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

Abstract

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 (T dev) 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 CT max 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 T dev 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 T dev. The effect of stressful larval conditions (i.e., different developmental temperatures and, to some extent, altered TH levels) on SMR and particularly 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.

Thermal tolerance and acclimation capacity in the European common frog (Rana temporaria) change throughout ontogeny

“…This study identifies young larvae as the most‐temperature‐sensitive life stages in the life cycle of R. temporaria and highlights that early life stages might define the climate change vulnerability of amphibian populations. Given that this widely distributed species possesses a high capacity for developmental (Laurila & Kujasalo, 1999; Lind & Johansson, 2007; Merilä et al, 2004), morphological (Ruthsatz, Giertz, et al, 2019), and physiological plasticity (present study; Burraco et al, 2017; Ruthsatz, Dausmann, Reinhardt, et al, 2020), compared to other amphibian species (Laurila & Kujasalo, 1999; Ruthsatz et al, 2018; Vences et al, 2017), this bottleneck in the life cycle might be more pronounced in the vast majority of amphibian populations and species. Much of what is currently known about acclimation capacity in amphibians and other ectotherms has been gained from studies conducted on adults or from meta‐analyses that pool data across life stages (rev.…”

“…The ontogenetic stage was determined by evaluating the status of key morphological features as detailed in Gosner (1960). Each animal was assigned an ontogenetic stage group according to the procedure of Ortiz‐Santaliestra and Sparling (2007), Ruthsatz, Dausmann, et al (2019), resulting in seven consecutive groups: (1) pre‐limb (absence of hind limbs; Gosner stages 24–26), (2) limb bud (hind limb visible, but no clear joint formed; Gosner stages 27–34), (3) middle hind limb (knee joint apparent, but toes not completely separated; Gosner stages 35–37), (4) late hind limb (hind limb tubercles and subarticular patches formed; Gosner stages 38–41), (5) onset of metamorphic climax (at least one forelimb present; Gosner stage 42), (6) end of the metamorphic climax (complete resorption of the tail; Gosner stage 46), and (7) juvenile (Gosner stage 46 + 7 days; Ruthsatz, Dausmann, et al, 2019, 2020; Ruthsatz, Dausmann, Reinhardt, et al, 2020). Hereafter, we refer to stages 1–5 as tadpoles and to stages 6–7 as froglets.…”

Could Glyphosate and Glyphosate-Based Herbicides Be Associated With Increased Thyroid Diseases Worldwide?

“…The first evidence of thyroid toxicity was observed in amphibians (83). They are considered environmental sentinels for human health due to their sensitivity to the action of thyroid hormones during metamorphosis, since this process depends on the action of these hormones (84)(85)(86). Tadpoles were exposed to GBH formulations containing or not polyoxyethyleneamine (POEA) surfactant, glyphosate or only POEA surfactant and changes in metamorphosis were observed in tadpoles exposed to GBH containing POEA surfactant and in the group exposed only to POEA, but not in the group treated with glyphosate and GBH without POEA.…”

Acute toxic effects on hematological and histological features in adult frogs, Rana tigrina exposed to lambda-cyhalothrin pesticide

“…Five frogs were taken from those paddy fields where no insecticides were used and selected as a control group. Twenty frogs were taken for the research work and were kept in separate glass aquariums having 50 liters capacity filled with 20 liters water (Ruthsatz et al, 2020) and suitable environmental conditions were provided with respect to the rules of the INS laboratory of Zoology Researchers. Five frogs were kept in each aquarium to acclimatize them for 72 hours, granted with typical food (arthropods, insects), and were adjusted to the laboratory with careful surroundings for 1 week.…”