Impact of global warming in holarctic and neotropical communities of amphibians

Resumen

Climate change has been a part of Earth's history since its beginnings and in the past there have been periods of heating and cooling of Earth's atmosphere (Zachos et al. 2001). During the 20th century, Earth's mean temperature has already increased 0.6°C (IPCC 2013). Current predictions by the IPCC (2013) for the 21st century estimate that mean temperature will increase up to 3°C and be accompanied by an increase of extreme climatic events (Schär et al. 2004, Diffenbaugh and Ashfaq 2010) and alteration of global precipitation patterns. These climate changes have already caused changes in the phenology and geographic distribution of several species, including endothermic and ectothermic vertebrates, (Walther et al. 2002, Parmesan and Yohe 2003, Genner et al. 2004, Nussey et al. 2005, Pearce-Higgins et al. 2005, Parmesan 2006, Lenoir et al. 2008, le Roux and McGeoch 2008, Chen et al. 2009, Steltzer and Post 2009) and concern has been raised over further erosion of diversity by an extinction process which may already be underway (Sinervo et al. 2010). Predicting the impacts of climate changes in the assemblage of species and biomes is currently one of the big challenges of the scientific community (Schwenk et al. 2009). As temperature affects virtually all physiological processes, by determining rates of chemical reactions (Hochachka and Somero 2002) and many ecological interactions (Dunson and Travis 1991), forecasting biological responses to global warming requires understanding how a species¿ physiology varies through space and time (Kearney and Porter 2009, Helmuth et al. 2010) and assessing how changes in physiological function due to increasing temperature may interact with phenotypic changes caused by other types of environmental variation (Chown and Terblanche 2007, Pörtner and Farrell 2008, Hoffmann 2010, Chown et al. 2010). Furthermore, determining how close organisms are to their thermal limits in nature and knowing how organisms are able to adjust or acclimatize their thermal sensitivity (Stillman 2003, Gilman et al. 2006) will help identify which species are more susceptible to global warming. Species with low tolerance to warming, limited acclimation ability, reduced dispersal, and/or that are unable to behaviourally compensate environmental changes are less likely to be able to avoid or adjust to new challenging conditions and therefore can be more vulnerable to rapid environmental changes. In addition, response to selection on thermal sensitivity is expected to be relatively fast in species that have short generation times, pronounced heritable variation in thermal sensitivity, large population size, limited inbreeding and thermally specialized physiologies (Huey and Kingsolver 1993, Kearney et al. 2009a, Kingsolver 2009, Chevin et al. 2010, Huey et al. 2012). Therefore, it is also important to consider the species' evolutionary potential and thus, if they are genetically capable of keeping pace with shifting climates or whether they will increasingly lag behind and eventually go extinct (Huey et al. 2012). Most of the animal terrestrial biodiversity is comprised by ectotherms and, given that their physiology, development and behaviour are strongly affected by temperature, they are expected to be particularly vulnerable to global warming. Since the projected rate of climate warming is lower in the tropics than in higher latitudes (IPCC, 2007), impacts of global warming on biodiversity are often assumed to be geographically dependent. There are wide indications that thermal tolerance in different groups of ectotherms is related to the magnitude of temperature variation they normally experience (Janzen 1967, Addo-Bediako et al. 2000, Ghalambor et al. 2006), which should increase with latitude. Most evidence suggests that species from temperate zones should have relatively broader thermal tolerances than tropical species, primarily because they are more tolerant to cold temperatures. Some works are consistent with the prediction that body temperature variability is reduced in the tropics and increases with latitude, for example in salamanders (Feder and Lynch 1982), lizards (Van Berkum 1988) and crabs (Stillman and Somero 2000). Furthermore, tropical ectotherms appear to be thermal specialists with lower acclimation capacity than higher¿latitude ectotherms (Van Berkum 1988, Addo-Bediako et al. 2000, Hoffmann et al. 2003a, Ghalambor et al. 2006, Gilman et al. 2006, Deutsch et al. 2008, Calosi et al. 2008). This doctoral thesis is divided in two different approaches; one with a broader approach to the thesis theme and a second consisting of several more specific approaches. The first approach, which is also the main objective of this thesis, aims to extend current knowledge on amphibian optimum temperatures (including thermal performance curves) and assess whether tropical amphibians species (living normally under higher environmental temperatures) are more vulnerable to global warming than temperate species (living normally under colder environmental temperatures). Chapter 1, "Coping with increasing environmental temperatures: how vulnerable are amphibians to climate change?", addresses this question by studying the thermal physiology of tadpoles from over 70 species, encompassing different biomes and countries. A large dataset was created by determining the thermal physiology of these species, with the use of thermal performance curves, and by measuring each species' environmental temperatures. Using the metrics established in Deutsch et al. (2008), this dataset allowed the identification of amphibian