on chemical compounds and other impacts of anthropogenic and natural origins that are adversely affecting reproduction and development. The main sink of these endocrine disruptors (EDs) is surface waters, where they mostly endanger aquatic vertebrates, like teleost fish and amphibians. For regulatory purposes, EDs are categorized into EATS modalities (oestrogenic, androgenic, thyroidal, steroidogenesis), only addressing endocrine systems being assessable by validated tests. However, there is evidence that non-EATS modalities-and even natural sources, such as decomposition products of plants or parasitic infections-can affect vertebrate endocrine systems. Recently, the disturbance of natural circadian light rhythms by artificial light at night (ALAN) has been identified as another ED. Reviewing the knowledge about EDs affecting teleosts and amphibians leads to implications for risk assessment. The generally accepted WHO-definition for EDs, which focuses exclusively on 'exogenous substances' and neglects parasitic infections or ALAN, seems to require some adaptation. Natural EDs have been involved in coevolutionary processes for ages without resulting in a general loss of biodiversity. Therefore, to address the 'One Health'-principle, future research and regulatory efforts should focus on minimizing anthropogenic factors for endocrine disruption. This article is part of the theme issue 'Endocrine responses to environmental variation: conceptual approaches and recent developments'.

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.

Thyroid and reproduction in amphibians and reptiles.

The relationship between the thyroid gland and reproduction in amphibians and reptiles has been studied for more than 100 years. Most studies suggest a positive involvement of thyroid hormones with some aspects of reproduction, but some studies support a negative role for thyroid hormones at certain life stages. Comprehensive studies of gene activation/suppression by thyroid hormones and their absence at various levels of the hypothalamo-pituitary-gonadal axis coupled with observations of adrenocorticoid activity, reproductive performance, and metabolic involvement are needed to understand this complex relationship.

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.

Cell-Based Therapies: Strategies for Regeneration.

The neural retina of mammals, like most of the rest of the central nervous system, does not regenerate new neurons after they are lost through damage or disease. The ability of nonmammalian vertebrates, like fish and amphibians, is remarkable, and lessons learned over the last 20 years have revealed some of the mechanisms underlying this potential. This knowledge has recently been applied to mammals to develop methods that can stimulate regeneration in mice. In this review, we highlight the progress in this area, and propose a "wish list" of how the clinical implementation of regenerative strategies could be applicable to various human retinal diseases.

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.

Do functional and phylogenetic nestedness follow the same mechanisms as taxonomic nestedness? Evidence from amphibians in the largest archipelago of China.

Nested subset pattern (nestedness) has been raised to explain the distribution of species on islands and habitat fragments for over 60 years. However, previous studies on nestedness focused on species richness and composition and overlooked the role of species traits and phylogeny in generating and explaining nestedness. To address this gap, we sampled amphibians on 37 land-bridge islands in the largest archipelago of China, the Zhoushan Archipelago, to explore nestedness as well as the underlying causal processes through three facets of diversity, that is, taxonomic, functional and phylogenetic diversity. The taxonomic nestedness was measured through organizing the species incidence matrix to achieve a maximum value, while the functional and phylogenetic nestedness were quantified by incorporating the similarity of species in terms of their ecological traits and phylogeny. We also obtained six island characteristics and seven species traits as predictors of nestedness. Amphibian metacommunities were significantly nested in these three facets of diversity. When relating different predictors to nestedness, island area, habitat diversity and species traits were highly correlated with taxonomic nestedness. Moreover, island area and habitat diversity significantly influenced functional and phylogenetic nestedness. Therefore, the results support the selective extinction and habitat nestedness hypotheses. Interestingly, although we did not observe significant influences of island isolation on taxonomic nestedness, functional and phylogenetic diversities were significantly higher than expected when matrices were ordered by increasing distance to mainland. The result suggests that there are more functionally and phylogenetically diverse species on less-isolated islands, reflecting a selective colonization process overlooked by the traditional analysis of taxonomic nestedness. Although the three facets of nestedness and underlying processes were largely congruent, we detected the distance-related functional and phylogenetic nestedness for amphibian assemblages. Therefore, we highlight that a framework that simultaneously considers taxonomic, functional and phylogenetic nestedness can contribute to a complementary understanding of nestedness processes. In addition, it also improves our ability to conserve insular biodiversity from different perspectives.

