Dynamics of an emerging disease drive large-scale amphibian population extinctions

Department of Biology, San Francisco State University, San Francisco, CA 94132-1722, USA.
Proceedings of the National Academy of Sciences (Impact Factor: 9.67). 05/2010; 107(21):9689-94. DOI: 10.1073/pnas.0914111107
Source: PubMed


Epidemiological theory generally suggests that pathogens will not cause host extinctions because the pathogen should fade out when the host population is driven below some threshold density. An emerging infectious disease, chytridiomycosis, caused by the fungal pathogen Batrachochytrium dendrobatidis (Bd) is directly linked to the recent extinction or serious decline of hundreds of amphibian species. Despite continued spread of this pathogen into uninfected areas, the dynamics of the host-pathogen interaction remain unknown. We use fine-scale spatiotemporal data to describe (i) the invasion and spread of Bd through three lake basins, each containing multiple populations of the mountain yellow-legged frog, and (ii) the accompanying host-pathogen dynamics. Despite intensive sampling, Bd was not detected on frogs in study basins until just before epidemics began. Following Bd arrival in a basin, the disease spread to neighboring populations at approximately 700 m/yr in a wave-like pattern until all populations were infected. Within a population, infection prevalence rapidly reached 100% and infection intensity on individual frogs increased in parallel. Frog mass mortality began only when infection intensity reached a critical threshold and repeatedly led to extinction of populations. Our results indicate that the high growth rate and virulence of Bd allow the near-simultaneous infection and buildup of high infection intensities in all host individuals; subsequent host population crashes therefore occur before Bd is limited by density-dependent factors. Preventing infection intensities in host populations from reaching this threshold could provide an effective strategy to avoid the extinction of susceptible amphibian species in the wild.

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Available from: Vance T Vredenburg, Apr 14, 2014
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    • "In our study, frogs gained and lost infection frequently, consistent with previous field 444 data on mountain yellow-legged frogs (Rana muscosa and R. sierrae) in temperate 445 USA (Briggs, Knapp & Vredenburg 2010), and some individuals demonstrated 446 numerous state transitions. Comparing two-and three-state analyses helped resolve 447 the nature and magnitude of transition probabilities between disease states (Figs 3c, 4c 448 and 4d). "
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    ABSTRACT: 1.Pathogens can be critical drivers of the abundance and distribution of wild animal populations. The presence of an over-dispersed pathogen load distribution between hosts (where few hosts harbor heavy parasite burdens and light infections are common) can have an important stabilizing effect on host-pathogen dynamics where infection intensity determines pathogenicity. This may potentially lead to endemicity of an introduced pathogen rather than extirpation of the host and/or pathogen. 2.Over-dispersed pathogen load distributions have rarely been considered in wild animal populations as an important component of the infection dynamics of microparasites such as bacteria, viruses, protozoa and fungi. 3.Here we examined the abundance, distribution and transmission of the model fungal pathogen Batrachochytrium dendrobatidis (Bd, cause of amphibian chytridiomycosis) between wild-caught Litoria rheocola (common mist frogs) to investigate the effects of an over-dispersed pathogen load distribution on the host population in the wild. We quantified host survival, infection incidence and recovery probabilities relative to infectious burden, and compared the results of models where pathogen over-dispersion either was or was not considered an important feature of host-pathogen dynamics. 4.We found the distribution of Bd load between hosts to be highly over-dispersed. We found that host survival was related to infection burden, and that accounting for pathogen over-dispersion allowed us to better understand infection dynamics and their implications for disease control. In addition, we found that the pattern of host infections and recoveries varied markedly with season whereby (i) infections established more in winter, consistent with temperature dependent effects on fungal growth, and (ii) recoveries (loss of infection) occurred frequently in the field throughout the year but were less likely in winter. 5.Our results suggest that pathogen over-dispersion is an important feature of endemic chytridiomycosis, and that intensity of infection determines disease impact. These findings have important implications for our understanding of chytridiomycosis dynamics and the application of management strategies for disease mitigation. We recommend quantifying individual infectious burdens rather than infection state where possible in microparasitic diseases. This article is protected by copyright. All rights reserved.
    Full-text · Article · Feb 2016 · Journal of Animal Ecology
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    • "The spread of declines in areas of North and Central America enabled researchers to monitor Bd at remaining sites with abundant amphibians. The disease arrived in well studied sites in both Panama and California in 2004 and researchers documented a steep rise in Bd prevalence as amphibian populations crashed (Lips et al., 2006; Vredenburg et al., 2010). Transmission experiments with pure cultures involving even low numbers of zoospores resulted in fatal infections (Berger et al., 1999, 2004; Woodhams et al., 2003; Carey et al., 2006). "
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    ABSTRACT: Batrachochytrium dendrobatidis (Bd) emerged in the 1970s in Australia and the Americas, causing rapid and catastrophic declines and extinctions of naïve amphibian populations as it spread through remote rainforest and alpine regions. The description of chytridiomycosis in 1998 stimulated a large and diverse global research effort, including studies on phylogeny, distribution, ecology, and virulence - but mitigating its effect remains a major challenge. In 2010 a second Batrachochytrium species, B. salamandrivorans (Bsal), emerged after spreading to Europe from Asia and has decimated fire salamanders in the Netherlands and Belgium. Bsal appears to be restricted to salamanders and newts whereas Bd can infect all amphibian orders. These cases show that despite the current advanced state of globalisation, severe pathogens are still spreading and some may currently be excluded by geographic barriers, hence biosecurity still has potential to mitigate spread of undiscovered and unpredictable pathogens of wildlife.
    Full-text · Article · Feb 2016 · Fungal Ecology
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    • "Third, some countries that are highly vulnerable to IAS (such as those reported here) still lack IAS policies, e.g. countries in Central and South America[40]. It is crucial that the governments of these countries improve their actions in this regard. "

    Full-text · Article · Jan 2016 · Proceedings of the Royal Society B: Biological Sciences
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