Temperature-induced developmental plasticity could allow amphibian larvae to complete metamorphosis successfully despite new thermal challenges and increased desiccation risk due to climate change. Here we investigated how the capacity for temperature-induced developmental plasticity varies with latitude and whether population-specific biogeographic background accounts for the different degree of plastic responses to temperature. We carried out a combined analysis based on the data from 150 studies (93 articles) performed on 64 amphibian species. We collected empirical data for age and size at metamorphosis in amphibian larvae acclimated to different temperatures during development and found that all larvae from all populations in these studies revealed a change in metamorphic traits with a given change in temperature and thus, were able to exhibit temperature-induced developmental plasticity. Age at metamorphosis was more affected by temperature than size at metamorphosis. Age and size at the onset of metamorphosis were generally lowest at warmest temperatures during development. Furthermore, populations from tropical latitudes were less sensitive to a change in developmental temperature compared to populations from higher latitudes. Accordingly, we suggest tropical populations to be the most vulnerable to increasing temperatures during metamorphosis. Our analyses reveal biases with respect to taxonomy, biogeographic distribution of species, and study design. Data from tropical populations are underrepresented and thus, the capacity for developmental plasticity of the most threatened species probably remains poorly understood. Future studies should focus on under-represented regions, most threatened species, and include a broader range of temperatures during development in order to make robust projections on future sensitivity of populations to climate change.
Global changes in temperature, predator introductions, and pollution might challenge animals by altering food conditions. A fast-growing source of environmental pollution are microplastics. If ingested with the natural food source, microplastics act as artificial fibers that reduce food quality by decreasing nutrient and energy density with possible ramifications for growth and development. Animals might cope with altered food conditions with digestive plasticity. We examined experimentally whether larvae of the African clawed frog (Xenopus laevis) exhibit digestive morphology plasticity (i.e., gut length, mass, and diameter) in response to microplastics ingestion. As natural systems contain non-digestible particles similar in size and shape to microplastics, we included cellulose as a natural fiber control group. Gut length and mass increased in response to microplastics and cellulose ingestion indicating that both types of fibers induced digestive plasticity. Body mass and body condition were similar across experimental groups, indicating that larvae fully compensated for low nutrient and energy density by developing longer intestines. The ability of a species to respond plastically to environmental variation, as X. laevis responded, indicates that this species might have the potential to cope with new conditions during global change, although it is uncertain whether this potential may be reduced in a multi-stressor environment.
Phenotypic plasticity may allow ectotherms with complex life histories such as amphibians to cope with climate-driven changes in their environment. Plasticity in thermal tolerance (i.e., shifts of thermal limits via acclimation to higher temperatures) has been proposed as a mechanism to cope with warming and extreme thermal events. However, thermal tolerance and, hence, acclimation capacity, is known to vary with life stage. Using the common frog (Rana temporaria) as a model species, we measured the capacity to adjust lower (CTmin) and upper (CTmax) critical thermal limits at different acclimation temperatures. We calculated the acclimation response ratio as a metric to assess the stage-specific acclimation capacity at each of seven consecutive ontogenetic stages and tested whether acclimation capacity was influenced by body mass and/or age. We further examined how acclimation temperature, body mass, age, and ontogenetic stage influenced CTmin and CTmax. In the temperate population of R. temporaria that we studied, thermal tolerance and acclimation capacity were affected by ontogenetic stage. However, acclimation capacity at both thermal limits was well below 100% at all life stages tested. The lowest and highest acclimation capacity in thermal limits was observed in young and late larvae, respectively. The relatively low acclimation capacity of young larvae highlights a clear risk of amphibian populations to ongoing climate change. Ignoring stage-specific differences in thermal physiology may drastically underestimate the climate vulnerability of species which will hamper successful conservation actions.
