Paul M. Cryan

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

Experimental infection of bats with Geomyces destructans causes white-nose syndrome

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.

A comparison of bats and rodents as reservoirs of zoonotic viruses: are bats special?

White-nose syndrome (WNS) has caused recent catastrophic declines among multiple species of bats in eastern North America. The disease’s name derives from a visually apparent white growth of the newly discovered fungus Geomyces destructans on the skin (including the muzzle) of hibernating bats. Colonization of skin by this fungus is associated with characteristic cutaneous lesions that are the only consistent pathological finding related to WNS. However, the role of G. destructans in WNS remains controversial because evidence to implicate the fungus as the primary cause of this disease is lacking. The debate is fuelled, in part, by the assumption that fungal infections in mammals are most commonly associated with immune system dysfunction. Additionally, the recent discovery that G. destructans commonly colonizes the skin of bats of Europe, where no unusual bat mortality events have been reported, has generated further speculation that the fungus is an opportunistic pathogen and that other unidentified factors are the primary cause of WNS. Here we demonstrate that exposure of healthy little brown bats (Myotis lucifugus) to pure cultures of G. destructans causes WNS. Live G. destructans was subsequently cultured from diseased bats, successfully fulfilling established criteria for the determination of G. destructans as a primary pathogen. We also confirmed that WNS can be transmitted from infected bats to healthy bats through direct contact. Our results provide the first direct evidence that G. destructans is the causal agent of WNS and that the recent emergence of WNS in North America may represent translocation of the fungus to a region with a naive population of animals. Demonstration of causality is an instrumental step in elucidating the pathogenesis and epidemiology of WNS and in guiding management actions to preserve bat populations against the novel threat posed by this devastating infectious disease.

Inoculation of bats with European Geomyces destructans supports the novel pathogen hypothesis for the origin of white-nose syndrome.

Bats are the natural reservoirs of a number of high-impact viral zoonoses. We present a quantitative analysis to address the hypothesis that bats are unique in their propensity to host zoonotic viruses based on a comparison with rodents, another important host order. We found that bats indeed host more zoonotic viruses per species than rodents, and we identified life-history and ecological factors that promote zoonotic viral richness. More zoonotic viruses are hosted by species whose distributions overlap with a greater number of other species in the same taxonomic order (sympatry). Specifically in bats, there was evidence for increased zoonotic viral richness in species with smaller litters (one young), greater longevity and more litters per year. Furthermore, our results point to a new hypothesis to explain in part why bats host more zoonotic viruses per species: the stronger effect of sympatry in bats and more viruses shared between bat species suggests that interspecific transmission is more prevalent among bats than among rodents. Although bats host more zoonotic viruses per species, the total number of zoonotic viruses identified in bats (61) was lower than in rodents (68), a result of there being approximately twice the number of rodent species as bat species. Therefore, rodents should still be a serious concern as reservoirs of emerging viruses. These findings shed light on disease emergence and perpetuation mechanisms and may help lead to a predictive framework for identifying future emerging infectious virus reservoirs.

SEASONAL DISTRIBUTION OF MIGRATORY TREE BATS (LASIURUS AND LASIONYCTERIS ) IN NORTH AMERICA

White-nose syndrome (WNS) is an emerging disease of hibernating bats associated with cutaneous infection by the fungus Geomyces destructans (Gd), and responsible for devastating declines of bat populations in eastern North America. Affected bats appear emaciated and one hypothesis is that they spend too much time out of torpor during hibernation, depleting vital fat reserves required to survive the winter. The fungus has also been found at low levels on bats throughout Europe but without mass mortality. This finding suggests that Gd is either native to both continents but has been rendered more pathogenic in North America by mutation or environmental change, or that it recently arrived in North America as an invader from Europe. Thus, a causal link between Gd and mortality has not been established and the reason for its high pathogenicity in North America is unknown. Here we show that experimental inoculation with either North American or European isolates of Gd causes WNS and mortality in the North American bat, Myotis lucifugus. In contrast to control bats, individuals inoculated with either isolate of Gd developed cutaneous infections diagnostic of WNS, exhibited a progressive increase in the frequency of arousals from torpor during hibernation, and were emaciated after 3–4 mo. Our results demonstrate that altered torpor-arousal cycles underlie mortality from WNS and provide direct evidence that Gd is a novel pathogen to North America from Europe.

