Gary F. McCracken

Economic Importance of Bats in Agriculture

Insectivorous bat populations, adversely impacted by white-nose syndrome and wind turbines, may be worth billions of dollars to North American agriculture. White-nose syndrome (WNS) and the increased development of wind-power facilities are threatening populations of insectivorous bats in North America. Bats are voracious predators of nocturnal insects, including many crop and forest pests. We present here analyses suggesting that loss of bats in North America could lead to agricultural losses estimated at more than

Host Phylogeny Constrains Cross-Species Emergence and Establishment of Rabies Virus in Bats

3.7 billion/year. Urgent efforts are needed to educate the public and policy-makers about the ecological and economic importance of insectivorous bats and to provide practical conservation solutions.

Bat Mating Systems

Threats to and from Bats Bats appear to be able to host an assortment of alarming pathogens, which, if they do not extirpate the bats, have implications for human health (see the Perspective by Daszak). For example, exposure to bats is the main source of human rabies in the Americas. But rabies is not generally transmitted among people; humans are a dead end for the virus. Streicker et al. (p. 676, see the cover) show that rabies virus lineages tend to be specific for bat lineages. It seems that although rabies viruses have the potential for rapid evolution, this property alone is not enough to overcome genetic barriers, which inhibit the onward transmission of rabies virus into a new species. White-nose syndrome, an exotic fungal infection of bats, has, over the past 3 years, spread from upstate New York to West Virginia, killing on average 70% of the animals in a hibernating colony. The infection makes bats restless over winter when they should be dormant, which makes them exhaust their fat reserves, resulting in the death of over a million bats. Frick et al. (p. 679) have analyzed population data collected on bats in the northeastern United States for the past 30 years and show that, mainly owing to white-nose syndrome, the once abundant little brown bat is heading for regional extinction in the next 16 years or so. This scale of loss of an insectivorous mammal is expected to have repercussions for ecosystem integrity and for the economic costs of agricultural pest control. Rabies virus’ innate capacity to replicate and adapt cannot overcome host genetic barriers to cross-species transfer. For RNA viruses, rapid viral evolution and the biological similarity of closely related host species have been proposed as key determinants of the occurrence and long-term outcome of cross-species transmission. Using a data set of hundreds of rabies viruses sampled from 23 North American bat species, we present a general framework to quantify per capita rates of cross-species transmission and reconstruct historical patterns of viral establishment in new host species using molecular sequence data. These estimates demonstrate diminishing frequencies of both cross-species transmission and host shifts with increasing phylogenetic distance between bat species. Evolutionary constraints on viral host range indicate that host species barriers may trump the intrinsic mutability of RNA viruses in determining the fate of emerging host-virus interactions.

Genetic variation and migration in the Mexican free‐tailed bat (Tadarida brasiliensis mexicana)

Publisher Summary This chapter describes the mating systems of bats, emphasizing research from the last 20 years. For completeness, the chapter lists all species where mating systems are defined, but it discusses only those where there is new information or where additional interpretations are possible. In total, it includes information on the mating systems of 66 species of bats in 10 families. Bats from the largest families (Vespertilionidae, Pteropodidae, Phyllostomidae) are best represented in this literature. In proportion to their species diversity, bats in the Rhinolophidae and Molossidae have received the least attention. Bats from the zoogeographic regions with the greatest numbers of species (Ethiopian, Neotropical, Oriental) also have received the most study. In proportion to regional species richness, mating systems have been least studied in bats from the Australian and Oriental regions. Combined with detailed field studies, the immediate future is likely to see an increasing emphasis on the use of these new molecular methods to resolve the big issues in bat mating systems. It is anticipated that these issues are the questions of apparent monogamy, the significance of multiple mating by females, and the roles of female choice and sperm competition.

EFFECT OF HABITAT AND FORAGING HEIGHT ON BAT ACTIVITY IN THE COASTAL PLAIN OF SOUTH CAROLINA

Incomplete lineage sorting can genetically link populations long after they have diverged, and will exert a more powerful influence on larger populations. The effects of this stochastic process can easily be confounded with those of gene flow, potentially leading to inaccurate estimates of dispersal capabilities or erroneous designation of evolutionarily significant units (ESUs). We have used phylogenetic, population genetic, and coalescent methods to examine genetic structuring in large populations of a widely dispersing bat species and to test hypotheses concerning the influences of coalescent stochasticity vs. gene flow. The Mexican free‐tailed bat, Tadarida brasiliensis mexicana, exhibits variation in both migratory tendency and route over its range. Observations of the species’ migratory behaviour have led to the description of behaviourally and geographically defined migratory groups, with the prediction that these groups compose structured gene pools. Here, we used mtDNA sequence analyses coupled with existing information from allozyme, banding, and natural history studies to evaluate hypotheses regarding the relationship between migration and genetic structure. Analyses of molecular variance revealed no significant genetic structuring of behaviourally distinct migratory groups. Demographic analyses were consistent with population growth, although the timing of population expansion events differs between migratory and nonmigratory populations. Hypotheses concerning the role of gene flow vs. incomplete lineage sorting on these data are explored using coalescent simulations. Our study demonstrates the importance of accounting for coalescent stochasticity in formulating phylogeographical hypotheses, and indicates that analyses that do not take such processes into account can lead to false conclusions regarding a species’ phylogeographical history.

