Variety is the spice of life : flying-foxes exploit a variety of native and exotic food plants in an urban landscape mosaic

Generally, urbanization is a major threat to biodiversity; however, urban areas also provide habitats that some species can exploit. Flying-foxes (Pteropus spp.) are becoming increasingly urbanized; which is thought to be a result of increased availability and temporal stability of urban food resources, diminished natural food resources, or both. Previous research has shown that urban-roosting grey-headed flying-foxes (Pteropus poliocephalus) preferentially forage in human-modified landscapes. However, which land-use areas and food plants support its presence in urban areas is unknown. We tracked nine P. poliocephalus roosting in Adelaide, South Australia, between December 2019 and May 2020, using global positioning systems (GPS), to investigate how individuals used the urban landscape mosaic for feeding. The most frequently visited land-use category was “residential” (40% of fixes) followed by “road-side,” “reserves” and “primary production” (13–14% each). However, “reserves” were visited four times more frequently than expected from their areal availability, followed by the “residential” and “road-side” categories that were visited approximately twice more than expected each; in contrast, the “primary production” category was visited approximately five times less than expected. These results suggest that while residential areas provide most foraging resources supporting Adelaide’s flying-fox population, reserves contain foraging resources that are particularly attractive to P. poliocephalus. Primary production land was relatively less utilized, presumably because it contains few food resources. Throughout, flying-foxes visited an eclectic mixture of diet plants (49 unique species), with a majority of feeding fixes (63%) to locally indigenous Australian native species; however, in residential areas 53% of feeding visits were to non-locally indigenous species, vs only 13% in reserves. Flowering and fruiting phenology records of the food plants visited further indicated that non-locally indigenous species increase the temporal availability of foraging resources for P. poliocephalus in urban Adelaide. Our findings demonstrate the importance of residential areas for urban-roosting P. poliocephalus, and suggest that the anthropogenic mixture of food resources available in the urban landscape mosaic supports the species’ year-round presence in urban areas. Our results further highlight the importance of conserving natural habitats within the urban landscape mosaic, and stress the need for accounting for wildlife responses to urban greening initiatives

Temperature effects on metabolic rate and torpor in southern forest bats (Vespadelus regulus)

I measured the metabolic rate (MR) of four male southern forest bats (Vespadelus regulus; 5.5g) exposed to a diurnal increase in air temperature (T a) from 13 to 26°C, simulating conditions in natural tree roosts. Three bats remained in torpor throughout the day, despite the rise in T a, whereas one bat aroused at a T a of 25.2°C and was normothermic for 108min until re-entering torpor when T a declined in the afternoon. All bats aroused shortly after lights off. Torpid MR increased exponentially with rising T a, yet even at 26°C remained only 16% of minimum resting MR at the same T a. Rest-phase energy expenditure (12h), including the estimated cost of an evening arousal, ranged from 0.62 to 1.23kJ. Thus, torpor provides these small bats with an enormous reduction in energy consumption even at T a close to their thermoneutral zone

Survivable hypothermia or torpor in a wild-living rat : rare insights broaden our understanding of endothermic physiology

Maintaining a high and stable body temperature as observed in endothermic mammals and birds is energetically costly. Thus, it is not surprising that we discover more and more heterothermic species that can reduce their energetic needs during energetic bottlenecks through the use of torpor. However, not all heterothermic animals use torpor on a regular basis. Torpor may also be important to an individual’s probability of survival, and hence fitness, when used infrequently. We here report the observation of a single, ~ 5.5 h long hypothermic bout with a decrease in body temperature by 12 °C in the native Australian bush rat (Rattus fuscipes). Our data suggest that bush rats are able to rewarm from a body temperature of 24 °C, albeit with a rewarming rate lower than that expected on the basis of their body mass. Heterothermy, i.e. the ability to withstand and overcome periods of reduced body temperature, is assumed to be an evolutionarily ancestral (plesiomorphic) trait. We thus argue that such rare hypothermic events in species that otherwise appear to be strictly homeothermic could be heterothermic rudiments, i.e. a less derived form of torpor with limited capacity for rewarming. Importantly, observations of rare and extreme thermoregulatory responses by wild animals are more likely to be discovered with long-term data sets and may not only provide valuable insight about the physiological capability of a population, but can also help us to understand the constraints and evolutionary pathways of different phenologies

