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Volume 21, Number 6—June 2015

Dispatch

Invasion Dynamics of White-Nose Syndrome Fungus, Midwestern United States, 2012–2014

Kate E. Langwig1, Jiang Feng1, Katy L. Parise, Joe Kath, Dan Kirk, Winifred F. Frick, Jeffrey T. Foster, and A. Marm KilpatrickComments to Author 
Author affiliations: University of California, Santa Cruz, California, USA (K.E. Langwig, J.R. Hoyt, W.F. Frick, A.M. Kilpatrick); Northern Arizona University, Flagstaff, Arizona, USA (K.L. Parise, J.T. Foster); Illinois Department of Natural Resources, Springfield, Illinois, USA (J. Kath, D. Kirk); University of New Hampshire, Durham, New Hampshire, USA (J.T. Foster)

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EID Langwig KE, Feng J, Parise KL, Kath J, Kirk D, Frick WF, et al. Invasion Dynamics of White-Nose Syndrome Fungus, Midwestern United States, 2012–2014. Emerg Infect Dis. 2015;21(6):1023-1026. https://dx.doi.org/10.3201/eid2106.150123
AMA Langwig KE, Feng J, Parise KL, et al. Invasion Dynamics of White-Nose Syndrome Fungus, Midwestern United States, 2012–2014. Emerging Infectious Diseases. 2015;21(6):1023-1026. doi:10.3201/eid2106.150123.
APA Langwig, K. E., Feng, J., Parise, K. L., Kath, J., Kirk, D., Frick, W. F....Kilpatrick, A. (2015). Invasion Dynamics of White-Nose Syndrome Fungus, Midwestern United States, 2012–2014. Emerging Infectious Diseases, 21(6), 1023-1026. https://dx.doi.org/10.3201/eid2106.150123.

Abstract

White-nose syndrome has devastated bat populations in eastern North America. In Midwestern United States, prevalence increased quickly in the first year of invasion (2012–13) but with low population declines. In the second year (2013–14), environmental contamination led to earlier infection and high population declines. Interventions must be implemented before or soon after fungal invasion to prevent population collapse.

Invasion of novel wildlife diseases has caused widespread declines or species extinction among birds, amphibians, and mammals (14). White-nose syndrome (WNS), caused by the fungal pathogen Pseudogymnoascus destructans, is a recently emerged disease of hibernating bats (5) that has caused substantial declines in 6 species; bats of 2 species are predicted to become globally extinct (3). In little brown bats (Myotis lucifugus), tissue damage from fungal infection results in a cascade of physiologic disruptions resulting in death 70–100 days after infection (6).

Although the seasonal dynamics of P. destructans were recently characterized (7), the dynamics of P. destructans invasion of new sites has yet to be described. In the 2 years since the identification of P. destructans, the extent of the population decline differed each year and among species for unknown reasons (3). Furthermore, the role of P. destructans in the environment remains unclear (8) because no study has reported co-occurring patterns of P. destructans in bats and on substrates. We hypothesized that yearly differences in death rates result from changes in the timing of infection as P. destructans becomes established and that the environment serves as a source of infection for bats (bats that leave summer maternity sites are not infected; 7).

The Study

To test our hypothesis, we studied the invasion dynamics of the WNS fungus by sampling bats of 5 species at 2 hibernacula in central Illinois, USA. We collected samples twice each winter for 2 years (2012–13 and 2013–14). The hibernacula were moderately sized (5–10 hectares, 2–5 m high) abandoned limestone mines that bats use for fall mating and hibernation from September through April. During each visit, we counted all visible bats at each site, which produced complete census data for 4 of the 5 species. Accurately collecting census data for bats of the remaining species (Eptesicus fuscus) was difficult because these bats, unlike those of other species, roosted primarily behind crumbling slabs of rock around mine entrances, which were dangerous and difficult to survey.

During each site visit we sampled 15–20 bats of each species by epidermal swabbing (7). We also sampled the wall or ceiling of hibernacula under, near (10–20 cm), and far from (>2 m) roosting bats by using the same swabbing technique. Samples were tested for P. destructans by using real-time PCR (9); according to a serial dilution experiment, the limit of detection was ≈50 conidia.

Figure 1

Thumbnail of Pseudogymnoascus destructans prevalence (±1 SE, calculated from the variance of a binomial distribution sample) over 2 winters, 2012–13 and 2013–14, at 2 sites (diamonds and triangles) in Illinois, USA, on bats of 5 species (A, B); prevalence of P. destructans on substrate under bats of each species (C, D; dashed lines), and prevalence of P. destructans under, near (10–20 cm), and far from (>2 m) bats (E, F). No substrate samples far from bats were taken in the first winter. Line

Figure 1. Pseudogymnoascus destructans prevalence (±1 SE, calculated from the variance of a binomial distribution sample) over 2 winters, 2012–13 and 2013–14, at 2 sites (diamonds and triangles) in Illinois, USA, on bats...

