10.25349/D9SG75
Wilber, Mark
0000-0002-8274-8025
University of California, Santa Barbara
Briggs, Cheryl
University of California, Santa Barbara
Johnson, Pieter
University of Colorado Boulder
Disease's hidden death toll: Using parasite aggregation patterns to
quantify landscape-level host mortality in a wildlife system
Dryad
dataset
2020
FOS: Natural sciences
National Institute of General Medical Sciences
https://ror.org/04q48ey07
R01GM109499
National Institute of General Medical Sciences
https://ror.org/04q48ey07
R01GM135935
National Science Foundation
https://ror.org/021nxhr62
1149308
National Science Foundation
https://ror.org/021nxhr62
1754171
2020-08-21T00:00:00Z
2020-08-21T00:00:00Z
en
575737 bytes
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CC0 1.0 Universal (CC0 1.0) Public Domain Dedication
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.
Lab data: We used controlled laboratory experiments to estimate the
dose-response curves between R. ondatrae exposure and survival for larvae
of the four amphibian species. We collected recently deposited amphibian
egg masses (P. regilla, A. boreas, and T. torosa) from field sites or
reproductive adults (T. granulosa) 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 (Helisoma trivolvis) naturally infected with R. ondatrae 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. Field data: 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 R. ondatrae infections acquired during aquatic
development. To measure Ribeiroia 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 R. ondatrae metacercariae.
See accompanying README file for metadata.