Laura E. Ellison

Host and viral ecology determine bat rabies seasonality and maintenance

Rabies is an acute viral infection that is typically fatal. Most rabies modeling has focused on disease dynamics and control within terrestrial mammals (e.g., raccoons and foxes). As such, rabies in bats has been largely neglected until recently. Because bats have been implicated as natural reservoirs for several emerging zoonotic viruses, including SARS-like corona viruses, henipaviruses, and lyssaviruses, understanding how pathogens are maintained within a population becomes vital. Unfortunately, little is known about maintenance mechanisms for any pathogen in bat populations. We present a mathematical model parameterized with unique data from an extensive study of rabies in a Colorado population of big brown bats (Eptesicus fuscus) to elucidate general maintenance mechanisms. We propose that life history patterns of many species of temperate-zone bats, coupled with sufficiently long incubation periods, allows for rabies virus maintenance. Seasonal variability in bat mortality rates, specifically low mortality during hibernation, allows long-term bat population viability. Within viable bat populations, sufficiently long incubation periods allow enough infected individuals to enter hibernation and survive until the following year, and hence avoid an epizootic fadeout of rabies virus. We hypothesize that the slowing effects of hibernation on metabolic and viral activity maintains infected individuals and their pathogens until susceptibles from the annual birth pulse become infected and continue the cycle. This research provides a context to explore similar host ecology and viral dynamics that may explain seasonal patterns and maintenance of other bat-borne diseases.

ANESTHESIA AND BLOOD SAMPLING OF WILD BIG BROWN BATS (EPTESICUS FUSCUS) WITH AN ASSESSMENT OF IMPACTS ON SURVIVAL

We anesthetized and blood sampled wild big brown bats (Eptesicus fuscus) in Fort Collins, Colorado (USA) in 2001 and 2002 and assessed effects on survival. Inhalant anesthesia was delivered into a specially designed restraint and inhalation capsule that minimized handling and bite exposures. Bats were immobilized an average of 9.1±5.1 (SD) min (range 1–71, n=876); blood sample volumes averaged 58±12 μl (range 13–126, n=718). We randomly selected control (subject to multiple procedures before release) and treatment (control procedures plus inhalant anesthesia and 1% of body weight blood sampling) groups in 2002 to assess treatment effects on daily survival over a 14-day period for adult female and volant juvenile bats captured at maternity roosts in buildings. We monitored survival after release using passive integrated transponder tag detection hoops placed at openings to selected roosts. Annual return rates of bats sampled in 2001 were used to assess long-term outcomes. Comparison of 14-day maximum-likelihood daily survival estimates from control (86 adult females, 92 volant juveniles) and treated bats (187 adult females, 87 volant juveniles) indicated no adverse effect from anesthesia and blood sampling (juveniles: χ2=22.22, df=27, P>0.05; adults: χ2=9.72, df=18, P>0.05). One-year return rates were similar among adult female controls (81%, n=72, 95% confidence interval [CI] =70–91%), females treated once (82%, n=276, 95% CI=81–84%), and females treated twice (84%, n=50, 95% CI=74–94%). Lack of an effect was also noted in 1-yr return rates of juvenile female controls (55%, n=29, 95% CI=37–73%), juveniles treated once (66%, n=113, 95% CI=58–75%), and juveniles treated twice (71%, n=17, 95% CI=49–92%). These data suggest that anesthesia and blood sampling for health monitoring did not measurably affect survival of adult female and volant juvenile big brown bats.

Survival and Condition of Big Brown Bats (Eptesicus fuscus) After Radiotagging

Abstract We tested the 5% rule for the ratio of radiotransmitter mass to body mass by applying radiotransmitters and passive integrated transponders (PIT tags) or PIT tags alone to adult, female big brown bats (Eptesicus fuscus) roosting in buildings in Fort Collins, Colorado. We used records from PIT readers at roosts to compute apparent annual survival of both groups from 2001 to 2003 and found them to be similar. All bats examined 1 year after radiotagging were reproductively active and had body masses similar to bats not radiotagged. Big brown bats do not appear to suffer from major long-term effects of carrying transmitters within the 5% rule.

FACTORS INFLUENCING MOVEMENT PROBABILITIES OF BIG BROWN BATS (EPTESICUS FUSCUS) IN BUILDINGS

We investigated movements of female big brown bats (Eptesicus fuscus) roosting in maternity colonies in buildings in Fort Collins, Colorado (USA), during the summers of 2002, 2003, and 2005. This behavior can be of public health concern where bats that may carry diseases (e.g., rabies) move among buildings occupied by people. We used passive integrated transponders (PIT tags) to mark individual bats and hoop PIT readers at emergence points to passively monitor the use of building roosts by marked adult females on a daily basis during the lactation phase of reproduction. Multi-strata models were used to examine movements among roosts in relation to ambient temperatures and ectoparasite loads. Our results suggest that high ambient temperatures influence movements. Numbers of mites (Steatonyssus occidentalis) did not appear to influence movements of female bats among building roosts. In an urban landscape, periods with unusually hot conditions are accompanied by shifting of bats to different buildings or segments of buildings, and this behavior may increase the potential for contact with people in settings where, in comparison to their more regularly used buildings, the bats may be more likely to be of public concern as nuisances or health risks.

