Hot climate, hot koalas: the role of weather, behaviour and disease on thermoregulation.

Thermoregulation is critical for endotherms living in hot, dry conditions, and maintaining optimal core body temperature (Tb) in a changing climate is an increasingly challenging task for mammals. Koalas (Phascolarctos cinereus) have evolved physiological and behavioural strategies to maintain homeostasis and regulate their Tb but are thought to be vulnerable to prolonged heat. We investigated how weather, behaviour and disease influence Tb for wild, free-living koalas during summer in north-west New South Wales. We matched Tb with daily behavioural observations in an ageing population where chlamydial disease is prevalent. Each individual koala had similar Tb rhythms (average Tb = 36.4 ± 0.05°C), but male koalas had higher Tb amplitude and more pronounced daily rhythm than females. Disease disrupted the 24-hr circadian pattern of Tb. Koala Tb increased with ambient temperature (Ta). On the hottest day of the study (maximum Ta = 40.8°C), we recorded the highest (Tb = 40.8°C) but also the lowest (Tb = 32.4°C) Tb ever documented for wild koalas, suggesting that they are more heterothermic than previously recognized. This requires individuals to predict days of extreme Ta from overnight and early morning conditions, adjusting Tb regulation accordingly, and it has never been reported before for koalas. The large diel amplitude and low minimum Tb observed suggest that koalas at our study site are energetically and nutritionally compromised, likely due to their age. Behaviour (i.e. tree hugging and drinking water) was not effective in moderating Tb. These results indicate that Ta and koala Tb are strongly interconnected and reinforce the importance of climate projections for predicting the future persistence of koalas throughout their current distribution. Global climate models forecast that dry, hot weather will continue to escalate and drought events will increase in frequency, duration and severity. This is likely to push koalas and other arboreal folivores towards their thermal limit.

Comparison of home range size, habitat use and the influence of resource variations between two species of greater gliders (Petauroides minor and Petauroides volans).

Knowledge of the spatial requirements of a species is fundamental to understanding its environmental requirements. However, this can be challenging as the size of a species' home range can be influenced by ecological factors such as diet and size-dependent metabolic demands, as well as factors related to the quality of their habitat such as the density and distribution of resources needed for food and shelter. Until recently, the genus Petauroides was thought to include only a single species with a widespread distribution across eastern Australia. However, a recent study has provided genetic and morphological evidence supporting Petauroides minor as a distinct northern species. Previous studies have focused on the ecology of P. volans, but there has been inadequate research on P. minor. Data on home range and habitat use were obtained for both species using a combination of techniques including GPS collar locations, radiotelemetry, and spotlighting and comparisons were made using consistent methodology. Home range sizes of P. minor (4.79 ha ± 0.97 s.d., KUD .95) were significantly larger than those of P. volans (2.0 ha ± 0.42 s.d., KUD .95). There were no significant differences between male and female home range sizes in either species. Both species showed site-specific preferences for tree species and for larger diameter trees for both forage and shelter. Tree size and biomass/ha were significantly greater in the P. volans study sites than the P. minor study sites and there was a negative correlation between home range size and eucalypt biomass. Larger home range size is likely driven by the substantial differences in biomass between northern (tropical) and southern (temperate) eucalypt-dominated habitats affecting the quality and quantity of resources for food and shelter. Understanding landscape use and habitat requirements within each species of Petauroides can provide important information regarding limiting factors and in directing conservation and management planning.

Food intake: an overlooked driver of climate change casualties?

Reduced voluntary food intake is a common response of endotherms to warmer temperatures. However, the implications of this are rarely considered for wild animals exposed to higher temperatures caused by climate change. We provide a conceptual model to demonstrate the potential consequences of elevated temperatures on food intake and survival.

Genetic evidence supports three previously described species of greater glider, Petauroides volans, P. minor, and P. armillatus.

