Disassembly of a tadpole community by a multi‐host fungal pathogen with limited evidence of recovery

Abstract

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.

Eco‐evolutionary rescue promotes host–pathogen coexistence

“…, DiRenzo et al. ). The amphibian community in El Copé can be considered a metapopulation, because there is high gene flow among the streams studied and less dispersal to and from far away sites (Robertson et al.…”

“…Typically, when Bd arrives in a na€ ıve amphibian community, pathogen prevalence and host infection increase rapidly (Lips et al 2006, Crawford et al 2010, which often correlate with high host mortality and mass amphibian die-offs (e.g., , Heard et al 2014, but see Reeder et al 2012. Within months, the remaining amphibian community differs substantially from the original community in measures of host density, species richness, and community composition (e.g., Smith et al 2009a, Crawford et al 2010, Angeli et al 2015, DiRenzo et al 2016). The amphibian community in El Cop e can be considered a metapopulation, because there is high gene flow among the streams studied and less dispersal to and from far away sites (Robertson et al 2008).…”

Biodiversity is decimated by the cascading effects of the amphibian-killing chytrid fungus

“…Biotic homogenization can decrease biodiversity, increase incidence and distribution of infectious disease, and reduce resiliency to ecosystem-level disturbances [ 43 ]. Because the loss of amphibians from Bd is not random across and within species, we tend to find biotic homogenization occurring in amphibian communities following a Bd invasion, resulting in reduced taxonomic diversity, in which common species persist [ 37 , 44 ]. Interestingly, the indirect impacts of a Bd-related chytridiomycosis epizootic have a similar nonrandom effect on other taxonomic groups impacted by the loss of amphibians.…”

Preparing for invasion: Assessing risk of infection by chytrid fungi in southeastern plethodontid salamanders

“…Bd is now established in many amphibian communities across the globe whereas Bsal is more limited in both the extent of its distribution and host preferences (Fisher & Garner, 2020; James et al, 2015; O'Hanlon et al, 2018). Chytrid‐related mortality led to the homogenization of amphibian communities, the extinction of 90 species of amphibians and resulted in severe shifts in community assembly at higher trophic levels (DiRenzo et al, 2017; Scheele et al, 2019; Smith et al, 2009; Zipkin et al, 2020). Although amphibian pathogenic chytrid fungi are widespread across continents, new invasion events are still possible in areas dominated by one genetic lineage of Bd and/or in areas where Bsal has not yet been found (Lips, 2016).…”