Hibernation and daily torpor minimize mammalian extinctions

Small mammals appear to be less vulnerable to extinction than large species, but the underlying reasons are poorly understood. Here, we provide evidence that almost all (93.5%) of 61 recently extinct mammal species were homeothermic, maintaining a constant high body temperature and thus energy expenditure, which demands a high intake of food, long foraging times, and thus exposure to predators. In contrast, only 6.5% of extinct mammals were likely heterothermic and employed multi-day torpor (hibernation) or daily torpor, even though torpor is widespread within more than half of all mammalian orders. Torpor is characterized by substantial reductions of body temperature and energy expenditure and enhances survival during adverse conditions by minimizing food and water requirements, and consequently reduces foraging requirements and exposure to predators. Moreover, because life span is generally longer in heterothermic mammals than in related homeotherms, heterotherms can employ a 'sit-and-wait' strategy to withstand adverse periods and then repopulate when circumstances improve. Thus, torpor is a crucial but hitherto unappreciated attribute of small mammals for avoiding extinction. Many opportunistic heterothermic species, because of their plastic energetic requirements, may also stand a better chance of future survival than homeothermic species in the face of greater climatic extremes and changes in environmental conditions caused by global warming

Hibernation by tree-roosting bats

In summer, long-eared bats (Nyctophilus spp.) roost under bark and in tree cavities, where they appear to benefit from diurnal heating of roosts. In contrast, hibernation is thought to require a cool stable temperature, suggesting they should prefer thermally insulated tree cavities during winter. To test this prediction, we quantified the winter thermoregulatory physiology and ecology of hibernating tree-roosting bats, Nyctophilus geoffroyi and N. gouldi in the field. Surprisingly, bats in winter continued to roost under exfoliating bark (65%) on the northern, sunny side of trees and in shallow tree cavities (35%). Despite passive re-warming of torpid bats by 10-20°C per day, torpor bouts lasted up to 15 days, although shorter bouts were also common. Arousals occurred more frequently and subsequent activity lasted longer on warmer nights, suggesting occasional winter foraging. We show that, because periodic arousals coincide with maximum roost temperatures, when costs of rewarming and normothermic thermoregulation are minimal, exposure to a daily temperature cycle could largely reduce energy expenditure during hibernation. Our study provides further evidence that models of torpor patterns and energy expenditure from hibernators in cold temperate climates are not directly applicable in milder climates, where prolonged torpor can be interspersed with more frequent arousals and occasional foraging

Thermal climate linked variation in annual survival rate of hibernating rodents : shorter winter dormancy and lower survival in warmer climates

In seasonal climates, many animals, including a wide range of small mammals, are physiologically capable of prolonged dormancy (˜hibernation), when foraging-related activity ceases entirely for part the year. Low metabolic rates while dormant minimise energy and water requirements, but the behavioural state of inactivity also reduces exposure to mortality risks, especially predation. Thermal effects on activity underlie spatial patterns in annual survival rate of ectothermic animals. We hypothesised that, because local thermal conditions affect the duration of mammalian hibernation, positive effects of dormancy on survival could also underlie a negative relationship between spatial variation in thermal climate and annual survival rate among populations of hibernating rodents. We applied mixed models to test for effects of local thermal climate on collated data of hibernation duration and annual survival rate among populations of hibernating and a representative sample of non-hibernating rodent species. Our analyses revealed strong negative effects of mean annual temperature on hibernation duration and adult annual survival rate within hibernating species (β: −8•6 day and −5•1% per 1 °C) but no effect in non-hibernating rodent species. This thermal climate-linked pattern in annual survival rate seems to be unique among mammals. A parsimonious explanation lies in the large increase in monthly survival rates during hibernation compared to activity. The current spatial pattern suggests ongoing climate warming might reduce annual survival rates of hibernating rodents by shortening their hibernation season. Decreased annual survival because of increased activity in warmer climates with shorter winter seasons is an unappreciated mechanism leading to impacts of global warming on animal populations in temperate climates

Torpor reduces predation risk by compensating for the energetic cost of antipredator foraging behaviours

