Continuous low-intensity predation by owls (Strix aluco) on bats (Nyctalus lasiopterus) in Spain and the potential effect on bat colony stability.

Owls prey on bats, but information on owl predation is scarce, its impact on bat mortality is unclear, and reports on behavioural responses, including roost-switching and fission-fusion behaviour, are equivocal. To study the link between owl predation and anti-predator behaviour in bats, we evaluated seven months of video recordings at roosts and the behaviour of 51 passive integrated transponder (PIT)-tagged bats and bats without tags in a geographically isolated colony of greater noctule bats (Nyctalus lasiopterus) in Spain. We found the tawny owl Strix aluco to almost continuously hunt N. lasiopterus, from perches and on the wing, well after the bats emerged at dusk and when they returned to their roosts. We recorded 39 unsuccessful and three successful attacks. Nonetheless, we found no evidence that owl predation modifies bat behaviour. While the bats constituted only a very small proportion of the owls' diet, owl predation accounted for an estimated 30-40% of bat mortality, which may have a significant impact on small, local or isolated bat populations, in particular, and thereby shape regional bat distributions. We hypothesize that low roost availability may also affect the bats' potential response to predation, which could lead to natural predation having an excessive impact on bat populations.

Identifying migratory pathways of Nathusius' pipistrelles (Pipistrellus nathusii) using stable hydrogen and strontium isotopes.

RATIONALE: Identifying migratory corridors of animals is essential for their effective protection, yet the exact location of such corridors is often unknown, particularly for elusive animals such as bats. While migrating along the German coastline, Nathusius' pipistrelles (Pipistrellus nathusii) are regularly killed at wind turbines. Therefore, we explored the paths taken on their annual journey. METHODS: We used isotope ratio mass spectrometry to measure stable hydrogen and strontium isotope ratios in fur keratin of 59 Nathusius' pipistrelles captured on three offshore islands. Samples were pre-treated before analysis to report exclusively stable isotope ratios of non-exchangeable hydrogen. We generated maps to predict summer origins of bats using isoscape models. RESULTS: Bats were classified as long-distance migrants, mostly originating from Eastern Europe. Hydrogen analysis suggested for some bats a possible Fennoscandian origin, yet additional information from strontium analysis excluded this possibility. Instead, our data suggest that most Nathusius' pipistrelles migrating along the German coastline were of continental European summer origin, but also highlight the possibility that Nathusius' pipistrelles of Baltorussian origin may travel offshore from Fennoscandia to Germany. CONCLUSIONS: Our findings demonstrate the benefit of using complementary isotopic tracers for analysing the migratory pathways of bats and also potentially other terrestrial vertebrate species. Furthermore, data from our study suggest an offset of fur strontium isotope ratios in relation to local bedrock.

Dispersal and group formation dynamics in a rare and endangered temperate forest bat (Nyctalus lasiopterus, Chiroptera: Vespertilionidae).

For elusive mammals like bats, colonization of new areas and colony formation are poorly understood, as is their relationship with the genetic structure of populations. Understanding dispersal and group formation behaviors is critical not only for a better comprehension of mammalian social dynamics, but also for guiding conservation efforts of rare and endangered species. Using nuclear and mitochondrial markers, we studied patterns of genetic diversity and differentiation among and within breeding colonies of giant noctule bats (Nyctalus lasiopterus), their relation to a new colony still in formation, and the impact of this ongoing process on the regionwide genetic makeup. Nuclear differentiation among colonies was relatively low and mostly nonsignificant. Mitochondrial variation followed this pattern, contrasting with findings for other temperate bat species. Our results suggest that this may indicate a recent population expansion. On average, female giant noctules were not more closely related to other colony members than to foreign individuals. This was also true for members of the newly forming colony and those of another, older group sampled shortly after its formation, suggesting that contrary to findings for other temperate bats, giant noctule colonies are not founded by relatives. However, mother-daughter pairs were found in the same populations more often than expected under random dispersal. Given this indication of philopatry, the lack of mitochondrial differentiation among most colonies in the region is probably due to the combination of a recent population expansion and group formation events.

Concealed by darkness: interactions between predatory bats and nocturnally migrating songbirds illuminated by DNA sequencing.

