Flexible Employment of Torpor in Squirrel Gliders (Petaurus norfolcensis): An Adaptation to Unpredictable Climate?

AbstractTorpor is a highly effective response to counter various ecological and physiological bottlenecks in endotherms. In this study, we examined interrelations between thermoregulatory responses and key environmental variables in free-living squirrel gliders (Petaurus norfolcensis) in a habitat with drastic climatic and ecological changes across seasons. To this end, we measured body temperature (Tb) and heart rate (fH) simultaneously throughout the year using implanted data loggers. Squirrel gliders in our study experienced fluctuations in ambient temperature (Ta) between -4.0°C and 44.1°C and expressed torpor at different times during the year. In contrast to our expectations, torpor seemed to be employed flexibly, on demand, and most frequently in spring rather than during the coldest and/or hottest periods. Torpor bouts lasted, on average, about 5 h, and Tb during torpor dropped as low as 17.9°C. The fH during torpor decreased below 50 bpm, which is about one-third of the basal level. The ability to record fH alongside Tb enabled us to also report periods of low fH during thermoconforming hyperthermia at Ta's above 35°C that likely occurred to conserve energy and water. Our findings double the body size of Australian gliders for which data on torpor are available and advance our ecological understanding of the dynamics of torpor expression in wild mammals and of how animals cope with varying conditions. Moreover, they highlight that the flexibility of physiology and thermoregulatory responses are clearly more complex than previously thought.

Limited flexibility in departure timing of migratory passerines at the East-Mediterranean flyway.

The rapid pace of current global warming lead to the advancement of spring migration in the majority of long-distance migratory bird species. While data on arrival timing to breeding grounds in Europe is plentiful, information from the African departure sites are scarce. Here we analysed changes in arrival timing at a stopover site in Israel and any links to Enhanced Vegetation Index (EVI) on the species-specific African non-breeding range in three migratory passerines between 2000-2017. Differences in wing length between early and late arriving individuals were also examined as a proxy for migration distance. We found that male redstart, but not females, advanced arrival to stopover site, but interestingly, not as a response to EVI phenology. Blackcap and barred warbler did not shift arrival timing significantly, although the arrival of blackcap was dependent on EVI. Barred warbler from the early arrival phase had longer wings, suggesting different populations. Our study further supports the existence species-specific migration decisions and inter-sexual differences, which may be triggered by both exogenous (local vegetation condition) and endogenous cues. Given rapid rate of changes in environmental conditions at higher latitudes, some migrants may experience difficulty in the race to match global changes to ensure their survival.

Do small precocial birds enter torpor to conserve energy during development?

Precocial birds hatch feathered and mobile, but when they become fully endothermic soon after hatching, their heat loss is high and they may become energy depleted. These chicks could benefit from using energy-conserving torpor, which is characterised by controlled reductions of metabolism and body temperature (Tb). We investigated at what age the precocial king quail Coturnix chinensis can defend a high Tb under a mild thermal challenge and whether they can express torpor soon after achieving endothermy to overcome energetic and thermal challenges. Measurements of surface temperature (Ts) using an infrared thermometer showed that king quail chicks are partially endothermic at 2-10 days, but can defend high Tb at a body mass of ∼13 g. Two chicks expressed shallow nocturnal torpor at 14 and 17 days for 4-5 h with a reduction of metabolism by >40% and another approached the torpor threshold. Although chicks were able to rewarm endogenously from the first torpor bout, metabolism and Ts decreased again by the end of the night, but they rewarmed passively when removed from the chamber. The total metabolic rate increased with body mass. All chicks measured showed a greater reduction of nocturnal metabolism than previously reported in quails. Our data show that shallow torpor can be expressed during the early postnatal phase of quails, when thermoregulatory efficiency is still developing, but heat loss is high. We suggest that torpor may be a common strategy for overcoming challenging conditions during development in small precocial and not only altricial birds.

Water level affects availability of optimal feeding habitats for threatened migratory waterbirds.

Extensive ephemeral wetlands at Poyang Lake, created by dramatic seasonal changes in water level, constitute the main wintering site for migratory Anatidae in China. Reductions in wetland area during the last 15 years have led to proposals to build a Poyang Dam to retain high winter water levels within the lake. Changing the natural hydrological system will affect waterbirds dependent on water level changes for food availability and accessibility. We tracked two goose species with different feeding behaviors (greater white-fronted geese Anser albifrons [grazing species] and swan geese Anser cygnoides [tuber-feeding species]) during two winters with contrasting water levels (continuous recession in 2015; sustained high water in 2016, similar to those predicted post-Poyang Dam), investigating the effects of water level change on their habitat selection based on vegetation and elevation. In 2015, white-fronted geese extensively exploited sequentially created mudflats, feeding on short nutritious graminoid swards, while swan geese excavated substrates along the water edge for tubers. This critical dynamic ecotone successively exposes subaquatic food and supports early-stage graminoid growth during water level recession. During sustained high water levels in 2016, both species selected mudflats, but also to a greater degree of habitats with longer established seasonal graminoid swards because access to tubers and new graminoid growth was restricted under high-water conditions. Longer established graminoid swards offer less energetically profitable forage for both species. Substantial reduction in suitable habitat and confinement to less profitable forage by higher water levels is likely to reduce the ability of geese to accumulate sufficient fat stores for migration, with potential carryover effects on subsequent survival and reproduction. Our results suggest that high water levels in Poyang Lake should be retained during summer, but permitted to gradually recede, exposing new areas throughout winter to provide access for waterbirds from all feeding guilds.