species and biomes that are more vulnerable to climate changes. Forecasting biological responses to current climatic changes emphasizes the necessity of understanding species thermal physiology and to assess their potential to face these changes via either plasticity or evolution. The second approach addresses the plasticity of thermal physiology of amphibian species, with a particular focus on thermal performance curves, and what this variation means to the vulnerability assessment made in chapter 1. Large global comparative studies have additional difficulties, such as logistics and time constraints, which can limit the outcome of the work. Since only one population per species was used in chapter 1 to keep species sampling and testing on a reasonable scale, it is important to determine how much variation exists within a species and if a single population can be representative of that species' thermal physiology and vulnerability estimates. Chapter 2, "Thermal physiology variation and vulnerability to thermal stress in Pelodytes spp. populations from the Iberian Peninsula", is a study on variation in CTmax and thermal performance curves (including optimum temperature) of populations from two different Pelodytes species, and investigates whether their thermal physiology is phylogenetic constrained or if there is local adaptation to the thermal environment. It also includes an evaluation of each population¿s susceptibility to acute and chronic thermal changes (increasing environmental temperatures) by calculating their Warming Tolerance and their Thermal Safety Margins respectively, again by applying the metrics defined in Deutsch et al. (2008). Studies like those conducted in the first two chapters of this thesis are usually performed under laboratory conditions. Although they give very important information on the thermal physiology of species, it is also important to keep in mind that organisms are exposed to a set of environmental conditions that can vary. Hence, there is a need to understand how a species¿ physiology varies through space and time and assess how changes in physiological function due to environmental changes may interact with phenotypic changes caused by other types of environmental variation. Amphibian larvae are well known for expressing environmentally induced phenotypes, but relatively little is known about how these responses might interact with changing temperatures and the thermal physiology of organisms. This question is addressed in chapter 3, entitled "Swimming with predators and pesticides: How environmental stressors affect the thermal physiology of tadpoles", where the thermal physiology of grey treefrog tadpoles (Hyla versicolor) is studied by determining whether exposures to predator cues and an herbicide (Roundup®) can alter the tadpole¿s critical maximum temperature (CTmax) and swimming speed across a range of temperatures. This provides estimates of optimal temperature (Topt) for swimming speed and the shape of the thermal performance curve (TPC) and highlights the importance of considering the plastic responses of CTmax and TPC to different inducing environments when forecasting biological responses to global warming. As mentioned before, amphibians have a number of physiological, ecological and life¿history characteristics that make them highly susceptible to environmental change, including a complex life¿cycle (Wells 2007). Metamorphosis occurs in the amphibian's life-cycle, and it is presumed to be an adaptation to the sequential occupation of temporary wetlands and terrestrial environments (Wells 2007). However, for organisms such as amphibians that experience different selective environments during their development, genetic correlations between ontogenetic stages can mean that selection on a trait at one stage induces maladaptive change in the same trait at other stages (Watkins 2001). Hence, metamorphosis is commonly seen as being beneficial since it may break the developmental and genetic relationships between traits expressed at different stages (Ebenman 1992, Moran 1994), and thereby allow the pre- and postmetamorphic stages to adapt independently to their respective environments (Watkins 2001) - the adaptive decoupling hypothesis (Moran 1994, Watkins 2001). Since thermal physiology traits such as CTmax and optimum temperature have been shown to be evolutionarily correlated with environmental temperature (Chapter 1; Duarte et al., 2012), thus reflecting species adaptation to their thermal habitat, chapter 4 of this thesis, "Vulnerability to climate change across life-stages in amphibian species", is a study on two stages of the amphibian life-cycle to determine if adaptation to the thermal environment in one stage can result in maladaptive traits in another stage. Here, the thermal physiology of the tadpole and juvenile stages is compared, using thermal performance curves to estimate optimum temperature and other related physiology traits. This also allows the comparison of Thermal Safety Margins of tadpoles and juveniles to determine if there is a life-stage that may be more vulnerable to suffer long-term chronic effects from increasing environmental temperatures, such as diminished physiological, developmental or behavioral performance at higher temperatures, and would determine if estimates of vulnerability to climate change in a life-stage can be extrapolated to the whole life-cycle of the amphibian species. Finally, apart from the discussion in each chapter, the main results are compiled in "General Conclusions" and summarize the most important contributions of this doctoral thesis to current questions addressed by the scientific community.