Herpetology Notes, volume 13: 101-103 (2020) (published online on 05 February 2020)

It is getting hot in here: behavioural thermal tolerance of Amphisbaena alba Linnaeus, 1758 (Squamata: Amphisbaenidae)

Juan C. Díaz-Ricaurte1,2,* and Filipe Serrano1

Ectothermic animals are tightly dependent on Amphisbaenians are fossorial limbless squamates with suitable temperature conditions to optimize multiple some being frequently associated with ant nests such as physiological functions like moving and feeding Amphisbaena alba (Azevedo-Ramos and Moutinho, (Licht, 1965; Angilletta et al., 2002; McConnachie 1994). They are still understudied mainly due to their and Alexander, 2004; Fontaine et al., 2018). Several secretive habits (Kearney, 2003). Amphisbaena alba is a reptile species use behaviour to thermoregulate when large-sized cis-Andean species with a wide distribution temperatures fall outside their preferred range (Cowles in South America (Colli and Zamboni, 1999), occurring and Bogert, 1944). However, given the increase in from lowland forests (e.g. Amazonia) to dry savannas global temperatures, the ability of these organisms and xeric shrublands (e.g. Cerrado and Caatinga). to remain within these limits may be compromised, Herein we report the first values of behavioural thermal potentially causing local extinctions and changes in their tolerance of A. alba. distribution (Sunday et al., 2012). Exposure to stressful Between 15 and 17 March 2018 two individuals of A. temperatures often generates an evasion response, known alba were caught at Estação Ecológica de Santa Bárbara, as Voluntary Thermal Maximum (VTMax), which leads municipality of Águas de Santa Bárbara (22.9488°S, the animals to retreat to colder microhabitats (Cowles 43.2862°W; WGS84, 590 m a.s.l.), one of the most and Bogert, 1944; Camacho and Rusch, 2017). Unable important remnants of Cerrado savannas in the state of to do so, they can reach their Critical Thermal Maximum São Paulo, Brazil. The first individual, an adult female

(CTMax), which can result in death (Cowles and Bogert, (snout-vent length [SVL]= 420mm, 110 g; collection 1944; Lutterschmidt and Hutchison, 1997; Zug et al., Marcio Roberto Costa Martins – MRCM 1261), was 2001; Angilletta, 2009). However, data on preferred found moving on the ground (ground temperature of and tolerated temperatures is rarely reported (Sinervo et 30.7ºC, measured with a Etekcity Lasergrip 800 Infrared al., 2010), being especially scarce for fossorial reptiles. Thermometer Gun) at 0950 in open “campo cerrado”, Understanding how thermal constraints affects species’ while the second individual, a juvenile (SVL= 213mm, behaviour and distribution means understanding the 12 g; collection code MRCM 1269), was caught in a thermal physiology of organisms (e.g. Camacho et al. pitfall trap in forested cerrado. 2018). In the laboratory, we taped each individual with an aluminium thermocouple (type T, Omega ®) attached to a Fieldlogger PicoLog TC-08 data logger in order to record its body temperature every ten seconds. Each individual was placed in a metal box (35x25x15 cm) 1 Laboratório de Ecologia, Evolução e Conservação de with no substrate. We then gradually increased the Anfíbios e Répteis, Departamento de Ecologia, Instituto de temperature of the box at a rate of 0.5ºC per minute by Biociências, Universidade de São Paulo, Rua do Matão, São using an electrical resistance located at its base. The box Paulo, SP 05508-090, Brazil. had a lid, which could be opened by the individual at 2 Grupo de Investigación en Biodiversidad y Desarrollo any time. The recorded body temperature when it left Amazónico, Programa de Biología, Facultad de Ciencias . Each individual Básicas, Universidad de la Amazonía, Cl. 17 Diagonal 17 the box was considered the VTMax con Cra. 3F, Florencia, Caquetá, Colombia. was tested only once to avoid residuals effects of prior * Corresponding author. E-mail: [email protected] experiments. 102 Juan C. Díaz-Ricaurte & Filipe Serrano

