Herpetology Notes, volume 13: 941-946 (2020) (published online on 26 November 2020)

Aspects of the thermal ecology of Liolaemus etheridgei Laurent, 1998 (Reptilia: Liolaemidae) from the Andes of Peru

Irbin B. Llanqui1,2,3,*

Abstract. Liolaemus etheridgei is a lizard distributed in the Andes of southern Peru with very little knowledge about its thermal ecology. Thus, this study sought to report aspects of thermal ecology using field data on body temperature (Tb), air temperature (Ta), and substrate temperature at capture points (Ts). The variabilities of temperatures were estimated. Likewise, all temperatures were compared, and the relationships between them were determined through correlation analyses. L. etheridgei showed a labile Tb (26.03 ± 1.81 ºC, Range: 18-34.6 ºC), suggesting that it is a thermal generalist. Mean Tb was 6.28 ºC (± 4.46) higher than Ta, but similar to Ts. There was a significant correlation between Ta and Tb (r = 0.624, P < 0.001), but not between Ts and Tb (r = 0.278, P = 0.1), thus indicating that L. etheridgei would most likely be a heliothermic rather than a thigmothermic species. This study represents the first effort to understand the thermal ecology of L. etheridgei.

Keywords. ectotherm, heliothermy, cloacal temperature, thermoregulation, Arequipa

Introduction of the environment can affect their fitness significantly (Vitt and Caldwell, 2014), as well as limit their capacity Most aspects of species biology are affected by to maintain body temperature within a tolerable range environmental temperatures. Accordingly, organisms (Labra et al., 2009). Hence, ectotherms represent have developed a variety of mechanisms (behavioural, an attractive group to study how organisms develop physiological and so forth) to cope with thermal strategies to respond to the thermal heterogeneity of an heterogeneity (Angilletta, 2009). Such mechanisms environment (Angilletta et al., 2002). are arranged in a continuum of two dimensions The Liolaemus genus includes 271 lizard species (Uetz which can describe the thermal ecology of any and Hošek, 2019) distributed in South America across a species: 1) thermosensitivity (thermal generalist and variety of thermal environments, thus being a suitable thermal specialist) and 2) thermoregulation (perfect group to test hypotheses on thermal biology (Medina thermoregulator and perfect thermoconformer) et al., 2012). Indeed, the research on thermal biology (Angilletta, 2009; Angilletta et al., 2006). In particular, in Liolaemus has been fruitful, contributing to a better ectotherms use the environment as a heat source, understanding of the influence of evolutionary history gaining heat either by short-wavelength solar radiation in the development of thermal strategies (Labra et al., (heliothermy) or by direct contact with a warm 2009; Vitt and Caldwell, 2014). It has also allowed us to substratum (thigmothermy) (Garrick, 2008; Pianka and make predictions on the future of ectotherm populations Vitt, 2003). As a consequence, the thermal conditions in the current scenario of climate change (Medina et al., 2012). Liolaemus etheridgei Laurent, 1999 is a viviparous lizard with sexual dimorphism (Fig. 1B, C) endemic to Moquegua and Arequipa Regions, southern Peru, 1 Universidad Nacional de San Agustín, Museo de Historia between 2,000 and 4,200 m (Laurent, 1998; Zeballos Natural (MUSA), Ca. Alcides Carrion s/n, Cercado, et al., 2002; Gutiérrez et al., 2010; Llanqui, 2017). Arequipa, Peru. Due to its wide altitudinal distribution, this species is 2 Centro de Ecología y Biodiversidad, PJ El Sol 103, Barranco, exposed to thermal gradients. Thus, it is expected that Lima, Peru. 3 Escuela de Ciencias Biológicas, Universidad Nacional Mayor L. etheridgei exhibits strategies for adapting to such de San Marcos, Av. Venezuela s/n, Lima, Peru. thermal conditions, in accordance to the ecological * Corresponding author. E-mail: [email protected] versatility of the Liolaemus genus for dealing with harsh 942 Irbin B. Llanqui climatic conditions (Medina et al., 2012). However, while little is known about the ecology of L. etheridgei, the thermal ecology remains entirely unknown. Herein,

I investigated the body temperature (Tb) of L. etheridgei and its association with substrate (Ts) and air (Ta) temperatures. Despite the absence of previous studies about the thermal ecology of L. etheridgei, it is common to see this species basking on rocks. Thus, it is expected that the results of this study will be coherent with a thermoregulatory behaviour. Likewise, a significant correlation between air and body temperature is anticipated, which would correspond to an heliothermic strategy. As such, this study aims to reveal an insight into the thermal ecology of L. etheridgei.

