Artificially raised roost temperatures lead to larger body sizes in wild bats.

Climate warming has major consequences for animal populations, as ambient temperature profoundly influences all organisms' physiology, behavior, or both.1 Body size in many organisms has been found to change with increased ambient temperatures due to influences on metabolism and/or access to resources.2,3,4,5,6 Changes in body size, in turn, can affect the dynamics and persistence of populations.7 Notably, in some species, body size has increased over the last decades in response to warmer temperatures.3,8 This has primarily been attributed to higher food availability,3 but might also result from metabolic savings in warmer environments.9,10 Bechstein's bats (Myotis bechsteinii) grow to larger body sizes in warmer summers,11 which affects their demography as larger females reproduce earlier at the expense of a shorter life expectancy.12,13 However, it remains unclear whether larger body sizes in warmer summers were due to thermoregulatory benefits or due to increased food availability. To disentangle these effects, we artificially heated communal day roosts of wild maternity colonies over four reproductive seasons. We used generalized mixed models to analyze these experimental results along with 25 years of long-term data comprising a total of 741 juveniles. We found that individuals raised in heated roosts grew significantly larger than those raised in unheated conditions. This suggests that metabolic savings in warmer conditions lead to increased body size, potentially resulting in the decoupling of body growth from prey availability. Our study highlights a direct mechanism by which climate change may alter fitness-relevant traits, with potentially dire consequences for population persistence.

Heat over heritability: Increasing body size in response to global warming is not stabilized by genetic effects in Bechstein's bats.

How well populations can cope with global warming will often depend on the evolutionary potential and plasticity of their temperature-sensitive, fitness-relevant traits. In Bechstein's bats (Myotis bechsteinii), body size has increased over the last decades in response to warmer summers. If this trend continues it may threaten populations as larger females exhibit higher mortality. To assess the evolutionary potential of body size, we applied a Bayesian 'animal model' to estimate additive genetic variance, heritability and evolvability of body size, based on a 25-year pedigree of 332 wild females. Both heritability and additive genetic variance were reduced in hot summers compared to average and cold summers, while evolvability of body size was generally low. This suggests that the observed increase in body size was mostly driven by phenotypic plasticity. Thus, if warm summers continue to become more frequent, body size likely increases further and the resulting fitness loss could threaten populations.

Long-term field study reveals that warmer summers lead to larger and longer-lived females only in northern populations of Natterer's bats.

Animals often respond to climate change with changes in morphology, e.g., shrinking body size with increasing temperatures, as expected by Bergmann's rule. Because small body size can have fitness costs for individuals, this trend could threaten populations. Recent studies, however, show that morphological responses to climate change and the resulting fitness consequences cannot be generalized even among related species. In this long-term study, we investigate the interaction between ambient temperature, body size and survival probability in a large number of individually marked wild adult female Natterer's bats (Myotis nattereri). We compare populations from two geographical regions in Germany with a different climate. In a sliding window analysis, we found larger body sizes in adult females that were raised in warmer summers only in the northern population, but not in the southern population that experienced an overall warmer climate. With a capture-mark-recapture approach, we showed that larger individuals had higher survival rates, demonstrating that weather conditions in early life could have long-lasting fitness effects. The different responses in body size to warmer temperatures in the two regions highlight that fitness-relevant morphological responses to climate change have to be viewed on a regional scale and may affect local populations differently.

Global warming leads to larger bats with a faster life history pace in the long-lived Bechstein's bat (Myotis bechsteinii).

Whether species can cope with environmental change depends considerably on their life history. Bats have long lifespans and low reproductive rates which make them vulnerable to environmental changes. Global warming causes Bechstein's bats (Myotis bechsteinii) to produce larger females that face a higher mortality risk. Here, we test whether these larger females are able to offset their elevated mortality risk by adopting a faster life history. We analysed an individual-based 25-year dataset from 331 RFID-tagged wild bats and combine genetic pedigrees with data on survival, reproduction and body size. We find that size-dependent fecundity and age at first reproduction drive the observed increase in mortality. Because larger females have an earlier onset of reproduction and shorter generation times, lifetime reproductive success remains remarkably stable across individuals with different body sizes. Our study demonstrates a rapid shift to a faster pace of life in a mammal with a slow life history.

Long-term field studies in bat research: importance for basic and applied research questions in animal behavior.

