Heart rate monitoring reveals differential seasonal energetic trade-offs in male noctule bats.

Understanding how animals meet their daily energy requirements is critical in our rapidly changing world. Small organisms with high metabolic rates can conserve stored energy when food availability is low or increase energy intake when energetic requirements are high, but how they balance this in the wild remains largely unknown. Using miniaturized heart rate transmitters, we continuously quantified energy expenditure, torpor use and foraging behaviour of free-ranging male bats (Nyctalus noctula) in spring and summer. In spring, bats used torpor extensively, characterized by lowered heart rates and consequently low energy expenditures. In contrast, in summer, bats consistently avoided torpor, even though they could have used this low-energy mode. As a consequence, daytime heart rates in summer were three times as high compared with the heart rates in spring. Daily energy use increased by 42% during summer, despite lower thermogenesis costs at higher ambient temperatures. Likely, as a consequence, bats nearly doubled their foraging duration. Overall, our results indicate that summer torpor avoidance, beneficial for sperm production and self-maintenance, comes with a high energetic cost. The ability to identify and monitor such vulnerable energetic life-history stages is particularly important to predict how species will deal with increasing temperatures and changes in their resource landscapes.

Seasonal shifts in insect ephemerality drive bat foraging effort.

Animal foraging is fundamentally shaped by food distribution and availability.1 However, the quantification of spatiotemporal food distribution is rare2 but crucial to explain variation in foraging behavior among species, populations, or individuals. Clumped but ephemeral food sources enable rapid energy intake but require increased effort to find,3 can generate variable foraging success,4 and force animals to forage more efficiently. We quantified seasonal shifts in the availability of such resources to test the proximate effects of food distribution on changes in movement patterns. The neotropical lesser bulldog bat (Noctilio albiventris) forages in a seasonal environment on emerging aquatic insects, whose numbers peak shortly after dusk.5,6 We GPS-tracked bats and quantified nocturnal insect distribution in their foraging area using floating camera traps across wet and dry seasons. Surprisingly, insects were 75% less abundant and swarms were 60% shorter lived (more ephemeral) in the wet season. As a result, wet season bats had to fly twice as far (total and maximum distance fromroost distances) and 45% longer (duration) per night. Within foraging bouts, wet season bats spent less time in each insect patch and searched longer for subsequent patches, reflecting increased temporal ephemerality and decreased spatial predictability of insects. Our results highlight the tight link between foraging effort and spatiotemporal distribution of food and the influence of constraints imposed by reproduction on behavioral flexibility and adaptations to the highly dynamic resource landscapes of mobile prey.7,8 Examining foraging behavior in light of spatiotemporal dynamics of resources can help predict how animals respond to shifts in food availability caused by escalating environmental changes.

High temporal resolution data reveal low bat and insect activity over managed meadows in central Europe.

Increasing agriculture and pesticide use have led to declines in insect populations and biodiversity worldwide. In addition to insect diversity, it is also important to consider insect abundance, due to the importance of insects as food for species at higher trophic levels such as bats. We monitored spatiotemporal variation in abundance of nocturnal flying insects over meadows, a common open landscape structure in central Europe, and correlated it with bat feeding activity. Our most important result was that insect abundance was almost always extremely low. This was true regardless of management intensity of the different meadows monitored. We also found no correlation of insect abundance or the presence of insect swarms with bat feeding activity. This suggests that insect abundance over meadows was too low and insect swarms too rare for bats to risk expending energy to search for them. Meadows appeared to be poor habitat for nocturnal flying insects, and of low value as a foraging habitat for bats. Our study highlights the importance of long-term monitoring of insect abundance, especially at high temporal scales to identify and protect foraging habitats. This will become increasingly important given the rapid decline of insects.

Robust evidence for bats as reservoir hosts is lacking in most African virus studies: a review and call to optimize sampling and conserve bats.

