Assessing threats to North American bats: impacts of white-nose syndrome and climate on reproduction and survival
Many cave-hibernating North American bat species currently face the threat of extinction due to the newly emergent wildlife disease, white-nose syndrome (WNS). WNS is a fungal disease that has been causing catastrophic declines of bat populations in the eastern United States and Canada since it first emerged in 2006. The fungal pathogen, Pseudogymnoascus destructans, infects the wings, ears and nose of bats that hibernate in caves in winter while both cave temperatures and bats’ body temperatures are low. The hibernating bats' immune systems do not respond to the infection, leading to wing damage, emaciation, depletion of fat stores, and often death. Infected bats that survive winter mount a vigorous immune response upon exiting hibernation. These bats typically clear the infection, regenerate wing tissue and survive. WNS mortality varies greatly by species. Some species have suffered greater than 90% population declines, while other species appear to have not declined at all. Although researchers have made great strides in the last nine years in understanding WNS, there are still many unknowns. The vast majority of our knowledge of the effects of WNS comes from M. lucifugus because it is one of the most abundant North American species, and is also heavily affected by WNS (population declines > 90%). Aside from estimates of rates of population declines at hibernation sites, the effects of WNS on species other than M. lucifugus are not well resolved. In the next most abundant species, E. fuscus, estimates of population declines range from 0% to 40%. Wing damage had not been studied prior to WNS, making inferences about the relationship between wing damage and WNS difficult. The effects of WNS on reproduction are unknown. Population viability analyses of M. lucifugus determined that population growth is most influenced by survival of reproductive females, but the factors that affect reproductive female survival remain unknown. Currently, the primary WNS population model assumes no effect on reproductive function due to lack of data on the subject. If WNS reduces reproductive output, this model will need to be adjusted to accurately project bat population growth in the post-WNS era. Climate change is another factor that could affect the accuracy of models that project bats' likelihoods of persistence in the post-WNS era. There are few publications on the effects of a changing climate on North American cave-hibernating bats. Climate change has the potential to impact the persistence of cave-hibernating bat species, which have annual cycles of activity and hibernation that are precisely timed to coincide with the availability of their insect prey and temperatures that are conducive to reproduction. Published data on the effects of climate on bat survival are limited to a study of the little brown myotis (Myotis lucifugus) in New Hampshire and the big brown bat (Eptesicus fuscus) in Colorado. These studies indicate that M. lucifugus survival increases with high precipitation in the Northeastern United States, and E. fuscus survival decreases during drought periods in the Rocky Mountain region. This suggests an overall positive relationship between bat survival and precipitation, but the universality of this relationship is unclear without comparable data on multiple species from multiple regions. To my knowledge, Rick Adams’s six-species Colorado study is the only published data of the effects of climate on reproduction in temperate-zone North American bats. He found that four of the six species had significantly lower proportions of reproductive females in drought years. Again, it is unclear how universally this applies to the other 42 bat species of the United States, and the extent to which it affects populations outside of the severely water-limited Rocky Mountain region. My dissertation addresses aspects of the knowledge gaps described above. I conducted a survey of wing damage on bats that had been captured in Illinois prior to the arrival of WNS. I found that wing discoloration in particular is common among multiple species of bats. Additionally, I found that in E. fuscus wing discoloration increases in severity in early summer then decreases in severity in late summer, and also varies by year (possibly decreasing in drought years). I conducted a mark-recapture study of M. lucifugus and E. fuscus at a site in western Illinois to test predictions of trends in survival and reproduction in years that varied in temperature and precipitation. This study also modeled population-level effects on the two species as WNS entered the region. I found that reproduction decreased significantly in the drought year for both species, but did not find an effect of temperature or precipitation on survival rates. Survival rates for M. lucifugus dropped drastically in the presumed post-WNS year. There was no change in survival for E. fuscus, nor was there any significant difference in reproduction for either species in the presumed post-WNS year. I conducted an additional study of M. lucifugus at this site on the effects of annual spring temperature on parturition dates, and the effects of parturition date on maternal survival. I found that parturition dates occurred significantly earlier in the hottest year, but did not find an effect of parturition date on maternal survival. Finally, I conducted a study of the effects of WNS on M. lucifugus female fertility during hibernation, and estimated the impact of those effects on population growth rates. I found no effect of WNS on female fertility. My models demonstrated that even if fertility were reduced by 17% (the maximum included in the 95% confidence intervals of my results), post-WNS populations would not become extinct any sooner than they would if there were no effect of WNS on fertility. Unexpectedly, I observed that both infected and uninfected females had neutrophils (a white blood cell that responds to infection) present in their reproductive tracts where sperm were present. This was surprising given that all published studies of the P. destructans-infected wing tissue in hibernating bats report an absence of neutrophils and other white blood cells. The studies that I present in this dissertation contribute to our knowledge of WNS and bat conservation in several ways. I found that wing discoloration should not be interpreted as an indicator of WNS, and that researchers should anticipate changes in the severity of this type of damage from season-to-season and year-to-year. In a rare bit of good news from WNS studies, I found that the current WNS population model is accurate in terms of reproductive output: there is no effect of WNS on reproduction in hibernation, and no effect during the summer maternity season. However, I did find that reproduction drops in drought years for both species studied. This is similar to results from a previously published study in Colorado, and indicates that bat populations in both the Midwest and Rocky Mountain regions may face declines if the climate becomes hotter and drier in coming years. My results do not show evidence of reduced survival in drought years. This also comes as good news, because bat population growth is influenced more by survival than by reproduction. Additionally, I found a clue that may improve our understanding of bats’ immune function during hibernation: Although hibernating bats do not mount an immune response to P. destructans infection, they are capable of immune cell recruitment. I look forward to investigating this apparent paradox in future studies.
Myotis lucifugus, Eptesicus fuscus, population growth, fertility, maternity, hibernation, white-nose syndrome
University of Illinois - Urbana-Champaign
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University of Illinois at Urbana-Champaign