Ecological countermeasures to prevent pathogen spillover and subsequent pandemics.

Substantial global attention is focused on how to reduce the risk of future pandemics. Reducing this risk requires investment in prevention, preparedness, and response. Although preparedness and response have received significant focus, prevention, especially the prevention of zoonotic spillover, remains largely absent from global conversations. This oversight is due in part to the lack of a clear definition of prevention and lack of guidance on how to achieve it. To address this gap, we elucidate the mechanisms linking environmental change and zoonotic spillover using spillover of viruses from bats as a case study. We identify ecological interventions that can disrupt these spillover mechanisms and propose policy frameworks for their implementation. Recognizing that pandemics originate in ecological systems, we advocate for integrating ecological approaches alongside biomedical approaches in a comprehensive and balanced pandemic prevention strategy.

Geographically widespread and novel hemotropic mycoplasmas and bartonellae in Mexican free-tailed bats and sympatric North American bat species.

Bacterial pathogens remain poorly characterized in bats, especially in North America. We describe novel (and in some cases panmictic) hemoplasmas (12.9% positivity) and bartonellae (16.7% positivity) across three colonies of Mexican free-tailed bats (Tadarida brasiliensis), a partially migratory species that can seasonally travel hundreds of kilometers. Molecular analyses identified three novel Candidatus hemoplasma species most similar to another novel Candidatus species in Neotropical molossid bats. We also detected novel hemoplasmas in sympatric cave myotis (Myotis velifer) and pallid bats (Antrozous pallidus), with sequences in the latter 96.5% related to C. Mycoplasma haemohominis. We identified eight Bartonella genotypes, including those in cave myotis, with 96.7% similarity to C. Bartonella mayotimonensis. We also detected Bartonella rochalimae in migratory Tadarida brasiliensis, representing the first report of this human pathogen in bats. The seasonality and diversity of these bacteria observed here suggest that additional longitudinal, genomic, and immunological studies in bats are warranted.

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.

Conservation: Tracking bats around wind turbines.

Alternative energy is essential for a green future but comes at a high risk for animals. New research shows that forest-based wind turbines may create an ecological trap for bats that typically are repelled by wind turbines.

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.

A partial migrant relies upon a range-wide cue set but uses population-specific weighting for migratory timing.

BACKGROUND: Many birds species range over vast geographic regions and migrate seasonally between their breeding and overwintering sites. Deciding when to depart for migration is one of the most consequential life-history decisions an individual may make. However, it is still not fully understood which environmental cues are used to time the onset of migration and to what extent their relative importance differs across a range of migratory strategies. We focus on departure decisions of a songbird, the Eurasian blackbird Turdus merula, in which selected Russian and Polish populations are full migrants which travel relatively long-distances, whereas Finnish and German populations exhibit partial migration with shorter migration distances. METHODS: We used telemetry data from the four populations (610 individuals) to determine which environmental cues individuals from each population use to initiate their autumn migration. RESULTS: When departing, individuals in all populations selected nights with high atmospheric pressure and minimal cloud cover. Fully migratory populations departed earlier in autumn, at longer day length, at higher ambient temperatures, and during nights with higher relative atmospheric pressure and more supportive winds than partial migrants; however, they did not depart in higher synchrony. Thus, while all studied populations used the same environmental cues, they used population-specific and locally tuned thresholds to determine the day of departure. CONCLUSIONS: Our data support the idea that migratory timing is controlled by general, species-wide mechanisms, but fine-tuned thresholds in response to local conditions.

Bats use topography and nocturnal updrafts to fly high and fast.

During the day, flying animals exploit the environmental energy landscape by seeking out thermal or orographic uplift, or extracting energy from wind gradients.1-6 However, most of these energy sources are not thought to be available at night because of the lower thermal potential in the nocturnal atmosphere, as well as the difficulty of locating features that generate uplift. Despite this, several bat species have been observed hundreds to thousands of meters above the ground.7-9 Individuals make repeated, energetically costly high-altitude ascents,10-13 and others fly at some of the fastest speeds observed for powered vertebrate flight.14 We hypothesized that bats use orographic uplift to reach high altitudes,9,15-17 and that both this uplift and bat high-altitude ascents would be highly predictable.18 By superimposing detailed three-dimensional GPS tracking of European free-tailed bats (Tadarida teniotis) on high-resolution regional wind data, we show that bats do indeed use the energy of orographic uplift to climb to over 1,600 m, and also that they reach maximum sustained self-powered airspeeds of 135 km h-1. We show that wind and topography can predict areas of the landscape able to support high-altitude ascents, and that bats use these locations to reach high altitudes while reducing airspeeds. Bats then integrate wind conditions to guide high-altitude ascents, deftly exploiting vertical wind energy in the nocturnal landscape.

Foraging movements are density-independent among straw-coloured fruit bats.

