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

Summary 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.

[1]  A. Gargas,et al.  Geomyces destructans sp. nov. associated with bat white-nose syndrome. , 2009 .

[2]  P. Cryan,et al.  White-Nose Syndrome Fungus (Geomyces destructans) in Bats, Europe , 2010, Emerging infectious diseases.

[3]  C. Graham,et al.  Selecting pseudo-absence data for presence-only distribution modeling: How far should you stray from what you know? , 2009 .

[4]  A. Peterson,et al.  Modeling ecological niches and predicting geographic distributions: a test of six presence-only methods Modelado de nichos ecológicos y predicción de distribuciones geográfi cas: comparación de seis métodos , 2008 .

[5]  Alan C. Hicks,et al.  Morphological and Molecular Characterizations of Psychrophilic Fungus Geomyces destructans from New York Bats with White Nose Syndrome (WNS) , 2010, PloS one.

[6]  A. Gargas,et al.  Histopathologic Criteria to Confirm White-nose Syndrome in Bats , 2009, Journal of veterinary diagnostic investigation : official publication of the American Association of Veterinary Laboratory Diagnosticians, Inc.

[7]  A. Peterson,et al.  Effects of sample size on the performance of species distribution models , 2008 .

[8]  Miguel Nakamura Savoy Predicting species distributions from small numbers of occurrence records: a test case using cryptic geckos in Madagascar , 2007 .

[9]  Sunil Kumar,et al.  Spatial heterogeneity influences native and nonnative plant species richness. , 2006, Ecology.

[10]  J. Boyles,et al.  Could localized warm areas inside cold caves reduce mortality of hibernating bats affected by white-nose syndrome? , 2010 .

[11]  Richard S Ostfeld,et al.  Investigating and managing the rapid emergence of white-nose syndrome, a novel, fatal, infectious disease of hibernating bats. , 2011, Conservation biology : the journal of the Society for Conservation Biology.

[12]  D. Gutiérrez,et al.  HABITAT DISTRIBUTION MODELS: ARE MUTUALIST DISTRIBUTIONS GOOD PREDICTORS OF THEIR ASSOCIATES? , 2005 .

[13]  W. Davis Chapter 8 – Hibernation: Ecology and Physiological Ecology , 1970 .

[14]  Miroslav Dudík,et al.  Modeling of species distributions with Maxent: new extensions and a comprehensive evaluation , 2008 .

[15]  S. Puechmaille,et al.  Pan-European Distribution of White-Nose Syndrome Fungus (Geomyces destructans) Not Associated with Mass Mortality , 2011, PloS one.

[16]  C. White,et al.  RECOVERY OF LITTLE BROWN BATS (MYOTIS LUCIFUGUS) FROM NATURAL INFECTION WITH GEOMYCES DESTRUCTANS, WHITE-NOSE SYNDROME , 2011, Journal of wildlife diseases.

[17]  Robert E. Wolfe,et al.  Vegetation Phenology Metrics Derived from Temporally Smoothed and Gap-Filled MODIS Data , 2008, IGARSS 2008 - 2008 IEEE International Geoscience and Remote Sensing Symposium.

[18]  D. Reeder,et al.  A Five-year Assessment of Mortality and Geographic Spread of White-Nose Syndrome in North American Bats, with a Look at the Future. Update of White-Nose Syndrome in Bats. , 2011 .

[19]  Steven J. Phillips,et al.  Sample selection bias and presence-only distribution models: implications for background and pseudo-absence data. , 2009, Ecological applications : a publication of the Ecological Society of America.

[20]  A. Townsend Peterson,et al.  Novel methods improve prediction of species' distributions from occurrence data , 2006 .

[21]  Sunil Kumar,et al.  Maxent modeling for predicting suitable habitat for threatened and endangered tree Canacomyrica monticola in New Caledonia , 2009 .

[22]  Richard Speare,et al.  Assessing spatial patterns of disease risk to biodiversity: Implications for the management of the amphibian pathogen, Batrachochytrium dendrobatidis , 2011 .

[23]  Z. Hubálek,et al.  Increasing Incidence of Geomyces destructans Fungus in Bats from the Czech Republic and Slovakia , 2010, PloS one.

[24]  B. Benito,et al.  Assessing extinction-risk of endangered plants using species distribution models: a case study of habitat depletion caused by the spread of greenhouses , 2009, Biodiversity and Conservation.

[25]  K. Abromeit Music Received , 2023, Notes.

[26]  Robert J. Rudd,et al.  Bat White-Nose Syndrome: An Emerging Fungal Pathogen? , 2009, Science.

[27]  D. Reeder,et al.  Experimental infection of bats with Geomyces destructans causes white-nose syndrome , 2011, Nature.

[28]  S. Puechmaille,et al.  White-nose syndrome: is this emerging disease a threat to European bats? , 2011, Trends in ecology & evolution.

[29]  Sunil Kumar,et al.  Potential habitat distribution for the freshwater diatom Didymosphenia geminata in the continental US , 2009 .

[30]  J. Speakman,et al.  How hot is a hibernaculum? A review of the temperatures at which bats hibernate , 1996 .

[31]  S. Puechmaille,et al.  White-Nose Syndrome Fungus (Geomyces destructans) in Bat, France , 2010, Emerging infectious diseases.

[32]  M. Wojciechowski,et al.  Evaporative water loss is a plausible explanation for mortality of bats from white-nose syndrome. , 2011, Integrative and comparative biology.

[33]  R. Ransome The natural history of hibernating bats , 1990 .

[34]  T. Kunz,et al.  An Emerging Disease Causes Regional Population Collapse of a Common North American Bat Species , 2010, Science.

[35]  J. Speakman,et al.  Climate-mediated energetic constraints on the distribution of hibernating mammals , 2002, Nature.

[36]  A. Peterson,et al.  Ecologic Niche Modeling of Blastomyces dermatitidis in Wisconsin , 2008, PloS one.

[37]  R. Alford,et al.  Distribution models for the amphibian chytrid Batrachochytrium dendrobatidis in Costa Rica: proposing climatic refuges as a conservation tool , 2009 .

[38]  Robert P. Anderson,et al.  Maximum entropy modeling of species geographic distributions , 2006 .

[39]  J. Boyles,et al.  Body temperature and body mass of hibernating little brown bats Myotis lucifugus in hibernacula affected by white-nose syndrome , 2011, Acta Theriologica.

[40]  John Bell,et al.  A review of methods for the assessment of prediction errors in conservation presence/absence models , 1997, Environmental Conservation.

[41]  B. McNab THE BEHAVIOR OF TEMPERATE CAVE BATS IN A SUBTROPICAL ENVIRONMENT , 1974 .

[42]  Alan C. Hicks,et al.  Little Brown Myotis Persist Despite Exposure to White-Nose Syndrome , 2011 .

[43]  T. Kunz,et al.  DNA-based detection of the fungal pathogen Geomyces destructans in soils from bat hibernacula , 2011, Mycologia.

[44]  P. Cryan,et al.  Wing pathology of white-nose syndrome in bats suggests life-threatening disruption of physiology , 2010, BMC Biology.

[45]  A. Townsend Peterson,et al.  Modelado de nichos ecológicos y predicción de distribuciones geográficas: comparación de seis métodos , 2008 .

[46]  P. Hernandez,et al.  The effect of sample size and species characteristics on performance of different species distribution modeling methods , 2006 .

[47]  Jeffrey T. Morisette,et al.  Bounding Species Distribution Models , 2011 .

[48]  Journal of Applied Ecology , 1965, Nature.