Browsing by Author "Kilpatrick, A. Marm"

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    Bacteria Isolated from Bats Inhibit the Growth of Pseudogymnoascus destructans, the Causative Agent of White-Nose Syndrome
    Hoyt, Joseph R.; Cheng, Tina L.; Langwig, Kate E.; Hee, Mallory M.; Frick, Winifred F.; Kilpatrick, A. Marm (PLOS, 2015-04-08)
    Emerging infectious diseases are a key threat to wildlife. Several fungal skin pathogens have recently emerged and caused widespread mortality in several vertebrate groups, including amphibians, bats, rattlesnakes and humans. White-nose syndrome, caused by the fungal skin pathogen Pseudogymnoascus destructans, threatens several hibernating bat species with extinction and there are few effective treatment strategies. The skin microbiome is increasingly understood to play a large role in determining disease outcome. We isolated bacteria from the skin of four bat species, and co-cultured these isolates with P. destructans to identify bacteria that might inhibit or kill P. destructans.We then conducted two reciprocal challenge experiments in vitro with six bacterial isolates (all in the genus Pseudomonas) to quantify the effect of these bacteria on the growth of P. destructans. All six Pseudomonas isolates significantly inhibited growth of P. destructans compared to noninhibitory control bacteria, and two isolates performed significantly better than others in suppressing P. destructans growth for at least 35 days. In both challenge experiments, the extent of suppression of P. destructans growth was dependent on the initial concentration of P. destructans and the initial concentration of the bacterial isolate. These results show that bacteria found naturally occurring on bats can inhibit the growth of P. destructans in vitro and should be studied further as a possible probiotic to protect bats from white-nose syndrome. In addition, the presence of these bacteria may influence disease outcomes among individuals, populations, and species.
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    Continued preference for suboptimal habitat reduces bat survival with white-nose syndrome
    Hopkins, Skylar R.; Hoyt, Joseph R.; White, J. Paul; Kaarakka, Heather M.; Redell, Jennifer A.; DePue, John E.; Scullon, William H.; Kilpatrick, A. Marm; Langwig, Kate E. (Springer Nature, 2021)
    Habitat alteration can influence suitability, creating ecological traps where habitat preference and fitness are mismatched. Despite their importance, ecological traps are notoriously difficult to identify and their impact on host–pathogen dynamics remains largely unexplored. Here we assess individual bat survival and habitat preferences in the midwestern United States before, during, and after the invasion of the fungal pathogen that causes white-nose syndrome. Despite strong selection pressures, most hosts continued to select habitats where disease severity was highest and survival was lowest, causing continued population declines. However, some individuals used refugia where survival was higher. Over time, a higher proportion of the total population used refugia than before pathogen arrival. Our results demonstrate that host preferences for habitats with high disease-induced mortality can create ecological traps that threaten populations, even in the presence of accessible refugia.
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    Environmental reservoir dynamics predict global infection patterns and population impacts for the fungal disease white-nose syndrome
    Hoyt, Joseph R.; Langwig, Kate E.; Sun, Keping; Parise, Katy L.; Li, Aoqiang; Wang, Yujuan; Huang, Xiaobin; Worledge, Lisa; Miller, Helen; White, J. Paul; Kaarakka, Heather M.; Redell, Jennifer A.; Görföl, Tamás; Boldogh, Sándor András; Fukui, Dai; Sakuyama, Muneki; Yachimori, Syuuji; Sato, Akiyoshi; Dalannast, Munkhnast; Jargalsaikhan, Ariunbold; Batbayar, Nyambayar; Yovel, Yossi; Amichai, Eran; Natradze, Ioseb; Frick, Winifred E.; Foster, Jeffrey T.; Feng, Jiang; Kilpatrick, A. Marm (National Academy of Sciences, 2020-03-16)
    Disease outbreaks and pathogen introductions can have significant effects on host populations, and the ability of pathogens to persist in the environment can exacerbate disease impacts by fueling sustained transmission, seasonal epidemics, and repeated spillover events. While theory suggests that the presence of an environmental reservoir increases the risk of host declines and threat of extinction, the influence of reservoir dynamics on transmission and population impacts remains poorly described. Here we show that the extent of the environmental reservoir explains broad patterns of host infection and the severity of disease impacts of a virulent pathogen. We examined reservoir and host infection dynamics and the resulting impacts of Pseudogymnoascus destructans, the fungal pathogen that causes white-nose syndrome, in 39 species of bats at 101 sites across the globe. Lower levels of pathogen in the environment consistently corresponded to delayed infection of hosts, fewer and less severe infections, and reduced population impacts. In contrast, an extensive and persistent environmental reservoir led to early and widespread infections and severe population declines. These results suggest that continental differences in the persistence or decay of P. destructans in the environment altered infection patterns in bats and influencedwhether host populations were stable or experienced severe declines from this disease. Quantifying the impact of the environmental reservoir on disease dynamics can provide specific targets for reducing pathogen levels in the environment to prevent or control future epidemics.