The identification and classification of species are essential for effective conservation management. This year, Australia experienced a bushfire season of unprecedented severity, resulting in widespread habitat loss and mortality. As a result, there has been an increased focus on understanding genetic diversity and structure across the range of individual species to protect resilience in the face of climate change. The greater glider (Petauroides volans) is a large, gliding eucalypt folivore. This nocturnal arboreal marsupial has a wide distribution across eastern Australia and is considered the sole extant member of the genus Petauroides. Differences in morphology have led to suggestions that the one accepted species is actually three. This would have substantial impacts on conservation management, particularly given a recent history of declining populations, coupled with extensive wildfires. Until now, genetic evidence to support multiple species has been lacking. For the first time, we used DArT sequencing on greater glider tissue samples from multiple regions and found evidence of three operational taxonomic units (OTUs) representing northern, central and southern groups. The three OTUs were also supported by our morphological data. These findings have important implications for greater glider management and highlight the role of genetics in helping to assess conservation status.

Genomic comparisons reveal biogeographic and anthropogenic impacts in the koala (Phascolarctos cinereus): a dietary-specialist species distributed across heterogeneous environments.

The Australian koala is an iconic marsupial with highly specific dietary requirements distributed across heterogeneous environments, over a large geographic range. The distribution and genetic structure of koala populations has been heavily influenced by human actions, specifically habitat modification, hunting and translocation of koalas. There is currently limited information on population diversity and gene flow at a species-wide scale, or with consideration to the potential impacts of local adaptation. Using species-wide sampling across heterogeneous environments, and high-density genome-wide markers (SNPs and PAVs), we show that most koala populations display levels of diversity comparable to other outbred species, except for those populations impacted by population reductions. Genetic clustering analysis and phylogenetic reconstruction reveals a lack of support for current taxonomic classification of three koala subspecies, with only a single evolutionary significant unit supported. Furthermore, ~70% of genetic variance is accounted for at the individual level. The Sydney Basin region is highlighted as a unique reservoir of genetic diversity, having higher diversity levels (i.e., Blue Mountains region; AvHecorr=0.20, PL% = 68.6). Broad-scale population differentiation is primarily driven by an isolation by distance genetic structure model (49% of genetic variance), with clinal local adaptation corresponding to habitat bioregions. Signatures of selection were detected between bioregions, with no single region returning evidence of strong selection. The results of this study show that although the koala is widely considered to be a dietary-specialist species, this apparent specialisation has not limited the koala's ability to maintain gene flow and adapt across divergent environments as long as the required food source is available.

Substantial reduction in thermo-suitable microhabitat for a rainforest marsupial under climate change.

Increases in mean temperatures caused by anthropogenic climate change increase the frequency and severity of temperature extremes. Although extreme temperature events are likely to become increasingly important drivers of species' response to climate change, the impacts are poorly understood owing mainly to a lack of understanding of species' physiological responses to extreme temperatures. The physiological response of Pseudochirops archeri (green ringtail possum) to temperature extremes has been well studied, demonstrating that heterothermy is used to reduce evaporative water loss at temperatures greater than 30°C. Dehydration is likely to limit survival when animals are exposed to a critical thermal regime of ≥30°C, for ≥5 h, for ≥4 consecutive days. In this study, we use this physiological information to assess P. archeri's vulnerability to climate change. We identify areas of current thermo-suitable habitat (validated using sightings), then estimate future thermo-suitable habitat for P. archeri, under four emission scenarios. Our projections indicate that up to 86% of thermo-suitable habitat could be lost by 2085, a serious conservation concern for the species. We demonstrate the potential applicability of our approach for generating spatio-temporally explicit predictions of the vulnerability of species to extreme temperature events, providing a focus for efficient and targeted conservation and habitat restoration management.

Hydroregulation in a tropical dry-skinned ectotherm.

While temperature effects on species' vulnerability to climate change are well studied, desiccation effects receive comparatively little attention. In addition, we poorly understand the capacity of ectotherms, and especially reptiles, to control water loss rates behaviourally by selecting suitable microhabitats. This study examined water loss rates and behavioural hydroregulation in the tropical rainforest skink Carlia rubrigularis to assess whether this dry-skinned ectotherm actively avoids desiccation and whether trade-offs occur between desiccation avoidance and selection of optimal temperatures, as previously shown in amphibians. Higher temperatures elicited humid refuge choice despite placing individuals in suboptimal thermal conditions, as indicated by preferred substrate temperatures. This finding emphasizes the importance of water loss even for taxa traditionally assumed to be highly desiccation resistant, and highlights this factor's potential influence on vulnerability to climate change by limiting activity times or by restricting individuals to thermally suboptimal microhabitats.