Africa experiences frequent emerging disease outbreaks among humans, with bats often proposed as zoonotic pathogen hosts. We comprehensively reviewed virus-bat findings from papers published between 1978 and 2020 to evaluate the evidence that African bats are reservoir and/or bridging hosts for viruses that cause human disease. We present data from 162 papers (of 1322) with original findings on (1) numbers and species of bats sampled across bat families and the continent, (2) how bats were selected for study inclusion, (3) if bats were terminally sampled, (4) what types of ecological data, if any, were recorded and (5) which viruses were detected and with what methodology. We propose a scheme for evaluating presumed virus-host relationships by evidence type and quality, using the contrasting available evidence for Orthoebolavirus versus Orthomarburgvirus as an example. We review the wording in abstracts and discussions of all 162 papers, identifying key framing terms, how these refer to findings, and how they might contribute to people's beliefs about bats. We discuss the impact of scientific research communication on public perception and emphasize the need for strategies that minimize human-bat conflict and support bat conservation. Finally, we make recommendations for best practices that will improve virological study metadata.

Induction of kidney-related gene programs through co-option of SALL1 in mole ovotestes.

Changes in gene expression represent an important source of phenotypic innovation. Yet how such changes emerge and impact the evolution of traits remains elusive. Here, we explore the molecular mechanisms associated with the development of masculinizing ovotestes in female moles. By performing integrative analyses of epigenetic and transcriptional data in mole and mouse, we identified the co-option of SALL1 expression in mole ovotestes formation. Chromosome conformation capture analyses highlight a striking conservation of the 3D organization at the SALL1 locus, but an evolutionary divergence of enhancer activity. Interspecies reporter assays support the capability of mole-specific enhancers to activate transcription in urogenital tissues. Through overexpression experiments in transgenic mice, we further demonstrate the capability of SALL1 to induce kidney-related gene programs, which are a signature of mole ovotestes. Our results highlight the co-option of gene expression, through changes in enhancer activity, as a plausible mechanism for the evolution of traits.

Domestication effect of reduced brain size is reverted when mink become feral.

A typical consequence of breeding animal species for domestication is a reduction in relative brain size. When domesticated animals escape from captivity and establish feral populations, the larger brain of the wild phenotype is usually not regained. In the American mink (Neovison vison), we found an exception to this rule. We confirmed the previously described reduction in relative braincase size and volume compared to their wild North American ancestors in mink bred for their fur in Poland, in a dataset of 292 skulls. We then also found a significant regrowth of these measures in well-established feral populations in Poland. Closely related, small mustelids are known for seasonal reversible changes in skull and brain size. It seems that these small mustelids are able to regain the brain size, which is adaptive for living in the wild, and flexibly respond to selection accordingly.

Contrasting Torpor Use by Reproductive Male Common Noctule Bats in the Laboratory and in the Field.

Metabolic processes of animals are often studied in controlled laboratory settings. However, these laboratory settings often do not reflect the animals' natural environment. Thus, results of metabolic measurements from laboratory studies must be cautiously applied to free-ranging animals. Recent technological advances in animal tracking allow detailed eco-physiological studies that reveal when, where, and how physiological measurements from the field differ from those from the laboratory. We investigated the torpor behavior of male common noctule bats (Nyctalus noctula) across different life history stages using two approaches: in controlled laboratory experiments and in the field using calibrated heart rate telemetry. We predicted that non-reproductive males would extensively use torpor to conserve energy, whereas reproductive males would reduce torpor use to promote spermatogenesis. We did not expect differences in torpor use between captive and wild animals as we simulated natural temperature conditions in the laboratory. We found that during the non-reproductive phase, both captive and free-ranging bats used torpor extensively. During reproduction, bats in captivity unexpectedly also used torpor throughout the day, while only free-ranging bats showed the expected reduction in torpor use. Thus, depending on life history stage, torpor behavior in the laboratory was markedly different from the wild. By implementing both approaches and at different life history stages, we were able to better explore the limitations of eco-physiological laboratory studies and make recommendations for when they are an appropriate proxy for natural behavior.

Histological and MRI brain atlas of the common shrew, Sorex araneus, with brain region-specific gene expression profiles.

