What you need is what you eat? Prey selection by the bat Myotis daubentonii

Optimal foraging theory predicts that predators are selective when faced with abundant prey, but become less picky when prey gets sparse. Insectivorous bats in temperate regions are faced with the challenge of building up fat reserves vital for hibernation during a period of decreasing arthropod abundances. According to optimal foraging theory, prehibernating bats should adopt a less selective feeding behaviour – yet empirical studies have revealed many apparently generalized species to be composed of specialist individuals. Targeting the diet of the bat Myotis daubentonii, we used a combination of molecular techniques to test for seasonal changes in prey selectivity and individual‐level variation in prey preferences. DNA metabarcoding was used to characterize both the prey contents of bat droppings and the insect community available as prey. To test for dietary differences among M. daubentonii individuals, we used ten microsatellite loci to assign droppings to individual bats. The comparison between consumed and available prey revealed a preference for certain prey items regardless of availability. Nonbiting midges (Chironomidae) remained the most highly consumed prey at all times, despite a significant increase in the availability of black flies (Simuliidae) towards the end of the season. The bats sampled showed no evidence of individual specialization in dietary preferences. Overall, our approach offers little support for optimal foraging theory. Thus, it shows how novel combinations of genetic markers can be used to test general theory, targeting patterns at both the level of prey communities and individual predators.     

Food availability dictates the timing of parturition in insectivorous mouse-eared bats

Which of these two confounding factors, weather or food availability – that largely correlate and interact – controls the timing of parturition in insectivorous bats? To answer this question, we took advantage of a predator‐prey system that offers a unique opportunity to perform natural experiments. The phenology of reproduction of two sibling bat species that inhabit the same colonial roosts, but exploit different feeding niches, was investigated. Myotis myotis feeds mainly on carabid beetles, a food source available from the end of hibernation onwards, whereas bush crickets, the main prey of M. blythii, are not available early in the season due to their successive instars; cockchafers are actually the sole possible alternative prey for M. blythii at that time of the year, but they occur every third year only, independently of local weather conditions. By comparing the species responses to the presence/absence of cockchafers, we could test the hypothesis that food availability, rather than climate, influences the timing of bat parturition. Our data show that M. blythii gave birth, on average, 10 d later than M. myotis in years without cockchafers, whilst parturition (1) was synchronous during cockchafer years, and (2) did not show much among‐year time variation in M. myotis. This suggests that food availability is the chief factor regulating the timing of parturition in mouse‐eared bats.     

Numerical and Functional Responses of Forest Bats to a Major Insect Pest in Pine Plantations

Global change is expected to modify the frequency and magnitude of defoliating insect outbreaks in forest ecosystems. Bats are increasingly acknowledged as effective biocontrol agents for pest insect populations. However, a better understanding is required of whether and how bat communities contribute to the resilience of forests to man- and climate-driven biotic disturbances. We studied the responses of forest insectivorous bats to a major pine defoliator, the pine processionary moth pityocampa, which is currently expanding its range in response to global warming. We used pheromone traps and ultrasound bat recorders to estimate the abundance and activity of moths and predatory bats along the edge of infested pine stands. We used synthetic pheromone to evaluate the effects of experimentally increased moth availability on bat foraging activity. We also evaluated the top-down regulation of moth population by estimating T. pityocampa larval colonies abundance on the same edges the following winter. We observed a close spatio-temporal matching between emergent moths and foraging bats, with bat activity significantly increasing with moth abundance. The foraging activity of some bat species was significantly higher near pheromone lures, i.e. in areas of expected increased prey availability. Furthermore moth reproductive success significantly decreased with increasing bat activity during the flight period of adult moths. These findings suggest that bats, at least in condition of low prey density, exhibit numerical and functional responses to a specific and abundant prey, which may ultimately result in an effective top-down regulation of the population of the prey. These observations are consistent with bats being useful agents for the biocontrol of insect pest populations in plantation forests.     