Wing pathology of white-nose syndrome in bats suggests life-threatening disruption of physiology

Abstract Despite evidence of migration in North American tree bats (genera Lasiurus and Lasionycteris), details regarding seasonal movements in these widely distributed species are few. This study attempted to clarify patterns of seasonal distribution by mapping museum occurrence records by month. Monthly changes in the distribution of records indicate seasonal movements of tree bats. Northward migration during spring by Lasiurus cinereus appears to stem from wintering grounds in California and Mexico. During summer, male L. cinereus is mainly distributed in western North America, whereas females dominate samples from eastern regions. Lasiurus borealis winters in southeastern areas and expands its range into more northern regions during warmer months. Seasonal dispersal of Lasiurus blossevillii from California is apparently limited, and it is unclear if this group mixes with others to the south and east. Lasionycteris noctivagans also shows movement at the continental scale, although movements may differ between western and eastern groups. Museum records provide little evidence of major movement by any species between North and South America. Despite inherent biases, museum records are a viable means of investigating bat migration.

Causes of bat fatalities at wind turbines: hypotheses and predictions.

White-nose syndrome (WNS) is causing unprecedented declines in several species of North American bats. The characteristic lesions of WNS are caused by the fungus Geomyces destructans, which erodes and replaces the living skin of bats while they hibernate. It is unknown how this infection kills the bats. We review here the unique physiological importance of wings to hibernating bats in relation to the damage caused by G. destructans and propose that mortality is caused by catastrophic disruption of wing-dependent physiological functions. Mechanisms of disease associated with G. destructans seem specific to hibernating bats and are most analogous to disease caused by chytrid fungus in amphibians.

White-Nose Syndrome Fungus (Geomyces destructans) in Bats, Europe

Abstract Thousands of industrial-scale wind turbines are being built across the world each year to meet the growing demand for sustainable energy. Bats of certain species are dying at wind turbines in unprecedented numbers. Species of bats consistently affected by turbines tend to be those that rely on trees as roosts and most migrate long distances. Although considerable progress has been made in recent years toward better understanding the problem, the causes of bat fatalities at turbines remain unclear. In this synthesis, we review hypothesized causes of bat fatalities at turbines. Hypotheses of cause fall into 2 general categories—proximate and ultimate. Proximate causes explain the direct means by which bats die at turbines and include collision with towers and rotating blades, and barotrauma. Ultimate causes explain why bats come close to turbines and include 3 general types: random collisions, coincidental collisions, and collisions that result from attraction of bats to turbines. The random collision hypothesis posits that interactions between bats and turbines are random events and that fatalities are representative of the bats present at a site. Coincidental hypotheses posit that certain aspects of bat distribution or behavior put them at risk of collision and include aggregation during migration and seasonal increases in flight activity associated with feeding or mating. A surprising number of attraction hypotheses suggest that bats might be attracted to turbines out of curiosity, misperception, or as potential feeding, roosting, flocking, and mating opportunities. Identifying, prioritizing, and testing hypothesized causes of bat collisions with wind turbines are vital steps toward developing practical solutions to the problem.

STABLE HYDROGEN ISOTOPE ANALYSIS OF BAT HAIR AS EVIDENCE FOR SEASONAL MOLT AND LONG-DISTANCE MIGRATION

Unlike bats in North America, bats in Europe are not killed by this fungus.

Bat flight and zoonotic viruses

Abstract Although hoary bats (Lasiurus cinereus) are presumed to be migratory and capable of long-distance dispersal, traditional marking techniques have failed to provide direct evidence of migratory movements by individuals. We measured the stable hydrogen isotope ratios of bat hair (δDh) and determined how these values relate to stable hydrogen isotope ratios of precipitation (δDp). Our results indicate that the major assumptions of stable isotope migration studies hold true for hoary bats and that the methodology provides a viable means of determining their migratory movements. We present evidence that a single annual molt occurs in L. cinereus prior to migration and that there is a strong relationship between δDh and δDp during the molt period. This presumably reflects the incorporation of local δDp into newly grown hair. Furthermore, we present evidence that individual hoary bats are capable of traveling distances in excess of 2,000 km and that hair is grown at a wide range of latitudes and elevations. Stable hydrogen isotope analysis offers a promising new tool for the study of bat migration.