Shifts in sensitivity of amphibian metamorphosis to endocrine disruption: the common frog (Rana temporaria) as a case study

Abstract

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.

Effects of Desiccation on Metamorphic Climax in Bombina variegata: Changes in Levels and Patterns of Oxidative Stress Parameters

“…The body size can reflect on various processes and fitness traits in amphibian larvae, including metabolism, resistance to pathogens, feeding behavior, locomotion, escape from predators [6,20]. In adults, body size can also affect mortality rate, age and size at first reproduction or fecundity [6,13].…”

“…This shift, however, carries trade-offs that may have short-and long-term costs [9]. Costs could be seen in various morphological and physiological traits, e.g., reduced size at metamorphosis, leading to smaller maturation size, lower fecundity, reduction of hindlimb length, accelerated development, higher metabolic rates and alterations in oxidative metabolism and the immune system [6][7][8][10][11][12][13].…”

Living in a multi-stressor world: nitrate pollution and thermal stress interact to affect amphibian larvae

“…A temperature probe submerged in water at the same temperature as the respiration vials provided temperature compensation for dissolved oxygen measurements. No fasting prior to the respiratory measurements was needed because larvae stop feeding due to the remodeling of mouthparts and digestive tract during metamorphosis (Hourdry et al 1996;Ruthsatz et al 2019Ruthsatz et al ,2020b.…”

Acclimation Capacity to Global Warming of Amphibians and Freshwater Fishes: Drivers, Patterns, and Data Limitations

“…In animals with complex life histories, thermal tolerance and acclimation capacity are thought to change during ontogeny according to physiological and morphological reorganizations and concomitant aerobic capacities in relation to oxygen demand (Pörtner 2002; Pörtner & Peck 2010; Ruthsatz et al 2020a,b, 2022a) as well as energetic costs associated with developmental processes (Ruthsatz et al 2019). Furthermore, life stages might differ in their ability for behavioral thermoregulation (Navas et al 2008; Little & Seebacher 2017) resulting in stage-specific adaptations in thermal traits (Huey et al 1999).…”