Comparison of Brain Transcriptome of the Greater Horseshoe Bats (Rhinolophus ferrumequinum) in Active and Torpid Episodes

Hibernation is an energy-saving strategy which is widely adopted by heterothermic mammals to survive in the harsh environment. The greater horseshoe bat (Rhinolophus ferrumequinum) can hibernate for a long period in the hibernation season. However, the global gene expression changes between hibernation and non-hibernation season in the greater horseshoe bat remain largely unknown. We herein reported a comprehensive survey of differential gene expression in the brain between winter hibernating and summer active greater horseshoe bats using next-generation sequencing technology. A total of 90,314,174 reads were generated and we identified 1,573 differentially expressed genes between active and torpid states. Interestingly, we found that differentially expressed genes are over-represented in some GO categories (such as metabolic suppression, cellular stress responses and oxidative stress), which suggests neuroprotective strategies might play an important role in hibernation control mechanisms. Our results determined to what extent the brain tissue of the greater horseshoe bats differ in gene expression between summer active and winter hibernating states and provided comprehensive insights into the adaptive mechanisms of bat hibernation.     

Growth of horseshoe bats (Chiroptera: Rhinolophidae) in temperate continental conditions and the influence of climate

Growth characteristics of three species of horseshoe bats (Rhinolophus ferrumequinum, R. euryale and R. mehelyi) were studied in northern Bulgaria, and measurements of cohorts born there in different years were compared interannually. Bulgarian horseshoe bats are usually born in the first 3 weeks of June and start to leave the roost at an age of about 3 weeks. Young horseshoe bats of all three species had attained more than 95% of the adult dimensions at the time when they started to regularly leave the cave to forage on their own in mid of July. Individually marked juvenile R. ferrumequinum reached adult dimensions in most external wing measurements in the first half of August. Accordingly the pooled measurements of all juveniles did not differ anymore from those of adult bats in the second half of August. The same pattern was found in R. mehelyi and R. euryale.We found a clear relationship between the climatic conditions prevailing in each year and the final size of individuals born respectively in those years. Whereas previous studies have addressed climatic effects only on several bat species along their northern limits of distribution, these data provide the first evidence for an influence of climate on the growth of individuals in the centre of the species’ distributions.     

Body size as an important factor determining trophic niche partitioning in three syntopic rhinolophid bat species

We investigated a community of syntopically occurring horseshoe bats (Rhinolophus hipposideros, R. euryale, R. ferrumequinum) in southern Slovakia. The faecal pellets of these bat species were collected in the field and later analysed under a dissecting microscope. The three species studied are known to be very similar as far as their ecology, echolocation and preferred habitats are concerned, but they diverge significantly in their body sizes. In this study, all three species fed predominantly on moths [59–80 percentage frequency (%f); 87–95 percentage volume (%vol)], but their diet compositions differed in the size of individuals consumed. The smallest bat species (R. hipposideros) fed only on the smallest moths (%f = 59; %vol = 87), the medium-sized species (R. euryale) mainly on medium-sized moths (%f = 60; %vol = 74) and the largest one (R. ferrumequinum) especially on the largest moths (%f = 54; %vol = 89). Despite similar preferred habitat and the main prey category, the rates of trophic niche overlap were surprisingly low. The trophic niche percentage overlap was 7–31% (computed from %f data) and 1–20% (computed from %vol data), respectively and suggests an extraordinary importance of mere divergences of bats in their body sizes for trophic niche partitioning and stable species coexistence.     

Insectivorous bats selectively source moths and eat mostly pest insects on dryland and irrigated cotton farms

Insectivorous bats are efficient predators of pest arthropods in agroecosystems. This pest control service has been estimated to be worth billions of dollars to agriculture globally. However, few studies have explicitly investigated the composition and abundance of dietary prey items consumed or assessed the ratio of pest and beneficial arthropods, making it difficult to evaluate the quality of the pest control service provided. In this study, we used metabarcoding to identify the prey items eaten by insectivorous bats over the cotton‐growing season in an intensive cropping region in northern New South Wales, Australia. We found that seven species of insectivorous bat (n = 58) consumed 728 prey species, 13 of which represented around 50% of total prey abundance consumed. Importantly, the identified prey items included major arthropod pests, comprising 65% of prey relative abundance and 13% of prey species recorded. Significant cotton pests such as Helicoverpa punctigera (Australian bollworm) and Achyra affinitalis (cotton webspinner) were detected in at least 76% of bat fecal samples, with Teleogryllus oceanicus (field crickets), Helicoverpa armigera (cotton bollworm), and Crocidosema plebejana (cotton tipworm) detected in 55% of bat fecal samples. Our results indicate that insectivorous bats are selective predators that exploit a narrow selection of preferred pest taxa and potentially play an important role in controlling lepidopteran pests on cotton farms. Our study provides crucial information for farmers to determine the service or disservice provided by insectivorous bats in relation to crops, for on‐farm decision making.     