Is vertebral shape variability in caecilians (Amphibia: Gymnophiona) constrained by forces experienced during burrowing?

Caecilians are predominantly burrowing, elongate, limbless amphibians that have been relatively poorly studied. Although it has been suggested that the sturdy and compact skulls of caecilians are an adaptation to their head-first burrowing habits, no clear relationship between skull shape and burrowing performance appears to exist. However, the external forces encountered during burrowing are transmitted by the skull to the vertebral column, and, as such, may impact vertebral shape. Additionally, the muscles that generate the burrowing forces attach onto the vertebral column and consequently may impact vertebral shape that way as well. Here, we explored the relationships between vertebral shape and maximal in vivo push forces in 13 species of caecilian amphibians. Our results show that the shape of the two most anterior vertebrae, as well as the shape of the vertebrae at 90% of the total body length, is not correlated with peak push forces. Conversely, the shape of the third vertebrae, and the vertebrae at 20% and 60% of the total body length, does show a relationship to push forces measured in vivo. Whether these relationships are indirect (external forces constraining shape variation) or direct (muscle forces constraining shape variation) remains unclear and will require quantitative studies of the axial musculature. Importantly, our data suggest that mid-body vertebrae may potentially be used as proxies to infer burrowing capacity in fossil representatives.

The effect of thermal microenvironment in upper thermal tolerance plasticity in tropical tadpoles. Implications for vulnerability to climate warming.

Current climate change is generating accelerated increase in extreme heat events and organismal plastic adjustments in upper thermal tolerances, (critical thermal maximum -CTmax ) are recognized as the quicker mitigating mechanisms. However, current research casts doubt on the actual mitigating role of thermal acclimation to face heat impacts, due to its low magnitude and weak environmental signal. Here, we examined these drawbacks by first estimating maximum extent of thermal acclimation by examining known sources of variation affecting CTmax expression, such as daily thermal fluctuation and heating rates. Second, we examined whether the magnitude and pattern of CTmax plasticity is dependent of the thermal environment by comparing the acclimation responses of six species of tropical amphibian tadpoles inhabiting thermally contrasting open and shade habitats and, finally, estimating their warming tolerances (WT = CTmax - maximum temperatures) as estimator of heating risk. We found that plastic CTmax responses are improved in tadpoles exposed to fluctuating daily regimens. Slow heating rates implying longer duration assays determined a contrasting pattern in CTmax plastic expression, depending on species environment. Shade habitat species suffer a decline in CTmax whereas open habitat tadpoles greatly increase it, suggesting an adaptive differential ability of hot exposed species to quick hardening adjustments. Open habitat tadpoles although overall acclimate more than shade habitat species, cannot capitalize this beneficial increase in CTmax, because the maximum ambient temperatures are very close to their critical limits, and this increase may not be large enough to reduce acute heat stress under the ongoing global warming.

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.

Vulnerability to climate change of species in protected areas in Thailand.

Although 23% of Thailand's land is in protected areas, these are vulnerable to climate change. We used spatial distribution modelling for 866 vertebrate and 591 plant species to understand potential climate change impacts on species in protected areas. Most mammals, birds, and plants were projected to decline by 2070, but most amphibians and reptiles were projected to increase. By 2070 under RCP8.5, 54% of modeled species will be threatened and 11 nationally extinct. However, SDMs are sensitive to truncation of the climate space currently occupied by habitat loss and hunting, and apparent truncation by data limitations. In Thailand, lowland forest clearance has biased records for forest-dependent species to cooler uplands (> 250 m a.s.l.) and hunting has confined larger vertebrates to well-protected areas. In contrast, available data is biased towards lowland non-forest taxa for amphibians and reptiles. Niche truncation may therefore have resulted in overestimation of vulnerability for some mammal and plant species, while data limitations have likely led to underestimation of the threat to forest-dependent amphibians and reptiles. In view of the certainty of climate change but the many uncertainties regarding biological responses, we recommend regular, long-term monitoring of species and communities to detect early signals of climate change impacts.

The Amphibian Heart.

Currently, there are more than 8200 amphibian species described, including the orders Anura (frogs and toads), Caudata (salamanders and newts) and Gymnophiona (caecilians). Amphibians have 3 heart chambers: 2 atria and 1 ventricle. Their heart anatomy, histology, and physiology are reviewed. The basic morphology of the heart is similar in all amphibians with some differences due to their lifestyle. Blood flow, blood mixing, and blood oxygenation show variation due to interindividual and interspecific differences. Finally, different diagnostic methods to investigate the amphibian heart are described and reported amphibian heart diseases are summarized, including genetic, congenital, infectious, and neoplastic heart diseases.