Recently, several species of aerial-hawking bats have been found to prey on migrating songbirds, but details on this behaviour and its relevance for bird migration are still unclear. We sequenced avian DNA in feather-containing scats of the bird-feeding bat Nyctalus lasiopterus from Spain collected during bird migration seasons. We found very high prey diversity, with 31 bird species from eight families of Passeriformes, almost all of which were nocturnally flying sub-Saharan migrants. Moreover, species using tree hollows or nest boxes in the study area during migration periods were not present in the bats' diet, indicating that birds are solely captured on the wing during night-time passage. Additional to a generalist feeding strategy, we found that bats selected medium-sized bird species, thereby assumingly optimizing their energetic cost-benefit balance and injury risk. Surprisingly, bats preyed upon birds half their own body mass. This shows that the 5% prey to predator body mass ratio traditionally assumed for aerial hunting bats does not apply to this hunting strategy or even underestimates these animals' behavioural and mechanical abilities. Considering the bats' generalist feeding strategy and their large prey size range, we suggest that nocturnal bat predation may have influenced the evolution of bird migration strategies and behaviour.

Non-invasive monitoring of stress hormones in the bat Eptesicus isabellinus - Do fecal glucocorticoid metabolite concentrations correlate with survival?

Chronic stress may negatively impact fitness and survival in wildlife. Stress hormone analysis from feces is a non-invasive tool for identifying stressors and deducing about individual and population level fitness. Although many bat populations are endangered, fecal stress hormone analysis has not been established in bats as a method for focusing conservation efforts. The isabelline serotine bat, Eptesicus isabellinus, is exposed to human disturbance as its roosts are mostly found in anthropogenic structures. Moreover, this bat is host to various diseases and survival rates between colonies may vary significantly. To validate the analysis of fecal glucocorticoid metabolites, we applied an adrenocorticotropic hormone (ACTH) challenge and tested four different enzyme immunoassays (EIA) for measuring glucocorticoid concentrations. Cortisol and its metabolites showed the highest increase in blood and feces after the ACTH challenge, but corticosterone and its metabolites also increased significantly. Baseline fecal cortisol metabolite (FCM) concentrations did not increase until 1.5h after the animals were captured, which is a convenient time lag for sample collection from captured animals. We furthermore compared baseline FCM concentrations between five colonies of E. isabellinus in Andalusia, Spain, and tested for their correlation with survival rates. FCM concentrations did not vary between colonies, but FCM levels increased with the animals' age. FCM analysis may prove a useful tool for identifying bat colonies that experience uncommon environmental stress. However, inter-individual variation in hormone secretion, due to factors such as age, may require additional information to properly interpret differences in hormone concentrations.

Seasonal variation in stable carbon and nitrogen isotope values of bats reflect environmental baselines.

The stable carbon and nitrogen isotope composition of animal tissues is commonly used to trace wildlife diets and analyze food chains. Changes in an animal's isotopic values over time are generally assumed to indicate diet shifts or, less frequently, physiological changes. Although plant isotopic values are known to correlate with climatic seasonality, only a few studies restricted to aquatic environments have investigated whether temporal isotopic variation in consumers may also reflect environmental baselines through trophic propagation. We modeled the monthly variation in carbon and nitrogen isotope values in whole blood of four insectivorous bat species occupying different foraging niches in southern Spain. We found a common pattern of isotopic variation independent of feeding habits, with an overall change as large as or larger than one trophic step. Physiological changes related to reproduction or to fat deposition prior to hibernation had no effect on isotopic variation, but juvenile bats had higher δ13C and δ15N values than adults. Aridity was the factor that best explained isotopic variation: bat blood became enriched in both 13C and 15N after hotter and/or drier periods. Our study is the first to show that consumers in terrestrial ecosystems reflect seasonal environmental dynamics in their isotope values. We highlight the danger of misinterpreting stable isotope data when not accounting for seasonal isotopic baselines in food web studies. Understanding how environmental seasonality is integrated in animals' isotope values will be crucial for developing reliable methods to use stable isotopes as dietary tracers.

Crowding in the city: losing and winning competitors of an invasive bird.