Animal species differ considerably in longevity. Among mammals, short-lived species such as shrews have a maximum lifespan of about a year, whereas long-lived species such as whales can live for more than two centuries. Because of their slow pace of life, long-lived species are typically of high conservation concern and of special scientific interest. This applies not only to large mammals such as whales, but also to small-sized bats and mole-rats. To understand the typically complex social behavior of long-lived mammals and protect their threatened populations, field studies that cover substantial parts of a species' maximum lifespan are required. However, long-term field studies on mammals are an exception because the collection of individualized data requires considerable resources over long time periods in species where individuals can live for decades. Field studies that span decades do not fit well in the current career and funding regime in science. This is unfortunate, as the existing long-term studies on mammals yielded exciting insights into animal behavior and contributed data important for protecting their populations. Here, I present results of long-term field studies on the behavior, demography, and life history of bats, with a particular focus on my long-term studies on wild Bechstein's bats. I show that long-term studies on individually marked populations are invaluable to understand the social system of bats, investigate the causes and consequences of their extraordinary longevity, and assess their responses to changing environments with the aim to efficiently protect these unique mammals in the face of anthropogenic global change.

Data-driven modelling of group formation in the fission-fusion dynamics of Bechstein's bats.

Communal roosting in Bechstein's bat colonies is characterized by the formation of several groups that use different day roosts and that regularly dissolve and re-merge (fission-fusion dynamics). Analysing data from two colonies of different sizes over many years, we find that (i) the number of days that bats stay in the same roost before changing follows an exponential distribution that is independent of the colony size and (ii) the number and size of groups that bats formed for roosting depend on the size of the colony, such that above a critical colony size two to six groups of different sizes are formed. To model these two observations, we propose an agent-based model in which agents make their decisions about roosts based on both random and social influences. For the latter, they copy the roost preference of another agent which models the transfer of the respective information. Our model is able to reproduce both the distribution of stay length in the same roost and the emergence of groups of different sizes dependent on the colony size. Moreover, we are able to predict the critical system size at which the formation of different groups emerges without global coordination. We further comment on dynamics that bridge the roosting decisions on short time scales (less than 1 day) with the social structures observed at long time scales (more than 1 year).

Precipitation during two weeks in spring influences reproductive success of first-year females in the long-lived Natterer's bat.

Bats are characterized by low reproductive rates in contrast with most of other small mammals. This makes their populations vulnerable when inclement environmental conditions such as cold and rainy weather impair the reproductive success of females. The fine-scale effect of weather on bats, however, remains largely unknown. Using a sliding window analysis approach on an 18-year individualized dataset on six Natterer's bat (Myotis nattereri) colonies, we investigated the effect of fine-scale weather conditions on age-specific reproductive success. We found that increased precipitation during a short time window in spring strongly reduced the probability of successful reproduction of first-year (FY) females. Our data suggest that this time window is concomitant with implantation or early pregnancy, before substantial investment into embryo development. In addition, larger FY had higher reproductive success, suggesting that reproduction may be condition dependent in young females. Reproductive success of older females was not affected by either weather or individual parameters. Our results show that changes in precipitation pattern may compromise the reproductive success of FY females. Further studies are needed to better understand the impact of weather conditions on reproductive success in long-lived bats under climate change scenarios.

Long-term individualized monitoring of sympatric bat species reveals distinct species- and demographic differences in hibernation phenology.

BACKGROUND: Hibernation allows species to conserve energy and thereby bridge unfavorable environmental conditions. At the same time, hibernation imposes substantial ecological and physiological costs. Understanding how hibernation timing differs within and between species can provide insights into the underlying drivers of this trade-off. However, this requires individualized long-term data that are often unavailable. Here, we used automatic monitoring techniques and a reproducible analysis pipeline to assess the individualized hibernation phenology of two sympatric bat species. Our study is based on data of more than 1100 RFID-tagged Daubenton's bats (Myotis daubentonii) and Natterer's bats (Myotis nattereri) collected over seven years at a hibernaculum in Germany. We used linear mixed models to analyze species-, sex- and age-specific differences in entrance, emergence and duration of the longest continuous period spent in the hibernaculum. RESULTS: Overall, Daubenton's bats entered the hibernaculum earlier and emerged later than Natterer's bats, resulting in a nearly twice as long hibernation duration. In both species, adult females entered earlier and emerged from hibernation later than adult males. Hibernation duration was shorter for juveniles than adults with the exception of adult male Natterer's bats whose hibernation duration was shortest of all classes. Finally, hibernation timing differed among years, but yearly variations in entrance and emergence timing were not equally shifted in both species. CONCLUSIONS: Our results suggest that even in sympatric species, and across sex and age classes, hibernation timing may be differentially affected by environmental conditions. This highlights the necessity of using individualized information when studying the impact of changing environments on hibernation phenology.