For the individual MRCM 1261, temperatures were Amphisbaena for which VTMax values are available, obtained during 36 min (mean = 31.63ºC; SD = 1.73; despite having been obtained through a different n = 226 records) and for the individual MRCM 1269, methodology (see Kubisch et al., 2016). These two during 50 min mean = 32.66; SD = 1.55; n = 308 species are sympatric and often syntopic in our study records). MRCM 1261 started with a body temperature area. Further studies are necessary to investigate of 30.6°C, reaching a VTMax of 34.7°C. Individual whether VTMax differences determine the spatial ecology MRCM 1269 started with a body temperature of 30.8°C, of these species. Furthermore, our results suggest reaching a VTMax of 34.4°C. Despite showing similar that Amphisbaena alba is a thigmothermic species values of VTMax, the two individuals showed distinct thermoregulating its body temperature mainly by direct thermal profiles (Fig. 1). contact to the ground. Even though measuring the VTMax Although thermoregulatory behaviour and thermal of an additional number of individuals would greatly tolerance have been extensively studied in other increase the confidence of the values for this species, our ectotherms (Adolph, 1990; Grant and Dunham, 1998; observation of two individuals should provide a starting Sinervo et al., 2010; Clusella-Trullas et al., 2011), point and a baseline reference for A. alba. Moreover, in many taxa only some general aspects of thermal our results can be incorporated into thermal databases tolerance are known (Winne and Keck, 2005). From field such as GlobTherm (Bennett et al., 2018), allowing for measurements (Abe and Johansen, 1987), the preferred further comparative studies with different taxa. body temperature for A. alba is predicted to be around Acknowledgments. We thank the helpful comments and 25°C, which is lower than our measured VTMax. Thus, it could mean that there is a wide range above the preferred suggestions made by the editor, Fábio Hepp. We also thank Bruno temperature that A. alba can tolerate before resorting to Ferreto for providing the photo used in this work. This study was financed in part by the Coordenação de Aperfeiçoamento de moving to colder microhabitats. This tolerance might Pessoal de Nível Superior – Brasil (CAPES) – Finance Code 001” be promoted by physiological mechanisms such as and supported by the Fundação de Amparo à Pesquisa do Estado respiration. For A. alba these mechanisms play a role de São Paulo (FAPESP; Proc. 2018/14091-1). in regulating temperature before reaching the VTMax (Abe and Johansen, 1987), also suggested for A. munoai References (Matias and Verrastro, 2018). Abe, A.S. (1984): Experimental and field record of preferred Our values of VT are also much higher than those Max temperature in the neotropical amphisbaenid Amphisbaena found for A. mertensii Strauch, 1881 (mean = 23.1ºC; mertensi Stauch, 1881 (Reptilia, Amphisbaenidae). Comparative Abe, 1984). This species is the only other species of Biochemistry and Physiology A: Physiology 1: 251–253. Abe, S., Johansen, K. (1987): Gas exchange and ventilatory responses to hypoxia and hypercapnia in Amphisbaena alba (Reptilia: Amphisbaenia). Journal of Experimental Biology 127: 159–172. Adolph, S.C. (1990): Influence of behavioral thermoregulation on microhabitat use by two Sceloporus lizards. Ecology 71: 315–327. Angilleta, M.J. (2009): Thermal adaptation: a theoretical and empirical synthesis. Oxford, USA, Oxford University Press. Angilletta, M.J., Niewiarowski, P.H., Navas, C.A. (2002): The evolution of thermal physiology in ectotherms. Journal of Thermal Biology 27: 249–268. Azevedo-Ramos, C., Moutinho, P.R.S. (1994): Amphisbaenians (Reptilia, Amphisbaenidae) in nests of Atta sexdens (Hymenoptera, Formicidae) in eastern Amazonia, Brazil. Entomological News 105: 183–184. Bennett, J.M., Calosi, P., Clusella-Trullas, S., Martínez, B., Sunday, J., Algar, A.C., Araújo, M.B., Hawkins, B.A., Keith, S., Kühn, I., Rahbek, C., Rodríguez, L., Singer, A., Villalobos, F., Olalla- Tárraga, M.Á., Morales-Castilla, I. (2018): GlobTherm, a Figure 1. Body temperature of two individuals of Amphisbaena global database on thermal tolerances for aquatic and terrestrial alba (Photo by Bruno Ferreto Fiorillo). The individual in the organisms. Scientific Data 5 (180022): 1–7. photo was not tested in this study. Camacho, A., Rusch, T.W. (2017): Methods and pitfalls of It is getting hot in here: behavioural thermal tolerance of Amphisbaena alba 103

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Accepted by Fábio Hepp