Invasive species can take advantage of resources unexploited by natives (opportunism hypothesis) or they can exploit the same resources but more aggressively or efficiently (competition hypothesis), thus impacting native species. However, invasive species tend to exploit anthropogenic habitats that are inefficiently used by natives such as urban environments. Focusing on the ring-necked parakeet (Psittacula krameri), one of the most invasive birds worldwide, we combined observations of interspecific aggressions, species-specific cavity-nest preferences and the spatial distribution of the native cavity-nesting vertebrate community to determine the invasion process as well as its potential impacts on native species in a Mediterranean city. Our results support the competition hypothesis, suggesting that ring-necked parakeets are outcompeting native species sharing nest-site preferences. Parakeets initiated and won most interspecific aggressions, which were directed towards competitors but also towards predators. This behaviour could explain the spatial arrangement of natives, with most bird species breeding close to parakeets possibly to take advantage of their effective antipredatory behaviour. However, temporal and spatial patterns of segregation suggest that a threatened bat species is negatively affected by parakeets. This demonstrates that common species gain benefits and threatened ones (in this study, a bat and possibly a falcon) lose nest sites due to invaders. Therefore, the conservation status of the native species that pay the costs of competition with invaders should be considered. This scenario of winners and losers may, however, shift towards more losers if the ring-necked parakeet population continues to grow, thus requiring close monitoring and control/eradication programs to avoid further impacts.

A triple-isotope approach to predict the breeding origins of European bats.

Despite a commitment by the European Union to protect its migratory bat populations, conservation efforts are hindered by a poor understanding of bat migratory strategies and connectivity between breeding and wintering grounds. Traditional methods like mark-recapture are ineffective to study broad-scale bat migratory patterns. Stable hydrogen isotopes (δD) have been proven useful in establishing spatial migratory connectivity of animal populations. Before applying this tool, the method was calibrated using bat samples of known origin. Here we established the potential of δD as a robust geographical tracer of breeding origins of European bats by measuring δD in hair of five sedentary bat species from 45 locations throughout Europe. The δD of bat hair strongly correlated with well-established spatial isotopic patterns in mean annual precipitation in Europe, and therefore was highly correlated with latitude. We calculated a linear mixed-effects model, with species as random effect, linking δD of bat hair to precipitation δD of the areas of hair growth. This model can be used to predict breeding origins of European migrating bats. We used δ(13)C and δ(15)N to discriminate among potential origins of bats, and found that these isotopes can be used as variables to further refine origin predictions. A triple-isotope approach could thereby pinpoint populations or subpopulations that have distinct origins. Our results further corroborated stable isotope analysis as a powerful method to delineate animal migrations in Europe.

The roosting spatial network of a bird-predator bat.

The use of roosting sites by animal societies is important in conservation biology, animal behavior, and epidemiology. The giant noctule bat (Nyctalus lasiopterus) constitutes fission-fusion societies whose members spread every day in multiple trees for shelter. To assess how the pattern of roosting use determines the potential for information exchange or disease spreading, we applied the framework of complex networks. We found a social and spatial segregation of the population in well-defined modules or compartments, formed by groups of bats sharing the same trees. Inside each module, we revealed an asymmetric use of trees by bats representative of a nested pattern. By applying a simple epidemiological model, we show that there is a strong correlation between network structure and the rate and shape of infection dynamics. This modular structure slows down the spread of diseases and the exchange of information through the entire network. The implication for management is complex, affecting differently the cohesion inside and among colonies and the transmission of parasites and diseases. Network analysis can hence be applied to quantifying the conservation status of individual trees used by species depending on hollows for shelter.

Bats' conquest of a formidable foraging niche: the myriads of nocturnally migrating songbirds.

Along food chains, i.e., at different trophic levels, the most abundant taxa often represent exceptional food reservoirs, and are hence the main target of consumers and predators. The capacity of an individual consumer to opportunistically switch towards an abundant food source, for instance, a prey that suddenly becomes available in its environment, may offer such strong selective advantages that ecological innovations may appear and spread rapidly. New predator-prey relationships are likely to evolve even faster when a diet switch involves the exploitation of an unsaturated resource for which few or no other species compete. Using stable isotopes of carbon and nitrogen as dietary tracers, we provide here strong support to the controversial hypothesis that the giant noctule bat Nyctalus lasiopterus feeds on the wing upon the multitude of flying passerines during their nocturnal migratory journeys, a resource which, while showing a predictable distribution in space and time, is only seasonally available. So far, no predator had been reported to exploit this extraordinarily diverse and abundant food reservoir represented by nocturnally migrating passerines.