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Emerging infectious diseases can cause host community disassembly, but the mechanisms driving the order of species declines and extirpations following a disease outbreak are unclear. We documented the community disassembly of a Neotropical tadpole community during a chytridiomycosis outbreak, triggered by the generalist fungal pathogen, Batrachochytrium dendrobatidis (Bd). Within the first 11 months of Bd arrival, tadpole density and occupancy rapidly declined. Species rarity, in terms of tadpole occupancy and adult relative abundance, did not predict the odds of tadpole occupancy declines. But species losses were taxonomically selective, with glassfrogs (Family: Centrolenidae) disappearing the fastest and tree frogs (Family: Hylidae) and dart-poison frogs (Family: Dendrobatidae) remaining the longest. We detected biotic homogenization of tadpole communities, with post-decline communities resembling one another more strongly than pre-decline communities. The entire tadpole community was extirpated within 22 months following Bd arrival, and we found limited signs of recovery within 10 years post-outbreak. Because of imperfect species detection inherent to sampling species-rich tropical communities and the difficulty of devising a single study design protocol to sample physically complex tropical habitats, we used simulations to provide recommendations for future surveys to adequately sample diverse Neotropical communities. Our unique data set on tadpole community composition before and after Bd arrival is a valuable baseline for assessing amphibian recovery. Our results are of direct relevance to conservation managers and community ecologists interested in understanding the timing, magnitude, and consequences of disease outbreaks as emerging infectious diseases spread globally.
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- 2006. Multivariate dispersion as a measure of beta diversity. Ecology Letters 9: 683–693.
- 2015. Effects of density on spatial aggregation and habitat associations of the glass frog Espadarana (Centrolene) prosoblepon. Journal of Herpetology 49: 388–394.
- 2014. Assessing the utility of statistical adjustments for imperfect detection in tropical conservation science. Journal of Applied Ecology 51: 849–859.
- 1999. Rapid bioassessment protocols for use in wadeable streams and rivers: periphyton, benthic macroinvertebrates, and fish. United States Environmental Protection Agency, Office of Water, Washington, D.C., USA.
- 2015. Evidence for the persistence of food web structure after amphibian extirpation in a Neotropical stream. Ecology 96: 2106–2116.
- 1998. Chytridiomycosis causes amphibian mortality associated with population declines in the rain forests of Australia and Central America. Proceedings of the National Academy of Sciences USA 95: 9031–9036.
- 2008. Batrachochytrium dendrobatidis infection patterns among Panamanian amphibian species, habitats and elevations during epizootic and enzootic stages. Diseases of Aquatic Organisms 81: 189–202.
- 2010. Enzootic and epizootic dynamics of the chytrid fungal pathogen of amphibians. Proceedings of the National Academy of Sciences USA 107: 9695–9700.
- 1998. General methods for monitoring convergence of iterative simulations. Journal of Computational and Graphical Statistics 7: 434–455.
- 1973. Natural mortality of tadpoles in a population of Rana aurora. Ecology 54: 741–758.
- 2007. Drought mediates the importance of stochastic community assembly. Proceedings of the National Academy of Sciences USA 104: 17430–17434.
- 2010. Stream invertebrate responses to a catastrophic decline in consumer diversity. Journal of the North American Benthological Society 29: 1185–1198.
- 2008. Changes in stream primary producer communities resulting from large-scale catastrophic amphibian declines: Can small-scale experiments predict effects of tadpole loss? Ecosystems 11: 1262–1276.
- 2008. Phylogenetic autocorrelation of extinction threat in globally imperiled amphibians. Diversity and Distributions 14: 614–629.
- 2010. Epidemic disease decimates amphibian abundance, species diversity, and evolutionary history in the highlands of central Panama. Proceedings of the National Academy of Sciences USA 107: 13777–13782.
- 2011. Models for estimating abundance from repeated counts of an open metapopulation. Biometrics 67: 577–587.
- 1986. The biology of amphibians. McGraw-Hill Books, New York, New York, USA.
- 2007. A large-scale deforestation experiment: effects of patch area and isolation on Amazon birds. Science 315: 238–241.
- 2012. Emerging fungal threats to animal, plant and ecosystem health. Nature 484: 186–194.
- 2012. AD Model Builder: using automatic differentiation for statistical inference of highly parameterized complex nonlinear models. Optimization Methods and Software 27: 233–249.
- 2009. Life history tradeoffs influence mortality associated with the amphibian pathogen Batrachochytrium dendrobatidis. Oikos 118: 783–791.
- 2014. Convergence in mycorrhizal fungal communities due to drought, plant competition, parasitism, and susceptibility to herbivory: consequences for fungi and host plants. Frontiers in Microbiology 5: 1–9.
- 2014. Bayesian data analysis. Volume 2. Chapman and Hall/CRC, Boca Raton, Florida.
- 2006. Application of random effects to the study of resource selection by animals. Journal of Animal Ecology 75: 887–898.
- 2011. Impact of sampling with replacement in occupancy studies with spatial replication. Methods in Ecology and Evolution 2: 401–406.
- 2010. Design of occupancy studies with imperfect detection. Methods in Ecology and Evolution 1: 131–139.
- 2011. Species occupancy modeling for detection data collected along a transect. Journal of Agricultural, Biological, and Environmental Statistics 16: 301–317.
- 2008. GEIGER: investigating evolutionary radiations. Bioinformatics 24: 129–131.
- 2006. Assessing detection probabilities for the endangered growling grass frog (Litoria raniformis) in southern Victoria. Wildlife Research 33: 557–564.
- 1976. Studies in larval amphibian habitat partitioning. Smithsonian Contributions in Zoology 242: 1–27.