Despite an enormous boost of digital teaching due to Covid-19-related restrictions, the amount of open-access online teaching resources in zoology is relatively scarce beyond rather generalized high-school-level materials. For our own teaching, Katharina Ruthsatz, Mark D. Scherz, and Miguel Vences have developed a season of 14 guided video courses in animal anatomy and morphology for a general zoology lab for undergraduates at Braunschweig University of Technology (in German language). We are also making these videos available in English via a dedicated YouTube channel called Anatomy Insights. The videos give a brief overview of the taxonomy, biology, and ecology of the respective taxa and provide a step-by-step/real-time manual for dissection. While there is no substitute for practical anatomical experience, and dissection videos should supplement and must not replace hands-on dissection in anatomy courses at university level, such globally available resources serve to democratize access to education opportunities in animal morphology and taxonomy, while reducing the associated environmental and ethical footprint.
In Brazil’s Atlantic Forest (AF) biodiversity conservation is of key importance since the fungal pathogen Batrachochytrium dendrobatidis (Bd) has led to the rapid loss of amphibian populations here and worldwide. The impact of Bd on amphibians is determined by the host's immune system, of which the skin microbiome is a critical component. The richness and diversity of such cutaneous bacterial communities are known to be shaped by abiotic factors which thus may indirectly modulate host susceptibility to Bd. This study aimed to contribute to understanding the environment-host–pathogen interaction determining skin bacterial communities in 819 treefrogs (Anura: Hylidae and Phyllomedusidae) from 71 species sampled across the AF. We investigated whether abiotic factors influence the bacterial community richness and structure on the amphibian skin. We further tested for an association between skin bacterial community structure and Bd co-occurrence. Our data revealed that temperature, precipitation, and elevation consistently correlate with richness and diversity of the skin microbiome and also predict Bd infection status. Surprisingly, our data suggest a weak but significant positive correlation of Bd infection intensity and bacterial richness. We highlight the prospect of future experimental studies on the impact of changing environmental conditions associated with global change on environment-host–pathogen interactions in the AF.
Effective conservation actions require knowledge on the sensitivity of species to pollution and other anthropogenic stressors. Many of these stressors are endocrine disruptors (EDs) that can impair the hypothalamus–pituitary–thyroid axis and thus alter thyroid hormone (TH) levels with physiological consequences to wildlife. Due to their specific habitat requirements, amphibians are often sentinels of environmental degradation. We investigated how altered TH levels affected the bioenergetics of growth and development (i.e. age, size, metabolism, cardiac function and energy stores) before, during and after metamorphosis in the European common frog (Rana temporaria). We also determined how ontogenetic stage affected susceptibility to endocrine disruption and estimated juvenile performance. TH levels significantly affected growth and energetics at all developmental stages. Tadpoles and froglets exposed to high TH levels were significantly younger, smaller and lighter at all stages compared to those in control and low TH groups, indicating increased developmental and reduced growth rates. Across all ontogenetic stages tested, physiological consequences were rapidly observed after exposure to EDs. High TH increased heart rate by an average of 86% and reduced energy stores (fat content) by 33% compared to controls. Effects of exposure were smallest after the completion of metamorphosis. Our results demonstrate that both morphological and physiological traits of the European common frog are strongly impacted by endocrine disruption and that ontogenetic stage modulates the sensitivity of this species to endocrine disruption. Since endocrine disruption during metamorphosis can impair the physiological stress response in later life stages, long-term studies examining carry-over effects will be an important contribution to the conservation physiology of amphibians.
Environmental stress induced by natural and anthropogenic processes including climate change may threaten the productivity of species and persistence of populations. Ectotherms can potentially cope with stressful conditions such as extremes in temperature by exhibiting physiological plasticity. Amphibian larvae experiencing stressful environments display altered thyroid hormone (TH) status with potential implications for physiological traits and acclimation capacity. We investigated how developmental temperature (Tdev) and altered TH levels (simulating proximate effects of environmental stress) influence the standard metabolic rate (SMR), body condition (BC), and thermal tolerance in metamorphic and post-metamorphic anuran larvae of the common frog (Rana temporaria) reared at five constant temperatures (14°-28°C). At metamorphosis, larvae that developed at higher temperatures had higher maximum thermal limits but narrower ranges in thermal tolerance. Mean CTmax was 37.63°C ± 0.14 (low TH), 36.49°C ± 0.31 (control), and 36.43°C ± 0.68 (high TH) in larvae acclimated to different temperatures. Larvae were able to acclimate to higher Tdev by adjusting their thermal tolerance, but not their SMR, and this effect was not impaired by altered TH levels. BC was reduced by 80% (metamorphic) and by 85% (postmetamorphic) at highest Tdev.The effect of stressful larval conditions (i.e. different developmental temperatures and, to some extent, altered TH levels) on SMR and particulary on BC at the onset of metamorphosis was carried over to froglets at the end of metamorphic climax. This has far reaching consequences since body condition at metamorphosis is known to determine metamorphic success and, thus, is indirectly linked to individual fitness in later life stages.
