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Paul M. Cryan

Publications and source records attributed to Paul M. Cryan.

At least 55 records · Page 3Linked to original sources

Pathophysiology of white-nose syndrome in bats: A mechanistic model linking wing damage to mortality

White-nose syndrome is devastating North American bat populations but we lack basic information on disease mechanisms. Altered blood physiology owing to epidermal invasion by the fungal pathogen Geomyces destructans ( Gd ) has been hypothesized as a cause of disrupted torpor patterns of affected hibernating bats, leading to mortality. Here, we present data on blood electrolyte concentration, haematology and acid–base balance of hibernating little brown bats, Myotis lucifugus , following experimental inoculation with Gd . Compared with controls, infected bats showed electrolyte depletion (i.e. lower plasma sodium), changes in haematology (i.e. increased haematocrit and decreased glucose) and disrupted acid–base balance (i.e. lower CO 2 partial pressure and bicarbonate). These findings indicate hypotonic dehydration, hypovolaemia and metabolic acidosis. We propose a mechanistic model linking tissue damage to altered homeostasis and morbidity/mortality.

Biology Letters

On estimating the economic value of insectivorous bats: Prospects and priorities for biologists

Bats are among the most economically important nondomesticated mammals in the world. They are well-known pollinators and seed dispersers, but crop pest suppression is probably the most valuable ecosystem service provided by bats. Scientific literature and popular media often include reports of crop pests in the diet of bats and anecdotal or extrapolated estimates of how many insects are eaten by bats. However, quantitative estimates of the ecosystem services provided by bats in agricultural systems are rare, and the few estimates that are available are limited to a single cotton-dominated system in Texas. Despite the tremendous value for conservation and economic security of such information, surprisingly few scientific efforts have been dedicated to quantifying the economic value of bats. Here, we outline the types of information needed to better quantify the value of bats in agricultural ecosystems. Because of the complexity of the ecosystems involved, creative experimental design and innovative new methods will help advance our knowledge in this area. Experiments involving bats in agricultural systems may be needed sooner than later, before population declines associated with white-nose syndrome and wind turbines potentially render them impossible.

Book chapter

Roost selection by western long-eared myotis (Myotis evotis) in burned and unburned piñon–juniper woodlands of southwestern Colorado

All 16 species of bats known to occur in western Colorado are found at Mesa Verde National Park (MVNP) in the southwestern United States. Since 1996, wildfires have burned more than 70% of MVNP (> 15,000 ha), potentially altering food and roosting resources for bats. During the summers of 2006–2007, we investigated roost use by reproductive female western long-eared myotis ( Myotis evotis ). We located 33 bat roosts in rock crevices and 1 in a juniper snag. All but 2 of the roosts were in unburned habitat. Bats roosted alone or in small groups (≤3 individuals) and switched roosts frequently (1–7 roosts per bat, median = 1.5 roosts per bat, SE = 0.5 roosts per bat). We compared occupied roosts with randomly selected unoccupied crevices and used an information theoretic approach to determine which variables were most important in determining roost use at microhabitat and landscape scales. At the microhabitat scale, maternity roosts were higher above the ground and deeper than random, unoccupied rock crevices. At the landscape scale, roosts were closer to water and farther from burned habitat than random crevices, providing reproductive female M. evotis with the best opportunities to drink and forage for insects. Tree roosts are apparently not a vital resource for reproductive female M. evotis during the summer months at our study site, presumably because of the extensive availability of rock crevices. Understanding site-specific roosting behavior is important for proper management of bat populations because differences can exist between geographic regions, even among areas with similar plant communities.