- 1975. Tadpoles, predation and pond habitats in the tropics. Biotropica 7: 100–111.
- 1994. Measuring and monitoring biological diversity. Standard methods for amphibians. Smithsonian Institution Press, Washington, D.C., USA.
- 2010. Tigers on trails: occupancy modeling for cluster sampling. Ecological Applications 20: 1456–1466.
- 1986. Organization of a community of tadpoles in rain forest streams in Borneo. Journal of Tropical Ecology 2: 193–205.
- 2015. Disentangling host, pathogen, and environmental determinants of a recently emerged wildlife disease: lessons from the first 15 years of amphibian chytridiomycosis research. Ecology and Evolution 5: 4079–4097.
- 2010. Introduction to WinBUGS for ecologists: Bayesian approach to regression, ANOVA, mixed models and related analyses. Academic Press, Burlington, MA.
- 1993. Risks of population extinction from demographic and environmental stochasticity and random catastrophes. American Naturalist 142: 911–927.
- 2014. Susceptibility to the amphibian chytrid fungus varies with ontogeny in the direct-developing frog, Eleutherodactylus coqui. Journal of Wildlife Diseases 50: 438–446.
- 2012. Sociality, density-dependence and microclimates determine the persistence of populations suffering from a novel fungal disease, white-nose syndrome. Ecology Letters 15: 1050–1057.
- 2005. Extinction order and altered community structure rapidly disrupt ecosystem functioning. Ecology Letters 8: 538–547.
- 2008. Understanding trait-dependent community disassembly: dung beetles, density functions, and forest fragmentation. Conservation Biology 22: 1288–1298.
- 1998. Decline of a tropical montane amphibian fauna. Conservation Biology 12: 106–117.
- 1999. Mass mortality and population declines of anurans at an upland site in western Panama. Conservation Biology 13: 117–125.
- 2003. Ecological traits predicting amphibian population declines in Central America. Conservation Biology 17: 1078–1088.
- 2006. Emerging infectious disease and the loss of biodiversity in a Neotropical amphibian community. Proceedings of the National Academy of Sciences USA 103: 3165–3170.
- 2012. The BUGS book: a practical introduction to Bayesian analysis. CRC Press, Boca Raton, Florida, USA.
- 2005. Designing occupancy studies: general advice and allocating survey effort. Journal of Applied Ecology 42: 1105–1114.
- 2006. Occupancy estimation and modeling: inferring patterns and dynamics of species occurrence. Elsevier Academic Press, London, UK.
- 2013. Survival and abundance in males of the glass frog Espadarana (Centrolene) prosoblepon in Central Panama. Journal of Herpetology 46: 213–220.
- 1999. Tadpoles: the biology of the anuran larvae. University of Chicago Press, Chicago, Illinois, USA.
- 1999. Biotic homogenization: a few winners replacing many losers in the next mass extinction. Trends in Ecology and Evolution 14: 450–453.
- 2004. Ecological and evolutionary consequences of biotic homogenization. Trends in Ecology and Evolution 19: 18–24.
- 2004. Fungal pathogen causes competitive and developmental stress in larval amphibian communities. Ecology 85: 3385–3395.
- 2009. Effects on ecosystem resilience of biodiversity, extinctions, and the structure of regional species pools. Theoretical Ecology 2: 177–187.
- 2015. rjags: Bayesian Graphical Models using MCMC. R package version 3-15. http://CRAN.R-project.org/package=rjags
- R Development Core Team. 2015. R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. http://www.R-project.org/
- 1981. Seven forms of rarity. Pages 205–217 in H. Synge, editor. The biological aspects of rare plant conservation. John Wiley and Sons, Hoboken, New Jersey, USA.
- 2007. Quantifying the disease transmission function: effects of density on Batrachochytrium dendrobatidis transmission in the mountain yellow-legged frog Rana muscosa. Journal of Animal Ecology 76: 711–721.
- 2006. Emerging infectious disease as a proximate cause of amphibian mass mortality. Ecology 87: 1671–1683.
- 2014. The winners and losers of land use intensification: pollinator community disassembly is non-random and alters functional diversity. Diversity and Distributions 20: 908–917.
- 2004. Neotropical tadpoles influence stream benthos: evidence for the ecological consequences of decline in amphibian populations. Freshwater Biology 49: 274–285.
- 2010. Occupancy dynamics in a tropical bird community: unexpectedly high forest use by birds classified as non-forest species. Journal of Applied Ecology 47: 621–630.
- 2002. The amphibians and reptiles of Costa Rica. The University of Chicago Press, Chicago, Illinois, USA.
- 2015. Generalized Linear Mixed Models using ‘AD Model Builder’. R package version 0.8.3.2. http://glmmadmb.r-forge.r-project.org/
- 2007. Associations between anuran tadpoles and salinity in a landscape mosaic of wetlands impacted by secondary salinisation. Freshwater Biology 52: 75–84.
- 2009. Selecting for extinction: nonrandom disease-associated extinction homogenizes amphibian biotas. Ecology Letters 12: 1069–1078.
- 1990. Rana warszewitschii (Schmidt). Catalogue of American amphibians and reptiles. Society for the Study of Amphibians and Reptiles 459: 1–459.2.
- 2013. Fitting and interpreting occupancy models. PLoS ONE 8: e52015.
- 2013. Disease-driven amphibian declines alter ecosystem processes in a tropical stream. Ecosystems 16: 146–157.
- 2007. Changes in nestedness in experimental communities of soil fauna undergoing extinction. Pedobiologia 50: 497–503.
- 2009. Ecosystem responses to community disassembly. Annals of the New York Academy of Sciences 1162: 311–333.