Mechanisms Underlying Host Persistence Following Amphibian Disease Emergence Determine Appropriate Management Strategies
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Ecology Letters, (2020) doi: 10.1111/ele.13621 REVIEW AND SYNTHESIS Mechanisms underlying host persistence following amphibian disease emergence determine appropriate management strategies Abstract Laura A. Brannelly,1* Emerging infectious diseases have caused many species declines, changes in communities and even Hamish I. McCallum,2 extinctions. There are also many species that persist following devastating declines due to disease. Laura F. Grogan,2,3 The broad mechanisms that enable host persistence following declines include evolution of resis- Cheryl J. Briggs,4 tance or tolerance, changes in immunity and behaviour, compensatory recruitment, pathogen Maria P. Ribas,3,5 attenuation, environmental refugia, density-dependent transmission and changes in community Matthijs Hollanders,3 composition. Here we examine the case of chytridiomycosis, the most important wildlife disease 2 of the past century. We review the full breadth of mechanisms allowing host persistence, and syn- Thais Sasso, thesise research on host, pathogen, environmental and community factors driving persistence fol- Mariel Familiar Lopez, 6 lowing chytridiomycosis-related declines and overview the current evidence and the information David A. Newell3 and required to support each mechanism. We found that for most species the mechanisms facilitating Auston M. Kilpatrick7 persistence have not been identified. We illustrate how the mechanisms that drive long-term host population dynamics determine the most effective conservation management strategies. Therefore, understanding mechanisms of host persistence is important because many species continue to be threatened by disease, some of which will require intervention. The conceptual framework we describe is broadly applicable to other novel disease systems. Keywords Chytridiomycosis, compensatory recruitment, density-dependent transmission, environmental refu- gia, host–pathogen, management, population persistence, population recovery, resistance, tolerance. Ecology Letters (2020) or recovery following severe disease-associated declines are INTRODUCTION often diverse, nuanced and context dependent and therefore less Ecological communities can be devastated by the introduction understood (Greenberg et al., 2017), particularly in cases where of novel pathogens, and the role of disease in declines and initial disease-associated declines are severe. extinction has probably been underestimated (Preece et al., To date, the pathogen emergence posing the greatest threat 2017). Well-known examples include the invasion of the Mor- to biodiversity is the amphibian chytrid fungus, Batra- billivirus rinderpest into African ungulate communities (Holdo chochytrium dendrobatidis (Bd), the causative agent of the et al., 2009), the impact of avian malaria (van Riper et al., 1986) amphibian disease chytridiomycosis (Box 1) (Berger et al., and bird pox (Warner, 1968) on the Hawaiian avifauna and 1998; Skerratt et al., 2007; Scheele et al., 2019a). The global white nose syndrome which has had a major impact on bat pop- spread of this pathogen has had catastrophic impacts on bio- ulations across North America (Langwig et al., 2012). Key dri- diversity, causing extinctions and major declines in amphibian vers of host extinction from disease include (1) stochasticity populations (Skerratt et al., 2007; Wake and Vredenburg, related to small pre- or post-epidemic populations, (2) non-den- 2008; Scheele et al., 2019a). Multiple species throughout a sity-dependent pathogen transmission and (3) the existence of range of environments have been affected by Bd infection, alternate biotic or abiotic reservoirs that maintain a high force resulting in a variety of population outcomes. of infection even as a species declines (De Castro and Bolker, Despite the devastation of many amphibian communities 2005). In contrast, the mechanisms that enable host persistence following the arrival of the fungal pathogen, some amphibian 1Veterinary BioSciences, Faculty of Veterinary and Agricultural Sciences, The 5Wildlife Conservation Medicine Research Group, Departament de Medicina i University of Melbourne, Werribee, Vic 3030, Australia Cirurgia Animals, Universitat Autonoma de Barcelona, Bellaterra 08193, Spain 2Environmental Futures Research Institute and School of Environment and 6School of Environment and Sciences, Griffith University, Gold Coast, Qld. Science, Griffith University, Nathan, Qld. 4111, Australia 4215, Australia 3Forest Research Centre, School of Environment, Science and Engineering, 7Department of Ecology and Evolutionary Biology, University of California Southern Cross University, Lismore, NSW 2480, Australia Santa Cruz, Santa Cruz, CA 