Foraging activity is needed for energy intake but increases the risk of predation, and antipredator behavioural responses, such as reduced activity, generally reduce energy intake. Hence, the mortality and indirect effects of predation risk are dependent on the energy requirements of prey. Torpor, a controlled reduction in resting metabolism and body temperature, is a common energy-saving mechanism of small mammals that enhances their resistance to starvation. Here we test the hypothesis that torpor could also reduce predation risk by compensating for the energetic cost of antipredator behaviours. We measured the foraging behaviour and body temperature of house mice in response to manipulation of perceived predation risk by adjusting levels of ground cover and starvation risk by 24 h food withdrawal every third day. We found that a voluntary reduction in daily food intake in response to lower cover (high predation risk) was matched by the extent of a daily reduction in body temperature. Our study provides the first experimental evidence of a close link between energy-saving torpor responses to starvation risk and behavioural responses to perceived predation risk. By reducing the risk of starvation, torpor can facilitate stronger antipredator behaviours. These results highlight the interplay between the capacity for reducing metabolic energy expenditure, optimal decisions about foraging behaviour and the life-history ecology of prey

Timing of the daily temperature cycle affects the critical arousal temperature and energy expenditure of lesser long-eared bats

Daily patterns of body temperature (Tb) and energy expenditure in heterothermic endotherms are affected by changes in ambient temperature (Ta) and selection of suitable microclimates, yet most laboratory studies employ constant Ta to measure metabolic rates. In particular, exposure to a daily temperature cycle, even within rest shelters, may be important in timing of torpor and arousal and determining resting energy costs in wild animals. We tested how captive bats (Nyctophilus geoffroyi; 7 g) exposed to a diurnal Ta fluctuation (between 13°C and 27°C), similar to natural conditions in their summer tree roosts, adjusted the timing of daily arousals. To distinguish the effects of Ta and passive rewarming from time of the day, we shifted the heating phase to commence at 06:00h, 09:00h or 12:00h on each day. Bats entered torpor overnight and aroused the next day at a time corresponding to rising Ta and passive rewarming. The critical Ta (and torpid Tb) for arousal was not fixed, however, but was lower when heating occurred later in the rest phase, providing the first evidence that the critical arousal Ta is affected by time of the day. Bats re-entered torpor in response to cooling late in the afternoon, yet always aroused at lights off. A period of normothermic thermoregulation was therefore closely synchronised with maximum daily Ta, indicating a trade-off between the benefits and energetic costs of normothermia during resting. Our experiment clearly shows that a daily Ta cycle affects the thermoregulatory behaviour and energetics of these small bats. More generally, these results demonstrate the critical influence of behavioural decisions on the daily energy expenditure of small heterothermic mammals

Torpor use and body mass gain during pre-hibernation in late-born juvenile garden dormice exposed to food shortage

Prior to hibernation, juvenile hibernators have to sustain both somatic growth and fattening to reach a sufficient body mass to survive the following winter season. This high demand for energy is especially challenging for juveniles born late in the season, since they might already experience reduced food availability and decreasing temperatures. In this study, we asked whether late-born juvenile garden dormice can use torpor to counteract intermittent food shortages and, if so, whether the use of torpor enables them to compensate the energy deficit and to maintain rates of body mass gain similar to well-fed juveniles. We measured daily torpor use, food intake, and body mass in weaned late-born juvenile dormice exposed to intermittent fasting (n = 5) or fed ad libitum (n = 4) under natural photoperiod and ambient temperature during 6 weeks prior to hibernation (13 September-! November). We found that fasted juveniles frequently used torpor and despite eating less food grew at a significantly greater rate compared to juveniles fed ad libitum. Torpor frequency was positively related to body mass gain, but this effect was statistically significant only in the fasted group. Consequently, fasted juvenile dormice reached a critical body mass and entered into hibernation 1 week earlier than ad libitum fed juveniles. If fasted juveniles reached a similar pre-hibernation fat content compared to animals fed ad libitum, and how any difference in fat versus fat-free mass might affect hibernation propensity and winter survival, remains to be determined

Survival, aging, and life-history tactics in mammalian hibernators

Hibernation is commonly viewed as an adaptation that simply allows animals to survive periods of food shortage and climatically harsh conditions. Here, we review accumulating evidence suggesting that hibernation is part of a specific "slow-paced" mammalian life-history tactic that is associated with increased survival, retarded physiological aging, increased maximum longevity, low rates of fecundity, and long generation times. We argue that these traits can be explained if the primary function of hibernation-at least in many species-is the reduction of extrinsic mortality risks, namely predation, under environmental conditions that are not lifethreatening, but do not favor reproduction. According to this view, hibernation is but one element of a life-history strategy that maximizes fitness by bet-hedging, i.e., reducing the risk oflosing offspring by spreading lifetime reproductive effort over a number of temporally separated bouts. Further, increased survival and spreading of reproductive bouts should allow hibernators to produce young at times when climate and food resources are optimal for the rearing of offspring