Disease's hidden death toll: Using parasite aggregation patterns to quantify landscape-level host mortality in a wildlife system

Worldwide, infectious diseases represent a major source of mortality in
humans and livestock. For wildlife populations, disease-induced mortality
is likely even greater, but remains notoriously difficult to estimate
-- especially for endemic infections. Approaches for quantifying
wildlife mortality due to endemic infections have historically been
limited by an inability to directly observe wildlife mortality in nature.
Here, we address a question that can rarely be answered for endemic
pathogens of wildlife: what are the population- and landscape-level
effects of infection on host mortality? We combined laboratory
experiments, extensive field data, and novel mathematical models to
indirectly estimate the magnitude of mortality induced by an endemic,
virulent trematode parasite (Ribeiroia ondatrae) on hundreds of amphibian
populations spanning four native species. We developed a flexible
statistical model that uses patterns of aggregation in parasite abundance
to infer host mortality.  Our model improves on previous
approaches for inferring host mortality from parasite abundance data by
i.) relaxing restrictive assumptions on the timing of host mortality and
sampling, ii.) placing all mortality inference within a Bayesian framework
to better quantify uncertainty, and iii.) accommodating data from
laboratory experiments and field sampling to allow for estimates and
comparisons of mortality within and among host populations. Applying our
approach to 301 amphibian populations, we found that trematode infection
was associated with an average of between 13 and 40% population-level
mortality. For three of the four amphibian species, our models predicted
that some populations experienced >90% mortality due to infection,
leading to mortality of thousands of amphibian larvae within a pond.
 At the landscape scale, the total number of amphibians predicted
to succumb to infection was driven by a few high mortality sites, with
fewer than 20% of sites contributing to greater than 80% of amphibian
mortality on the landscape. The mortality estimates in this study provide
a rare glimpse into the magnitude of effects that endemic parasites can
have on wildlife populations and our theoretical framework for indirectly
inferring parasite-induced mortality can be applied to other host-parasite
systems to help reveal the hidden death toll of pathogens on wildlife
hosts.