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    Field trial of a probiotic bacteria to protect bats from white-nose syndrome
    Hoyt, Joseph R.; Langwig, Kate E.; White, J. Paul; Kaarakka, Heather M.; Redell, Jennifer A.; Parise, Katy L.; Frick, Winifred F.; Foster, Jeffrey T.; Kilpatrick, A. Marm (Nature Research, 2019-06-24)
    Tools for reducing wildlife disease impacts are needed to conserve biodiversity. White-nose syndrome (WNS), caused by the fungus Pseudogymnoascus destructans, has caused widespread declines in North American bat populations and threatens several species with extinction. Few tools exist for managers to reduce WNS impacts. We tested the efficacy of a probiotic bacterium, Pseudomonas fluorescens, to reduce impacts of WNS in two simultaneous experiments with caged and free-flying Myotis lucifugus bats at a mine in Wisconsin, USA. In the cage experiment there was no difference in survival between control and P. fluorescens-treated bats. However, body mass, not infection intensity, predicted mortality, suggesting that within-cage disturbance influenced the cage experiment. In the free-flying experiment, where bats were able to avoid conspecific disturbance, infection intensity predicted the date of emergence from the mine. In this experiment treatment with P. fluorescens increased apparent overwinter survival five-fold compared to the control group (from 8.4% to 46.2%) by delaying emergence of bats from the site by approximately 32 days. These results suggest that treatment of bats with P. fluorescens may substantially reduce WNS mortality, and, if used in combination with other interventions, could stop population declines.
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    Field trial of a probiotic bacteria to protect bats from white-nose syndrome
    Hoyt, Joseph R.; Langwig, Kate E.; White, J. Paul; Kaarakka, Heather M.; Redell, Jennifer A.; Parise, Katy L.; Frick, Winifred F.; Foster, Jeffrey T.; Kilpatrick, A. Marm (Nature Research, 2019-06-24)
    Tools for reducing wildlife disease impacts are needed to conserve biodiversity. White-nose syndrome (WNS), caused by the fungus Pseudogymnoascus destructans, has caused widespread declines in North American bat populations and threatens several species with extinction. Few tools exist for managers to reduce WNS impacts. We tested the efficacy of a probiotic bacterium, Pseudomonas fluorescens, to reduce impacts of WNS in two simultaneous experiments with caged and free-flying Myotis lucifugus bats at a mine in Wisconsin, USA. In the cage experiment there was no difference in survival between control and P. fluorescens-treated bats. However, body mass, not infection intensity, predicted mortality, suggesting that within-cage disturbance influenced the cage experiment. In the free-flying experiment, where bats were able to avoid conspecific disturbance, infection intensity predicted the date of emergence from the mine. In this experiment treatment with P. fluorescens increased apparent overwinter survival five-fold compared to the control group (from 8.4% to 46.2%) by delaying emergence of bats from the site by approximately 32 days. These results suggest that treatment of bats with P. fluorescens may substantially reduce WNS mortality, and, if used in combination with other interventions, could stop population declines.