Response to thermal and hydric regimes point to differential inter- and intraspecific vulnerability of tropical amphibians to climate warming.

In Puerto Rico, an island threatened by climate warming, only one of two species of frogs that share part of their distribution has undergone a recent range contraction to higher elevations. We questioned if differences in their physiological response to temperature and dehydration might explain this distributional change. We studied a lowland and a highland population of Eleutherodactylus coqui, a widespread generalist, and E. portoricensis, an endangered species that is currently found only above 600 m. We compared various physiological aspects: operative temperature; temperature selection; critical temperatures; and their response to jumping performance tests at various thermal and hydric regimes. Results revealed that E. portoricensis had the highest CTmin and lowest CTmax and selected a cooler range of temperatures from the experimental gradient. Jumping performance increased with temperature for the three populations until attaining maximum performance. Afterwards, performance dropped drastically until reaching CTmax. Dehydration had a negative effect on performance for both species, particularly on maximum performance. This effect was greatest for E. portoricensis, followed by high-elevation E. coqui. The significantly greater thermo-hydric physiological limitations of E. portoricensis may explain its recent range contraction, potentially, as a response to climate warming. Low-elevation E. coqui had the lowest operative warming tolerance and was the only population to select temperatures like those encountered in their environment, indicating it may be narrowly adapted to local thermal conditions and thus, also vulnerable to climate change. Our results point towards plasticity in the response of E. coqui to varying climatic conditions, and present evidence of different physiological responses between closely related species at the same locality. This work highlights the importance of studying the combined effects of temperature and hydration to understand the response of ectotherms to warming environments and presents further evidence that desiccation may be a limiting factor determining which species may survive.

Extending the biologging revolution to amphibians: Implantation, extraction, and validation of miniature temperature loggers.

Quantifying ectotherm body temperature is important to understand physiological performance under environmental change. The increasing availability of small, commercially-available animal-borne biologgers increases accessibility to high-quality body temperature data. However, amphibians present several challenges to successful datalogger implantation including small body sizes and physiologically active skin. We developed a method for the implantation, extraction, and validation of temperature biologgers in captive salamanders. We assessed the effect of biologger implantation and extraction surgery on body condition. Implantation had no effects on short or long-term body condition. Body condition also did not differ between implant and control groups after datalogger extraction. Biologgers did not alter preferred temperature in a laboratory thermal gradient, indicating that temperature data would not be biased by implantation. We provide detailed recommendations for datalogger placement and refinement of surgical techniques to further improve outcomes, enhance our understanding of fitness, species range limitations, and responses to environmental and climatic change.

Terrestrial reproduction and parental care drive rapid evolution in the trade-off between offspring size and number across amphibians.

The trade-off between offspring size and number is central to life history strategies. Both the evolutionary gain of parental care or more favorable habitats for offspring development are predicted to result in fewer, larger offspring. However, despite much research, it remains unclear whether and how different forms of care and habitats drive the evolution of the trade-off. Using data for over 800 amphibian species, we demonstrate that, after controlling for allometry, amphibians with direct development and those that lay eggs in terrestrial environments have larger eggs and smaller clutches, while different care behaviors and adaptations vary in their effects on the trade-off. Specifically, among the 11 care forms we considered at the egg, tadpole and juvenile stage, egg brooding, male egg attendance, and female egg attendance increase egg size; female tadpole attendance and tadpole feeding decrease egg size, while egg brooding, tadpole feeding, male tadpole attendance, and male tadpole transport decrease clutch size. Unlike egg size that shows exceptionally high rates of phenotypic change in just 19 branches of the amphibian phylogeny, clutch size has evolved at exceptionally high rates in 135 branches, indicating episodes of strong selection; egg and tadpole environment, direct development, egg brooding, tadpole feeding, male tadpole attendance, and tadpole transport explain 80% of these events. By explicitly considering diversity in parental care and offspring habitat by stage of offspring development, this study demonstrates that more favorable conditions for offspring development promote the evolution of larger offspring in smaller broods and reveals that the diversity of parental care forms influences the trade-off in more nuanced ways than previously appreciated.