Extensive Acclimation in Ectotherms Conceals Interspecific Variation in Thermal Tolerance Limits.

Species' tolerance limits determine their capacity to tolerate climatic extremes and limit their potential distributions. Interspecific variation in thermal tolerances is often proposed to indicate climatic vulnerability and is, therefore, the subject of many recent meta-studies on differential capacities of species from climatically different habitats to deal with climate change. Most studies on thermal tolerances do not acclimate animals or use inconsistent, and insufficient, acclimation times, limiting our knowledge of the shape, duration and extent of acclimation responses. Consequently patterns in thermal tolerances observed in meta-analyses, based on data from the literature are based on inconsistent, partial acclimation and true trends may be obscured. In this study we describe time-course of complete acclimation of critical thermal minima in the tropical ectotherm Carlia longipes and compare it to the average acclimation response of other reptiles, estimated from published data, to assess how much acclimation time may contribute to observed differences in thermal limits. Carlia longipes decreased their lower critical thermal limits by 2.4°C and completed 95% of acclimation in 17 weeks. Wild populations did not mirror this acclimation process over the winter. Other reptiles appear to decrease cold tolerance more quickly (95% in 7 weeks) and to a greater extent, with an estimated average acclimation response of 6.1°C. However, without data on tolerances after longer acclimation times available, our capacity to estimate final acclimation state is very limited. Based on the subset of data available for meta-analysis, much of the variation in cold tolerance observed in the literature can be attributed to acclimation time. Our results indicate that (i) acclimation responses can be slow and substantial, even in tropical species, and (ii) interspecific differences in acclimation speed and extent may obscure trends assessed in some meta-studies. Cold tolerances of wild animals are representative of cumulative responses to recent environments, while lengthy acclimation is necessary for controlled comparisons of physiological tolerances. Measures of inconsistent, intermediate acclimation states, as reported by many studies, represent neither the realised nor the potential tolerance in that population, are very likely underestimates of species' physiological capacities and may consequently be of limited value.

Tree-hugging koalas demonstrate a novel thermoregulatory mechanism for arboreal mammals.

How climate impacts organisms depends not only on their physiology, but also whether they can buffer themselves against climate variability via their behaviour. One of the way species can withstand hot temperatures is by seeking out cool microclimates, but only if their habitat provides such refugia. Here, we describe a novel thermoregulatory strategy in an arboreal mammal, the koala Phascolarctos cinereus. During hot weather, koalas enhanced conductive heat loss by seeking out and resting against tree trunks that were substantially cooler than ambient air temperature. Using a biophysical model of heat exchange, we show that this behaviour greatly reduces the amount of heat that must be lost via evaporative cooling, potentially increasing koala survival during extreme heat events. While it has long been known that internal temperatures of trees differ from ambient air temperatures, the relevance of this for arboreal and semi-arboreal mammals has not previously been explored. Our results highlight the important role of tree trunks as aboveground 'heat sinks', providing cool local microenvironments not only for koalas, but also for all tree-dwelling species.

Spatial requirements of free-ranging Huon tree kangaroos, Dendrolagus matschiei (Macropodidae), in upper montane forest.