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    Impact of censusing and research on wildlife populations
    Kilpatrick, A. Marm; Hoyt, Joseph R.; King, R. Andrew; Kaarakka, Heather M.; Redell, Jennifer A.; White, J. Paul; Langwig, Kate E. (2020-11)
    Population monitoring and research are essential for conserving wildlife, but these activities may directly impact the populations under study. These activities are often restricted to minimize disturbance, and impacts must be weighed against knowledge gained. However, few studies have quantified the effects of research or census-related visitation frequency on populations, and low visitation rates have been hypothesized to have little effect. Hibernating bats have been hypothesized to be especially sensitive to visitation because they have limited energetic stores to survive winter, and disturbance may partly deplete these stores. We examined the effect of site visitation frequency on population growth rates of three species of hibernating bats, little brown bats (Myotis lucifugus), Indiana bats (Myotis sodalis) and tri-colored bats (Perimyotis subflavus), both before and after detection of the disease white-nose syndrome. We found no evidence that more frequent visits decreased population growth rates for any of these species. Estimated coefficients were either the opposite sign as hypothesized (population growth rates increased with visitation frequency) or were very small (difference in population growth rates 0.067% [SE 2.5%]-1.8% [SE 9.8%]) relative to spatial and temporal variation (5.9-32%). In contrast, white-nose syndrome impacts on population growth rates were easily detected and well-characterized statistically (effect sizes 4.4-8.0; severe population declines occurred in the second and third years after pathogen detection) indicating that we had sufficient power to detect effects. These results indicate that visitation frequency (forM. sodalis:annual vs. semi-annual counts; forM. lucifugusandP. subflavus:1-3 three research visits per year) had undetectable impacts on bat population growth rates both with and without the additional stress of an emerging infectious disease. Knowledge gained from censuses and research may outweigh disturbance due to human visitation if it can be used to understand and conserve the species.
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    Mobility and infectiousness in the spatial spread of an emerging fungal pathogen
    Langwig, Kate E.; White, J. Paul; Parise, Katy L.; Kaarakka, Heather M.; Redell, Jennifer A.; DePue, John E.; Scullon, William H.; Foster, Jeffrey T.; Kilpatrick, A. Marm; Hoyt, Joseph R. (2021-05)
    Emerging infectious diseases can have devastating effects on host communities, causing population collapse and species extinctions. The timing of novel pathogen arrival into naive species communities can have consequential effects that shape the trajectory of epidemics through populations. Pathogen introductions are often presumed to occur when hosts are highly mobile. However, spread patterns can be influenced by a multitude of other factors including host body condition and infectiousness. White-nose syndrome (WNS) is a seasonal emerging infectious disease of bats, which is caused by the fungal pathogen Pseudogymnoascus destructans. Within-site transmission of P. destructans primarily occurs over winter; however, the influence of bat mobility and infectiousness on the seasonal timing of pathogen spread to new populations is unknown. We combined data on host population dynamics and pathogen transmission from 22 bat communities to investigate the timing of pathogen arrival and the consequences of varying pathogen arrival times on disease impacts. We found that midwinter arrival of the fungus predominated spread patterns, suggesting that bats were most likely to spread P. destructans when they are highly infectious, but have reduced mobility. In communities where P. destructans was detected in early winter, one species suffered higher fungal burdens and experienced more severe declines than at sites where the pathogen was detected later in the winter, suggesting that the timing of pathogen introduction had consequential effects for some bat communities. We also found evidence of source-sink population dynamics over winter, suggesting some movement among sites occurs during hibernation, even though bats at northern latitudes were thought to be fairly immobile during this period. Winter emergence behaviour symptomatic of white-nose syndrome may further exacerbate these winter bat movements to uninfected areas. Our results suggest that low infectiousness during host migration may have reduced the rate of expansion of this deadly pathogen, and that elevated infectiousness during winter plays a key role in seasonal transmission. Furthermore, our results highlight the importance of both accurate estimation of the timing of pathogen spread and the consequences of varying arrival times to prevent and mitigate the effects of infectious diseases.
