Endocrine Disruption Alters Developmental Energy Allocation and Performance in Rana temporaria

Abstract

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 (Rana 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.

Differences in responsiveness and sensitivity to exogenous disruptors of the thyroid gland in three anuran species

“…The exposure of early state premetamorphic tadpoles of P. borelli and L. chaquensis to methimazole increases both body size and total size as is reported for Rana temporaria exposed to thyroid inhibitors (Ruthsatz et al, ). In P. borelli and L. chaquensis , direct effects of the methimazole on the thyroid gland correspond to the overall hyperthrophy (Grim et al, ).…”

“…The exposure of early state premetamorphic tadpoles of P. borelli and L. chaquensis to methimazole increases both body size and total size as is reported for Rana temporaria exposed to thyroid inhibitors (Ruthsatz et al, 2019). In P. borelli and L. chaquensis, direct effects of the methimazole on the thyroid gland correspond to the overall hyperthrophy (Grim et al, 2009 borellii or 16 days for L. chaquensis and D. muelleri) showed sensitivity to accelerate development, trigger metamorphic transformation and produce thyroid gland atrophy.…”

Post-metamorphic carry-over effects of altered thyroid hormone level and developmental temperature: physiological plasticity and body condition at two life stages in Rana temporaria

“…Body condition typically is strongly correlated with body size, particularly in amphibian metamorphs (Scott et al 2007). However, we could show that body condition and juvenile performance might be size-independent due to the altered energy allocation during metamorphic climax (Ruthsatz et al 2019). As metamorphosis is an energy-consuming process (Sheridan and Kao 1998;Beck and Congdon 2003), it is advantageous to maintain a low SMR.…”

“…The SMI accounts for the allometric relationship between mass and a body structure, and is a standardized measure of the body condition that can be directly compared among individuals (Peig and Green 2009, 2010; MacCracken and Stebbings 2012). The SMI has been previously employed as a condition index in anuran larvae (Mac-Cracken and Stebbings 2012;Dittrich et al 2016;Ruthsatz et al 2018b;Ruthsatz et al 2019). A high SMI suggests larger energy storages and, thus, a good body condition.…”

“…Larval traits that may influence juvenile fitness include morphological and physiological traits, such as larval size, develpopmental rate, and age (Ficetola and De Bernardi 2006;Crean et al 2011;Yagi and Green 2017). Juvenile performance and, thus, survival are often associated size-dependent due to better predator avoidance, thermoregulation, and water content in individuals of larger size (John-Alder and Morin 1990; Goater et al 1993;Beck and Congdon 2000;Alvarez and Nicieza 2002;Ruthsatz et al 2019). Even if size at metamorphosis has been proven as a reliable fitness predictor in several studies (Berven and Gill 1983, Rana sylvatica;Berven 1990, Rana sylvatica;Goater 1994, Bufo bufo;Morey and Reznick 2001, Spea hammondii), other studies have found that much more is carried from the larval period than size (Pechenik 2006;Van Allen et al 2010).…”