Tree kangaroos (Macropodidae, Dendrolagus) are some of Australasia's least known mammals. However, there is sufficient evidence of population decline and local extinctions that all New Guinea tree kangaroos are considered threatened. Understanding spatial requirements is important in conservation and management. Expectations from studies of Australian tree kangaroos and other rainforest macropodids suggest that tree kangaroos should have small discrete home ranges with the potential for high population densities, but there are no published estimates of spatial requirements of any New Guinea tree kangaroo species. Home ranges of 15 Huon tree kangaroos, Dendrolagus matschiei, were measured in upper montane forest on the Huon Peninsula, Papua New Guinea. The home range area was an average of 139.6±26.5 ha (100% MCP; n = 15) or 81.8±28.3 ha (90% harmonic mean; n = 15), and did not differ between males and females. Home ranges of D. matschiei were 40-100 times larger than those of Australian tree kangaroos or other rainforest macropods, possibly due to the impact of hunting reducing density, or low productivity of their high altitude habitat. Huon tree kangaroos had cores of activity within their range at 45% (20.9±4.1 ha) and 70% (36.6±7.5 ha) harmonic mean isopleths, with little overlap (4.8±2.9%; n = 15 pairs) between neighbouring females at the 45% isopleth, but, unlike the Australian species, extensive overlap between females (20.8±5.5%; n = 15 pairs) at the complete range (90% harmonic mean). Males overlapped each other and females to a greater extent than did pairs of females. From core areas and overlap, the density of female D. matschiei was one per 19.4 ha. Understanding the cause of this low density is crucial in gaining greater understanding of variations in density of tree kangaroos across the landscape. We consider the potential role of habitat fragmentation, productivity and hunting pressure in limiting tree kangaroo density in New Guinea rainforests.

Phenotypic integration in response to incubation environment adaptively influences habitat choice in a tropical lizard.

Phenotypic integration, in which a suite of traits change in a correlated or covarying response to shifts in environmental conditions, may enhance an organism's fitness. In skinks, rocky environments select for longer limbs and rapid running and climbing. We examined whether differences in nest temperature coincident with specific habitats caused phenotypically integrated effects on morphology, locomotor performance, and behavior in the skink Carlia longipes. Specifically, we determined whether microhabitat choices were integrated with adaptive morphology for each habitat. Using a split-clutch design, we incubated eggs at thermal regimes that mimicked the thermal environments of nests from two habitat types (forest = warm; rocky = cool). Hatchlings from cool incubation environments had longer limbs and greater running and climbing speeds, which are likely to be beneficial for rocky habitats. In addition, individuals from cool incubation environments selected rocky microhabitats more frequently than did hatchlings from warm incubation environments. We demonstrate phenotypic integration in response to nest temperature that affected morphology, performance, and ultimately habitat selection in a way that should increase hatchling fitness.

The distribution and abundance of an island population of Koalas (Phascolarctos cinereus) in the far north of their geographic range.

Koalas are an iconic species of charismatic megafauna, of substantial social and conservation significance. They are widely distributed, often at low densities, and individuals can be difficult to detect, making population surveys challenging and costly. Consequently, koala population estimates have been limited and the results inconsistent. The aims of this study were to estimate the distribution, relative abundance and population size of the koalas on Magnetic Island, far north Queensland. Population densities were estimated in 18 different vegetation types present on the island using a Fecal Standing Crop Method. Koala density ranged from 0.404 ha(-1), recorded in forest red gum and bloodwood woodland, to absence from eight of the vegetation types surveyed. The second highest density of 0.297 koalas ha(-1) was recorded in mixed eucalypt woodland, which covers 45% of the island. The total abundance of koalas on Magnetic Island, not including those present in urban areas, was estimated at 825±175 (SEM). The large variation in koala density across vegetation types reinforces the need for sampling stratification when calculating abundance over large areas, as uniformity of habitat quality cannot be assumed. In this context, koala populations also occur in low densities in areas generally regarded as poor quality koala habitat. These results highlight the importance of protecting vegetation communities not traditionally considered to have high conservation value to koalas, as these habitats may be essential for maintaining viable, widespread, low-density populations. The results from this study provide a baseline to assess future trends in koala distribution, density and abundance on Magnetic Island.

Integrating phylogeography and physiology reveals divergence of thermal traits between central and peripheral lineages of tropical rainforest lizards.

Tropical ectotherms are regarded as being especially threatened by global warming, but the extent to which populations vary in key thermal physiological traits is little known. In general, central and peripheral populations are most likely to differ where divergent selection pressures are un-opposed by gene flow. This leads to the prediction that persistent and long-isolated lineages in peripheral regions, as revealed by phylogeography, may differ physiologically from larger centrally located lineages. We test this prediction through comparative assays of critical thermal limits (minimum and maximum critical thermal limits, CT(min), CT(max)) and optimal performance parameters (B80 and T(opt)) across central and peripheral lineages of three species of ground-dwelling skinks endemic to the rainforests of northeast Australia. Peripheral lineages show significantly increased optimal performance temperatures (T(opt)) relative to central populations as well as elevated CT(min), with the latter trait also inversely related to elevation. CT(max) did not vary between central and peripheral lineages, but was higher in a forest edge species than in the forest interior species. The results suggest that long-isolated populations in peripheral rainforests harbour genotypes that confer resilience to future warming, emphasizing the need to protect these as well as larger central habitats.