Mosquito Consumption by Insectivorous Bats: Does Size Matter?

Insectivorous bats have often been touted as biological control for mosquito populations. However, mosquitoes generally represent only a small proportion of bat diet. Given the small size of mosquitoes, restrictions imposed on prey detectability by low frequency echolocation, and variable field metabolic rates (FMR), mosquitoes may not be available to or profitable for all bats. This study investigated whether consumption of mosquitoes was influenced by bat size, which is negatively correlated with echolocation frequency but positively correlated with bat FMR. To assess this, we investigated diets of five eastern Australian bat species (Vespadelus vulturnus Thomas, V. pumilus Gray, Miniopterus australis Tomes, Nyctophilus gouldi Tomes and Chalinolobus gouldii Gray) ranging in size from 4-14 g in coastal forest, using molecular analysis of fecal DNA. Abundances of potential mosquito and non-mosquito prey were concurrently measured to provide data on relative prey abundance. Aedes vigilax was locally the most abundant mosquito species, while Lepidoptera the most abundant insect order. A diverse range of prey was detected in bat feces, although members of Lepidoptera dominated, reflecting relative abundance at trap sites. Consumption of mosquitoes was restricted to V. vulturnus and V. pumilus, two smaller sized bats (4 and 4.5 g). Although mosquitoes were not commonly detected in feces of V. pumilus, they were present in feces of 55 % of V. vulturnus individuals. To meet nightly FMR requirements, Vespadelus spp. would need to consume ~600-660 mosquitoes on a mosquito-only diet, or ~160-180 similar sized moths on a moth-only diet. Lower relative profitability of mosquitoes may provide an explanation for the low level of mosquito consumption among these bats and the absence of mosquitoes in feces of larger bats. Smaller sized bats, especially V. vulturnus, are likely to be those most sensitive to reductions in mosquito abundance and should be monitored during mosquito control activities.     

Host and pathogen ecology drive the seasonal dynamics of a fungal disease,white-nose syndrome

Seasonal patterns in pathogen transmission can influence the impact of disease on populations and the speed of spatial spread. Increases in host contact rates or births drive seasonal epidemics in some systems, but other factors may occasionally override these influences. White-nose syndrome, caused by the emerging fungal pathogen Pseudogymnoascus destructans, is spreading across North America and threatens several bat species with extinction. We examined patterns and drivers of seasonal transmission of P. destructans by measuring infection prevalence and pathogen loads in six bat species at 30 sites across the eastern United States. Bats became transiently infected in autumn, and transmission spiked in early winter when bats began hibernating. Nearly all bats in six species became infected by late winter when infection intensity peaked. In summer, despite high contact rates and a birth pulse, most bats cleared infections and prevalence dropped to zero. These data suggest the dominant driver of seasonal transmission dynamics was a change in host physiology, specifically hibernation. Our study is the first, to the best of our knowledge, to describe the seasonality of transmission in this emerging wildlife disease. The timing of infection and fungal growth resulted in maximal population impacts, but only moderate rates of spatial spread.     

