Abstract
White-Nose Syndrome (WNS) is an epizootic disease in hibernating bats caused by the fungus Pseudogymnoascus destructans. Surveillance for P. destructans at bat hibernacula consists primarily of visual surveys of bats, collection of potentially infected bats, and submission of these bats for laboratory testing. Cryptic infections (bats that are infected but display no visual signs of fungus) could lead to the mischaracterization of the infection status of a site and the inadvertent spread of P. destructans. We determined the efficacy of visual detection of P. destructans by examining visual signs and molecular detection of P. destructans on 928 bats of six species at 27 sites during surveys conducted from January through March in 2012–2014 in the southeastern USA on the leading edge of the disease invasion. Cryptic infections were widespread with 77% of bats that tested positive by qPCR showing no visible signs of infection. The probability of exhibiting visual signs of infection increased with sampling date and pathogen load, the latter of which was substantially higher in three species (Myotis lucifugus, M. septentrionalis, and Perimyotis subflavus). In addition, M. lucifugus was more likely to show visual signs of infection than other species given the same pathogen load. Nearly all infections were cryptic in three species (Eptesicus fuscus, M. grisescens, and M. sodalis), which had much lower fungal loads. The presence of M. lucifugus or M. septentrionalis at a site increased the probability that P. destructans was visually detected on bats. Our results suggest that cryptic infections of P. destructans are common in all bat species, and visible infections rarely occur in some species. However, due to very high infection prevalence and loads in some species, we estimate that visual surveys examining at least 17 individuals of M. lucifugus and M. septentrionalis, or 29 individuals of P. subflavus are still effective to determine whether a site has bats infected with P. destructans. In addition, because the probability of visually detecting the fungus was higher later in winter, surveys should be done as close to the end of the hibernation period as possible.
Highlights
Disease surveillance in wildlife is often limited by diagnostic techniques that are cost-effective, rapid, and feasible for use on wild animals [1, 2]
The best-fitting model of the probability of visual detection included fungal load, sampling date, and an additive species effect (AIC weight = 0.55; Fitted equation for M. lucifugus = Pr(Detection) ~ -12.9 (±1.5) + 1.77 (±0.2) Ã log10(load) + 0.02 (±0.01) Ã; For M. septentrionalis and P. subflavus the intercept equaled -14.01 (±1.6); For the three other species (Eptesicus fuscus, Myotis grisescens, and Myotis sodalis) the intercept equaled -13.47 (±1.6)), suggesting that the probability of visually detecting P. destructans on a bat increased with pathogen load measured by qPCR, but the slope did not differ among species (Table 2, Fig 2)
Our results suggest that cryptic infections are widespread and that solely using visible signs of P. destructans greatly underestimates infection prevalence in bats even during mid to late winter (January-March) when the majority of surveillance surveys for White-Nose Syndrome (WNS) are conducted
Summary
Disease surveillance in wildlife is often limited by diagnostic techniques that are cost-effective, rapid, and feasible for use on wild animals [1, 2]. For diseases where hosts display visible symptoms, visual surveys are often cost-effective and can be appealing for surveillance because they typically impose minimal disturbance on host populations [3, 4]. Estimating the efficacy of visual surveys for a particular disease is necessary to determine whether this low-cost and minimally disruptive survey method is an appropriate surveillance approach. White-Nose Syndrome (WNS) is a rapidly spreading epizootic disease that has caused widespread declines in six species of hibernating bats in North America, raising substantial concern about the risk of extirpation and extinction of species [5,6,7,8]. The exact origin of P. destructans remains unclear, recent genetic data suggest the fungus was introduced to North America from the Western Palearctic [19, 20]
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