The vulnerability of microhylid frogs, Cophixalus spp., to climate change in the Australian Wet Tropics

Climate change is a global phenomenon attributable to a change in concentration of greenhouse gases in the atmosphere as a consequence of human activities since the beginning of industrialisation. The change in climatic patterns direct and indirectly affects biodiversity by, for example, promoting geographic distribution changes (elevational or latitudinal) or affecting the biological interactions of species. These effects have been proposed to more severely affect ectotherms, especially in tropical regions. Tropical regions, due to annual climatic stability, may have promoted the evolution of species with reduced thermal tolerances. The endemic Microhylid frogs, genus Cophixalus, of the Australian Wet Tropics Bioregion (AWT) are considered one of the most threatened groups of vertebrates of the region by climate change. This vulnerability mainly comes from a reduced geographic distribution, restricted to a one or few mountain tops in the coldest, wettest and aseasonal parts of the AWT. These nocturnal frogs are forest floor dwellers and reproduce via direct development (i.e. eggs are deposited terrestrially and development occurs within the egg with froglets hatching from the egg capsule). During day time they seek shelter from ambient environmental conditions in refuges (mainly under logs, rocks or fallen epiphytes). Correlative models of distribution of this group of frogs predict a reduction of suitable climatic area in the future, however the mechanisms behind the potential changes are poorly understood. The ecological characteristics of Cophixalus and their high regional species richness (thirteen species) make this group ideal to test hypotheses about factors that influence their geographical distribution limits and potentially will influence their response to future climates. A more accurate assessment of the vulnerability of these Cophixalus frogs to climate change depends on the understanding of the conditions the species actually are exposed to and their sensitivity to environmental change. Exposure requires accurate microenvironmental data and an understanding of seasonal or daily behavioural activity, while sensitivity can be assessed by directly quantifying the physiological thermal tolerances of the animals. Cophixalus frogs show a consistent daily and seasonal activity pattern showing adaptations to exploit available refuges with potentially better buffering capacity, which may be important to face warmer conditions in the future. Based on behavioural observations, a sequence of actual exposure conditions for Cophixalus frogs was constructed. Exposure conditions were found to be behaviourally buffered from ambient air conditions (by nocturnality and microhabitat use). This magnitude of the buffering varies with season, being higher during the warmest months. Sensitivity of Cophixalus frogs was directly measured using several techniques including a dynamic method to determine critical thermal maximum and minimum. The experimental device increased or decreased temperature at a rate of approximate 1˚C/minute, until organisms lost righting capacity. The analysis of the sensitivity of organisms to climate change must be based on empirical evidence, to improve the assessment of future climate impacts. Observed thermal tolerances and limits of the Australian Wet Tropics Cophixalus frogs was not predicted by phylogenetic history, but instead was correlated with contemporary environmental conditions associated with the geographical distribution of individual species. Cophixalus frogs have narrow thermal ranges that may be explained by their narrow geographical restriction to rainforest habitats. Historical stability of environmental conditions within this ecosystem, has been proposed as a major driver of species distribution patterns and subsequent geographic species richness in this region. The maximum thermal tolerance (CTmax) of the eleven species of Cophixalus examined, ranged from 28.1 °C to 35.9 °C, and the minimum (CTmin) ranged from 8.6 °C to 14.3 °C. Thermal tolerance range was extremely narrow compared with other tropical anurans, even for the species with the widest tolerance, Cophixalus exiguus (25.5 °C). Mean and mode of the preferred temperature showed similar values ranging from 20 °C to 29 °C across the 13 species. The combination of measured thermal tolerances, microenvironmental exposure and ecology of species will be fundamental for the development of more accurate assessment of vulnerability to climate change. For restricted species, the analysis of these factors may also allow the identification of parameters that may be limiting their distributions. In this study, available evidence suggests that thermal physiology parameters of individual Cophixalus frogs, such as CTmax is correlated to different distribution characteristics (e.g. maximum and mid-altitude of the species distribution). These data also allow us to determine whether species are actually filling their fundamental thermal niche. It is suggested that some species are not filling their niche. This finding may open the possibility to explore conservation strategies that may include translocation of individuals to regions where they are not currently present but environmental conditions would not act as a limitation. When predictions of temperature change are included in the analysis, the results may be used to guide decisions about the regions and time frames when conservation strategies are required. Climate conditions under present, and two future frames (2035 and 2065) were evaluated. Our results suggest that some species may be experiencing suppressed fitness due to environmental warming even under current environmental conditions. This decrease is related to exposure to conditions warmer than their preferred temperature. The exposure to these stressful conditions are expected to occur first in the lower elevational areas of the distribution and increase in magnitude into the future. One of the most important findings of this research is that our data suggests that no population of any Cophixalus species occurring in the AWT will be exposed to temperatures that directly cause fatalities within the timeframes evaluated. This is important because it suggests that drastic interventions to avoid local extinctions will not be necessary by 2065. However, the potential for serious indirect, or synergistic, impacts remains. It is possible too that physiological responses to environmental parameters other than temperature may limit distributions of Cophixalus species. Another contribution of this study was to develop an experimental apparatus capable of quantifying tolerance to desiccation in hard field conditions. We provide a description of the experimental apparatus and detailed methodology as an input for future studied focused on this environmental parameter and also include some preliminary data on desiccation rates as an appendix. Cophixalus frogs show an increase of water loss with temperature, implying an increase in vulnerability to drying in the future. Cophixalus neglectus in particular seems to be highly sensitive to desiccation. Cophixalus saxatilis presents low levels of desiccation that can be explained by larger size of the species and relative low relation between surface-area and volume of individuals. Cophixalus monticola shows low water loss rates compared to close relatives of similar size. This pattern may be related to specialisation on Limnospadix palms as a preferred microhabitat which may offer less protection against water loss than other microhabitats. The combined information assembled in this research addresses some of the important knowledge gaps identified by national authorities, needed to improving the understanding of mechanisms behind climate change impacts. This new knowledge provides a basis for the development of more robust and accurate conservation strategies that will increase the success of adaptive management focused on the conservation of species threatened with extinction, such as the Australian endemic Cophixalus frogs