Thermal Acclimation to the Highest Natural Ambient Temperature Compromises Physiological Performance in Tadpoles of a Stream-Breeding Savanna Tree Frog.

Leonardo S Longhini,Gabriela Da Silva Leandro,Aline C G Rocha,Cynthia P A Prado,Kênia C Bícego,Luciane H Gargaglioni,Lucas A Zena,Elias T Polymeropoulos

doi:10.3389/fphys.2021.726440

Abstract

Amphibians may be more vulnerable to climate-driven habitat modification because of their complex life cycle dependence on land and water. Considering the current rate of global warming, it is critical to identify the vulnerability of a species by assessing its potential to acclimate to warming temperatures. In many species, thermal acclimation provides a reversible physiological adjustment in response to temperature changes, conferring resilience in a changing climate. Here, we investigate the effects of temperature acclimation on the physiological performance of tadpoles of a stream-breeding savanna tree frog (Bokermannohyla ibitiguara) in relation to the thermal conditions naturally experienced in their microhabitat (range: 18.8–24.6°C). We quantified performance measures such as routine and maximum metabolic rate at different test (15, 20, 25, 30, and 34°C) and acclimation temperatures (18 and 25°C). We also measured heart rate before and after autonomic blockade with atropine and sotalol at the respective acclimation temperatures. Further, we determined the critical thermal maximum and warming tolerance (critical thermal maximum minus maximum microhabitat temperature), which were not affected by acclimation. Mass-specific routine and mass-specific maximum metabolic rate, as well as heart rate, increased with increasing test temperatures; however, acclimation elevated mass-specific routine metabolic rate while not affecting mass-specific maximum metabolic rate. Heart rate before and after the pharmacological blockade was also unaffected by acclimation. Aerobic scope in animals acclimated to 25°C was substantially reduced, suggesting that physiological performance at the highest temperatures experienced in their natural habitat is compromised. In conclusion, the data suggest that the tadpoles of B. ibitiguara, living in a thermally stable environment, have a limited capacity to physiologically adjust to the highest temperatures found in their micro-habitat, making the species more vulnerable to future climate change.

Highlights

Ectotherms, for instance, are likely to be affected by global warming since many physiological rates such as heart rate and metabolism are strongly influenced by environmental temperature (Ta)
The effect of Ta on metabolic rate typically follows an exponential curve in many ectotherms, roughly doubling for every 10◦C increase in Ta (i.e., Q10 = ∼2, Rocha and Branco, 1998; Overgaard et al, 2012), which is generally accompanied by similar increases in heart rate (f H) (Bícego-Nahas and Branco, 1999; Hedrick et al, 1999; Seebacher and Franklin, 2011; Overgaard et al, 2012; Zena et al, 2015, 2016)
Animals were transported in plastic bags to our laboratory at the Department of Animal Morphology and Physiology, UNESP, Jaboticabal, Brazil, where they were maintained in two glass aquariums (90 L) under natural photoperiod and temperature set for each acclimation group – 18 and 25◦C)

Summary

Introduction

Global warming affects the behavior, distribution, and physiology of many animal species (Parmesan and Yohe, 2003; Parmesan, 2006; Charmantier et al, 2008; Chen et al, 2009; Clusella-Trullas and Chown, 2013; Foden et al, 2013; Settele et al, 2014; Seebacher et al, 2015; Sandblom et al, 2016a; Pacifici et al, 2017). Cardiorespiratory functions such as heart rate reset, so that the initially elevated values progressively decrease upon prolonged exposure to moderately high temperatures (Overgaard et al, 2012; Sandblom et al, 2014; Seebacher et al, 2015; Ekström et al, 2016) Such a phenomenon can occur via two mechanisms: (1) reduction of the intrinsic f H; (2) increase in cholinergic tone and reduction of f H, or even a combination of both. This plasticity of cardiovascular control after prolonged exposure to high Ta has already been observed in fish (Ekström et al, 2016; Sandblom et al, 2016b)

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