Activity following arousal in winter in North American vespertilionid bats

• 1 Many bat species hibernate to conserve energy during winter and like all hibernators they commonly arouse. During these arousals, some bats may undertake activities away from the hibernation site. Systematic ecological studies of the frequency and purpose of winter activity in temperate zone bats of North America are rare and much of the literature involves observations of single individuals or unmarked populations.
• 2 We review the available literature on winter activity among North American vespertilionid bats to highlight the paucity of data on this subject and to stimulate future research. Due to the lack of repeated, systematic studies on most North American species, the conclusions drawn are general or pertain only to parts of the geographical range of any species.
• 3 We suggest that winter activity is ubiquitous among temperate zone bats, but the degree and purpose of activity varies greatly between and within species. In general, cave‐dwelling bats tend to be relatively inactive compared with tree and foliage roosting bats during winter.
• 4 Cave‐dwelling and tree cavity‐dwelling species do not appear to feed, but they do drink and occasionally copulate during the hibernation period. Species that hibernate in foliage or leaf litter are the most active species during winter and may feed and drink throughout winter, although they probably do not copulate because of their solitary nature.
• 5 We encourage researchers to conduct studies on all aspects of winter activity for North American vespertilionids across wide latitudinal and altitudinal gradients. We suggest studies in the near future be focused on estimating the energetic costs and benefits of winter activity through determination of the frequency and intensity of winter feeding activity and more thorough examinations of movements within and among caves. Studies on common, wide‐ranging species have the potential to illuminate large‐scale patterns and differences and should be favoured over studies on rarer species.

     

Molecular identification of Eimeria species in Spanish bats

This is the first study reporting the detection and molecular characterization of Eimeria in bats in Spain, specifically in 12 of 32 chiropteran species described in the Iberian Peninsula. A total of 76 faecal samples were collected from different bat roosting sites across Spanish territory. The DNA was extracted from the samples and sequenced by targeting the Eimeria SSU-rRNA gene. Two Eimeria species were detected in 29 of the 76 faecal samples (38%), and the bat-specific Eimeria rioarribaensis and rodent-specific Eimeria jerfinica were detected in 4 (5%) and 25 (33%) of the samples, respectively. This is the first report of E. rioarribaensis in the bats Rhinolophus euryale, Myotis myotis and Nyctalus lasiopterus, extending the host and geographical ranges for this bat coccidian parasite. The identification of the rodent-specific parasite species E. jerfinica in bats indicates the occurrence of this species in Spain, although its presence has not previously been reported in wild rodents in this country. Considering that most of the Eimeria spp. reported in bats were described only on the basis of morphometric data, molecular studies are required to determined which Eimeria species occur in bats, to complete the identification of these species and to clarify the phylogeny.     

Assessing niche partitioning of co‐occurring sibling bat species by DNA metabarcoding

Niche partitioning through foraging is a mechanism likely involved in facilitating the coexistence of ecologically similar and co‐occurring animal species by separating their use of resources. Yet, this mechanism is not well understood in flying insectivorous animals. This is particularly true of bats, where many ecologically similar or cryptic species coexist. The detailed analysis of the foraging niche in sympatric, cryptic sibling species provides an excellent framework to disentangle the role of specific niche factors likely involved in facilitating coexistence. We used DNA metabarcoding to determine the prey species consumed by a population of sympatric sibling Rhinolophus euryale and Rhinolophus mehelyi whose use of habitat in both sympatric and allopatric ranges has been well established through radio tracking. Although some subtle dietary differences exist in prey species composition, the diet of both bats greatly overlapped (O_jk = 0.83) due to the consumption of the same common and widespread moths. Those dietary differences we did detect might be related to divergences in prey availabilities among foraging habitats, which prior radio tracking on the same population showed are differentially used and selected when both species co‐occur. This minor dietary segregation in sympatry may be the result of foraging on the same prey‐types and could contribute to reduce potential competitive interactions (e.g., for prey, acoustic space). Our results highlight the need to evaluate the spatial niche dimension in mediating the co‐occurrence of similar insectivorous bat species, a niche factor likely involved in processes of bat species coexistence.     