95064, USA 4Ecology, Evolution and Marine Biology, University of California Santa Bar- *Correspondence: E-mail: [email protected] bara, Santa Barbara, CA 93106, USA © 2020 John Wiley & Sons Ltd. 2 L. A. Brannelly et al. Review and Synthesis HOST-ASSOCIATED MECHANISMS FOR COEXISTENCE Box 1. Biology of the fungal pathogen Batrachochytrium den- drobatidis (Bd), and the amphibian skin disease chytridiomycosis Increases in host resistance and/or tolerance to pathogens are key mechanisms that can reduce disease impacts and lead to Batrachochytrium dendrobatidis was first reported as the population persistence or recovery following disease invasion. cause of widespread frog declines in Australia and the Resistance can be defined as ‘the ability to limit parasite bur- Americas in 1998 (Berger et al., 1998). It has now been den’ and tolerance as ‘the ability to limit the harm caused by reported on all continents other than Antarctica and a given parasite burden’ (Raberg et al., 2009), but these mech- impacts over 500 species (Scheele et al., 2019a). It has a anisms are complex phenomena (see Box 2). Resistance or tol- biphasic life cycle consisting of infectious motile aquatic erance can occur at the level of the individual, through zoospores and sessile zoosporangia that grow within host adaptive immune or learned mechanisms, or at a population skin cells and are the reproductive stage of the pathogen. level, through natural selection of immunity, behaviour, life Batrachochytrium dendrobatidis can grow and reproduce in history, etc. (Brunner et al., 2005; Tuite and Gros, 2006; culture over a range of temperatures (4–25 °C), with opti- Tompkins et al., 2011; Curtis, 2014). Differences in resistance mal growth between 17 and 25 °C (Stevenson et al., 2013; and tolerance among amphibian populations or species can Voyles et al., 2017). Warmer sites and laboratory environ- result from variation in immune function, behaviour and/or ments are often associated with decreased infection loads the environment (Boots et al., 2012). (Bustamante et al., 2010; Murphy et al., 2011; Roznik To determine differences in amphibian resistance and toler- et al., 2015b) and one common treatment method in captiv- ance to Bd infection, we conducted a synthesis of experimen- ity is exposing infected animals to high temperatures tal infection studies (see Text S1, Figs S1–3). We used (Woodhams et al., 2003; Chatfield and Richards-Zawacki, pathogen load and survival during the experimental infection 2011). Batrachochytrium dendrobatidis causes mortality in to examine variation in resistance and tolerance among spe- affected amphibians primarily by interfering with cuta- cies and life stages (Figure 1) and found enormous variation neous osmoregulatory and ion regulation function (Voyles among amphibian species (Figure 1). While host resistance et al., 2007). Pathogenicity varies greatly between amphib- and/or tolerance are important, the wide variation among spe- ian species and increases strongly with zoospore load. In cies and life stages demonstrates that resistance/tolerance most species that are impacted by Bd, tadpoles can become alone cannot account for population persistence in all species. infected but do not experience mortality (Figure S3). Immune mechanisms of resistance and tolerance The immune system is the primary host defence against infec- species that initially declined or were thought to have become tion, and variation in host immune or physiological function extinct are persisting at lower densities or are even recovering can result in variation in resistance and/or tolerance to patho- (Newell et al., 2013; Skerratt et al., 2016; Scheele et al., gens. More broadly, an increase in the number of individuals 2017b). In this paper, we use amphibian chytridiomycosis as a that are resistant or tolerant due to innate or adaptive case study to examine the mechanisms of host persistence fol- immune mechanisms can promote population persistence over lowing declines caused by disease and show how these mecha- time (Anderson and May, 1978; Grogan et al., 2016; Wilber nisms have implications for conservation management. et al., 2017). In order to demonstrate that evolutionary shifts Understanding how these mechanisms of coexistence facilitate in immune or physiological mechanisms have led to host per- persistence of different species will help inform management sistence requires measurement of infection loads, immune/ strategies for species that are currently experiencing declines. physiological markers and survival during population decline We describe mechanisms enabling persistence following ini- and recovery. For example, a comparison of skin anti-micro- tial declines using the classic disease triangle of the host, the bial peptide secretions from frogs captured before and after pathogen and their combined environment