Changes in body condition of hibernating bats support the thrifty female hypothesis and predict consequences for populations with white-nose syndrome

White-nose syndrome (WNS) is a new disease of bats that has devastated populations in eastern North America. Infection with the fungus, Geomyces destructans, is thought to increase the time bats spend out of torpor during hibernation, leading to starvation. Little is known about hibernation in healthy, free-ranging bats and more data are needed to help predict consequences of WNS. Trade-offs presumably exist between the energetic benefits and physiological/ecological costs of torpor, leading to the prediction that the relative importance of spring energy reserves should affect an individual''s use of torpor and depletion of energy reserves during winter. Myotis lucifugus mate during fall and winter but females do not become pregnant until after spring emergence. Thus, female reproductive success depends on spring fat reserves while male reproductive success does not. Consequently, females should be “thrifty” in their use of fat compared to males. We measured body condition index (BCI; mass/forearm length) of 432 M. lucifugus in Manitoba, Canada during the winter of 2009/2010. Bats were captured during the fall mating period (n = 200), early hibernation (n = 125), and late hibernation (n = 128). Adult females entered hibernation with greater fat reserves and consumed those reserves more slowly than adult males and young of the year. Consequently, adult females may be more likely than males or young of the year to survive the disruption of energy balance associated with WNS, although surviving females may not have sufficient reserves to support reproduction.     

The tradeoff between torpor use and reproduction in little brown bats (Myotis lucifugus)

In mammals, reproduction, especially for females is energetically demanding. Therefore, during the reproductive period females could potentially adjust patterns of thermoregulation and foraging in concert to minimise the energetic constraints associated with pregnancy and lactation. We assessed the influence of pregnancy, lactation, and post-lactation on torpor use and foraging behaviour by female little brown bats, Myotis lucifugus. We measured thermoregulation by recording skin temperature and foraging by tracking bats which carried temperature-sensitive radio-tags. We found that individuals, regardless of reproductive condition, used torpor, but the patterns of torpor use varied significantly between reproductive (pregnant and lactating) females and post-lactating females. As we predicted, reproductive females entered torpor for shorter bouts than post-lactating females. Although all females used torpor frequently, pregnant females spent less time in torpor, and maintained higher skin temperatures than either lactating or post-lactating females. This result suggests that delayed offspring development which has been associated with torpor use during pregnancy, may pose a higher risk to an individual’s reproductive success than reduced milk production during lactation. Conversely, foraging behaviour of radio-tagged bats did not vary with reproductive condition, suggesting that even short, shallow bouts of torpor produce substantial energy savings, likely obviating the need to spend more time foraging. Our data clearly show that torpor use and reproduction are not mutually exclusive and that torpor use (no matter how short or shallow) is an important means of balancing the costs of reproduction for M. lucifugus.     

Summer heterothermy in Rafinesque’s big-eared bats (Corynorhinus rafinesquii) roosting in tree cavities in bottomland hardwood forests

Many small mammals are heterothermic endotherms capable of maintaining an elevated core body temperature or reducing their thermoregulatory set point to enter a state of torpor. Torpor can confer substantial energy savings, but also incurs ecological costs, such as hindering allocation of energy towards reproduction. We placed temperature-sensitive radio transmitters on 44 adult Rafinesque’s big-eared bats (Corynorhinus rafinesquii) and deployed microclimate dataloggers inside 34 day roosts to compare the use of torpor by different sex and reproductive classes of bats during the summer. We collected 324 bat-days of skin-temperature data from 36 females and 4 males. Reproductive females employed fewer torpor bouts per day than non-reproductive females and males (P < 0.0001), and pregnant and lactating females had higher average (P < 0.0001) and minimum (P < 0.0001) skin temperatures than non-reproductive females. Pregnant females spent less time torpid (P < 0.0001) than non-reproductive females, but lactating females used relatively deep, long torpor bouts. Microclimates varied inside tree species with different configurations of entrances to the roost cavity (P < 0.0001). Bats spent more time torpid when roosting in water tupelo (Nyssa aquatica) trees possessing only a basal entrance to the cavity (P = 0.001). Of the tree species used as roosts, water tupelo cavities exhibited the least variable daytime and nighttime temperatures. These data demonstrate that use of summer torpor is not uniform among sex and reproductive classes in Rafinesque’s big-eared bat, and variation in microclimate among tree roosts due to species and structural characteristics facilitates the use of different thermoregulatory strategies in these bats.     

