DOI: 10.25349/d9sg75
title: Disease's hidden death toll: Using parasite aggregation patterns to quantify landscape-level host mortality in a wildlife system

description: 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 &gt;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.
description: <strong>Lab data:</strong> We used controlled
 laboratory experiments to estimate the dose-response curves between
 <em>R. ondatrae</em> exposure and survival for larvae of the
 four amphibian species. We collected recently deposited amphibian egg
 masses (<em>P. regilla,</em> <em>A. boreas</em>,
 and <em>T. torosa</em>) from field sites or reproductive
 adults (<em>T. granulosa</em>) and allowed them to lay eggs in
 the laboratory. Hatching larvae were maintained in carbon-filtered,
 UV-sterilized tap water at 22 deg. C until being assigned randomly to one
 of five exposure dosages (0 [control], 20, 40, 100, or 200 cercariae).
 Snails (<em>Helisoma trivolvis</em>) naturally infected with
 <em>R. ondatrae</em> were collected from field sites, isolated
 into 50 ml vials, and allowed to release free-swimming cercariae that were
 harvested within 4 hr of emergence. Pooled cercariae from multiple snails
 were administered to an individual amphibian larva within 500 ml of water.
 Larval amphibians were exposed to cercariae in a single pulse event timed
 to correspond to early limb development (anurans stage 28, caudates stage
 2T). After exposure, we monitored amphibian larvae until death or 20 days
 following exposure, at which point we dissected hosts to quantify
 infection. <strong>Field data:</strong> To
 characterize patterns of infection in wild-caught amphibians among
 species, across populations, and through time, we sampled amphibian hosts
 from unique ponds (sites) in the East Bay region of California (Alameda,
 Contra Costa and Santa Clara counties) between 2009 and 2014. This
 included sites from publicly accessible parks, open space preserves,
 municipal watershed districts, and private ranches.  Parasitological
 sampling was timed to overlap with amphibian metamorphosis. We focused on
 recently metamorphosed amphibians, as these provide a reliable and
 standardized indicator of <em>R. ondatrae</em> infections
 acquired during aquatic development.  To measure
 <em>Ribeiroia</em> abundance per host, we performed a
 systematic examination of all major tissues and organs in sampled hosts.
 In the analysis of parasite-induced mortality, we focused on the 301
 site-by-year-by-host species combinations with at least five sampled hosts
 and five detected <em>R.
 ondatrae </em>metacercariae.
description: See accompanying README file for metadata.