Predicting organismal vulnerability to climate warming: roles of behaviour, physiology and adaptation.

A recently developed integrative framework proposes that the vulnerability of a species to environmental change depends on the species' exposure and sensitivity to environmental change, its resilience to perturbations and its potential to adapt to change. These vulnerability criteria require behavioural, physiological and genetic data. With this information in hand, biologists can predict organisms most at risk from environmental change. Biologists and managers can then target organisms and habitats most at risk. Unfortunately, the required data (e.g. optimal physiological temperatures) are rarely available. Here, we evaluate the reliability of potential proxies (e.g. critical temperatures) that are often available for some groups. Several proxies for ectotherms are promising, but analogous ones for endotherms are lacking. We also develop a simple graphical model of how behavioural thermoregulation, acclimation and adaptation may interact to influence vulnerability over time. After considering this model together with the proxies available for physiological sensitivity to climate change, we conclude that ectotherms sharing vulnerability traits seem concentrated in lowland tropical forests. Their vulnerability may be exacerbated by negative biotic interactions. Whether tropical forest (or other) species can adapt to warming environments is unclear, as genetic and selective data are scant. Nevertheless, the prospects for tropical forest ectotherms appear grim.

Food for folivores: nutritional explanations linking diets to population density.

Ecologists want to explain why populations of animals are not evenly distributed across landscapes and often turn to nutritional explanations. In seeking to link population attributes with food quality, they often contrast nutritionally positive traits, such as the concentration of nitrogen, against negative ones, such as fibre concentration, by using a ratio of these traits. This specific ratio has attracted attention because it sometimes correlates with the biomass of colobine primates across sites in Asia and Africa. Although empirically successful, we have identified problems with the ratio that may explain why it fails under some conditions to predict colobine biomass. First, available nitrogen, rather than total nitrogen, is nutritionally important, while the presence of tannins is the major factor reducing the availability of nitrogen in browse plant species. Second, tannin complexes inflate measures of fibre. Finally, simple ratios may be unsound statistically because they implicitly assume isometric relationships between variables. We used data on the chemical composition of plants from three continents to examine the relationships between the concentrations of nitrogen, available nitrogen, fibre and tannins in foliage and to evaluate the nitrogen to fibre ratio. Our results suggest that the ratio of the concentration of nitrogen to fibre in leaves does sometimes closely correlate with the concentration of available nitrogen. However, the ratio may give misleading results when leaves contain high concentrations of tannins. The concentration of available nitrogen, which incorporates measures of total nitrogen, dry matter digestibility and tannins, should give a better indication of the nutritional value of leaves for herbivorous mammals that can readily be extrapolated to habitats.

The limit to the distribution of a rainforest marsupial folivore is consistent with the thermal intolerance hypothesis.

Models of impacts of climate change on species are generally based on correlations between current distributions and climatic variables, rather than a detailed understanding of the mechanisms that actually limit distribution. Many of the vertebrates endemic to rainforests of northeastern Australia are restricted to upland forests and considered to be threatened by climate change. However, for most of these species, the factors controlling their distributions are unknown. We examined the role of thermal intolerance as a possible mechanism limiting the distribution of Pseudochirops archeri (green ringtail possum), a specialist arboreal folivore restricted to rainforests above an altitude of 300 m in Australia's Wet Tropics. We measured short-term metabolic responses to a range of ambient temperatures, and found that P. archeri stores heat when ambient temperatures exceed 30°C, reducing water requirements for evaporative cooling. Due to the rate at which body temperature increases with ambient temperatures >30°C, this strategy is not effective over periods longer than 5 h. We hypothesise that the distribution of P. archeri is limited by interactions between (i) the duration and severity of extreme ambient temperatures (over 30°C), (ii) the scarcity of free water in the rainforest canopy in the dry season, and (iii) constraints on water intake from foliage imposed by plant secondary metabolites and fibre. We predict that dehydration becomes limiting for P. archeri where extreme ambient temperatures (>30°C) persist for more than 5 h per day over 4-6 days or more. Consistent with our hypothesis, the abundance of P. archeri in the field is correlated with the occurrence of extreme temperatures, declining markedly at sites where the average maximum temperature of the warmest week of the year is above 30°C. Assuming the mechanism of limitation is based on extreme temperatures, we expect impacts of climate change on P. archeri to occur in discrete, rapid events rather than as a slow contraction in range.