Seasonal changes in daily torpor patterns of free-ranging female and male Daubenton’s bats (Myotis daubentonii)

Daily torpor can provide significant energy and water savings in bats during cold ambient temperatures and food scarcity. However, it may reduce rates of foetal and juvenile development. Therefore, reproductive females should optimize development by minimizing times in torpor. To test this hypothesis, the use of torpor by female and male free-ranging Daubenton’s bats (Myotis daubentonii) during reproduction (gestation, lactation, and post-lactation period) was investigated in 1998 and 1999. Temperature-sensitive radio transmitters were attached to the bats to measure skin temperature. Simultaneously, ambient temperature was recorded. While both sexes became torpid during daytime, male bats used daily torpor (>6°C below individual active temperature) significantly more often during reproductive period (mean: 78.4 % of day time in May and 43 % in June) than females. Female bats went into daily torpor, particularly in late summer when juveniles were weaned (mean: 66.6 % of daytime). Lowest skin temperatures occurred in a female bat with 21.0°C during post-lactation. Skin temperatures of male bats fluctuated from 16.8°C in torpor to 37.2°C during times of activity. There was a significant effect of reproductive period on skin temperature in females whereas mean ambient temperature had no significant effect. However, mean ambient temperature affected mean skin temperatures in males. Our findings indicate that female Daubenton’s bats adopt their thermoregulatory behaviour in particular to optimize the juvenile development.     

Stage of pregnancy dictates heterothermy in temperate forest-dwelling bats

Bats face high energetic requirements, as powered flight is costly and they have a disadvantageous surface-to-volume-ratio. To deal with those requirements energy saving mechanisms, such as heterothermy (torpor), have evolved. Torpor during pregnancy, however, reduces rates of foetal development and consequently prolongs pregnancy. Therefore, heterothermy has a great effect on reproduction, as an unhindered parturition can only be assured by high body temperatures. Regardless of these adverse affects of torpor the energetic requirements of bats during reproduction urge for energy savings and bats are known to enter torpor during pregnancy. The species in the current study differ in their torpor patterns and thus their heterothermic strategy. However, we hypothesized, that species-specific heterothermic behaviour should be revoked at the end of pregnancy. We analyzed skin temperatures of Myotis bechsteinii, Myotis nattereri and Plecotus auritus during pregnancy and found no differences in torpor depth between species during the last phase of pregnancy. Furthermore, we could show that individuals entered torpor frequently during pregnancy and only minimized torpor during the last stage of pregnancy. This suggests that close to the end of pregnancy, heterothermy is restricted but not species-specific and the required energy is allocated otherwise.     

Energy expenditure increases during the active season in the small,free-living hibernator Muscardinus avellanarius

Little is known about strategies employed by small mammals to reduce energy expenditure during the summer. To understand whether ambient conditions impact euthermic energy demands in a small free-living hibernator, we measured metabolic rate of hazel dormice (Muscardinus avellanarius) in the field. Furthermore, we aimed to reveal which variables influence torpor use. Our results show that hazel dormice altered euthermic energy expenditure during summer but not as expected as a response to environmental conditions. Euthermic resting metabolic rate was lowest directly after emergence from hibernation and increased by about 95% until the end of August. A considerable part of this increase was presumably caused by the changing influence of gender and rain on energy demands during different months, variation in food quality and quantity, and reversible size changes of organs that had been atrophied during hibernation. Torpor use in hazel dormice occurred more frequently when it was colder, earlier during the day, and in lighter individuals. Torpor was used routinely in males and non-reproductive females. We show that torpor is used more frequently than previously suggested by studies that only used visual proof of torpor use by surveying nest boxes.     