Adult survival and population growth rate in Colorado big brown bats (Eptesicus fuscus)

Abstract We studied adult survival and population growth at multiple maternity colonies of big brown bats (Eptesicus fuscus) in Fort Collins, Colorado. We investigated hypotheses about survival using information-theoretic methods and mark–recapture analyses based on passive detection of adult females tagged with passive integrated transponders. We constructed a 3-stage life-history matrix model to estimate population growth rate (λ) and assessed the relative importance of adult survival and other life-history parameters to population growth through elasticity and sensitivity analysis. Annual adult survival at 5 maternity colonies monitored from 2001 to 2005 was estimated at 0.79 (95% confidence interval [95% CI] = 0.77–0.82). Adult survival varied by year and roost, with low survival during an extreme drought year, a finding with negative implications for bat populations because of the likelihood of increasing drought in western North America due to global climate change. Adult survival during winter was higher than in summer, and mean life expectancies calculated from survival estimates were lower than maximum longevity records. We modeled adult survival with recruitment parameter estimates from the same population. The study population was growing (λ = 1.096; 95% CI = 1.057–1.135). Adult survival was the most important demographic parameter for population growth. Growth clearly had the highest elasticity to adult survival, followed by juvenile survival and adult fecundity (approximately equivalent in rank). Elasticity was lowest for fecundity of yearlings. The relative importances of the various life-history parameters for population growth rate are similar to those of large mammals.

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.

Recruitment in a Colorado population of big brown bats: breeding probabilities, litter size, and first-year survival

Abstract We used mark–recapture estimation techniques and radiography to test hypotheses about 3 important aspects of recruitment in big brown bats (Eptesicus fuscus) in Fort Collins, Colorado: adult breeding probabilities, litter size, and 1st-year survival of young. We marked 2,968 females with passive integrated transponder (PIT) tags at multiple sites during 2001–2005 and based our assessments on direct recaptures (breeding probabilities) and passive detection with automated PIT tag readers (1st-year survival). We interpreted our data in relation to hypotheses regarding demographic influences of bat age, roost, and effects of years with unusual environmental conditions: extreme drought (2002) and arrival of a West Nile virus epizootic (2003). Conditional breeding probabilities at 6 roosts sampled in 2002–2005 were estimated as 0.64 (95% confidence interval [95% CI]  =  0.53–0.73) in 1-year-old females, but were consistently high (95% CI  =  0.94–0.96) and did not vary by roost, year, or prior year breeding status in older adults. Mean litter size was 1.11 (95% CI  =  1.05–1.17), based on examination of 112 pregnant females by radiography. Litter size was not higher in older or larger females and was similar to results of other studies in western North America despite wide variation in latitude. First-year survival was estimated as 0.67 (95% CI  =  0.61–0.73) for weaned females at 5 maternity roosts over 5 consecutive years, was lower than adult survival (0.79; 95% CI  =  0.77–0.81), and varied by roost. Based on model selection criteria, strong evidence exists for complex roost and year effects on 1st-year survival. First-year survival was lowest in bats born during the drought year. Juvenile females that did not return to roosts as 1-year-olds had lower body condition indices in late summer of their natal year than those known to survive.

Bats of Mesa Verde National Park, Colorado: Composition, Reproduction, and Roosting Habits

ABSTRACT. 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.

A comparison of conventional capture versus PIT reader techniques for estimating survival and capture probabilities of big brown bats (Eptesicus fuscus)

ABSTRACT We compared conventional capture (primarily mist nets and harp traps) and passive integrated transponder (PIT) tagging techniques for estimating capture and survival probabilities of big brown bats (Eptesicus fuscus) roosting in buildings in Fort Collins, Colorado. A total of 987 female adult and juvenile bats were captured and marked by subdermal injection of PIT tags during the summers of 2001–2005 at five maternity colonies in buildings. Openings to roosts were equipped with PIT hoop-style readers, and exit and entry of bats were passively monitored on a daily basis throughout the summers of 2002–2005. PIT readers ‘recaptured’ adult and juvenile females more often than conventional capture events at each roost. Estimates of annual capture probabilities for all five colonies were on average twice as high when estimated from PIT reader data ( p̂ = 0.93–1.00) than when derived from conventional techniques ( p̂ = 0.26–0.66), and as a consequence annual survival estimates were more precisely estimated when using PIT reader encounters. Short-term, daily capture estimates were also higher using PIT readers than conventional captures. We discuss the advantages and limitations of using PIT tags and passive encounters with hoop readers vs. conventional capture techniques for estimating these vital parameters in big brown bats.

Sampling blood from big brown bats (Eptesicus fuscus) in the field with and without anesthesia: Impacts on survival

Blood was collected from wild big brown bats (Eptesicus fuscus) with and without anesthesia in Fort Collins, Colorado in 2004 to assess the impacts of these procedures on short-term survival and 1-yr return rates. Short-term survival and 1-yr return rates after release were passively monitored using PIT tag detection hoops placed at selected buildings. Comparison of 14-day maximum likelihood survival estimates from bats not bled (142 adult females, 62 volant juveniles), and bats sampled for blood with anesthesia (96 adult females, 23 volant juveniles) and without anesthesia (112 adult females, 22 volant juveniles) indicated no adverse effects of either treatment (juveniles: χ2=53.38, df=41, P=0.09; adults: χ2=39.09, df=44, P=0.68). Return rates of bats one year after sampling were similar among adult female controls (75.4%, n=142, 95% CI=67.4– 82.2%), females sampled for blood with anesthesia (83.0%, n=112, 95% CI=74.8–89.5%), and females sampled without anesthesia (87.5%, n=96, 95% CI=79.2–93.4%). Lack of an effect was also noted in 1-yr return rates of juvenile females. These data suggest that the use of anesthesia during sampling of blood has no advantages in terms of enhancement of survival in big brown bats.