Feeding alters the preferred body temperature of Cururu toads, Rhinella diptycha (Anura, Bufonidae)

https://doi.org/10.1016/j.cbpa.2020.110771Get rights and content

Highlights

  • The toad Rhinella diptycha increased its preferred body temperature (Tpref) following meal ingestion in a thermal gradient

  • This response lasted from days 2 to 4 post-feeding and elevated Tpref higher than before meal ingestion or in fasting toads

  • The Tpref variation was broader in fed toads compared to fasting ones, implying greater level of movement in the fed group

  • The increment of body temperature following meal ingestion is often associated to an optimization of digestive processes

  • It remains disputable whether the thermoregulatory response herein documented holds true for anuran amphibians in nature

Abstract

Ectothermic organisms depend primarily on external heat sources and behavioural adjustments to regulate body temperature. Under controlled conditions, in a thermal gradient, body temperature often clusters around a more or less defined range of preferred body temperatures (Tpref). However, Tpref may be modified in response to environmental parameters and/or physiological state. For example, meal ingestion is sometimes followed by a post-prandial thermophilic response leading to a transient increment in Tpref. Although thought to optimize digestive processes, its occurrence, magnitude, and possible determinants remains scarcely documented for anuran amphibians. Herein, we investigated whether the Cururu toad, Rhinella diptycha, exhibits a post-prandial thermophilic response by monitoring the body temperature of fasting and fed toads while they were maintained in a thermal gradient. We found that the toads' Tpref increased by about 13% from day 2 to 4 after feeding, in comparison with the Tpref recorded under fasting. Also, fed animals exhibited a broader range for Tpref at days 2 and 3 post-prandial, which reflects a greater level of locomotor activity compared to fasting individuals. We conclude that R. diptycha is capable to exhibit a post-prandial thermophilic response under the controlled conditions of a thermal gradient. Although this thermoregulatory adjustment is thought to optimize meal digestion yielding important energetic and ecological benefits, its occurrence in anuran amphibians in nature remains uncertain.

Introduction

Body temperature (Tb) regulation in ectothermic animals primarily depends on the behavioural selection of suitable thermal microhabitats available in the environment (Angilletta, 2001; Buckley et al., 2015; Huey and Stevenson, 1979). As a consequence, activity is influenced by ambient temperature and occasionally constrained by spatial and temporal variation (Abe, 1995; Noronha-de-Souza et al., 2015). In amphibians, variation in Tb has been correlated to altitudinal (Navas et al., 2013) and latitudinal (Brattstrom, 1968; Feder and Lynch, 1982) gradients, as well as to circadian and seasonal variation in ambient temperature (Anderson et al., 2018; Gibbons and Bennett, 1974). Under controlled conditions, some ectothermic vertebrates exhibit a consistent range of preferred body temperature (Tpref) when tested in a thermal gradient in which thermoregulatory opportunities are uniformily offered and thermoregulatory costs are cancelled (Hutchison and Dupré, 1992). However, Tpref is often influenced by changes in physiological state. For example, anurans infected with pathogens often exhibit higher body temperatures than non-infected individuals, displaying a behavioural fever that has being identified both in nature (Richards-Zawacki, 2010; Rowley and Alford, 2013) and in the laboratory (Karavlan and Venesky, 2016; Sherman et al., 1991; Sherman, 2008), and is thought to promote immune function and assist in warding off infections (Moretti et al., 2019; Rakus et al., 2017). On the other hand, anurans exposed to unfavorable conditions such as hypoxia (Wood and Malvin, 1991), dehydration (Anderson and Andrade, 2017), fasting (O'Connor and Tracy, 1992), and seasonal inactivity (Bícego-Nahas et al., 2001) often decrease Tpref toward colder temperatures.

Changes in Tpref may also influence meal digestion (Andrade et al., 2005; Secor, 2009). Indeed, warmer temperatures are known to shorten the post-prandial metabolic response (Secor and Boehm, 2006; Toledo et al., 2003), increase gastrointestinal motility, promote the secretion of gastric acids and digestive enzymes, and ameliorate intestinal absorption of nutrients (Andrade et al., 2005; Hailey and Davies, 1987; Skoczylas, 1970; Wang et al., 2003). Therefore, the change in Tpref toward warmer temperatures during meal digestion is largely accepted to be of adaptive value. Such interpretations, however, are largely drawn from studies biased toward reptiles, particularly Squamates (Spencer et al., 2020). In contrast, the occurrence of a post-prandial thermophilic response in amphibians has been rarely documented (Gvoždík, 2003; Lillywhite et al., 1973; Sanabria et al., 2020; Witters and Sievert, 2001), which limits our interpretations about its determinants and potential ecological and physiological implications for this particular group (see Hertz et al., 1999).

In the present study, we investigated whether the Neotropical toad, Rhinella diptycha (Anura, Bufonidae), exhibits a post-prandial thermophilic response after being fed with mice equaling 15% of its body mass. Rhinella diptycha is a terrestrial and nocturnal medium-sized toad (Haddad et al., 2013) that changes its Tpref seasonally (Bícego-Nahas et al., 2001) and in response to factors such as dehydration (Anderson and Andrade, 2017) and pathogens (Bicego et al., 2002). Rhinella diptycha is a generalist and opportunistic feeder known to occasionally prey on small vertebrates (Gavira et al., 2013; Oad and Landgraf, 2012; Vaz-Silva, 2003).

Section snippets

Animals

Seventeen adult Rhinella diptycha (Cope, 1862) of both sexes (9 males, 8 females; mean ± SD body mass = 246.6 ± 65.5 g) were collected in the municipality of Barbosa, northwest of São Paulo State, Brazil (21.25048°S, 49.92132°W) under the permits SISBIO (#22028-1) and ICMBio (#35081-3). Animals were captured in November, 2017, and immediately transferred to the Laboratory of Animal Physiology at the São Paulo State University, Rio Claro, SP, Brazil, where they remained in captivity until

Results

Sex influenced Tpref breadth (P = .036) and, therefore, was included during the analysis of this specific parameter. For all other tested variables, neither sex nor body mass had a significant effect (P > .05 in all cases) and, therefore, were excluded from subsequent analysis.

For the control group that was kept under continuos fast, daily Tpref did not vary along the duration of the experiment (X25 = 5.22, P = .38). On the other hand, toads in the fed group exhibited a significant increase in T

Discussion

Our results clearly indicate that R. diptycha is capable to adjust its thermoregulatory behaviour in response to meal ingestion. This postprandial thermophilic response was corroborated by both: the intragroup comparison in which the Tpref before feeding was elevated after meal ingestion in the fed group and by the comparison between the control fasted toads with the fed group along the duration of the experiment. In the later case, both groups exhibited virtually the same Tpref value before

Declaration of Competing Interest

The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.

Acknowledgments

We are grateful to Celso and Jacira Gavira for their hospitality at the site of animal collection and to Rafaela Godoy, Thiago Gastaldi, Ayrton Nascimento, and Fernando Roza for help with animal maintenance and experiments. We are also grateful to Regina Spranger and two anonymous Reviewers for proofreading an earlier version of this MS. and for the insightful comments provided. This study was supported by the National Council for Scientific and Technological Development (CNPq, #117126/2016-0

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