The influence of reproductive condition and concurrent environmental factors on torpor and foraging patterns in female big brown bats (Eptesicus fuscus)

Unlike many othe r mammals, bats in temperate regions employ short bouts of torpor throughout the reproductive period to maintain a positive energy balance. In addition to decreasing energy expenditure during the day, they typically alter foraging patterns as well. It is well known that various environmental conditions influence both torpor and foraging patterns, but studies of these factors often have focussed on one element in isolation thus it is not known how the two behaviours are collectively influencing temperate bats. The objective of our study was to assess how reproductive condition and environmental factors concurrently affect energy balance in female big brown bats (Eptesicus fuscus). We equipped pregnant and lactating bats in southwest Saskatchewan, Canada with temperature-sensitive radio-transmitters. While transmitters were active, skin temperature data were collected and foraging patterns were determined using triangulation. Of the various environmental and physiological parameters used to model torpor characteristics, roost type was the most important factor. Bats roosting in trees used deeper and longer torpor bouts than those roosting in buildings. Lactating bats had a tendency to forage for longer durations than pregnant bats, and often made more foraging trips. When taken together, we found that foraging duration and torpor duration were not directly related during pregnancy, but exhibited an inverse relationship during lactation. This provides support for the hypothesis that there are physiological trade-offs for reproductive bats and suggests that how bats compensate is not entirely predictable based on current environmental conditions.     

Hibernation by a free-ranging subtropical bat (Nyctophilus bifax)

Knowledge about torpor in free-ranging subtropical bats is scarce and it is widely believed that low and stable ambient temperatures are necessary for prolonged torpor. We present temperature-telemetry data from free-ranging male (n = 4) and female (n = 4) subtropical vespertilionid bats, Nyctophilus bifax (~10 g), exposed to pronounced daily fluctuations of ambient temperature. All bats used torpor on every day in winter and both males and females exhibited multi-day torpor bouts of up to 5.4 days. Although females were larger than males, patterns of torpor were similar in both sexes. Torpor use was correlated with prevailing weather conditions and, on days when bats remained torpid, maximum ambient temperature was significantly lower than on days when bats aroused. Moreover, the duration of interbout normothermic periods at night increased with increasing average nightly ambient temperature. Skin temperature of torpid bats varied by 10.2 ± 3.6°C day⁻¹ (n = 8, N = 47) and daily minimum skin temperature was positively correlated with the daily minimum ambient temperature. Our study shows that prolonged torpor is an important component of the winter ecology of a subtropical bat and that torpor and activity patterns of N. bifax predominantly reflect prevailing weather conditions.     

Will Temperature Effects or Phenotypic Plasticity Determine the Thermal Response of a Heterothermic Tropical Bat to Climate Change?

The proportion of organisms exposed to warm conditions is predicted to increase during global warming. To better understand how bats might respond to climate change, we aimed to obtain the first data on how use of torpor, a crucial survival strategy of small bats, is affected by temperature in the tropics. Over two mild winters, tropical free-ranging bats (Nyctophilus bifax, 10 g, n = 13) used torpor on 95% of study days and were torpid for 33.5±18.8% of 113 days measured. Torpor duration was temperature-dependent and an increase in ambient temperature by the predicted 2°C for the 21^st century would decrease the time in torpor to 21.8%. However, comparisons among Nyctophilus populations show that regional phenotypic plasticity attenuates temperature effects on torpor patterns. Our data suggest that heterothermy is important for energy budgeting of bats even under warm conditions and that flexible torpor use will enhance bats’ chance of survival during climate change.     

Do female newts modify thermoregulatory behavior to manipulate egg size?

Reproductive females manipulate offspring phenotypes by modifying conditions during embryogenesis. In ectotherms, the environmental control over embryogenesis is often realized by changes in maternal thermoregulation during gravidity. To determine if reproduction influences thermoregulatory behavior in species where females lay eggs shortly after fertilization (strict oviparity), we compared preferred body temperatures (T_p) between reproductive (egg-laying) and non-reproductive female newts, Ichthyosaura alpestris. Next, we exposed reproductive females to temperatures mimicking T_p ranges of reproductive and non-reproductive individuals to find out whether the maternally modified thermal regime influences ovum and jelly coat volume, and early cleavage rates at the time of oviposition. In the thermal gradient, reproductive females maintained their body temperatures within a narrower range than non-reproductive individuals. The exposure of ovipositing females to temperatures preferred during their reproductive and non-reproductive period had a negligible influence on egg size and early cleavage rates. We conclude that the modification of maternal thermoregulatory behavior provides a limited opportunity to manipulate egg traits in newts.     

