Bumblebee populations across the globe are experiencing substantial declines due to climate change, with major consequences for pollination services in both natural and agricultural settings. Using an economically important species, Bombus impatiens, we explored the physiological mechanisms that may cause susceptibility to extreme heat events. We tested the hypothesis that heat exposure limits the activity of the pentose phosphate pathway (PPP)-a parallel pathway to glycolysis that can use nectar sugar to generate antioxidant potential and combat oxidative stress. Using isotopically labelled glucose, we tracked PPP activity in B. impatiens at rest, during exercise and during a post-exercise recovery period under two different temperature regimes (22°C and 32°C). We found that the PPP is routinely used by B. impatiens at moderate temperatures, but that its activity is markedly reduced when ATP demands are high, such as during periods of exercise and heat exposure. We also exposed B. impatiens to either 22°C or 32°C for 5 hours and assessed levels of oxidative damage (lipid peroxidation, protein carbonyls) and antioxidant potential [reduced (GSH) and oxidized (GSSG) glutathione concentrations]. Interestingly, bees exhibited little oxidative damage after the thermal exposure, but we found a lower GSH:GSSG ratio in 32°C-exposed bees, reflecting lower antioxidant potential. Overall, our study demonstrates that acute heat stress severely limits PPP activity and may constrain antioxidant potential in B. impatiens. The repeated attenuation of this pathway in a warming climate may have more severe physiological consequences for this species, with potential implications for pollination services across North America.
Food availability determines the amount of energy animals can acquire and allocate to reproduction and other necessary functions. Female animals that are food limited thus experience reduced energy available for reproduction. When this occurs, females may reduce frequency of reproductive events or the number or size of offspring per reproductive bout. We assessed how maternal diet affects reproductive output in adult female Murray River short-necked turtles, Emydura macquarii, from four wetlands in Victoria. We previously found that turtle diets differ in the composition of plants and animals between our study wetlands. In this study, we tested whether differences in turtle diet composition (i.e. plants and animals) at these wetlands were associated with differences in clutch mass, individual egg mass, bulk egg composition and hatching success. We found total clutch mass increased with maternal body size at each site. At sites where filamentous green algae were scarce and E. macquarii were carnivorous, females produced smaller clutches relative to body size compared to females from sites where algae were abundant, and turtles were more herbivorous. Individual egg mass, bulk egg composition and hatching success did not differ across wetlands. Isotopic analysis revealed significant positive relationships between the carbon and nitrogen isotopes (δ13C, δ15N) of the eggs and those of the mothers, indicating that mothers allocated ratios of carbon and nitrogen isotopes to their eggs similar to those present in their tissues. Our study suggests that at sites where females are more carnivorous due to a relative absence of algae, females produce smaller clutches, but other aspects of their reproduction are not significantly impacted. The reduction in clutch size associated with differences in the availability of dietary plants and animals may have long-term consequences for E. macquarii and other freshwater turtle species that are experiencing population declines.
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.
Accretion of body fat by animals is an important physiological adaptation that may underpin seasonal behaviours, especially where it modulates risk associated with a particular behaviour. Using movement data from male Sierra Nevada bighorn sheep (Ovis canadensis sierrae), we tested the hypothesis that migratory behaviours were risk-sensitive to physiological state (indexed by body fat). Sierra bighorn face severe winter conditions at high elevations and higher predation risk at lower elevations. Given that large body fat stores ameliorate starvation risk, we predicted that having small body fat stores would force animals to migrate to lower elevations with more abundant food supplies. We also predicted that body fat stores would influence how far animals migrate, with the skinniest animals migrating the furthest down in elevation (to access the most abundant food supplies at that time of year). Lastly, we predicted that population-level rates of switching between migratory tactics would be inversely related to body fat levels because as body fat levels decrease, animals exhibiting migratory plasticity should modulate their risk of starvation by switching migratory tactics. Consistent with our predictions, probability of migration and elevational distance migrated increased with decreasing body fat, but effects differed amongst metapopulations. Population-level switching rates also were inversely related to population-level measures of body fat prior to migration. Collectively, our findings suggest migration was risk-sensitive to physiological state, and failure to accrete adequate fat may force animals to make trade-offs between starvation and predation risk. In complex seasonal environments, risk-sensitive migration yields a layer of flexibility that should aid long-term persistence of animals that can best modulate their risk by attuning behaviour to physiological state.
The mechanisms that determine the temperature tolerances of fish are poorly understood, creating barriers to disentangle how additional environmental challenges-such as CO2-induced aquatic acidification and fluctuating oxygen availability-may exacerbate vulnerability to a warming climate and extreme heat events. Here, we explored whether two acute exposures (~0.5 hours or ~72 hours) to increased CO2 impact acute temperature tolerance limits in a freshwater fish, rainbow trout (Oncorhynchus mykiss). We separated the potential effects of acute high CO2 exposure on critical thermal maximum (CTmax), caused via either respiratory acidosis (reduced internal pH) or O2 supply capacity (aerobic scope), by exposing rainbow trout to ~1 kPa CO2 (~1% or 10 000 μatm) in combination with normoxia or hyperoxia (~21 or 42 kPa O2, respectively). In normoxia, acute exposure to high CO2 caused a large acidosis in trout (blood pH decreased by 0.43 units), while a combination of hyperoxia and ~1 kPa CO2 increased the aerobic scope of trout by 28%. Despite large changes in blood pH and aerobic scope between treatments, we observed no impacts on the CTmax of trout. Our results suggest that the mechanisms that determine the maximum temperature tolerance of trout are independent of blood acid-base balance or the capacity to deliver O2 to tissues.
Body temperature is universally recognized as a dominant driver of biological performance. Although the critical distinction between the temperature of an organism and its surrounding habitat has long been recognized, it remains common practice to assume that trends in air temperature-collected via remote sensing or weather stations-are diagnostic of trends in animal temperature and thus of spatiotemporal patterns of physiological stress and mortality risk. Here, by analysing long-term trends recorded by biomimetic temperature sensors designed to emulate intertidal mussel temperature across the US Pacific Coast, we show that trends in maximal organismal temperature ('organismal climatologies') during aerial exposure can differ substantially from those exhibited by co-located environmental data products. Specifically, using linear regression to compare maximal organismal and environmental (air temperature) climatologies, we show that not only are the magnitudes of body and air temperature markedly different, as expected, but so are their temporal trends at both local and biogeographic scales, with some sites showing significant decadal-scale increases in organismal temperature despite reductions in air temperature, or vice versa. The idiosyncratic relationship between the spatiotemporal patterns of organismal and air temperatures suggests that environmental climatology cannot be statistically corrected to serve as an accurate proxy for organismal climatology. Finally, using quantile regression, we show that spatiotemporal trends vary across the distribution of organismal temperature, with extremes shifting in different directions and at different rates than average metrics. Overall, our results highlight the importance of quantifying changes in the entire distribution of temperature to better predict biological performance and dispel the notion that raw or 'corrected' environmental (and specially air temperature) climatologies can be used to predict organismal temperature trends. Hence, despite their widespread coverage and availability, the severe limitations of environmental climatologies suggest that their role in conservation and management policy should be carefully considered.