Intraspecific competition in large aggregations of animals should generate density-dependent effects on foraging patterns. To test how large differences in colony size affect foraging movements, we tracked seasonal movements of the African straw-coloured fruit bat (Eidolon helvum) from four colonies that range from 4000 up to 10 million animals. Contrary to initial predictions, we found that mean distance flown per night (9-99 km), number of nightly foraging sites (2-3) and foraging and commuting times were largely independent of colony size. Bats showed classic central-place foraging and typically returned to the same day roost each night. However, roost switching was evident among individuals in three of the four colonies especially towards the onset of migration. The relatively consistent foraging patterns across seasons and colonies indicate that these bats seek out roosts close to highly productive landscapes. Once foraging effort starts to increase due to local resource depletion they migrate to landscapes with seasonally increasing resources. This minimizes high intraspecific competition and may help to explain why long-distance migration, otherwise rare in bats, evolved in this highly gregarious species.

Metabolic rate in common shrews is unaffected by temperature, leading to lower energetic costs through seasonal size reduction.

Small endothermic mammals have high metabolisms, particularly at cold temperatures. In the light of this, some species have evolved a seemingly illogical strategy: they reduce the size of the brain and several organs to become even smaller in winter. To test how this morphological strategy affects energy consumption across seasonally shifting ambient temperatures, we measured oxygen consumption and behaviour in the three seasonal phenotypes of the common shrew (Sorex araneus), which differ in size by about 20%. Body mass was the main driver of oxygen consumption, not the reduction of metabolically expensive brain mass. Against our expectations, we found no change in relative oxygen consumption with low ambient temperature. Thus, smaller body size in winter resulted in significant absolute energy savings. This finding could only partly be explained by an increase of lower cost behaviours in the activity budgets. Our findings highlight that these shrews manage to avoid one of the most fundamental and intuitive rules of ecology, allowing them to subsist with lower resource availability and successfully survive the harsh conditions of winter.

Linking colony size with quantitative estimates of ecosystem services of African fruit bats.

Animal-mediated seed dispersal is a pivotal component of functioning forest ecosystems all over the globe. Animals that disperse seeds away from their parental plants increase the seeds' chances of survival by releasing them from competition and specialised predators and so contribute to maintain the biodiversity of forests. Furthermore, seeds dispersed into deforested areas provide the opportunity for reforestation. Forest regeneration especially depends on animals that cover large distances easily and cross forest gaps, in particular large-bodied frugivores or mobile species such as birds and bats [1]. Yet, frugivores have started to disappear from forests everywhere, with potentially dramatic consequences for forest composition, regeneration and overall forest biomass [2,3]. Identifying which species contribute substantially to the dispersal of viable seeds, and how these services are affected by fluctuations in population size, is thus pivotal to the understanding and conservation of forest ecosystems [4].

Common noctules exploit low levels of the aerosphere.

Aerial habitats present a challenge to find food across a large potential search volume, particularly for insectivorous bats that rely on echolocation calls with limited detection range and may forage at heights over 1000 m. To understand how bats use vertical space, we tracked one to five foraging flights of eight common noctules (Nyctalus noctula). Bats were tracked for their full foraging session (87.27 ± 24 min) using high-resolution atmospheric pressure radio transmitters that allowed us to calculate height and wingbeat frequency. Bats used diverse flight strategies, but generally flew lower than 40 m, with scouting flights to 100 m and a maximum of 300 m. We found no influence of weather on height, and high-altitude ascents were not preceded by an increase in foraging effort. Wingbeat frequency was independent from climbing or descending flight, and bats skipped wingbeats or glided in 10% of all observations. Wingbeat frequency was positively related to capture mass, and wingbeat frequency was positively related to time of night, indicating an effect of load increase over a foraging bout. Overall, individuals used a wide range of airspace including altitudes that put them at increased risk from human-made structures. Further work is needed to test the context of these flight decisions, particularly as individuals migrate throughout Europe.

Rapid behavioral changes during early development in Peters' tent-making bat (Uroderma bilobatum).

Bats transition from flightless, milk-sustained infants to volant, foraging juveniles in the span of a few weeks to a few months. This rapid development is accompanied by fast growth and weight gain, but behavioral development remains poorly understood. We addressed development of maternal support and pup independence for Peters' tent-making bat (Uroderma bilobatum) in light of population level reproductive patterns. Uroderma bilobatum exhibited seasonal bimodal polyoestry at our study site. Births occurred over one month within a reproductive bout, resulting in variable levels of behavioral development for pups in the same maternity group. Pups reached adult forearm length more quickly than adult mass, facilitating the ontogeny of flight. Maternal support consisted of nursing and thermoregulation, transporting pups between night and day roosts, and milk provisioning between foraging bouts. We did not observe provisioning with solid food. Pups interacted only with their own mother. Between 25 to 40 days into a reproductive bout they matured by suckling progressively less and fledging over multiple nights in a two-stage process assisted by mothers. We describe several parturition events as well as a novel form of stereotyped tactile stimulation involving forearm pulses by mothers against suckling pups that may serve to promote weaning. Rapid behavioral changes in both pups and mothers accompany pup morphological development through maturation.