Thermal physiology of pregnant and lactating female and male long-eared bats, Nyctophilus geoffroyi and N. gouldi

During roosting in summer, reproductive female bats appear to use torpor less frequently and at higher body temperatures (T _b) than male bats, ostensibly to maximise offspring growth. To test whether field observations result from differences in thermal physiology or behavioural thermoregulation during roosting, we measured the thermoregulatory response and energetics of captive pregnant and lactating female and male long-eared bats (Nyctophilus geoffroyi 8.9 g and N. gouldi 11.5 g) during overnight exposure to a constant ambient temperature (T _a) of 15°C. Bats were captured 1–1.5 h after sunset and measurements began at 21:22±0:36 h. All N. geoffroyi entered torpor commencing at 23:47±01:01 h. For N. gouldi, 10/10 males, 9/10 pregnant females and 7/8 lactating females entered torpor commencing at 01:10±01:40 h. The minimum T _b of torpid bats was 15.6±1.1°C and torpid metabolic rate (TMR) was reduced to 0.05±0.02 ml O₂ g⁻¹ h⁻¹. Sex or reproductive condition of either species did not affect the timing of entry into torpor (F=1.5, df=2, 19, P=0.24), minimum TMR (F=0.21, df=4, 40, P=0.93) or minimum T _b (F=0.76, df=5, 41, P=0.58). Moreover, sex or reproductive condition did not affect the allometric relationship between minimum resting metabolic rate and body mass (F=1.1, df=4, 37, P=0.37). Our study shows that under identical thermal conditions, thermal physiology of pregnant and lactating female and male bats are indistinguishable. This suggests that the observed reluctance by reproductive females to enter torpor in the field is predominantly because of ecological rather than physiological differences, which reflect the fact that females roost gregariously whereas male bats typically roost solitarily.     

Sexual abstinence and the cost of reproduction in adult male water snakes, Nerodia sipedon

Low frequency of reproduction among iteroparous organisms is most often observed among female ectothermic vertebrates and is thought to be a strategy used to defer reproductive costs. We assessed reproductive costs of male water snakes ( Nerodia sipedon ) to determine why half of adult males abstain from reproduction each year. There was no evidence of a short-term energetic cost of reproduction. Change in mass did not differ between reproductive and non-reproductive males during the one-month mating season or during the entire four-month activity season. Changes in mass of reproductive males were similar at two sites in which the spatial distribution of females differed. However, there were size-specific differences in growth and survival between reproductive and non-reproductive males. Among reproductive males growth rate decreased with body size at a lower rate than among non-reproductive males. Survival increased with body size for reproductive males, but decreased with body size among non-reproductive males. Most of the differential survival between reproductive and non-reproductive males did not occur during the mating season but rather during hibernation. Size-related differences between reproductive and non-reproductive males may reflect selection having eliminated low quality males from the larger size classes. Overall our results appear most consistent with there being high variance in male quality, such that the best males can bear the cost of reproducing and still grow and survive as well or better than low quality males that abstain from reproduction.     

Cool Sex? Hibernation and Reproduction Overlap in the Echidna

During hibernation there is a slowing of all metabolic processes, and thus it is normally considered to be incompatible with reproduction. In Tasmania the egg-laying mammal, the echidna (Tachyglossus aculeatus) hibernates for several months before mating in mid-winter, and in previous studies we observed males with females that were still hibernating. We monitored the reproductive activity of radio-tracked echidnas by swabbing the reproductive tract for sperm while external temperature loggers provided information on the timing of hibernation. Additional information was provided by camera traps and ultrasound imaging. More than a third of the females found in mating groups were torpid, and the majority of these had mated. Some females re-entered deep torpor for extended periods after mating. Ultrasound examination showed a developing egg in the uterus of a female that had repeatedly re-entered torpor. The presence of fresh sperm in cloacal swabs taken from this female on three occasions after her presumed date of fertilization indicated she mated several times after being fertilized. The mating of males with torpid females is the result of extreme competition between promiscuous males, while re-entry into hibernation by pregnant females could improve the possibility of mating with a better quality male.     