Material and Methods The study site was located in the buffer zone of Salinas y Aguada Blanca National Reserve (SABNR), Peru, specifically in two sectors called “El Simbral” (16º 23’S, 71º 19’W) and “Tuctumpaya” (16º 27’S, 71º 18’W). The vegetation of both sites is comprised predominately of trees and resinous shrubs, locally named as “Queñua” (Polylepis rugulosa) and “Tola” (Parastrephia spp.) (Fig. 1A). Sampling of individuals was carried out from July to November 2013 (mean ambient temperature 12.57 ºC, SENAMHI, datos hidrometeorológicos Estación Chiguata available at: https://www.senamhi.gob.pe/?&p=descarga-datos- hidrometeorologicos), corresponding to the dry season in the SANR (Montenegro, Zúñiga, and Zeballos, 2010). Individuals were caught by hand from 09:00 to 17:00 h. Only data of active animals were considered for the analyses in this study. Temperatures were recorded using a rapid read thermometer ThermoWorks RT600C- N (0.1 ºC precision), which was calibrated in the laboratory using a Miller-Weber standard thermometer (0.1 ºC precision). When an individual was caught, T b Figure 1. A. View of the habitat where temperature data were was immediately recorded by inserting the tip of the taken. The trees correspond to Queñua (Polylepis rugulosa), thermometer approximately 0.5 cm into the cloaca. T b a predominant vegetation in the study area. Liolaemus was recorded as fast as possible, handling individuals etheridgei: B. Adult male. C. Adult female. by the head to minimise heat transference (Gutiérrez et al., 2010; Stellatelli et al., 2017). Likewise, Ts was recorded on the surface and Ta 1 cm over the capture point (Bujes and Verrastro, 2006; Villavicencio et al., thus, the range and the coefficient of variation (V) was 2007; Ibargüengoytía et al., 2008). estimated as a measure of Tb variability. In determining The means and 95% confidence intervals for T , T , and b a how Tb differed from environmental temperatures, the

T were calculated. The methodology of Villavicencio confidence intervals of Tb were compared with those of et al. (2007) was used to determine thermosensitivity; Ta and Ts. Aspects of the thermal ecology of Liolaemus etheridgei from the Andes of Peru 943

The strength of the relationships between Tb and

Ta as well as Tb and Ts were estimated through partial correlations, controlling Ts and Ta respectively. Normality assumption was previously tested using the Shapiro- Wilk test. Due to the small dataset (n = 36), the effect of gender was not considered. Furthermore, differences in Tb with respect to sex are rare and minimal in lizards (Huey and Pianka, 2007), including Liolaemus species (Marquet et al., 1989; Labra et al., 2009). To determine thermal strategy, heliothermic was considered if Tb was significantly related to Ta, and thigmothermic if Tb was significantly related to Ts (Villavicencio et al., 2007; Gutiérrez et al., 2010; Medina et al., 2011; Stellatelli et al., 2017, 2018). All data analysis was done in R, version 3.5.1 (R Core Team, 2019). The data used in this study is available in the Supplementary Information.

Results A dataset of temperatures for 36 adult individuals was obtained. Several females were determined to have developed ovarian follicles (pregnancy), after an examination by palpation. According to the confidence intervals, the Tb mean of L. etheridgei (26.03 ± 1.81 ºC, n = 36) was significantly lower than Ta (19.75 ± 2.37

ºC, n = 36) but not different from Ts (25.12 ± 3.26 ºC, n = 36) (Fig. 2A). Also, the Tb varied within a range of

18-34.6 ºC (V = 20.59, n = 36), while Ta and Ts varied between 9.50-33 ºC (V = 35.5, n = 36) and 12.40-44.1 ºC (V = 38.33, n = 36), respectively. A significant correlation was found between Tb and Ta (r = 0.598, t33

= 4.29, P < 0.001, n = 36) but not between Tb and Ts (r

= 0.151, t33 = 0.877, P = 0.387, n = 36) (Fig. 2B, C). Finally, all temperatures tended to fluctuate similarly throughout the day, however, the fluctuations of Tb and

Ta were particularly similar (Fig. 3).

Discussion

The wide range of Tb in L. etheridgei (18 to 34.6 ºC) would represent an advantage to resist harsh thermal Figure 2. A. Body temperatures of Liolaemus etheridgei and conditions either if it is a perfect thermoregulator surrounding air and substrate temperatures. Bars indicate 95% confidence intervals. B. Relationship between body and air or thermoconformer, which could partially explain temperatures. C. Relationship between body and substrate its wide altitudinal distribution (2,000 to 4,200 m) temperatures. The shaded area represents the 95 % confidence (Laurent, 1998; Zeballos et al., 2002; Gutiérrez et al., intervals of trend lines. 2010). This variability in Tb could be associated to the physiological state of the individuals (e.g. pregnancy). For instance, Ibargüengoytía and Cussac (2002) observed that pregnant females of L. elongatus show lower Tb than nonpregnant females, associating this lower cloacal temperatures than other individuals. difference with an increase in the use of microhabitats Similarly, Smith and Ballinger (1994) found that that reduces predation risk but also reduces their pregnant females of Sceloporus jarrovii maintained exposition to sunlight (e.g. cracks). Péfaur et al. (1978) 944 Irbin B. Llanqui

Figure 3. Body temperature (Tb), air temperature (Ta), and substrate temperature (Ts) at different times of the day.