The common shrew, Sorex araneus, is a small mammal of growing interest in neuroscience research, as it exhibits dramatic and reversible seasonal changes in individual brain size and organization (a process known as Dehnel's phenomenon). Despite decades of studies on this system, the mechanisms behind the structural changes during Dehnel's phenomenon are not yet understood. To resolve these questions and foster research on this unique species, we present the first combined histological, magnetic resonance imaging (MRI), and transcriptomic atlas of the common shrew brain. Our integrated morphometric brain atlas provides easily obtainable and comparable anatomic structures, while transcriptomic mapping identified distinct expression profiles across most brain regions. These results suggest that high-resolution morphological and genetic research is pivotal for elucidating the mechanisms underlying Dehnel's phenomenon while providing a communal resource for continued research on a model of natural mammalian regeneration. Morphometric and NCBI Sequencing Read Archive are available at https://doi.org/10.17617/3.HVW8ZN.

A species-level trait dataset of bats in Europe and beyond.

Knowledge of species' functional traits is essential for understanding biodiversity patterns, predicting the impacts of global environmental changes, and assessing the efficiency of conservation measures. Bats are major components of mammalian diversity and occupy a variety of ecological niches and geographic distributions. However, an extensive compilation of their functional traits and ecological attributes is still missing. Here we present EuroBaTrait 1.0, the most comprehensive and up-to-date trait dataset covering 47 European bat species. The dataset includes data on 118 traits including genetic composition, physiology, morphology, acoustic signature, climatic associations, foraging habitat, roost type, diet, spatial behaviour, life history, pathogens, phenology, and distribution. We compiled the bat trait data obtained from three main sources: (i) a systematic literature and dataset search, (ii) unpublished data from European bat experts, and (iii) observations from large-scale monitoring programs. EuroBaTrait is designed to provide an important data source for comparative and trait-based analyses at the species or community level. The dataset also exposes knowledge gaps in species, geographic and trait coverage, highlighting priorities for future data collection.

A multi-species evaluation of digital wildlife monitoring using the Sigfox IoT network.

Bio-telemetry from small tags attached to animals is one of the principal methods for studying the ecology and behaviour of wildlife. The field has constantly evolved over the last 80 years as technological improvement enabled a diversity of sensors to be integrated into the tags (e.g., GPS, accelerometers, etc.). However, retrieving data from tags on free-ranging animals remains a challenge since satellite and GSM networks are relatively expensive and or power hungry. Recently a new class of low-power communication networks have been developed and deployed worldwide to connect the internet of things (IoT). Here, we evaluated one of these, the Sigfox IoT network, for the potential as a real-time multi-sensor data retrieval and tag commanding system for studying fauna across a diversity of species and ecosystems. We tracked 312 individuals across 30 species (from 25 g bats to 3 t elephants) with seven different device concepts, resulting in more than 177,742 successful transmissions. We found a maximum line of sight communication distance of 280 km (on a flying cape vulture [Gyps coprotheres]), which sets a new documented record for animal-borne digital data transmission using terrestrial infrastructure. The average transmission success rate amounted to 68.3% (SD 22.1) on flying species and 54.1% (SD 27.4) on terrestrial species. In addition to GPS data, we also collected and transmitted data products from accelerometers, barometers, and thermometers. Further, we assessed the performance of Sigfox Atlas Native, a low-power method for positional estimates based on radio signal strengths and found a median accuracy of 12.89 km (MAD 5.17) on animals. We found that robust real-time communication (median message delay of 1.49 s), the extremely small size of the tags (starting at 1.28 g without GPS), and the low power demands (as low as 5.8 µAh per transmitted byte) unlock new possibilities for ecological data collection and global animal observation.

Roost making in bats.

Structures created by animals can serve many purposes. Spiders weave intricate webs to trap prey; beavers engineer complex networks of dams to alter waterways; male bower birds construct and decorate elaborate bowers to attract mates. Animal architecture ranges widely in function, but by far the most common use is shelter. Animals can spend a large amount of time in their shelters, and this is often where they both sleep and rear young, two of the most vulnerable states in animal lives. To optimize the safety and suitability of refuges available to them, many animals have become architects and create their own shelters, ranging from simple holes in the ground to the large complex nests of some social insects.