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    Reducing environmentally mediated transmission to moderate impacts of an emerging wildlife disease
    Hoyt, Joseph R.; Parise, Katy L.; DePue, John E.; Kaarakka, Heather M.; Redell, Jennifer A.; Scullon, William H.; O'Reskie, Rich; Foster, Jeffrey T.; Kilpatrick, A. Marm; Langwig, Kate E.; White, J. Paul (Wiley, 2023-05)
    Emerging infectious diseases have caused population declines and biodiversity loss. The ability of pathogens to survive in the environment, independent of their host, can exacerbate disease impacts and increase the likelihood of species extinction. Control of pathogens with environmental stages remains a significant challenge for conservation and effective management strategies are urgently needed.We examined the effectiveness of managing environmental exposure to reduce the impacts of an emerging infectious disease of bats, white-nose syndrome (WNS). We used a chemical disinfectant, chlorine dioxide (ClO2), to experimentally reduce Pseudogymnoascus destructans, the fungal pathogen causing WNS, in the environment. We combined laboratory experiments with 3 years of field trials at four abandoned mines to determine whether ClO2 could effectively remove P. destructans from the environment, reduce host infection and limit population impacts.ClO2 was effective at killing P. destructans in vitro across multiple concentrations. In field settings, higher concentrations of ClO2 treatment were needed to sufficiently reduce viable P. destructans conidia in the environment.The reduction in the environmental reservoir at treatment sites resulted in lower fungal loads on bats compared to untreated control populations. Survival following treatment was also higher in little brown bats (Myotis lucifugus), and trended higher for tricolored bats (Perimyotis subflavus).Synthesis and applications. Our results highlight that targeted management of sources for environmental transmission can be an effective control strategy for wildlife disease. We found that successfully reducing pathogen in the environment decreased disease severity and increased survival, but required higher treatment exposure than was effective in laboratory experiments, and the effects varied among species. More broadly, our findings have implications for other emerging wildlife diseases with free-living pathogen stages by highlighting how the degree of environmental contamination can have cascading impacts on hosts, presenting an opportunity for intervention.
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    White-nose syndrome restructures bat skin microbiomes
    Ange-Stark, Meghan; Parise, Katy L.; Cheng, Tina L.; Hoyt, Joseph R.; Langwig, Kate E.; Frick, Winifred F.; Kilpatrick, A. Marm; Gillece, John; MacManes, Matthew D.; Foster, Jeffrey T. (American Society for Microbiology, 2023-10-27)
    The skin microbiome is an essential line of host defense against pathogens, yet our understanding of microbial communities and how they change when hosts become infected is limited. We investigated skin microbial composition in three North American bat species (Myotis lucifugus, Eptesicus fuscus, and Perimyotis subflavus) that have been impacted by the infectious disease, white-nose syndrome, caused by an invasive fungal pathogen, Pseudogymnoascus destructans. We compared bacterial and fungal composition from 154 skin swab samples and 70 environmental samples using a targeted 16S rRNA and internal transcribed spacer amplicon approach. We found that for M. lucifugus, a species that experiences high mortality from white-nose syndrome, bacterial microbiome diversity was dramatically lower when P. destructans was present. Key bacterial families—including those potentially involved in pathogen defense—significantly differed in abundance in bats infected with P. destructans compared to uninfected bats. However, skin bacterial diversity was not lower in E. fuscus or P. subflavus when P. destructans was present despite populations of the latter species declining sharply from white-nose syndrome. The fungal species present on bats substantially overlapped with the fungal taxa present in the environment at the site where the bat was sampled, but fungal community composition was unaffected by the presence of P. destructans for any of the three bat species. This species-specific alteration in bat skin bacterial microbiomes after pathogen invasion may suggest a mechanism for the severity of white-nose syndrome in M. lucifugus but not for other bat species impacted by the disease. IMPORTANCE Inherent complexities in the composition of microbiomes can often preclude investigations of microbe-associated diseases. Instead of single organisms being associated with disease, community characteristics may be more relevant. Longitudinal microbiome studies of the same individual bats as pathogens arrive and infect a population are the ideal experiment but remain logistically challenging; therefore, investigations like our approach that are able to correlate invasive pathogens to alterations within a microbiome may be the next best alternative. The results of this study potentially suggest that microbiome-host interactions may determine the likelihood of infection. However, the contrasting relationship between Pd and the bacterial microbiomes of Myotis lucifugus and Perimyotis subflavus indicate that we are just beginning to understand how the bat microbiome interacts with a fungal invader such as Pd.