recorded March to November as being the pregnancy critical temperatures, as well as performance curves, months for L. annectens, L. signifer and L. etheridgei are necessary to confirm L. etheridgei as a thermal (as L. multiformis distributed in Arequipa, Peru). As this generalist (Angilletta, 2009). It is worth mentioning study was from July to November, pregnant females of here that environmental temperatures could be near the

L. etheridgei were also found. Thus, the variability of Tb limit of thermal tolerance for this species as sampling recorded for L. etheridgei could be partially explained was located close to the altitudinal limit for this species. due to the presence of pregnant females within the Indeed, the sampling area included high hills (up to sample. However, a comparative study would be 4,183 m) where no individuals of L. etheridgei were required to confirm the existence of differences in Tb observed; instead, individuals of L. tacnae were found, of pregnant and nonpregnant females of L. etheridgei. a member of the alticolor-bibronii group (Lobo et al., If such differences exist, it would be appropriate to test 2010) suggesting niche segregation. whether they could be attributed to a difference in the It was evident that Tb of L. etheridgei was higher than use of microhabitats, such as proposed by Smith and Ta, which may suggest behavioural thermoregulation. Ballinger (1994). Still, this result does not constitute definitive evidence

The Tb of L. etheridgei varied in the range of 18-34.6 of thermoregulation as inanimate objects can also ºC (∆ = 16.6 ºC, V = 20.59), which is similar to the range show this tendency (Heath, 1964). Virtually, all living of L. pseudoanomalus 20.4-40.6 ºC (∆ = 20.02 ºC, V organisms exhibit some degree of thermoregulation = 12.28), the latter considered as a thermal generalist (Angilletta, 2009); thus L. etheridgei should exhibit at based on this information (Villavicencio et al., 2007). least a minimal degree of thermal regulation. Indeed, Thus, L. etheridgei could also be a thermal generalist, during the sampling period, several individuals especially if we consider that all individuals were active were observed basking, indicating thermoregulatory within the Tb range. Likewise, the idea that L. etheridgei behaviour (Navas, 2003; Bujes and Verrastro, 2006; Vitt is a thermal generalist would be coherent with its and Caldwell, 2014) considered as an essential strategy distribution across a wide altitudinal range (2,000- for lizards living at high elevations (Ibargüengoytía et 4,200 m) and thermal gradient. Nevertheless, studies al., 2008). involving the determination of minimum and maximum Aspects of the thermal ecology of Liolaemus etheridgei from the Andes of Peru 945

The range and variability of Tb suggests that L. 2010). Thus, the heliothermic strategy recorded for etheridgei is a thermal generalist (thermosensitivity). L. etheridgei could easily be part of a more complex At the same time, the activity of basking indicates mechanism, for which, long term studies are required. the existence of a behavioural mechanism for thermal regulation (thermoregulation), although it is not Acknowledgements. I dedicate this article to Richard E. possible to determine the magnitude in any dimension. Etheridge who encouraged me to finish this study. I thank If L. etheridgei is a perfect thermoconformer, basking Evaristo López, José Pérez, César Aguilar, Brian Crnobrna, Bryn behaviour should not be contributing to thermal Edwards and Rafael P. Bovo for their useful comments. Likewise, I thank my field assistants Oscar Calachua, Raquel Asto, Robert regulation, which would raise questions as to why it Cornejo, María Huaranca, and Jesús Postigo. I captured lizards exhibits such behaviour. On the contrary, if this species with permission of SABNR, Ministry of Environment, Peru. is a perfect thermoregulator its Tb should be nearly constant (Angilletta et al., 2009), which is not the case References either. Thus, a hypothesis coherent to the variability Angilletta, M.J. (2009): Thermal Adaptation. A theoretical and in Tb and basking behaviour is that L. etheridgei is a moderate thermoregulator (Huey and Slatkin, 1976). empirical synthesis. Oxford, UK, Oxford University Press. Angilletta, M.J., Bennett, A.F., Guderley, H., Navas, C.A., Moderate thermoregulation strategies have been Seebacher, F., Wilson, R.S. (2006): Coadaptation: A unifying recorded in several Liolaemus species such as L. bibroni principle in evolutionary thermal biology. Physiological and (Medina et al., 2009), L. pictus argentinus (Gutiérrez et Biochemical Zoology 79: 282–294. al., 2010), L. tandiliensis (Stellatelli et al., 2018) and L. Angilletta, M.J., Cooper, B.S., Schuler, M.S., Boyles, J.G. (2002): yanalcu (Valdecantos et al., 2013). To properly test this The evolution of thermal physiology in ectotherms. Journal of hypothesis, and to unveil if there is a tendency either Thermal Biology 27: 249–268. towards to be thermoconformer or thermoregulator, Bujes, C.S., Verrastro, L. (2006): Thermal biology of Liolaemus future investigations should analyse preferred and occipitalis (Squamata, Tropiduridae) in the coastal sand dunes of Rio Grande do Sul, Brazil. Brazilian Journal of Biology 66: operative temperatures (Hertz et al., 1993; Dzialowski, 945–954. 2005; Angilletta, 2009; Losos, 2009). Dzialowski, E.M. (2005): Use of operative temperature and

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