Population genetics as a tool to elucidate pathogen reservoirs: Lessons from Pseudogymnoascus destructans, the causative agent of White-Nose disease in bats.

Emerging infectious diseases pose a major threat to human, animal, and plant health. The risk of species-extinctions increases when pathogens can survive in the absence of the host. Environmental reservoirs can facilitate this. However, identifying such reservoirs and modes of infection is often highly challenging. In this study, we investigated the presence and nature of an environmental reservoir for the ascomycete fungus Pseudogymnoascus destructans, the causative agent of White-Nose disease. Using 18 microsatellite markers, we determined the genotypic differentiation between 1497 P. destructans isolates collected from nine closely situated underground sites where bats hibernate (i.e., hibernacula) in Northeastern Germany. This approach was unique in that it ensured that every isolate and resulting multilocus genotype was not only present, but also viable and therefore theoretically capable of infecting a bat. The distinct distribution of multilocus genotypes across hibernacula demonstrates that each hibernaculum has an essentially unique fungal population. This would be expected if bats become infected in their hibernaculum (i.e., the site they spend winter in to hibernate) rather than in other sites visited before they start hibernating. In one hibernaculum, both the walls and the hibernating bats were sampled at regular intervals over five consecutive winter seasons (1062 isolates), revealing higher genotypic richness on walls compared to bats and a stable frequency of multilocus genotypes over multiple winters. This clearly implicates hibernacula walls as the main environmental reservoir of the pathogen, from which bats become reinfected annually during the autumn.

Genetic diversity in a long-lived mammal is explained by the past's demographic shadow and current connectivity.

Within-species genetic diversity is crucial for the persistence and integrity of populations and ecosystems. Conservation actions require an understanding of factors influencing genetic diversity, especially in the context of global change. Both population size and connectivity are factors greatly influencing genetic diversity; the relative importance of these factors can, however, change through time. Hence, quantifying the degree to which population size or genetic connectivity are shaping genetic diversity, and at which ecological time scale (past or present), is challenging, yet essential for the development of efficient conservation strategies. In this study, we estimated the genetic diversity of 42 colonies of Rhinolophus hipposideros, a long-lived mammal vulnerable to global change, sampling locations spanning its continental northern range. Here, we present an integrative approach that disentangles and quantifies the contribution of different connectivity measures in addition to contemporary colony size and historic bottlenecks in shaping genetic diversity. In our study, the best model explained 64% of the variation in genetic diversity. It included historic bottlenecks, contemporary colony size, connectivity and a negative interaction between the latter two. Contemporary connectivity explained most genetic diversity when considering a 65 km radius around the focal colonies, emphasizing the large geographic scale at which the positive impact of connectivity on genetic diversity is most profound and hence, the minimum scale at which conservation should be planned. Our results highlight that the relative importance of the two main factors shaping genetic diversity varies through time, emphasizing the relevance of disentangling them to ensure appropriate conservation strategies.

Long-term study shows that increasing body size in response to warmer summers is associated with a higher mortality risk in a long-lived bat species.

Change in body size is one of the universal responses to global warming, with most species becoming smaller. While small size in most species corresponds to low individual fitness, small species typically show high population growth rates in cross-species comparisons. It is unclear, therefore, how climate-induced changes in body size ultimately affect population persistence. Unravelling the relationship between body size, ambient temperature and individual survival is especially important for the conservation of endangered long-lived mammals such as bats. Using an individual-based 24-year dataset from four free-ranging Bechstein's bat colonies (Myotis bechsteinii), we show for the first time a link between warmer summer temperatures, larger body sizes and increased mortality risk. Our data reveal a crucial time window in June-July, when juveniles grow to larger body sizes in warmer conditions. Body size is also affected by colony size, with larger colonies raising larger offspring. At the same time, larger bats have higher mortality risks throughout their lives. Our results highlight the importance of understanding the link between warmer weather and body size as a fitness-relevant trait for predicting species-specific extinction risks as consequences of global warming.