Analyses of stable isotope ratios are widely applied in studies on a large variety of aspects in trophic ecology. Most studies rely on a precise estimation of the relevant discrimination factor Δ (also called the fractionation factor), that reflects the fractionation or differences in isotope ratios of a certain element (mainly nitrogen N and carbon C) between an animal’s diet and its tissue and is used to identify one step in the food web. We experimentally determined ΔN and ΔC of two species of widespread amphibians in Europe, Rana temporaria and Bufo bufo, and tested for the effect of food source (cyanobacteria Spirulina vs. zooplanktonic Daphnia) on Δ and for interspecific differences. Our study shows high variation in Δ in relation to the food source, but low interspecific differences. Tadpoles that were fed with Spirulina did have considerably lower ΔN than tadpoles fed with Daphnia in both species, and lower ΔC only in R. temporaria. The range of Δ obtained here can be a useful baseline for future trophic studies on tadpoles of Rana and Bufo. The strong diet-dependency of Δ, however, argues strongly against the use of a fixed discrimination factor in future isotope studies.
Anuran larvae show phenotypic plasticity in age and size at metamorphosis as a response to temperature variation. The capacity for temperature-induced developmental plasticity is determined by the thermal adaptation of a population. Multiple factors such as physiological responses to changing environmental conditions, however, might influence this capacity as well. In anuran larvae, thyroid hormone (TH) levels control growth and developmental rate and changes in TH status are a well-known stress response to sub-optimal environmental conditions. We investigated how chemically altered TH levels affect the capacity to exhibit temperature-induced developmental plasticity in larvae of the African clawed frog (Xenopus laevis) and the common frog (Rana temporaria). In both species, TH level influenced growth and developmental rate and modified the capacity for temperature-induced developmental plasticity. High TH levels reduced thermal sensitivity of metamorphic traits up to 57% (R. temporaria) and 36% (X. laevis). Rates of growth and development were more plastic in response to temperature in X. laevis (+30%) than in R. temporaria (+6%). Plasticity in rates of growth and development is beneficial to larvae in heterogeneous habitats as it allows a more rapid transition into the juvenile stage where rates of mortality are lower. Therefore, environmental stressors that increase endogenous TH levels and reduce temperature-dependent plasticity may increase risks and the vulnerability of anuran larvae. As TH status also influences metabolism, future studies should investigate whether reductions in physiological plasticity also increases the vulnerability of tadpoles to global change.
Food conditions are changing due to anthropogenic activities and natural sources and thus, expose many species to new challenges. Animals might cope with altered quantitative and qualitative composition [i.e. variable protein, Nitrogen (N), and energy content] of food by exhibiting trophic and digestive plasticity. We examined experimentally whether tadpoles of the common frog (Rana temporaria) exhibit phenotypic plasticity of the oral apparatus and intestinal morphology when raised on a diet of either low (i.e. Spirulina algae) or high protein, N, and energy content (i.e., Daphnia pulex). Whereas intestinal morphology was highly plastic, oral morphology did not respond plastically to different chemical compositions of food. Tadpoles that were fed food with low protein and N content and low energy density developed significantly longer guts and a larger larval stomach than tadpoles raised on high protein and N and an energetically dense diet, and developed a different intestinal surface morphology. Body sizes of the treatment groups were similar, indicating that tadpoles fully compensated for low protein, N, and energy diet by developing longer intestines. The ability of a species to respond plastically to environmental variation, as R. temporaria, indicates that this species might have the potential to cope with new conditions during climate change.