Fifty years of data show the effects of climate on overall skull size and the extent of seasonal reversible skull size changes (Dehnel's phenomenon) in the common shrew.

Global climate change affects many aspects of biology and has been shown to cause body size changes in animals. However, suitable datasets allowing the analysis of long-term relationships between body size, climate, and its effects are rare. The size of the skull is often used as a proxy for overall body size. Skull size does not change much in fully grown vertebrates; however, some high-metabolic small mammals shrink in winter and regrow in spring, including their skull and brain. This is thought to be a winter adaptation, as a smaller brain size reduces energy requirements. Climate could thus affect not only the overall size but also the pattern of the size change, that is, Dehnel's phenomenon, in these animals. We assessed the impact of the changes in climate on the overall skull size and the different stages of Dehnel's phenomenon in skulls of the common shrew, Sorex araneus, collected over 50 years in the Bialowieza Forest, E Poland. Overall skull size decreased, along with increasing temperatures and decreasing soil moisture, which affected the availability of the shrews' main food source, earthworms. The skulls of males were larger than those of females, but the degree of the decrease in size did not differ between sexes. The magnitude of Dehnel's phenomenon increased over time, indicating an increasing selection pressure on animals in winter. Overall, climate clearly affected the common shrew's overall size as well as its seasonal size changes. With the current acceleration in climate change, the effects on the populations of this cold-adapted species may be quite severe in a large part of its distribution range.

Winter conditions, not resource availability alone, may drive reversible seasonal skull size changes in moles.

Seasonal changes in the environment can lead to astonishing adaptations. A few small mammals with exceptionally high metabolisms have evolved a particularly extreme strategy: they shrink before winter and regrow in spring, including changes of greater than 20% in skull and brain size. Whether this process is an adaptation to seasonal climates, resource availability or both remains unclear. We show that European moles (Talpa europaea) also decrease skull size in winter. As resources for closely related Iberian moles (Talpa occidentalis) are lowest in summer, we predicted they should shift the timing of size changes. Instead, they do not change size at all. We conclude that in moles, seasonal decrease and regrowth of skull size is an adaptation to winter climate and not to a changing resource landscape alone. We not only describe this phenomenon in yet another taxon, but take an important step towards a better understanding of this enigmatic cycle.

Flexible energy-saving strategies in female temperate-zone bats.

Torpor is characterized by an extreme reduction in metabolism and a common energy-saving strategy of heterothermic animals. Torpor is often associated with cold temperatures, but in the last decades, more diverse and flexible forms of torpor have been described. For example, tropical bat species maintain a low metabolism and heart rate at high ambient and body temperatures. We investigated whether bats (Nyctalus noctula) from the cooler temperate European regions also show this form of torpor with metabolic inhibition at high body temperatures, and whether this would be as pronounced in reproductive as in non-reproductive bats. We simultaneously measured metabolic rate, heart rate, and skin temperature in non-reproductive and pregnant females at a range of ambient temperatures. We found that they can decouple metabolic rate and heart rate from body temperature: they maintained an extremely low metabolism and heart rate when exposed to ambient temperatures changing from 0 to 32.5 °C, irrespective of reproductive status. When we simulated natural temperature conditions, all non-reproductive bats used torpor throughout the experiment. Pregnant bats used variable strategies from torpor, to maintaining normothermy, or a combination of both. Even a short torpor bout during the day saved up to 33% of the bats' total energy expenditure. Especially at higher temperatures, heart rate was a much better predictor of metabolic rate than skin temperature. We suggest that the capability to flexibly save energy across a range of ambient temperatures within and between reproductive states may be an important ability of these bats and possibly other temperate-zone heterotherms.

A conceptual framework to predict social information use based on food ephemerality and individual resource requirements.