We obtained 611 samples from bats and 444 from substrate. In early winter of 2012–13, only 1 individual (Myotis septentrionalis) of 129 bats of 5 species sampled was positive for P. destructans, and none of the 46 substrate samples were positive (Figure 1, panels A, C, E). Just 4 months later, in March 2013, prevalence was >85% for bats of 2 species (M. septentrionalis, M. lucifugus), 40%–75% for 2 species (E. fuscus, Myotis sodalis), and 15%–60% for 1 species (Perimyotis subflavus) at the 2 sites (Figure 1, panel A). The prevalence of P. destructans on the substrate under these bats varied from 0% to 67%, and substrate prevalence paralleled fungal prevalence for bats of each species (Figure 1, panel C). Despite widespread apparent infection of bats at this time, none of the 36 substrate samples taken just 10–20 cm from bats were positive for P. destructans (Figure 1, panel E).

In early winter of the next year (late November 2013), patterns differed markedly from those of the previous early winter. P. destructans was already widespread in the environment, found in 70% of samples from under bats, 22% of samples 10–20 cm from bats, and 14% of samples >2 m from bats (Figure 1, panels D, F). Prevalence among bats of 4 species was already >70%, and prevalence among bats of 1 of these species (P. subflavus), for which prevalence at the end of the previous winter had been lowest, was already 85%–100% (Figure 1, panel B). By the end of the second winter, 109 (98%) of 111 bats were positive for P. destructans, and P. destructans was present throughout the hibernacula (in 91% of samples from under bats, 66% of samples near bats, and 44% of samples far from bats) (Figure 1, panels B,D,F).

Figure 2

Thumbnail of Complete population counts on a log scale of 4 species of bats at 2 sites in Illinois, USA, over 2 winters, 2012–13 and 2013–14. Diamonds and triangles indicate sites.

Figure 2. Complete population counts on a log scale of 4 species of bats at 2 sites in Illinois, USA, over 2 winters, 2012–13 and 2013–14. Diamonds and triangles indicate sites.

Over these 2 years, the effect of WNS on bat populations mirrored the patterns of P. destructans prevalence. During the first winter, declines were limited at the larger site and moderate (50%–75%) at the smaller site (Figure 2). In contrast, over the second winter, counts of M. septentrionalis bats declined by 95%–99% and M. lucifugus bats by 81%–88% (20,000 bats of this species disappeared) (Figure 2, panel A). Populations of bats of the 2 other species also experienced moderate to severe declines in the second year (M. sodalis, 16%–96%; P. subflavus, 47%–73%) (Figure 2, panel B). Declines probably resulted from disease-related deaths because high hibernacula site fidelity makes emigration unlikely (10) and substantial numbers of dead bats were observed at both sites.

Conclusions

Early in the first winter studied, prevalence of P. destructans was very low, and although transmission resulted in most bats harboring P. destructans by winters’ end, declines in bat populations were limited. In contrast, early in the second winter, fungal prevalence among bats was already high and severe communitywide declines occurred over the next 4 months. The earlier timing of exposure in the second year would be expected to increase the effects of WNS because by winter’s end most bats would have been infected and in hibernation for at least 70–100 days (the approximate time between infection and death; 5). Few would be able to survive until spring, when bats cease hibernating and clear the fungus (7).

Patterns of P. destructans distribution in the environment mirrored prevalence among bats and population declines. Early in the first year, when P. destructans was rare on hibernacula substrates, most bats were not infected in early winter, and 4 months later, P. destructans was not detectable in one third of bats of 3 species. However, by the end of the first winter, P. destructans was present on hibernacula substrate under bats, probably resulting from bats shedding P. destructans into the environment. At the beginning of the following winter, P. destructans was widespread in the environment, and nearly all bats had fungus on them. The widespread occurrence of P. destructans in the environment at this time may have contributed to higher prevalence among bats because most bats clear infections during the summer, when their body temperature is too high for P. destructans growth (7,11). Long-term persistence of P. destructans in the absence of bats (8,12) suggests that an environmental reservoir of P. destructans may contribute to WNS persistence, as occurs for other diseases, such as cholera (13).

WNS continues to spread south, west, and north from New York, where it was first detected in 2006, and continues to cause widespread bat population declines. Potential control strategies include development of probiotic treatments (14) and alteration of hibernacula microclimates to make them cooler and drier (3,15). Our results suggest that if P. destructans invasion in other sites is similar to what we documented in Illinois, interventions must be implemented proactively, or quickly after P. destructans invasion, to prevent collapse of bat communities. Reduced bat populations will probably have a negative effect on humans because bats play a useful role in ecosystems by consuming disease vectors and many forest and agricultural insect pests.

Dr. Langwig is a disease ecologist at the University of California, Santa Cruz. Her research interests include epidemiology, population and community ecology, and conservation. Mr. Hoyt is a conservation biologist and disease ecologist at the University of California, Santa Cruz. His research interests include animal behavior and host–microbe interactions.

