Thermal ecological physiology of native and invasive frog species: do invaders perform better?

Volume 4 • 2016 10.1093/conphys/cow056 Research article Pablo A. Cortes1, Hans Puschel1, Paz Acuña2, José L. Bartheld3 and Francisco Bozinovic1,* 1 Departamento de Ecología, Center of Applied Ecology & Sustainability (CAPES), Facultad de Ciencias Biológicas, Pontificia Universidad Católica de Chile, Santiago 6513677, Chile. 2 Departamento de Ciencias Básicas, Universidad Santo Tomás, Santiago, Chile. 3 Instituto de Ciencias Ambientales y Evolutivas, Facultad de Ciencias, Universidad Austral de Chile, Campus Isla Teja, Valdivia, Chile. *Corresponding author: Departamento de Ecología, Center of Applied Ecology & Sustainability (CAPES), Facultad de Ciencias Biológicas, Pontificia Universidad Católica de Chile, Santiago 6513677, Chile. Tel: +562 2354 2618. Email: .............................................................................................................................................................. Biological invasions are recognized as an important biotic component of global change that threatens the composition, structure and functioning of ecosystems, resulting in loss of biodiversity and displacement of native species. Although ecological characteristics facilitating the establishment and spread of non-native species are widely recognized, little is known about organismal attributes underlying invasion success. In this study, we tested the effect of thermal acclimation on thermal tolerance and locomotor performance in the invasive Xenopus laevis and the Chilean native Calyptocephalella gayi. In particular, the maximal righting performance (μMAX), optimal temperature (TO), lower (CTmin) and upper critical thermal limits (CTmax), thermal breadth (Tbr) and the area under the performance curve (AUC) were studied after 6 weeks acclimation to 10 and 20°C. We observed higher values of μmax and AUC in X. laevis in comparison to C. gayi. On the contrary, the invasive species showed lower values of CTmin in comparison to the native one. In contrast, CTmax, TO and Tbr showed no interspecific differences. Moreover, we found that both species have the ability to acclimate their locomotor performance and lower thermal tolerance limit at low temperatures. Our results demonstrate that X. laevis is a better performer than C. gayi. Although there were differences in CTmin, the invasive and native frogs did not differ in their thermal tolerance. Interestingly, in both species the lower and upper critical thermal limits are beyond the minimal and maximal temperatures encountered in nature during the coldest and hottest month, respectively. Overall, our findings suggest that both X. laevis and C. gayi would be resilient to climate warming expectations in Chile. Key words: Acclimation, amphibians, central Chile, invasive species, thermal performance curve, thermal tolerance Editor: Steven Cooke Received 11 August 2016; Revised 3 October 2016; Editorial Decision 21 October 2016; accepted 26 October 2016 Cite as: Cortes PA, Puschel H, Acuña P, Bartheld JL, Bozinovic F (2016) Thermal ecological physiology of native and invasive frog species: do invaders perform better? Conserv Physiol 4(1): cow056; doi:10.1093/conphys/cow056. .............................................................................................................................................................. Introduction Biological invasions are recognized as an important biotic component of global change (Richardson et al., 2000; Ricciardi, 2007; Lockwood et al., 2013). Invasive species alter the composition, structure and functioning of ecosystems, resulting in loss of biodiversity and displacement of native species (Talley et al., 2001; Rochlin et al., 2013). An emergent concern is that other components of global change, such as climate warming, might enhance the capacity of alien species to invade new areas (Dukes and Mooney, 1999; Stachowicz et al., 2002; Hellmann et al., 2008; Rahel and Olden, 2008; .............................................................................................................................................................. © The Author 2016. Published by Oxford University Press and the Society for Experimental Biology. 1 This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/ by/4.0/), which permits unrestricted reuse, distribution, and reproduction in any medium, provided the original work is properly cited. Thermal ecological physiology of native and invasive frog species: do invaders perform better? Research article Conservation Physiology • Volume 4 2016 .............................................................................................................................................................. Walther et al., 2009; Robinet and Roques, 2010). Lejeusne et al. (2014) proposed that both components ‘constitute a deadly-duo threatening species abundance, distributions and biotic interactions’. In this context, Kelley (2014) proposed, tested and provided evidence supporting multiple hypotheses to untangle the role that thermal physiology plays in species invasion. Indeed, this author hypothesized that the ability to maintain physiological function across an extensive range of temperature tolerances (i.e. eurythermality) might explain the success of invasive species over native ones (‘greater eurythermal hypothesis’; see Lockwood and Somero, 2011; Zerebecky and Sorte, 2011; Tepolt and Somero, 2014). In addition, it has been proposed that acclimation to higher temperatures is associated with broader thermal tolerance in invasive species (Braby and Somero, 2006; Chown et al., 2007; Slabber et al., 2007; Hoffmann and Todgham, 2010; Tepolt and Somero, 2014). The Chilean frog Calyptocephalella gayi is an endemic aquatic species inhabiting central Chile (Donoso-Barros and Cei, 1962; Vélez, 2014). This species is the only representative of the genus Calyptocephalella and is sometimes referred to as a living fossil (Pyron and Wiens, 2011). Calyptocephalella gayi is currently restricted to deep ponds and small water reservoirs in central Chile (Veloso and Navarro, 1988; Rabanal and Nuñez, 2008; Muzzopappa and Nicoli, 2010; Veloso et al., 2010). This species is classified as vulnerable by the IUCN (Veloso et al., 2010), and current evidence indicates that populations of C. gayi are declining in its native range (Glade, 1983; Díaz-Páez and Ortiz, 2003). Moreover, the Chilean frog has been declared as a protected species by the Chilean government, who have prohibited its capture (Glade, 1983). The extensive alteration of Chile’s temperate and water regime that have occurred over the last decade plays a key role in creating adverse abiotic conditions for amphibian fauna (Diaz et al., 2007; Gutiérrez et al., 2012). More importantly, this species is also threatened by the introduction of the aquatic African clawed frog, Xenopus laevis (Lobos and Measey, 2002; Lobos and Ja (...truncated)