Determinants of spring migration departure decision in a bat.

Migratory decisions in birds are closely tied to environmental cues and fat stores, but it remains unknown if the same variables trigger bat migration. To learn more about the rare phenomenon of bat migration, we studied departure decisions of female common noctules (Nyctalus noctula) in southern Germany. We did not find the fattening period that modulates departure decisions in birds. Female noctules departed after a regular evening foraging session, uniformly heading northeast. As the day of year increased, migratory decisions were based on the interactions among wind speed, wind direction and air pressure. As the migration season progressed, bats were likely to migrate on nights with higher air pressure and faster tail winds in the direction of travel, and also show high probability of migration on low-pressure nights with slow head winds. Common noctules thus monitor complex environmental conditions to find the optimal migration night.

Cyclic bouts of extreme bradycardia counteract the high metabolism of frugivorous bats.

Active flight requires the ability to efficiently fuel bursts of costly locomotion while maximizing energy conservation during non-flying times. We took a multi-faceted approach to estimate how fruit-eating bats (Uroderma bilobatum) manage a high-energy lifestyle fueled primarily by fig juice. Miniaturized heart rate telemetry shows that they use a novel, cyclic, bradycardic state that reduces daily energetic expenditure by 10% and counteracts heart rates as high as 900 bpm during flight. Uroderma bilobatum support flight with some of the fastest metabolic incorporation rates and dynamic circulating cortisol in vertebrates. These bats will exchange fat reserves within 24 hr, meaning that they must survive on the food of the day and are at daily risk of starvation. Energetic flexibly in U. bilobatum highlights the fundamental role of ecological pressures on integrative energetic networks and the still poorly understood energetic strategies of animals in the tropics.

Stable carbon isotopes in breath reveal fast metabolic incorporation rates and seasonally variable but rapid fat turnover in the common shrew (Sorex araneus).

Small non-migratory mammals with Northern distribution ranges apply a variety of behavioural and physiological wintering strategies. A rare energy-saving strategy is Dehnel's phenomenon, involving a reduction and later regrowth of the body size, several organs and parts of the skeleton in red-toothed shrews (Soricidae). The size extremes coincide with major life stages. However, the physiological consequences for the shrew's metabolism remain poorly understood. In keeping with the energetic limitations that may induce the size changes, we hypothesised that metabolic incorporation rates should remain the same across the shrews' lifetimes. In contrast, fat turnover rates should be faster in smaller subadults than in large juveniles and regrown adults, as the metabolic activity of fat tissue increases in winter individuals (subadults). Measuring the changes in the ratio of exhaled stable carbon isotopes, we found that the baseline diet of shrews changed across the season. A diet switch experiment showed that incorporation rates were consistently rapid (t50=38.2±21.1-69.3±53.5 min) and did not change between seasons. As predicted, fat turnover rates were faster in size-reduced subadults (t50=2.1±1.3 h) compared with larger juveniles (t50=5.5±1.7 h) and regrown adults (t50=5.0±4.4 h). In all three age/size classes, all body fat was turned over after 9-24 h. These results show that high levels of nutrient uptake are independent of body size, whereas fat turnover rates are negatively correlated with body size. Thus, the shrews might be under higher pressure to save energy in winter and this may have supported the evolution of Dehnel's phenomenon.

Heart rate reveals torpor at high body temperatures in lowland tropical free-tailed bats.

Reduction in metabolic rate and body temperature is a common strategy for small endotherms to save energy. The daily reduction in metabolic rate and heterothermy, or torpor, is particularly pronounced in regions with a large variation in daily ambient temperature. This applies most strongly in temperate bat species (order Chiroptera), but it is less clear how tropical bats save energy if ambient temperatures remain high. However, many subtropical and tropical species use some daily heterothermy on cool days. We recorded the heart rate and the body temperature of free-ranging Pallas' mastiff bats (Molossus molossus) in Gamboa, Panamá, and showed that these individuals have low field metabolic rates across a wide range of body temperatures that conform to high ambient temperature. Importantly, low metabolic rates in controlled respirometry trials were best predicted by heart rate, and not body temperature. Molossus molossus enter torpor-like states characterized by low metabolic rate and heart rates at body temperatures of 32°C, and thermoconform across a range of temperatures. Flexible metabolic strategies may be far more common in tropical endotherms than currently known.

Common Noctule Bats Are Sexually Dimorphic in Migratory Behaviour and Body Size but Not Wing Shape.