Quantifying individual influence in leading-following behavior of Bechstein's bats.

Leading-following behavior as a way of transferring information about the location of resources is wide-spread in many animal societies. It represents active information transfer that allows a given social species to reach collective decisions in the presence of limited information. Although leading-following behavior has received much scientific interest in the form of field studies, there is a need for systematic methods to quantify and study the individual contributions in this information transfer, which would eventually lead us to hypotheses about the individual mechanisms underlying this behaviour. In this paper we propose a general methodology that allows us to (a) infer individual leading-following behaviour from discrete observational data and (b) quantify individual influence based on methods from social network analysis. To demonstrate our methodology, we analyze longitudinal data of the roosting behavior of two different colonies of Bechstein's bats in different years. Regarding (a) we show how the inference of leading-following events can be calibrated from data making it a general approach when only discrete observations are available. This allows us to address (b) by constructing social networks in which nodes represent individual bats and directed and weighted links-the leading-following events. We then show how social network theory can be used to define and quantify individual influence in a way that reflects the dynamics of the specific social network. We find that individuals can be consistently ranked regarding their influence in the information transfer. Moreover, we identify a small set of individuals that play a central role in leading other bats to roosts. In the case of Bechstein's bats this finding can direct future studies on the individual-level mechanisms that result in such collective pattern. More generally, we posit that our data-driven methodology can be used to quantify leading-following behavior and individual impact in other animal systems, solely based on discrete observational data.

Social structure and relatedness in the fringe-lipped bat (Trachops cirrhosus).

General insights into the causes and effects of social structure can be gained from comparative analyses across socially and ecologically diverse taxa, such as bats, but long-term data are lacking for most species. In the neotropical fringe-lipped bat, Trachops cirrhosus, social transmission of foraging behaviour is clearly demonstrated in captivity, yet its social structure in the wild remains unclear. Here, we used microsatellite-based estimates of relatedness and records of 157 individually marked adults from 106 roost captures over 6 years, to infer whether male and female T. cirrhosus have preferred co-roosting associations and whether such associations were influenced by relatedness. Using a null model that controlled for year and roosting location, we found that both male and female T. cirrhosus have preferred roosting partners, but that only females demonstrate kin-biased association. Most roosting groups (67%) contained multiple females with one or two reproductive males. Relatedness patterns and recapture records corroborate genetic evidence for female philopatry and male dispersal. Our study adds to growing evidence that many bats demonstrate preferred roosting associations, which has the potential to influence social information transfer.

Free-ranging bats combine three different cognitive processes for roost localization.

Animals have evolved different cognitive processes to localize crucial resources that are difficult to find. Relevant cognitive processes such as associative learning and spatial memory have commonly been studied in a foraging related context under controlled laboratory conditions. However, in natural environments, animals can use multiple cognitive processes to localize resources. In this field study, we used a pairwise choice experiment and automatic roost monitoring to assess how individually marked, free-ranging Bechstein's bats belonging to two different colonies use associative learning, spatial memory and social information when localizing suitable day roosts. To our knowledge, this study tests for the first time how associative learning, spatial memory and social information are used in the process of roost localization in bats under the natural conditions. We show that, when searching for new roosts, bats used associative learning to discriminate between suitable and unsuitable roosts. For re-localizing previously occupied roosts, bats used spatial memory rather than associative learning. Moreover, bats significantly improved the localization of suitable unfamiliar roosts and tended to increase their accuracy to re-localize previously occupied day roosts using social information. Our field experiments suggest that Bechstein's bats make hierarchical use of different cognitive processes when localizing day roosts. More generally, our study underlines that evaluating different cues under natural conditions is fundamental to understanding how natural selection has shaped the cognitive processes used for localizing resources.

Differences in seasonal survival suggest species-specific reactions to climate change in two sympatric bat species.