Is oxidative stress a physiological cost of reproduction? An experimental test in house mice

Investment in reproduction is costly and frequently decreases survival or future reproductive success. However, the proximate underlying causes for this are largely unknown. Oxidative stress has been suggested as a cost of reproduction and several studies have demonstrated changes in antioxidants with reproductive investment. Here, we test whether oxidative stress is a consequence of reproduction in female house mice (Mus musculus domesticus), which have extremely high energetic demands during reproduction, particularly through lactation. Assessing oxidative damage after a long period of reproductive investment, there was no evidence of increased oxidative stress, even when females were required to defend their breeding territory. Instead, in the liver, markers of oxidative damage (malonaldehyde, protein thiols and the proportion of glutathione in the oxidized form) indicated lower oxidative stress in reproducing females when compared with non-reproductive controls. Even during peak lactation, none of the markers of oxidative damage indicated higher oxidative stress than among non-reproductive females, although a positive correlation between protein oxidation and litter mass suggested that oxidative stress may increase with fecundity. Our results indicate that changes in redox status occur during reproduction in house mice, but suggest that females use mechanisms to cope with the consequences of increased energetic demands and limit oxidative stress.     

Influence of plant maturity, shoot reproduction and sex on vegetative growth in the dioecious plant Urtica dioica

Background and Aims

Stinging nettle (Urtica dioica) is a herbaceous, dioecious perennial that is widely distributed around the world, reproduces both sexually and asexually, and is characterized by rapid growth. This work was aimed at evaluating the effects of plant maturity, shoot reproduction and sex on the growth of leaves and shoots.

Methods

Growth rates of apical shoots, together with foliar levels of phytohormones (cytokinins, auxins, absicisic acid, jasmonic acid and salicylic acid) and other indicators of leaf physiology (water contents, photosynthetic pigments, α-tocopherol and F_v/F_m ratios) were measured in juvenile and mature plants, with a distinction made between reproductive and non-reproductive shoots in both males and females. Vegetative growth rates were not only evaluated in field-grown plants, but also in cuttings obtained from these plants. All measurements were performed during an active vegetative growth phase in autumn, a few months after mature plants reproduced during spring and summer.

Key Results

Vegetative growth rates in mature plants were drastically reduced compared with juvenile ones (48 % and 78 % for number of leaves and leaf biomass produced per day, respectively), which was associated with a loss of photosynthetic pigments (up to 24 % and 48 % for chlorophylls and carotenoids, respectively) and increases of α-tocopherol (up to 2·7-fold), while endogenous levels of phytohormones did not differ between mature and juvenile plants. Reductions in vegetative growth were particularly evident in reproductive shoots of mature plants, and occurred similarly in both males and females.

Conclusions

It is concluded that (a) plant maturity reduces vegetative growth in U. dioica, (b) effects of plant maturity are evident both in reproductive and non-reproductive shoots, but particularly in the former, and (c) these changes occur similarly in both male and female plants.     

Biochemical content, energy composition and reproductive effort in the broadcasting sea star Asterias vulgaris over the spawning period