Environmental change exposes wildlife to a wide array of environmental stressors that arise from both anthropogenic and natural sources. Many environmental stressors with the ability to alter endocrine function are known as endocrine disruptors, which may impair the hypothalamus-pituitary-thyroid axis resulting in physiological consequences to wildlife. In this study, we investigated how the alteration of thyroid hormone (TH) levels due to exposure to the environmentally relevant endocrine disruptor sodium perchlorate (SP; inhibitory) and exogenous L-thyroxin (T4; stimulatory) affects metabolic costs and energy allocation during and after metamorphosis in a common amphibian (R. temporaria). We further tested for possible carry-over effects of endocrine disruption during larval stage on juvenile performance. Energy allocated to development was negatively related to metabolic rate and thus, tadpoles exposed to T4 could allocate 24 % less energy to development during metamorphic climax than control animals. Therefore, the energy available for metamorphosis was reduced in tadpoles with increased TH level by exposure to T4. We suggest that differences in metabolic rate caused by altered TH levels during metamorphic climax and energy allocation to maintenance costs might have contributed to a reduced energetic efficiency in tadpoles with high TH levels. Differences in size and energetics persisted beyond the metamorphic boundary and impacted on juvenile performance. Performance differences are mainly related to strong size-effects as altered TH levels by exposure to T4 and SP significantly affected growth and developmental rate. Nevertheless, we assume that juvenile performance is influenced by a size-independent effect of achieved TH. Energetic efficiency varied between treatments due to differences in size allocation of internal macronutrient stores. Altered TH levels as caused by several environmental stressors lead to persisting effects on metamorphic traits and energetics and, thus, caused carry-over effects on performance of froglets. We demonstrate the mechanisms through which alterations in abiotic and biotic environmental factors can alter phenotypes at metamorphosis and reduce lifetime fitness in these and likely other amphibians.
Anurans exhibit plasticity in the timing of metamorphosis and tadpoles show phenotypic plasticity in age and size at metamorphosis as a response to temperature variation. This developmental plasticity to changing thermal conditions is expected to be a primary factor that dictates the vulnerability of amphibians to increasing ambient temperatures such as are predicted in climate change scenarios. We analyzed the patterns of thermal effects on size and age at metamorphosis to investigate whether the intraspecific “temperature-size rule” is applicable over a broad range of anuran species by carrying out a combined analysis based on the data from 25 studies performed on 18 anuran species. Furthermore, we tested whether the thermal background of respective populations impacts the capacity for a plastic response in metamorphic traits. We could confirm this pattern for across-population comparisons. All included populations developed faster and 75% were smaller at the onset of metamorphosis when developmental temperatures were warmer, but the sensitivity of growth and developmental rate to a given temperature change was different. We found that the thermal background of a population influences the sensitivity of metamorphic traits and thus, the capacity for a plastic response in growth and developmental rate. Warm adapted populations were less sensitive to temperature variation indicating a reduced capacity for developmental plasticity and therefore, those species may be more vulnerable to the impacts of climate change. Future studies should include a broader range of rearing temperatures and temperature fluctuations to determine full knowledge of the capacity for developmental plasticity within a species-specific thermal window.
Chemical, physical, and biological environmental stressors may affect the endocrine system such as the thyroid hormone axis in larval amphibians with consequences for energy partitioning among development, growth, and metabolism. We studied the effects of two thyroid hormone (TH) level affecting compounds, exogenous L-thyroxine (T4) and sodium perchlorate (SP), on various measures of development and body condition in larvae of the African clawed frog (Xenopus laevis). We calculated the scaled mass index, the hepatosomatic index, and the relative tail muscle mass as body condition indices to estimate fitness. Altered TH levels significantly altered the growth, development, survival, and body condition in metamorphic larvae in different directions. While exogenous T4 reduced growth and accelerated development, SP treatment increased growth but slowed down development. Altered TH levels improved body conditions in both treatments and especially in larvae of the SP treatment but to the detriment of lower survival rates in both TH level altering treatments. The hepatosomatic index was negatively affected by exogenous T4, but not by SP treatment indicating a lower lipid reserve in the liver in larvae of T4 treatment. These altered TH levels as caused by several environmental stressors may have influence on individual fitness across life since body condition at the onset of metamorphosis determines metamorphic and juvenile survival. Further research is needed to determine synergetic effects of environmental stressors on TH levels and its effects on physiological traits such as metabolic rate.