Long-lived animals with a low annual reproductive output need a long time to recover from population crashes and are, thus, likely to face high extinction risk, if the current global environmental change will increase mortality rates. To aid conservation of those species, knowledge on the variability of mortality rates is essential. Unfortunately, however, individual-based multiyear data sets that are required for that have only rarely been collected for free-ranging long-lived mammals. Here, we used a five-year data set comprising activity data of 1,445 RFID-tagged individuals of two long-lived temperate zone bat species, Natterer's bats (Myotis nattereri) and Daubenton's bats (Myotis daubentonii), at their joint hibernaculum. Both species are listed as being of high conservation interest by the European Habitats Directive. Applying mixed-effects logistic regression, we explored seasonal survival differences in these two species which differ in foraging strategy and phenology. In both species, survival over the first winter of an individual's life was much lower than survival over subsequent winters. Focussing on adults only, seasonal survival patterns were largely consistent with higher winter and lower summer survival but varied in its level across years in both species. Our analyses, furthermore, highlight the importance of species-specific time periods for survival. Daubenton's bats showed a much stronger difference in survival between the two seasons than Natterer's bats. In one exceptional winter, the population of Natterer's bats crashed, while the survival of Daubenton's bats declined only moderately. While our results confirm the general seasonal survival pattern typical for hibernating mammals with higher winter than summer survival, they also show that this pattern can be reversed under particular conditions. Overall, our study points toward a high importance of specific time periods for population dynamics and suggests species-, population-, and age class-specific responses to global climate change.

Testing the adaptive value of gastropod shell morphology to flow: a multidisciplinary approach based on morphometrics, computational fluid dynamics and a flow tank experiment.

A major question in stream ecology is how invertebrates cope with flow. In aquatic gastropods, typically, larger and more globular shells with larger apertures are found in lotic (flowing water) versus lentic (stagnant water) habitats. This has been hypothetically linked to a larger foot, and thus attachment area, which has been suggested to be an adaptation against risk of dislodgement by current. Empirical evidence for this is scarce. Furthermore, these previous studies did not discuss the unavoidable increase in drag forces experienced by the snails as a consequence of the increased cross sectional area. Here, using Potamopyrgus antipodarum as a study model, we integrated computational fluid dynamics simulations and a flow tank experiment with living snails to test whether 1) globular shell morphs are an adaptation against dislodgement through lift rather than drag forces, and 2) dislocation velocity is positively linked to foot size, and that the latter can be predicted by shell morphology. The drag forces experienced by the shells were always stronger compared to the lift and lateral forces. Drag and lift forces increased with shell height but not with globularity. Rotating the shells out of the flow direction increased the drag forces, but decreased lift. Our hypothesis that the controversial presence of globular shells in lotic environments could be explained by an adaptation against lift rather than drag forces was rejected. The foot size was only predicted by the size of the shell, not by shell shape or aperture size, showing that the assumed aperture/foot area correlation should be used with caution and cannot be generalized for all aquatic gastropod species. Finally, shell morphology and foot size were not related to the dislodgement speed in our flow tank experiment. We conclude that other traits must play a major role in decreasing dislodgement risk in stream gastropods, e.g., specific behaviours or pedal mucus stickiness. Although we did not find globular shells to be adaptations for reducing dislodgement risk, we cannot rule out that they are still flow-related adaptations. For instance, globular shells are more crush-resistant and therefore perhaps adaptive in terms of diminishing damage caused by tumbling after dislodgement or against lotic crush-type predators.

Male-biased dispersal and the potential impact of human-induced habitat modifications on the Neotropical bat Trachops cirrhosus.

Gene flow, maintained through natal dispersal and subsequent mating events, is one of the most important processes in both ecology and population genetics. Among mammalian populations, gene flow is strongly affected by a variety of factors, including the species' ability to disperse, and the composition of the environment which can limit dispersal. Information on dispersal patterns is thus crucial both for conservation management and for understanding the social system of a species. We used 16 polymorphic nuclear microsatellite loci in addition to mitochondrial DNA sequences (1.61 kbp) to analyse the population structure and the sex-specific pattern of natal dispersal in the frog-eating fringe-lipped bat, Trachops cirrhosus, in Central Panama. Our study revealed that-unlike most of the few other investigated Neotropical bats-gene flow in this species is mostly male-mediated. Nevertheless, distinct genetic clusters occur in both sexes. In particular, the presence of genetic differentiation in the dataset only consisting of the dispersing sex (males) indicates that gene flow is impeded within our study area. Our data are in line with the Panama Canal in connection with the widening of the Río Chagres during the canal construction acting as a recent barrier to gene flow. The sensitivity of T. cirrhosus to human-induced habitat modifications is further indicated by an extremely low capture success in highly fragmented areas. Taken together, our genetic and capture data provide evidence for this species to be classified as less mobile and thus vulnerable to habitat change, information that is important for conservation management.