Staying cold through dinner: cold-climate bats rewarm with conspecifics but not sunset during hibernation

For temperate endotherms (i.e., mammals and birds) energy costs are highest during winter but food availability is lowest and many mammals depend on hibernation as a result. Hibernation is made up of energy-saving torpor bouts [periods of controlled reduction in body temperature (T _b)], which are interrupted by brief periodic arousals to normothermic T _b. What triggers these arousals in free-ranging hibernators is not well understood. Some temperate bats with intermittent access to flying insects during winter synchronize arousals with sunset, which suggests that, in some species, feeding opportunities influence arousal timing. We tested whether hibernating bats from a cold climate without access to food during winter also maintain a circadian rhythm for arousals or whether cues from conspecifics in the same cluster are more important. We used temperature telemetry to monitor skin temperature (T _sk) of free-ranging little brown bats (Myotis lucifugus) hibernating in central Manitoba, Canada, where temperatures from 22 October to 22 March were too cold for flying insects. We found no evidence bats synchronized arousals with photoperiod but they did arouse synchronously with other bats in the same cluster. Thus, in the northern part of their range where flying insects are almost never available during winter, little brown bats exhibit no circadian pattern to arousals. Warming synchronously with others could reduce the energetic costs of arousal for individuals or could reflect disturbance of torpid bats by cluster-mates.     

Seasonal Shifts in Nocturnal Habitat Use by Coastal Bat Species

Sensitivity of bats to land use change depends on their foraging ecology, which varies among species based on ecomorphological traits. Additionally, because prey availability, vegetative clutter, and temperature change throughout the year, some species may display seasonal shifts in their nocturnal habitat use. In the Coastal Plain of South Carolina, USA, the northern long-eared bat (Myotis septentrionalis), southeastern myotis (Myotis austroriparius), tri-colored bat (Perimyotis subflavus), and northern yellow bat (Lasiurus intermedius) are species of conservation concern that are threatened by habitat loss. Our objective was to identify characteristics of habitat used by these species during their nightly active period and compare use between summer and winter. We conducted acoustic surveys at 125 sites during May–August and at 121 of the same 125 sites December–March 2018 and 2019 in upland forests, bottomland forests, fields, ponds, and salt marsh and used occupancy models to assess habitat use. The northern long-eared bat and southeastern myotis (i.e., myotis bats) used sites that were closer to hardwood stands, pine stands, and fresh water year-round. We did not identify any strong predictors of tri-colored bat habitat use in summer, but during winter they used bottomland forests, fields, and ponds more than salt marsh and upland forests. During summer and winter, northern yellow bats used sites close to fresh water and salt marsh. Additionally, during summer they used fields, ponds, and salt marsh more than upland and bottomland forests, but in winter they used bottomland forests, fields, and ponds more than upland forest and salt marsh. Our results highlight important land cover types for bats in this area (e.g., bottomland forests, ponds, and salt marsh), and that habitat use changes between seasons. Accounting for and understanding how habitat use changes throughout the year will inform managers about how critical habitat features may vary in their importance to bats throughout the year. © 2021 The Wildlife Society.     

Seasonal reliance on nectar by an insectivorous bat revealed by stable isotopes

Many animals have seasonally plastic diets to take advantage of seasonally abundant plant resources, such as fruit or nectar. Switches from insectivorous diets that are protein rich to fruits or nectar that are carbohydrate rich present physiological challenges, but are routinely done by insectivorous songbirds during migration. In contrast, insectivorous bat species are not known to switch diets to consume fruit or nectar. Here, we use carbon stable isotope ratios to establish the first known case of a temperate bat species consuming substantial quantities of nectar during spring. We show that pallid bats (Antrozous pallidus) switch from a diet indistinguishable from that of sympatric insectivorous bat species in winter (when no cactus nectar is present) to a diet intermediate between those of insectivorous bats and nectarivorous bats during the spring bloom of a bat-adapted cactus species. Combined with previous results that established that pallid bats are effective pollinators of the cardon cactus (Pachycereus pringlei), our results suggest that the interaction between pallid bats and cardon cacti represents the first-known plant-pollinator mutualism between a plant and a temperate bat. Diet plasticity in pallid bats raises questions about the degree of physiological adaptations of insectivorous bats for incorporation of carbohydrate-rich foods, such as nectar or fruit, into the diet.     