Environmental variability poses a range of challenges to foraging animals trying to meet their energetic needs. Where food patches are unpredictable but shareable, animals can use social information to locate patches more efficiently or reliably. However, resource unpredictability can be heterogeneous and complex. The behavioural strategies animals employ to exploit such resources also vary, particularly if, when, and where animals use available social information. We reviewed the literature on social information use by foraging animals and developed a novel framework that integrates four elements - (1) food resource persistence; (2) the relative value of social information use; (3) behavioural context (opportunistic or coordinated); and (4) location of social information use - to predict and characterize four strategies of social information use - (1) local enhancement; (2) group facilitation; (3) following; and (4) recruitment. We validated our framework by systematically reviewing the growing empirical literature on social foraging in bats, an ideal model taxon because they exhibit extreme diversity in ecological niche and experience low predation risk while foraging but function at high energy expenditures, which selects for efficient foraging behaviours. Our framework's predictions agreed with the observed natural behaviour of bats and identified key knowledge gaps for future studies. Recent advancements in technology, methods, and analysis will facilitate additional studies in bats and other taxa to further test the framework and our conception of the ecological and evolutionary forces driving social information use. Understanding the links between food distribution, social information use, and foraging behaviour will help elucidate social interactions, group structure, and the evolution of sociality for species across the animal kingdom.

Micro-sized open-source and low-cost GPS loggers below 1 g minimise the impact on animals while collecting thousands of fixes.

GPS-enabled loggers have been proven as valuable tools for monitoring and understanding animal movement, behaviour and ecology. While the importance of recording accurate location estimates is well established, deployment on many, especially small species, has been limited by logger mass and cost. We developed an open-source and low-cost 0.65 g GPS logger with a simple smartphone-compatible user interface, that can record more than 10,000 GPS fixes on a single 30 mAh battery charge (resulting mass including battery: 1.3 g). This low-budget 'TickTag' (currently 32 USD) allows scientists to scale-up studies while becoming a 'wearable' for larger animals and simultaneously enabling high-definition studies on small animals. Tests on two different species (domestic dog, Canis lupus familiaris and greater mouse-eared bats, Myotis myotis) showed that our combination of optimised hardware design and software-based recording strategies increases the number of achievable GPS fixes per g device mass compared to existing micro-sized solutions. We propose that due to the open-source access, as well as low cost and mass, the TickTag fills a technological gap in wildlife ecology and will open up new possibilities for wildlife research and conservation.

Dehnel's phenomenon.

Lázaro and Dechmann explain how some mammals that live through harsh winters exhibit seasonal shrinkage of the brain and skull, a process called Dehnel's phenomenon, which helps to spare energy during times of food shortage and high energetic demands.

Geographic patterns in seasonal changes of body mass, skull, and brain size of common shrews.

Some small mammals exhibit Dehnel's Phenomenon, a drastic decrease in body mass, braincase, and brain size from summer to winter, followed by a regrowth in spring. This is accompanied by a re-organization of the brain and changes in other organs. The evolutionary link between these changes and seasonality remains unclear, although the intensity of change varies between locations as the phenomenon is thought to lead to energy savings during winter.Here we explored geographic variation of the intensity of Dehnel's Phenomenon in Sorex araneus. We compiled literature on seasonal changes in braincase size, brain, and body mass, supplemented by our own data from Poland, Germany, and Czech Republic.We analyzed the effect of geographic and climate variables on the intensity of change and patterns of brain re-organization.From summer to winter, the braincase height decreased by 13%, followed by 10% regrowth in spring. For body mass, the changes were -21%/+82%, respectively. Changes increased toward northeast. Several climate variables were correlated with these transformations, confirming a link of the intensity of the changes with environmental conditions. This relationship differed for the decrease versus regrowth, suggesting that they may have evolved under different selective pressures.We found no geographic trends explaining variability in the brain mass changes although they were similar (-21%/+10%) to those of the braincase size. Underlying patterns of change in brain organization in northeastern Poland were almost identical to the pattern observed in southern Germany. This indicates that local habitat characteristics may play a more important role in determining brain structure than broad scale geographic conditions.We discuss the techniques and criteria used for studying this phenomenon, as well as its potential presence in other taxa and the importance of distinguishing it from other kinds of seasonal variation.