An experimental examination of interindividual variation in feather corticosterone content in the house sparrow, Passer domesticus in southeast Australia.

Non-invasive techniques for measuring glucocorticoids (GCs) have become more prevalent, due to the advantage of eliminating the effects of animal disturbance on GC levels and their potential to provide an integrated, historic estimate of circulating GC levels. In the case of birds, corticosterone (CORT) is deposited in feathers, and may reflect a bird's GC status over the period of feather synthesis. This technique thus permits a retrospective view of the average circulating GC levels during the moult period. While it is generally assumed that differences in feather CORT content (CORTf) between individuals reflects their different stress histories during either natural or induced moult, it is not clear how much of this variation is due to extrinsic versus intrinsic factors. We examined this question by determining CORTf in free-living house sparrows (Passer domesticus) from two populations, one urban and the other rural, that were plucked before and after exposure to different plasma CORT levels while held captive. We experimentally manipulated plasma CORT by implanting birds with either a corticosterone-filled, metyrapone-filled, or empty ('sham') silastic capsule as replacement feathers first emerged. The pattern of post-treatment CORTf was consistent with our expectations, based on plasma CORT levels of an experimentally implanted reference group. However, there was no statistically significant difference in CORTf between these treatment groups unless sex, population origin, and CORTf of original feathers for each individual were included in a model. Thus, birds with higher CORTf in feathers removed for this experiment tended to have higher CORTf in post-treatment replacement feathers, irrespective of treatment. In addition, we found that feather fault bar scores were significantly higher in CORT-treated birds than in the other two treatment groups, but did not vary directly with CORTf level. Our study therefore broadly confirms the use of feathers as a non-invasive tool to estimate plasma CORT during moult in birds, but importantly demonstrates the potential for intrinsic differences in stress characteristics between populations and individuals to obscure the effects extrinsic stressors might have on CORTf.

Why fly the extra mile? Latitudinal trend in migratory fuel deposition rate as driver of trans-equatorial long-distance migration.

Trans-equatorial long-distance migrations of high-latitude breeding animals have been attributed to narrow ecological niche widths. We suggest an alternative hypothesis postulating that trans-equatorial migrations result from a possible increase in the rate at which body stores to fuel migration are deposited with absolute latitude; that is, longer, migrations away from the breeding grounds surpassing the equator may actually enhance fueling rates on the nonbreeding grounds and therewith the chance of a successful, speedy and timely migration back to the breeding grounds. To this end, we first sought to confirm the existence of a latitudinal trend in fuel deposition rate in a global data set of free-living migratory shorebirds and investigated the potential factors causing this trend. We next tested two predictions on how this trend is expected to impact the migratory itineraries on northward migration under the time-minimization hypothesis, using 56 tracks of high-latitude breeding shorebirds migrating along the East Asian-Australasian Flyway. We found a strong positive effect of latitude on fuel deposition rate, which most likely relates to latitudinal variations in primary productivity and available daily foraging time. We next confirmed the resulting predictions that (1) when flying from a stopover site toward the equator, migrants use long jumps that will take them to an equivalent or higher latitude at the opposite hemisphere; and (2) that from here onward, migrants will use small steps, basically fueling only enough to make it to the next suitable staging site. These findings may explain why migrants migrate "the extra mile" across the equator during the nonbreeding season in search of better fueling conditions, ultimately providing secure and fast return migrations to the breeding grounds in the opposite hemisphere.

Why fly the extra mile? Using stress biomarkers to assess wintering habitat quality in migratory shorebirds.

Migratory birds make decisions about how far to travel based on cost-benefit trade-offs. However, in many cases the net effect of these trade-offs is unclear. We sought to address this question by measuring feather corticosterone (CORTf), leucocyte profile, avian malaria parasite prevalence and estimating fueling rates in three spatially segregated wintering populations of the migratory shorebird ruddy turnstone Arenaria interpres during their stay in the winter habitat. These birds fly from the high-Arctic breeding ground to Australia, but differ in that some decide to end their migration early (Broome, Western Australia), whereas others travel further to either South Australia or Tasmania. We hypothesized that the extra costs in birds migrating greater distances and overwintering in colder climates would be offset by benefits when reaching their destination. This would be evidenced by lower stress biomarkers in populations that travel further, owing to the expected benefits of greater resources and improved vitality. We show that avian malaria prevalence and physiological stress levels were lower in birds flying to South Australia and Tasmania than those overwintering in Broome. Furthermore, our modeling predicts that birds in the southernmost locations enjoy higher fueling rates. Our data are consistent with the interpretation that birds occupying more costly wintering locations in terms of higher migratory flight and thermoregulatory costs are compensated by better feeding conditions and lower blood parasite infections, which facilitates timely and speedy migration back to the breeding ground. These data contribute to our understanding of cost-benefit trade-offs in the decision making underlying migratory behaviour.