THERMAL IMAGING REVEALS SIGNIFICANTLY SMALLER BRAZILIAN FREE-TAILED BAT COLONIES THAN PREVIOUSLY ESTIMATED

Abstract We compared bat activity levels in the Coastal Plain of South Carolina among 5 habitat types: forested riparian areas, clearcuts, young pine plantations, mature pine plantations, and pine savannas. We used time-expansion radio-microphones and integrated detectors to simultaneously monitor bat activity at 3 heights (30, 10, 2 m) in each habitat type. Variation in vegetative clutter among sampling heights and among habitat types allowed us to examine the differential effect of forest vegetation on the spatial activity patterns of clutter-adapted and open-adapted bat species. Moreover, monitoring activity at 30, 10, and 2 m permitted us to also compare bat activity above and below the forest canopy. We detected calls of 5 species or species groups: eastern red/Seminole bats (Lasiurus borealis/L. seminolus), eastern pipistrelles (Pipistrellus subflavus), evening bats (Nycticeius humeralis), big brown bats (Eptesicus fuscus), and hoary bats (Lasiurus cinerius). At 2 and 10 m, bat activity was concentrated in riparian areas, whereas we detected relatively low levels of bat activity in upland habitats at those heights. Activity was more evenly distributed across the landscape at 30 m. Bat activity levels above the forest canopy were almost 3 times greater than within or below the canopy. We detected significantly greater activity levels of 2 open-adapted species (hoary and big brown bats) above rather than within or below the forest canopy. However, activity levels of 2 clutter-adapted species (eastern red/Seminole bats and eastern pipistrelles) did not differ above, within, or below the forest canopy. Despite classification as a clutter-adapted species, evening bat activity was greater above rather than within or below the forest canopy. We believe our results highlight the importance of riparian areas as foraging habitat for bats in pine-dominated landscapes in the southeastern United States. Although acoustical surveys conducted below forest canopies can provide useful information about species composition and relative activity levels of bats that forage in cluttered environments, our results showing activity above canopy suggest that such data may not accurately reflect relative activity of bats adapted to forage in more open conditions, and therefore may provide an inaccurate picture of bat community assemblage and foraging habitat use.

Vocal Recognition in Mexican Free-Tailed Bats: Do Pups Recognize Mothers?

Abstract Using data collected with thermal imaging technology, we found a major reduction in population estimates of colony size in the Brazilian free-tailed bat (Tadarida brasiliensis) from 54 million, obtained in 1957 without this technology, to 4 million in 6 major cave colonies in the southwestern United States. The 1957 census was based on human visual observations of cave emergence flights that were subject to potentially high errors. The recent census was produced using an accurate, reproducible counting method and based on complete temporal records of colony emergences. Analysis of emergence flights from dusk through darkness also revealed patterns in group behavior that would be difficult to capture without thermal infrared technology. Flow patterns of bats during emergence flights exhibited characteristic single, double, or triple episodes, with the peak flow during the 1st episode. A consistent rhythmic pattern of flow episodes and pauses was revealed across colonies and was independent of emergence tempo.

Individual variation in the isolation calls of Mexican free-tailed bat pups (Tadarida brasiliensis mexicana)

Abstract Mother Mexican free-tailed bats, Tadarida brasiliensis mexicana, produce ‘directive’ calls while searching for pups inside cave maternity roosts. These calls consist of highly repetitive pulses of sound uttered in rapid sequence. Calls are sufficiently intense that they are perceptible above the substantial background noise within roosts at distances of at least 1 m. Calls are stereotyped within individuals, and statistically discriminable between individuals. These characteristics are expected for vocalizations that function for mother—pup reunions, and are shared with directive calls described previously in other bats. Mother T. b. mexicana directive calls are statistically no less discriminable than are the isolation calls of pups. Playback experiments, using recordings made inside the cave colony, show that pups perceive directive calls and are strongly attracted to them.

Ecology of Zoonotic Infectious Diseases in Bats: Current Knowledge and Future Directions

Abstract Near-term pregnant females and female-pup nursing pairs of Mexican free-tailed bats (Tadarida brasiliensis mexicana) were captured from large maternity colonies in central Texas. A total of 337 isolation calls from 20 pups were recorded and nine call parameters were measured from each call either sonagraphically or with a spectrum analyser. Univariate and multivariate analyses of the call parameters show that the calls of different pups are structurally distinct. Discriminant function analysis using a random subset of calls correctly categorized 60·4% to the pup emitting them. These results suggest that the pups have individual vocal signatures. Calls also possess qualities which suggest that they are attractive in nature and easy to locate. Regression analyses show that several call parameters increase in frequency as pups age.

Multiple paternity in wild populations of the garter snake, Thamnophis sirtalis

Bats are hosts to a range of zoonotic and potentially zoonotic pathogens. Human activities that increase exposure to bats will likely increase the opportunity for infections to spill over in the future. Ecological drivers of pathogen spillover and emergence in novel hosts, including humans, involve a complex mixture of processes, and understanding these complexities may aid in predicting spillover. In particular, only once the pathogen and host ecologies are known can the impacts of anthropogenic changes be fully appreciated. Cross‐disciplinary approaches are required to understand how host and pathogen ecology interact. Bats differ from other sylvatic disease reservoirs because of their unique and diverse lifestyles, including their ability to fly, often highly gregarious social structures, long lifespans and low fecundity rates. We highlight how these traits may affect infection dynamics and how both host and pathogen traits may interact to affect infection dynamics. We identify key questions relating to the ecology of infectious diseases in bats and propose that a combination of field and laboratory studies are needed to create data‐driven mechanistic models to elucidate those aspects of bat ecology that are most critical to the dynamics of emerging bat viruses. If commonalities can be found, then predicting the dynamics of newly emerging diseases may be possible. This modelling approach will be particularly important in scenarios when population surveillance data are unavailable and when it is unclear which aspects of host ecology are driving infection dynamics.