Colorado

White-nose syndrome in bats: Illuminating the darkness

Happy ten-year anniversary to BMC Biology! We can attest to the effectiveness of the journal in reaching a great diversity of scientists based on reader responses to our commentary [1] about bat white-nose syndrome (WNS) two years ago. WNS is still on course to rank among the most destructive wildlife diseases to emerge in recent history, and it has continued to have unprecedented effects on populations of hibernating bats in eastern North America. At the time of our last writing in November 2010, the cold-adapted fungus then presumed to cause WNS ( Geomyces destructans ) had spread about 1,300 km from an index site in New York (Figure 1). In those early years of the epizootic, WNS caused a staggering wave of mass mortality among all six species of hibernating bats that occur in north-eastern North America. Since November 2010, WNS has spread into eight additional US states and two more Canadian provinces (Figure 1), and has continued to cause mortality in those six species most affected during the early years of the epizootic. Although part of a mostly tragic story has continued to unfold as new areas are affected, anecdotal signs are emerging that all may not be lost when it comes to hibernating bats and WNS. Amid the continued large-scale population declines of certain species, we have yet to see mass mortality in some of the more westerly areas where the fungus was detected two winters ago (Figure 1). Also, recently disease without obvious mortality was diagnosed in gray bats ( Myotis grisescens ) - an endangered species thought by many two years ago to be at high risk of extinction from WNS. Clearly, large gaps in our understanding of WNS remain, but some have been filled since we last communicated with readers of BMC Biology.

BMC Biology

Insect prey eaten by Hoary Bats ( Lasiurus cinereus ) prior to fatal collisions with wind turbines

Wind turbines are being deployed all across the world to meet the growing demand for energy, and in many areas, these turbines are causing the deaths of insectivorous migratory bats. One of the hypothesized causes of bat susceptibility is that bats are attracted to insects on or near the turbines. We examined insect remains in the stomachs and intestines of hoary bats ( Lasiurus cinereus ) found dead beneath wind turbines in New York and Texas to evaluate the hypothesis that bats die while feeding at turbines. Most of the bats we examined had full stomachs, indicating that they fed in the minutes to hours leading up to their deaths. However, we did not find prey in the mouths or throats of any bats that would indicate the bats died while capturing prey. Hoary bats fed mostly on moths, but we also detected the regular presence of beetles, true bugs, and crickets. Presence of terrestrial insects in stomachs indicates that bats may have gleaned them from the ground or the turbine surfaces, yet aerial capture of winged insect stages cannot be ruled out. Our findings confirm earlier studies that indicate hoary bats feed during migration and eat mostly moths. Future studies on bat behaviors and insect presence at wind turbines could help determine whether feeding at turbines is a major fatality risk for bats.

Western North American Naturalist

Electrolyte depletion in white-nose syndrome bats

The emerging wildlife disease white-nose syndrome is causing widespread mortality in hibernating North American bats. White-nose syndrome occurs when the fungus Geomyces destructans infects the living skin of bats during hibernation, but links between infection and mortality are underexplored. We analyzed blood from hibernating bats and compared blood electrolyte levels to wing damage caused by the fungus. Sodium and chloride tended to decrease as wing damage increased in severity. Depletion of these electrolytes suggests that infected bats may become hypotonically dehydrated during winter. Although bats regularly arouse from hibernation to drink during winter, water available in hibernacula may not contain sufficient electrolytes to offset winter losses caused by disease. Damage to bat wings from G. destructans may cause life-threatening electrolyte imbalances.

Journal of Wildlife Diseases

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

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.

Proceedings of the Royal Society B

Evidence of cryptic individual specialization in an opportunistic insectivorous bat

Habitat use and feeding behaviors of cryptic animals are often poorly understood. Analyses of stable isotope ratios in animal body tissues can help reveal an individual's location and resource use during tissue growth. We investigated variation in stable isotope ratios of 4 elements (H, C, N, and S) in the hair of a sedentary species of insectivorous bat (Eptesicus fuscus) inhabiting a chemically complex urban landscape. Our objective was to quantify population-level isotopic variation and test for evidence of resource specialization by individuals. Bats were sampled over 3 annual molt cycles at maternity roosts in buildings and variance components analysis was used to test whether intraindividual isotopic variation among molts differed from interindividual variation, after controlling for year and roost-group effects. Consistent with prior evidence that E. fuscus is opportunistic in its habitat use and foraging at the population level, we observed wide population-level variation for all isotopes. This variation likely reflects the chemical complexity of the urban landscape studied. However, isotopic variation among years within marked individuals was lower than variation among marked individuals within year for all isotopes, and carbon signatures indicated resource specialization by roost groups and individuals. This is the 1st study to examine variation in stable isotope ratios of individual wild bats over multiple years. Although our results suggest this population tends toward opportunistic habitat use or prey selection, or both, during molt periods, results also indicate that individuals and groups of bats composing the population might be habitat or dietary specialists—a novel finding for insectivorous bats.

