Behavioural plasticity in activity and sexual interactions in a social lizard at high environmental temperatures

PLOS ONE RESEARCH ARTICLE Behavioural plasticity in activity and sexual interactions in a social lizard at high environmental temperatures Nicola Rossi ID1,2*, Margarita Chiaraviglio1,2, Gabriela Cardozo1,2 1 Universidad Nacional de Córdoba, Facultad de Ciencias Exactas Fı́sicas y Naturales, Laboratorio de Biologı́a del Comportamiento, Córdoba, Argentina, 2 Consejo Nacional de Investigaciones Cientı́ficas y Técnicas (CONICET), Instituto de Diversidad y Ecologı́a Animal (IDEA), Córdoba, Argentina a1111111111 a1111111111 a1111111111 a1111111111 a1111111111 OPEN ACCESS Citation: Rossi N, Chiaraviglio M, Cardozo G (2023) Behavioural plasticity in activity and sexual interactions in a social lizard at high environmental temperatures. PLoS ONE 18(7): e0285656. https:// doi.org/10.1371/journal.pone.0285656 Editor: Christopher M. Somers, University of Regina, CANADA Received: October 7, 2022 Accepted: April 27, 2023 Published: July 26, 2023 Copyright: © 2023 Rossi et al. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Data Availability Statement: Data are uploaded and registered in OSF with the following DOI: 10. 17605/OSF.IO/WVQZN. Funding: N.R. - Student Research Grant 2019 Animal Behavior Society https://www. animalbehaviorsociety.org/web/index.php M. C. Consejo Nacional de Investigaciones Cientı́ficas y Técnicas "CONICET" (grant number: PIP 2011e2013); Fondo para la Investigación Cientı́fica y Tecnológica "Foncyt" (grant number: PICT-20111599 Res 140/12), https://www.argentina.gob.ar/ ciencia/agencia/fondo-para-la-investigacion- * Abstract Sexual selection often shapes social behavioural activities, such as movement in the environment to find possible partners, performance of displays to signal dominance and courtship behaviours. Such activities may be negatively influenced by increasing temperatures, especially in ectotherms, because individuals either have to withstand the unfavourable condition or are forced to allocate more time to thermoregulation by increasing shelter seeking behaviour. Thus, they “miss” opportunities for social and reproductive interactions. Moreover, behavioural displays of ectotherms closely depend on temperature; consequently, mate choice behaviours may be disrupted, ultimately modifying sexual selection patterns. Therefore, it would be interesting to elucidate how increasing temperatures associated with global warming may influence activity and social interactions in the species’ natural habitat and, specifically how high temperatures may modify intersexual interactions. Consequently, our aim was to explore differences in the daily pattern of social interactions in an ectotherm model, Tropidurus spinulosus, in two thermally different habitats and to determine how high temperatures modify mate choice. High environmental temperatures were found to be associated with a bimodal pattern in daily activity, which was closely linked to the daily variations in the thermal quality of the habitat; whereas the pattern and frequency of social displays showed less plasticity. The time allocated to mate choice generally decreased with increasing temperature since individuals increased the use of thermal refuges; this result supports the hypothesis of “missed opportunities”. Moreover, at high temperatures, both sexes showed changes in mate selection dynamics, with females possibly “rushing” mate choice and males showing an increase in intermale variability of reproductive displays. In our ectotherm model, plastic adjustments in the behavioural activity pattern induced by high temperatures, plus the modification of the displays during courtship may ultimately modify mate choice patterns and sexual selection dynamics. PLOS ONE | https://doi.org/10.1371/journal.pone.0285656 July 26, 2023 1 / 23 PLOS ONE cientifica-y-tecnologica-foncyt G.C. - "CONICET" (grant number: PIP 2011e2013); "Foncyt" (grant number: PICT-BICENTENARIO Nro. 2010-2782). Competing interests: The authors have declared that no competing interests exist. Behavioural plasticity in activity and sexual interactions in a lizard at high environmental temperatures 1. Introduction The behaviour of ectotherms has been the focus of research in recent decades, since it plays an important role in several aspects of their biology [1]. However, since behaviour is a temperature-related trait, it is under increasing pressure due to global warming [2, 3] and ectotherms are among the groups most susceptible to high temperatures [4]. Many ectotherms carefully regulate their activity time to adjust their daily needs (e.g. foraging, thermoregulation, habitat defence, social interactions) to suitable environmental temperatures; thus, they avoid overheating, which can trigger a heat stress response [4, 5]. Moreover, low plasticity in upper critical temperatures suggests a limitation of ectotherms to adapt to warming environments [6]. High temperatures increment the kinetic energy of biochemical reactions and lead to an increase of the metabolic rate [6, 7]. This metabolic effect may extend to a higher level of body organization, ultimately influencing the decision-making process of the individual [1]. Indeed, high temperature may induce changes in behaviour, for example in the pattern of movement related to shelter seeking in both thermoconformers and thermoregulators [8]. However, how behavioural changes modify social interactions, particularly reproductive ones, has been poorly studied so far in the light of global warming [9–11]. Therefore, an interesting question is how increasing temperatures may influence both the daily pattern of social interactions of ectotherms and intersexual interactions. Social interactions during the reproductive season are often modelled by sexual selection, i.e. a powerful evolutionary force that may favour or hinder the adaptation of a species to environmental stressors [12]. Pre-copulatory sexual selection involves several social activities that may contribute to an increase of individuals’ fitness, such as behavioural displays to signal their dominance and settle territorial boundaries [13], movements to find possible partners [14] and courtship behaviours [15]. However, such activities may be negatively influenced by increasing temperatures, because individuals either have to withstand the unfavourable condition by taking metabolic risks, or are forced to accommodate their time budgets to thermoregulate at the expense of other activities, such as intraspecific interactions [16–19]. It has been observed that a thermally stressed state makes lizards initiate a shelter-seeking behaviour [8]. Plasticity in behavioural thermoregulation, particularly shifts in microhabitat use like retreating into refuges, is an effective way to maintain their body temperature within their preferred ra (...truncated)