Environmental variation induced by natural and anthropogenic processes including climate change may threaten species by causing environmental stress. Anuran larvae experiencing environmental stress may display altered thyroid hormone (TH) status with potential implications for physiological traits. Therefore, any capacity to adapt to environmental changes through plastic responses provides a key to determine species vulnerability to environmental variation. We investigated whether developmental temperature (Tdev), altered TH levels, and the interactive effect of both affect standard metabolic rate (SMR), body condition (BC), survival, and thermal tolerance in larvae of the African clawed frog (Xenopus laevis) reared at five temperatures with experimentally altered TH levels. At metamorphosis, SMR, BC, and survival were significantly affected by Tdev, TH status and their interaction with the latter often intensifying impacts. Larvae developing at warmer temperatures exhibited significantly higher SMRs and BC was reduced at warm Tdev and high TH levels suggesting decreased ability to acclimate to variation in temperature. Accordingly, tadpoles that developed at warm temperatures had higher maximum thermal limits but more narrow thermal tolerance windows. High and low TH levels decreased and increased upper thermal limits, respectively. Thus, when experiencing both warmer temperatures and environmental stress, larvae may be less able to compensate for changes in Tdev. Our results demonstrate that physiological traits in larvae of X. laevis are strongly affected by increased TH levels and warmer temperatures. Altered TH levels and increasing Tdev due to global change may result in a reduced capacity for physiological plasticity. This has far reaching consequences since the energetic requirement at the onset of metamorphosis is known to determine metamorphic success and thus, is indirectly linked to individual fitness in later life stages.
08/2021113th Annual Meeting of the German Zoological Society (DZG)30. August – 3. September 2021 (virtual meeting) Poster: Ontogenetic thermal tolerance and acclimation capacity in Rana temporaria
01/2021Annual Meeting of the Society of Comparative and Integrative Biology3 January - 28 February 2021 in Washington D.C. (USA)
Oral presentation: Potential of thermal tolerance plasticity as a coping mechanism with global warming in amphibians
01/20209th World Congress of Herpetology5-10 January 2020 in Dunedin (NZL)
Oral presentation: Endocrine disruption alters developmental body condition, energy allocation, and juvenile performance in Rana temporaria
09/2019SEH 2019 20th European Congress of Herpetology2-7 September 2019 in Milan (I)
Oral presentation: Energetic efficiency of metamorphosis in Rana temporaria
11/2018International Conference of the German Herpetological Society (DGHT)24-25 November 2018 in Muenster/Westfalen (GER)
Oral presentation: Environmental temperature and developmental plasticity of the common frog (Rana temporaria)
09/2018111th Annual Meeting of the German Zoological Society (DZG)10-15 September 2018 in Greifswald (GER)
Oral presentation: Altered thyroid hormone levels and developmental temperature affect the capacity for physiological acclimation in tadpoles of Rana temporaria and Xenopus laevis
09/2017SEH 2017 19th European Congress of Herpetology18-23 September 2017 in Salzburg (AUT)
Oral presentation: Environmental stress as an endocrine disruptor in tadpoles of Xenopus laevis and Rana temporaria
09/2015108th Annual Meeting of the German Zoological Society (DZG)10-15 September 2015 in Graz (AUT)
Oral presentation: Food quality induces plasticity in oral and intestinal morphology in larval amphibians
Endocrine disruption affects the physiological ontogeny of a wide-spread European anuran
9th World Congress of Herpetology (2020). Ruthsatz K, Dausmann KH, Peck MA & Glos J
Energetic efficiency of metamorphosis in
9th World Congress of Herpetology (2020). Ruthsatz K, Dausmann KH, Peck MA & Glos J