Venom physiology and composition in a litter of Common Death Adders (Acanthophis antarcticus) and their parents.

Metabolic expenditure has been shown to increase abruptly in several snake species directly after venom expenditure, while the later stages of venom replenishment seem to involve minor costs. This study examines the dependence of increases in metabolic rate following venom expenditure on the stage of venom replenishment that the venom producing tissue is in at the time of venom extraction in the Common Death Adder, Acanthophis antarcticus. Potential changes in venom composition during venom replenishment are also explored to elucidate whether replenishment is achieved via low rates of synthesis of all venom components or by non-parallel protein production, i.e. initial production of some venom components and subsequent synthesis of others. The results of this study indicate that venom expenditure is followed by a sudden increase in metabolic rate when snakes have previously not expended venom for at least two days, suggesting that repetitive venom expenditure does not further increase the activity of venom gland tissue in this initial time period but that a second upregulation occurs when the tissue is past the initial activation stage. In addition, venom composition appears to remain constant during replenishment within an individual, while substantial variations can be observed even between siblings.

Costs of venom production in the common death adder (Acanthophis antarcticus).

The utilization of venom in predatory and defensive contexts is associated with benefits regarding minimization of energetic expenditure on hunting, maximization of success in prey acquisition and avoidance of injury from dangerous prey and aggressors. Multiple characteristics suggest that venom is quite expensive to produce, thereby creating a tradeoff between advantages and disadvantages associated with its possession. The metabolic costs of venom production have rarely been studied and no information on the detailed metabolic processes during venom replenishment exists. Where costs of venom production have been studied they are often not in context with other components of the energy budget of the study organism. Using flow-through respirometry, we examined changes in metabolic rate in the Australian elapid Acanthophis antarcticus after venom expenditure and feeding as well as during preparation for shedding to establish a comparison of the magnitude of energetic expenditure during venom replenishment and other common physiological processes. We also defined the temporal pattern of metabolic processes during venom replenishment at a higher resolution than has previously been attempted in snakes. Our results suggest that total costs of venom replenishment are relatively small when compared to costs of digestion and shedding. We conclude that, in spite of the manifold factors suggesting a high cost of venom in snakes, its production is less energetically costly than often assumed. Until further research can clarify the reasons for this more caution should therefore be applied when assuming that costs of venom production exert strong selection pressures on the ecology, behavior and evolution of venomous taxa.

Inter-population differences in the tolerance of a marsupial folivore to plant secondary metabolites.

Plant secondary metabolites (PSMs) strongly influence diet selection by mammalian herbivores. Concentrations of PSMs vary within and among plant species, and across landscapes. Therefore, local adaptations may cause different populations of herbivores to differ in their ability to tolerate PSMs. Here, we tested the food intake responses of three populations of a marsupial folivore, the common brushtail possum (Trichosurus vulpecula Kerr), from different latitudes and habitat types, to four types of PSMs. We found clear variation in the responses of northern and southern Australian possums to PSMs. Brushtail possums from southern Australia showed marked decreases in food intake in response to all four PSMs, while the two populations from northern Australia were not as sensitive and their responses did not differ from one another. These results were unexpected, based on our understanding of the experiences of these populations with PSMs in the wild. Our results suggest that geographically separated populations of possums may have evolved differing abilities to cope with PSMs, as a result of local adaptation to their natural environments. Our results provide the basis for future studies to investigate the mechanisms by which populations of mammalian species differ in their ability to tolerate PSMs.