Anthropogenic and Ecological Drivers of Amphibian Disease (Ranavirosis)

RESEARCH ARTICLE Anthropogenic and Ecological Drivers of Amphibian Disease (Ranavirosis) Alexandra C. North1*, David J. Hodgson2, Stephen J. Price3, Amber G. F. Griffiths1* 1 Environment and Sustainability Institute, University of Exeter, Penryn Campus, Penryn, Cornwall, United Kingdom, 2 Centre for Ecology and Conservation, University of Exeter, Penryn Campus, Penryn, Cornwall, United Kingdom, 3 UCL Genetics Institute, Gower Street, London, United Kingdom * (ACN); (AGFG) Abstract OPEN ACCESS Citation: North AC, Hodgson DJ, Price SJ, Griffiths AGF (2015) Anthropogenic and Ecological Drivers of Amphibian Disease (Ranavirosis). PLoS ONE 10(6): e0127037. doi:10.1371/journal.pone.0127037 Academic Editor: Jacob Lawrence Kerby, University of South Dakota, UNITED STATES Received: December 8, 2014 Accepted: April 10, 2015 Published: June 3, 2015 Copyright: © 2015 North et al. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Data Availability Statement: The data analysed in this manuscript has been deposited in Dryad (doi: http://dx.doi.org/10.5061/dryad.66k59). Third party data was obtained from Froglife and are therefore available through the charity Froglife (Registered Charity No. 1093372 in England and Wales). Please submit queries for data to and asking for access to the data for research purposes. Further contact details can also be found on their website http://www.froglife.org/contact-us/. Funding: This work received support from Marie Curie (http://ec.europa.eu/research/ mariecurieactions/) and the University of Exeter (http://www.exeter.ac.uk/). Ranaviruses are causing mass amphibian die-offs in North America, Europe and Asia, and have been implicated in the decline of common frog (Rana temporaria) populations in the UK. Despite this, we have very little understanding of the environmental drivers of disease occurrence and prevalence. Using a long term (1992-2000) dataset of public reports of amphibian mortalities, we assess a set of potential predictors of the occurrence and prevalence of Ranavirus-consistent common frog mortality events in Britain. We reveal the influence of biotic and abiotic drivers of this disease, with many of these abiotic characteristics being anthropogenic. Whilst controlling for the geographic distribution of mortality events, disease prevalence increases with increasing frog population density, presence of fish and wild newts, increasing pond depth and the use of garden chemicals. The presence of an alternative host reduces prevalence, potentially indicating a dilution effect. Ranavirosis occurrence is associated with the presence of toads, an urban setting and the use of fish care products, providing insight into the causes of emergence of disease. Links between occurrence, prevalence, pond characteristics and garden management practices provides useful management implications for reducing the impacts of Ranavirus in the wild. Introduction Amphibians are the most endangered taxonomic group on the planet, with one third of species currently holding a threatened status (IUCN categories Vulnerable, Endangered or Critically Endangered; [1], [2]). Emerging diseases are one main driver of these amphibian declines [3], alongside a range of other threats including over-exploitation, habitat loss and climate change [4]. Ranaviruses impact amphibians worldwide [5] and are causing notable die-offs in North America, Europe and Asia [5–11]. The pathogen has been implicated in population declines of several European species [10] including declines of over 80% in UK common frogs (Rana temporaria) [9] and models suggest that Ranavirus has the potential to cause local extinction in wood frog (Lithobates sylvaticus) populations [12]. Ranaviruses are large, double-stranded DNA viruses belonging to the family Iridoviridae [13] that infect amphibians, fish and reptiles [14], [15]. They can cause systemic disease PLOS ONE | DOI:10.1371/journal.pone.0127037 June 3, 2015 1 / 17 Anthropogenic and Ecological Drivers of Ranavirus Disease Competing Interests: Please note that one author (AGF Griffiths) is a PLOS One Editor. This does not alter the authors' adherence to PLOS ONE Editorial policies and criteria. (ranavirosis), resulting in cell death [13] and overt signs—ulcerations, haemorrhaging, muscle necrosis or lip erythema [16]—which may depend on the stage of disease progression [17]. In the wild, Ranavirus induced mortality rates can be in excess of 90%, with year on year re-occurrence of die-offs in the same amphibian populations [7] and observed die-offs as large as 200 individuals [9]. Susceptibility to Ranavirus does however differ between host developmental stages [18], populations [19], and species [15], [20], and is influenced by a range of biotic and abiotic characteristics, including differences in habitat [20] and temperature [21]. Differences in susceptibility may also relate to the virus genotype [22], though only a single species of Ranavirus is thought to be present in the UK [14]. Incidence of mortality events can show seasonal variation, peaking in summer months in the UK [23] in contrast to North America where incidence is highest in autumn and winter [24]. Emerging pathogens are classed as novel if, for example, they have been introduced to new regions by humans, and endemic if they were already present in a region but have moved into a new host or increased in pathogenicity [25]. The distinction is important since the different histories will likely warrant different management approaches. Ranavirus spread has been strongly linked to human activity, including international trade [14], [26]—[28], the use of infected salamanders as fishing bait [29] and industrial and agricultural activities [30]. Modelling the emergence of ranavirosis in the UK reveals human population density as an important predictor of spread [17], though it is challenging to determine which aspects of human activity are responsible. Commonly used anthropogenic chemicals such as pesticides are known to cause immunosuppression in amphibians [31]. The herbicide atrazine for example reduces leukocyte production and increases host susceptibility to Ranavirus [32], and the insecticide chlorpyrifos increases Ranavirus infection rates in the tiger salamander (Ambystoma tigrinum) [33]. Carbyl insecticide has also been shown to decrease host survival when in combination with Ranavirus and predator cues [34]. Few studies have however looked at the relationship between chemical use and Ranavirus infection in free living populations, and those that have, focus on North American species and correlates such as distance to agricultural or industrial activity [30] or other abiotic contaminants such as aluminium [35] and water ammonia levels [36]. Biotic characteristics such as the presence (...truncated)