Acknowledgments

We thank the members of the Illinois and Wisconsin Departments of Natural Resources; the volunteers; and T. Cheng, M. Hee, R. Von Linden, and A. Janicki for assistance with the bat censuses and sampling. We also thank the undergraduate volunteers at Northern Arizona University for assistance with molecular work.

Financial support was provided by the National Science Foundation (grants DGE-0741448, DEB-1115895, DEB-1336290, and EF-0914866), Bat Conservation International, and National Geographic. All work was performed under protocol FrickW1106 and approved by the University of California, Santa Cruz, Institutional Animal Care and Use Committee.

References

  1. LaDeau SL, Kilpatrick AM, Marra PP. West Nile virus emergence and large-scale declines of North American bird populations. Nature. 2007;447:7103. DOIPubMed
  2. Lips KR, Brem F, Brenes R, Reeve JD, Alford RA, Voyles J, Emerging infectious disease and the loss of biodiversity in a Neotropical amphibian community. Proc Natl Acad Sci U S A. 2006;103:316570. DOIPubMed
  3. Langwig KE, Frick WF, Bried JT, Hicks AC, Kunz TH, Kilpatrick AM. Sociality, density-dependence and microclimates determine the persistence of populations suffering from a novel fungal disease, white-nose syndrome. Ecol Lett. 2012;15:10507. DOIPubMed
  4. Vredenburg VT, Knapp RA, Tunstall TS, Briggs CJ. Dynamics of an emerging disease drive large-scale amphibian population extinctions. Proc Natl Acad Sci U S A. 2010;107:968994. DOIPubMed
  5. Warnecke L, Turner JM, Bollinger TK, Lorch JM, Misrae V, Cryan PM, Inoculation of bats with European Geomyces destructans supports the novel pathogen hypothesis for the origin of white-nose syndrome. Proc Natl Acad Sci U S A. 2012;109:69997003. DOIPubMed
  6. Warnecke L, Turner JM, Bollinger TK, Misra V, Cryan PM, Blehert DS, Pathophysiology of white-nose syndrome in bats: a mechanistic model linking wing damage to mortality. Biol Lett. 2013;9:20130177. DOIPubMed
  7. Langwig KE, Frick WF, Reynolds R, Parise KL, Drees KP, Hoyt JR, Host and pathogen ecology drive the seasonal dynamics of a fungal disease, white-nose syndrome. Proc Biol Sci. 2015;282:20142335.PubMed
  8. Lorch JM, Muller LK, Russell RE, O’Connor M, Lindner DL, Blehert DS. Distribution and environmental persistence of the causative agent of white-nose syndrome, Geomyces destructans, in bat hibernacula of the eastern United States. Appl Environ Microbiol. 2013;79:1293301. DOIPubMed
  9. Muller LK, Lorch JM, Lindner DL, O'Connor M, Gargas A, Blehert DS. Bat white-nose syndrome: a real-time TaqMan polymerase chain reaction test targeting the intergenic spacer region of Geomyces destructans. Mycologia. 2013;105:2539. DOIPubMed
  10. Davis WH, Hitchcock HB. Biology and migration of the bat, Myotis lucifugus, in New England. J Mammal. 1965;46:296313. DOI
  11. Verant ML, Boyles JG, Waldrep W, Wibbelt G, Blehert DS. Temperature-dependent growth of Geomyces destructans, the fungus that causes bat white-nose syndrome. PLoS ONE. 2012;7:e46280. DOIPubMed
  12. Hoyt JR, Okoniewski J, Langwig KE, Frick WF, Stone WB, Kilpatrick AM. Long-term persistence of Pseudogymnoascus destructans, the causative agent of white-nose syndrome, in the absence of bats. EcoHealth. 2014 [cited 2014 Sep 29].
  13. King AA, Ionides EL, Pascual M, Bouma MJ. Inapparent infections and cholera dynamics. Nature. 2008;454:87780. DOIPubMed
  14. Hoyt JR, Cheng TL, Langwig KE, Hee MM, Frick WF, Kilpatrick AM. Bacteria isolated from bats inhibit the growth of Pseudogymnoascus destructans, the causative agent of white-nose syndrome. PLoS ONE. 2015;10:e0121329 http://dx.doi.10.1371/journal.pone.0121329. DOIPubMed
  15. Langwig KE, Voyles J, Wilber MQ, Frick WF, Murray KA, Bolker BM, Context- dependent conservation responses to emerging wildlife diseases. Front Ecol Environ [cited 2015 May 1]. http://dx.doi.10.1890/140241

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Cite This Article

DOI: 10.3201/eid2106.150123

1These authors contributed equally to this article.

Table of Contents – Volume 21, Number 6—June 2015

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A. Marm Kilpatrick, Ecology and Evolutionary Biology, University of California, Santa Cruz, 1156 High St, Santa Cruz, CA 95064, USA


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