Within the large order of bats, sexual size dimorphism measured by forearm length and body mass is often female-biased. Several studies have explained this through the effects on load carrying during pregnancy, intrasexual competition, as well as the fecundity and thermoregulation advantages of increased female body size. We hypothesized that wing shape should differ along with size and be under variable selection pressure in a species where there are large differences in flight behaviour. We tested whether load carrying, sex differential migration, or reproductive advantages of large females affect size and wing shape dimorphism in the common noctule (Nyctalus noctula), in which females are typically larger than males and only females migrate long distances each year. We tested for univariate and multivariate size and shape dimorphism using data sets derived from wing photos and biometric data collected during pre-migratory spring captures in Switzerland. Females had forearms that are on average 1% longer than males and are 1% heavier than males after emerging from hibernation, but we found no sex differences in other size, shape, or other functional characters in any wing parameters during this pre-migratory period. Female-biased size dimorphism without wing shape differences indicates that reproductive advantages of big mothers are most likely responsible for sexual dimorphism in this species, not load compensation or shape differences favouring aerodynamic efficiency during pregnancy or migration. Despite large behavioural and ecological sex differences, morphology associated with a specialized feeding niche may limit potential dimorphism in narrow-winged bats such as common noctules and the dramatic differences in migratory behaviour may then be accomplished through plasticity in wing kinematics.

Group size, survival and surprisingly short lifespan in socially foraging bats.

BACKGROUND: The relationships between group size, survival, and longevity vary greatly among social species. Depending on demographic and ecological circumstances, there are both positive and negative effects of group size variation on individual survival and longevity. For socially foraging species in particular there may be an optimal group size that predicts maximum individual survival that is directly related to the potential for information transfer, social coordination, and costs of conspecific interference. Our aim was to investigate this central aspect of evolutionary ecology by focusing on a socially foraging bat, Molossus molossus. This species optimizes foraging success by eavesdropping on the echolocation calls of group members to locate ephemeral food patches. We expected to find the highest survival and longest lifespans in small groups as a consequence of a trade-off between benefits of information transfer on ephemeral resources and costs of conspecific interference. RESULTS: In a mark-recapture study of 14 mixed-sex M. molossus social groups in Gamboa, Panama, spanning several years we found the expected relatively small and intermediate, but stable groups, with a mean size of 9.6 ± 6.7 adults and juveniles. We estimated survival proxies using Cox proportional hazard models and multistate-mark recapture models generated with recapture data as well as automated monitoring of roost entrances in a subset of the groups. Median survival of females was very short with 1.8 years and a maximum estimated longevity of 5.6 years. Contrary to our expectations, we found no relationship between variation in group size and survival, a result similar to few other studies. CONCLUSIONS: Strong selection towards small group size may result from psychoacoustic and cognitive constraints related to acoustic interference in social foraging and the complexity of coordinated flight. The short lifespans were unexpected and may result from life at the energetic edge due to a highly specialized diet. The absence of a relationship between group size and survival may reflect a similar but optimized survival within the selected range of group sizes. We expect the pattern of small group sizes will be consistent in future research on species dependent on social information transfer about ephemeral resources.

No fever and leucocytosis in response to a lipopolysaccharide challenge in an insectivorous bat.

Bat immune systems may allow them to respond to zoonotic agents more efficiently than other mammals. As the first line of defence, the taxonomically conserved acute phase immune reaction of leucocytosis and fever is crucial for coping with infections, but it is unknown if this response is a key constituent to bat immunological success. We investigated the acute phase reaction to a standard lipopolysaccharide (LPS) challenge in Pallas's mastiff bats (Molossus molossus). Challenged bats lost mass, but in contrast to other mammals showed no leucocytosis or fever. There also was no influence on body temperature reduction during torpor. When compared to recent genome-wide assays for constituent immune genes, this lack of a conserved fever response to LPS contributes to a clearer understanding of the innate immune system in bat species and of the coevolution of bats with a wide diversity of pathogens.

Ring-tailed lemurs: a species re-imagined.

For over 50 years, ring-tailed lemurs have been studied continuously in the wild. As one of the most long-studied primate species, the length and breadth of their study is comparable to research on Japanese macaques, baboons and chimpanzees. They are also one of the most broadly observed of all primates, with comprehensive research conducted on their behaviour, biology, ecology, genetics, palaeobiology and life history. However, over the last decade, a new generation of lemur scholars, working in conjunction with researchers who have spent decades studying this species, have greatly enhanced our knowledge of ring-tailed lemurs. In addition, research on this species has expanded beyond traditional gallery forest habitats to now include high altitude, spiny thicket, rocky outcrop and anthropogenically disturbed coastal forest populations. The focus of this special volume is to 're-imagine' the 'flagship species of Madagascar', bringing together three generations of lemur scholars.