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.

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.

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.

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.