Seasonal variation in food availability and relative importance of dietary items in the Gambian epauletted fruit bat (Epomophorus gambianus)

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Antioxidant Defenses in the Brains of Bats during Hibernation

Hibernation is a strategy used by some mammals to survive a cold winter. Small hibernating mammals, such as squirrels and hamsters, use species- and tissue-specific antioxidant defenses to cope with oxidative insults during hibernation. Little is known about antioxidant responses and their regulatory mechanisms in hibernating bats. We found that the total level of reactive oxygen species (ROS) and reactive nitrogen species (RNS) in the brain of each of the two distantly related hibernating bats M. ricketti and R. ferrumequinum at arousal was lower than that at torpid or active state. We also found that the levels of malondialdehyde (product of lipid peroxidation) of the two hibernating species of bats were significantly lower than those of non-hibernating bats R. leschenaultia and C. sphinx. This observation suggests that bats maintain a basal level of ROS/RNS that does no harm to the brain during hibernation. Results of Western blotting showed that hibernating bats expressed higher amounts of antioxidant proteins than non-hibernating bats and that M. ricketti bats upregulated the expression of some enzymes to overcome oxidative stresses, such as superoxide dismutase, glutathione reductase, and catalase. In contrast, R. ferrumequinum bats maintained a relatively high level of superoxide dismutase 2, glutathione reductase, and thioredoxin-2 throughout the three different states of hibernation cycles. The levels of glutathione (GSH) were higher in M. ricketti bats than in R. ferrumequinum bats and were significantly elevated in R. ferrumequinum bats after torpor. These data suggest that M. ricketti bats use mainly antioxidant enzymes and R. ferrumequinum bats rely on both enzymes and low molecular weight antioxidants (e.g., glutathione) to avoid oxidative stresses during arousal. Furthermore, Nrf2 and FOXOs play major roles in the regulation of antioxidant defenses in the brains of bats during hibernation. Our study revealed strategies used by bats against oxidative insults during hibernation.     

Subtropical mouse-tailed bats use geothermally heated caves for winter hibernation

We report that two species of mouse-tailed bats (Rhinopoma microphyllum and R. cystops) hibernate for five months during winter in geothermally heated caves with stable high temperature (20°C). While hibernating, these bats do not feed or drink, even on warm nights when other bat species are active. We used thermo-sensitive transmitters to measure the bats’ skin temperature in the natural hibernacula and open flow respirometry to measure torpid metabolic rate at different ambient temperatures (T_a, 16–35°C) and evaporative water loss (EWL) in the laboratory. Bats average skin temperature at the natural hibernacula was 21.7 ± 0.8°C, and no arousals were recorded. Both species reached the lowest metabolic rates around natural hibernacula temperatures (20°C, average of 0.14 ± 0.01 and 0.16 ± 0.04 ml O₂ g⁻¹ h⁻¹ for R. microphyllum and R. cystops, respectively) and aroused from torpor when T_a fell below 16°C. During torpor the bats performed long apnoeas (14 ± 1.6 and 16 ± 1.5 min, respectively) and had a very low EWL. We hypothesize that the particular diet of these bats is an adaptation to hibernation at high temperatures and that caves featuring high temperature and humidity during winter enable these species to survive this season on the northern edge of their world distribution.     

The distribution of the Greater horse-shoe bat, Rhinolophus ferrum-equinum, during hibernation, in relation to environmental factors

Hibernation is a vital factor in the ability of bats to survive in temperate countries where insect availability is drastically reduced in winter. The value of hibernation in survival lies in the reduction of the bat's metabolic rate to very low levels, thus reducing their food requirements.
The selection of a site which fulfils the physiological requirements of hibernation must be important in the survival of the Greater horse-shoe bat. The present study shows that temperature is particularly important in the selection of a precise position for hibernation. The temperature required, however, varies throughout the winter.
In England this bat finds suitable conditions in caves, mines, tunnels, cellars, and house attics. All are dark where the bats are found and offer protection from predators. These considerations are not sufficient to explain the distribution of this bat in hibernation.
The present study shows that a large proportion of the population feeds outside the hibernaculum at times during the hibernation period. The evidence suggests that starvation is a cause of death. Hence it is not only the conditions inside the hibernacula which are important in the winter survival of a bat population. The environmental conditions outside may be just as vital.
The Greater horse-shoe bat is vulnerable since the bulk of its population depends upon relatively few sites. Its reproductive rate is very low and active conservation is needed in England, since populations are small. If conservation is to be successful however, both the physical conditions within hibernacula, and the environmental conditions outside will have to be satisfactory.