Journal of Mammalogy

Environmental conditions associated with bat white-nose syndrome in the north-eastern United States

1. White-nose syndrome (WNS) is an emerging disease of hibernating North American bats that is caused by the cold-growing fungus Geomyces destructans . Since first observed in the winter of 2007, WNS has led to unprecedented mortality in several species of bats and may threaten more than 15 additional hibernating bat species if it continues across the continent. Although the exact means by which fungal infection causes mortality are undetermined, available evidence suggests a strong role of winter environmental conditions in disease mortality. 2. By 2010, the fungus G. destructans was detected in new areas of North America far from the area it was first observed, as well as in eight European bat species in different countries, yet mortality was not observed in many of these new areas of North America or in any part of Europe. This could be because of the differences in the fungus, rates of disease progression and/or in life-history or physiological traits of the affected bat species between different regions. Infection of bats by G. destructans without associated mortality might also suggest that certain environmental conditions might have to co-occur with fungal infection to cause mortality. 3. We tested the environmental conditions hypothesis using Maxent to map and model landscape surface conditions associated with WNS mortality. This approach was unique in that we modelled possible requisite environmental conditions for disease mortality and not simply the presence of the causative agent. 4. The top predictors of WNS mortality were land use/land cover types, mean air temperature of wettest quarter, elevation, frequency of precipitation and annual temperature range. Model results suggest that WNS mortality is most likely to occur in landscapes that are higher in elevation and topographically heterogeneous, drier and colder during winter, and more seasonally variable than surrounding landscapes. 5. Synthesis and applications . This study mapped the most likely environmental surface conditions associated with bat mortality owing to WNS in the north-eastern United Sates; maps can be used for selection of priority monitoring sites. Our results provide a starting point from which to investigate and predict the potential spread and population impacts of this catastrophic emerging disease.

Journal of Applied Ecology

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

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.

Proceedings of the National Academy of Sciences

Bat ecology and public health surveillance for rabies in an urbanizing region of Colorado

We describe use of Fort Collins, Colorado, and nearby areas by bats in 2001–2005, and link patterns in bat ecology with concurrent public health surveillance for rabies. Our analyses are based on evaluation of summary statistics, and information-theoretic support for results of simple logistic regression. Based on captures in mist nets, the city bat fauna differed from that of the adjacent mountains, and was dominated by big brown bats ( Eptesicus fuscus ). Species, age, and sex composition of bats submitted for rabies testing locally and along the urbanizing Front Range Corridor were similar to those of the mist-net captures and reflected the annual cycle of reproduction and activity of big brown bats. Few submissions occurred November- March, when these bats hibernated elsewhere. In summer females roosted in buildings in colonies and dominated health samples; fledging of young corresponded to a summer peak in health submissions with no increase in rabies prevalence. Roosting ecology of big brown bats in buildings was similar to that reported for natural sites, including colony size, roost-switching behavior, fidelity to roosts in a small area, and attributes important for roost selection. Attrition in roosts occurred from structural modifications of buildings to exclude colonies by citizens, but without major effects on long-term bat reproduction or survival. Bats foraged in areas set aside for nature conservation. A pattern of lower diversity in urban bat communities with dominance by big brown bats may occur widely in the USA, and is consistent with national public health records for rabies surveillance.