To assess sex differences in reproductive effort, we examined the biochemical composition and energetic content of the principal body components of the broadcast spawning sea star Asterias vulgaris in the Mingan Islands in the northern Gulf of St. Lawrence, eastern Canada. The body wall was the most stable body component, showing no variations in mass or in lipid and protein content (and total energetic content) between sexes or during spawning. Patterns in the gonads differed between sexes and with spawning. The lipid, protein and carbohydrate content of the ovary dropped during spawning, while only the protein content of the testis decreased significantly. Reproductive effort, expressed as loss of energy in the gonads during spawning for an individual weighing 10 g in underwater mass (8.2 cm in radius), was six times greater in females (49.5 kJ) than males (7.9 kJ). The energetic content of the pyloric caeca also decreased during spawning, by 17.7 kJ in females and 21.5 kJ in males, mainly due to a decrease in lipids. If this decrease is included as reproductive effort, it lessens the gender difference. The caecum decrease possibly represented expenditures due to formation of aggregations or the expulsion of gametes during spawning. Effectively, we observed aggregations during a massive spawning in this population. The sex ratio did not differ from 1:1 in all size classes sampled. This suggests that, unless males suffer higher mortality, females manage to allocate as much energy to somatic growth as males, possibly by feeding at higher rates to compensate for their higher reproductive effort. Stomach protein content tended to be higher in females than males and may indicate greater muscular development to facilitate digestion.     

The effects of shell size and coil orientation on reproduction in female hermit crabs, Clibanarius vittatus

We investigated the effects of shell coil orientation and shell size on reproduction in field populations of the hermit crab, Clibanarius vittatus. Females were collected in the intertidal in Beaufort, NC. Shell parameters were measured and size (cephalothorax length) and reproductive status were determined for 70 females occupying Busycon shells. Crabs were categorized as berried (eggs on the pleopods), mature ovaries, or non-reproductive (no eggs). For berried females, the number of eggs was recorded. By offering a separate group of females access to empty shells, it was possible to calculate optimal shell size and the deficit in shell size for field-collected animals.Females that were berried were in shells closer to the optimal shell size than females with mature ovaries, both for shell weight and shell volume. And females with mature ovaries were in shells that were closer to the optimal size than females that were non-reproductive. For both categories of females without eggs on the pleopods, the majority of females were in shells that were too big (in weight and internal volume). While the percentage of berried females did not differ between dextral (Busycon carica) and sinistral (Busycon sinistrum) shells, the non-reproductive females had a much smaller deficit in volume in sinistral shells compared to dextral shells. For berried females, there was no relationship between the magnitude of their shell deficit and the number of eggs carried. Our results suggest that reproduction is inhibited when females occupy shells sufficiently greater than the optimal shell size.     

Thermal biology, torpor use and activity patterns of a small diurnal marsupial from a tropical desert: sexual differences

Many small desert dasyurids employ torpor almost daily during winter, because cold nights and low food availability impose high energetic costs. However, in Western Australia the arid zone extends into tropical, coastal regions, where winter temperature conditions are far less severe. We studied the thermal biology and activity patterns of free-ranging kaluta (~27 g), a dasyurid restricted to these tropical spinifex deserts, during the Austral winter (June–July) and in addition quantified activity patterns in captivity. Unlike most dasyurids, wild and captive kalutas were almost exclusively diurnal and retreated into underground burrows during the night. Despite being active during the warmer part of the day, kalutas entered torpor daily. However, torpor patterns differed remarkably between males and females. While females spent most of the night torpid at body temperatures (T _b) as low as 21°C, close to soil temperature, males entered multiple short and shallow bouts (T _b > 25°C) during the night. Males also maintained higher T _bs during the early morning when active, occupied larger home ranges and covered greater distances while foraging than females. Hence, males appear to expend more energy than the similar-sized females both while foraging and during the rest phase. We propose that physiological as well as behavioural preparations for the September mating season that culminate in a complete male die-off might already impose energetic costs on males during winter.     

The reproductive and heterosexual behaviours of adult patas monkeys in captivity

The reproductive, agonistic, and social interactions between the adult male and adult females of a patas monkey (Erythrocebus patas) harem were investigated. The occurrence of oestrus appeared to be influenced by both social and hormonal factors. Oestrus was not limited to the peri-ovulatory period, but also occurred at other times within the menstrual cycle and after conception. Mating behaviour was correlated with seasonal decreases in daylength and temperature. The male showed no clear preference for either non-pregnant or pregnant sexual partners. Female dominance rank appeared to have little influence on intrasexual competition for copulations. Of the non-reproductive behaviours studied, only two (female-to-male grooming and heterosexual sitting-close) showed significant fluctuations in frequency with changing female reproductive state. For both behaviours, non-pregnant oestrous females showed the highest frequencies.