Using Approximate Bayesian Computation to infer sex ratios from acoustic data.

Population sex ratios are of high ecological relevance, but are challenging to determine in species lacking conspicuous external cues indicating their sex. Acoustic sexing is an option if vocalizations differ between sexes, but is precluded by overlapping distributions of the values of male and female vocalizations in many species. A method allowing the inference of sex ratios despite such an overlap will therefore greatly increase the information extractable from acoustic data. To meet this demand, we developed a novel approach using Approximate Bayesian Computation (ABC) to infer the sex ratio of populations from acoustic data. Additionally, parameters characterizing the male and female distribution of acoustic values (mean and standard deviation) are inferred. This information is then used to probabilistically assign a sex to a single acoustic signal. We furthermore develop a simpler means of sex ratio estimation based on the exclusion of calls from the overlap zone. Applying our methods to simulated data demonstrates that sex ratio and acoustic parameter characteristics of males and females are reliably inferred by the ABC approach. Applying both the ABC and the exclusion method to empirical datasets (echolocation calls recorded in colonies of lesser horseshoe bats, Rhinolophus hipposideros) provides similar sex ratios as molecular sexing. Our methods aim to facilitate evidence-based conservation, and to benefit scientists investigating ecological or conservation questions related to sex- or group specific behaviour across a wide range of organisms emitting acoustic signals. The developed methodology is non-invasive, low-cost and time-efficient, thus allowing the study of many sites and individuals. We provide an R-script for the easy application of the method and discuss potential future extensions and fields of applications. The script can be easily adapted to account for numerous biological systems by adjusting the type and number of groups to be distinguished (e.g. age, social rank, cryptic species) and the acoustic parameters investigated.

Growing old, yet staying young: The role of telomeres in bats' exceptional longevity.

Understanding aging is a grand challenge in biology. Exceptionally long-lived animals have mechanisms that underpin extreme longevity. Telomeres are protective nucleotide repeats on chromosome tips that shorten with cell division, potentially limiting life span. Bats are the longest-lived mammals for their size, but it is unknown whether their telomeres shorten. Using >60 years of cumulative mark-recapture field data, we show that telomeres shorten with age in Rhinolophus ferrumequinum and Miniopterus schreibersii, but not in the bat genus with greatest longevity, Myotis. As in humans, telomerase is not expressed in Myotis myotis blood or fibroblasts. Selection tests on telomere maintenance genes show that ATM and SETX, which repair and prevent DNA damage, potentially mediate telomere dynamics in Myotis bats. Twenty-one telomere maintenance genes are differentially expressed in Myotis, of which 14 are enriched for DNA repair, and 5 for alternative telomere-lengthening mechanisms. We demonstrate how telomeres, telomerase, and DNA repair genes have contributed to the evolution of exceptional longevity in Myotis bats, advancing our understanding of healthy aging.

Stabilization of a bat-pitcher plant mutualism.

Despite the long persistence of many mutualisms, it is largely unknown which mechanisms stabilize these interactions. This is especially true if only one mutualism partner can choose alternative partners while the other cannot, resulting in a power asymmetry. According to biological market theory the choosing partner should prefer the more dependent partner if the latter offers commodities of higher quality than its competitors. We tested this prediction using Bornean carnivorous pitcher plants (Nepenthes hemsleyana) that strongly rely on faecal nitrogen of bats (Kerivoula hardwickii) which roost inside the pitchers. The bats also roost in furled leaves of various plants. Surprisingly, during field observations the bats did not always choose N. hemsleyana pitchers despite their superior quality but were generally faithful either to pitchers or to furled leaves. In behavioural experiments 21% of the leaf-roosting bats switched to pitchers, while the majority of these bats and all pitcher-roosting individuals were faithful to the roost type in which we had found them. Genetic differentiation cannot explain this faithfulness, which likely results from different roosting traditions. Such traditions could have stabilizing or destabilizing effects on various mutualisms and should be investigated in more detail.