Colorado

Investigating and managing the rapid emergence of white-nose syndrome, a novel, fatal, infectious disease of hibernating bats

White-nose syndrome (WNS) is a fatal disease of bats that hibernate. The etiologic agent of WNS is the fungus Geomyces destructans , which infects the skin and wing membranes. Over 1 million bats in six species in eastern North America have died from WNS since 2006, and as a result several species of bats may become endangered or extinct. Information is lacking on the pathogenesis of G. destructans and WNS, WNS transmission and maintenance, individual and site factors that contribute to the probability of an outbreak of WNS, and spatial dynamics of WNS spread in North America. We considered how descriptive and analytical epidemiology could be used to fill these information gaps, including a four-step (modified) outbreak investigation, application of a set of criteria (Hill's) for assessing causation, compartment models of disease dynamics, and spatial modeling. We cataloged and critiqued adaptive-management options that have been either previously proposed for WNS or were helpful in addressing other emerging diseases of wild animals. These include an ongoing program of prospective surveillance of bats and hibernacula for WNS, treatment of individual bats, increasing population resistance to WNS (through vaccines, immunomodulators, or other methods), improving probability of survival from starvation and dehydration associated with WNS, modifying hibernacula environments to eliminate G. destructans , culling individuals or populations, controlling anthropogenic spread of WNS, conserving genetic diversity of bats, and educating the public about bats and bat conservation issues associated with WNS.

Conservation Biology

Economic importance of bats in 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 $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.

Science

Bat white-nose syndrome in North America

* The newly described fungus, Geomyces destructans, causes an invasive skin infection in bats and is the likely agent of white-nose syndrome (WNS). * With immune system functions and body temperatures reduced during hibernation, bats may be unusually susceptible to a pathogenic fungus such as G. destructans. * WNS was first observed in a popular show cave near Albany, New York, leading some investigators to suspect that a visitor inadvertently introduced G. destructans at this site, triggering a wider WNS outbreak in North America. * Biologists trying to manage WNS within North American bat populations face major challenges, including the variety of susceptible host species, incredible dispersal capabilities of bats, difficulties in treating such populations, and persistence of the pathogen in their vulnerable underground habitats.

Microbe Magazine

Bats of Mesa Verde National Park, Colorado: Composition, reproduction, and roosting habits

We determined the bat fauna at Mesa Verde National Park (Mesa Verde) in 2006 and 2007, characterized bat elevational distribution and reproduction, and investigated roosting habits of selected species. We captured 1996 bats of 15 species in mist nets set over water during 120 nights of sampling and recorded echolocation calls of an additional species. The bat fauna at Mesa Verde included every species of bat known west of the Great Plains in Colorado, except the little brown bat ( Myotis lucifugus ). Some species showed skewed sex ratios, primarily due to a preponderance of males. Thirteen species of bats reproduced at Mesa Verde. Major differences in spring precipitation between the 2 years of our study were associated with differences in reproductive rates and, in some species, with numbers of juveniles captured. Reduced reproductive effort during spring drought will have a greater impact on bat populations with the forecasted increase in aridity in much of western North America by models of global climate change. We radiotracked 46 bats of 5 species to roosts and describe the first-known maternity colonies of spotted bats ( Euderma maculatum ) in Colorado. All 5 species that we tracked to diurnal roosts relied almost exclusively on rock crevices rather than trees or snags, despite the presence of mature forests at Mesa Verde and the use of trees for roosts in similar forests elsewhere by some of these species. Comparisons with past bat surveys at Mesa Verde and in surrounding areas suggest no dramatic evidence for effects of recent stand-replacing fires on the composition of the bat community.

Colorado

Wind Turbines as Landscape Impediments to the Migratory Connectivity of Bats

Unprecedented numbers of migratory bats are found dead beneath industrial-scale wind turbines during late summer and autumn in both North America and Europe. Prior to the wide-scale deployment of wind turbines, fatal collisions of migratory bats with anthropogenic structures were rarely reported and likely occurred very infrequently. There are no other well-documented threats to populations of migratory tree bats that cause mortality of similar magnitude to that observed at wind turbines. Just three migratory species comprise the vast majority of bat kills at turbines in North America and there are indications that turbines may actually attract migrating individuals toward their blades. Although fatality of certain migratory species is consistent in occurrence across large geographic regions, fatality rates differ across sites for reasons mostly unknown. Cumulative fatality for turbines in North America might already range into the hundreds of thousands of bats per year. Research into the causes of bat fatalities at wind turbines can ascertain the scale of the problem and help identify solutions. None of the migratory bats known to be most affected by wind turbines are protected by conservation laws, nor is there a legal mandate driving research into the problem or implementation of potential solutions.

Environmental Law