Amphibian declines: promising directions in understanding the role of disease


Jean-Marc Hero

The decline of amphibian populations worldwide is a recognized phenomenon. A variety of important causes have been linked to the declines but perhaps the most renowned cause, in terms of popular press exposure, funding dispersal and papers published, is disease. In particular, chytridiomycosis, a disease caused by the amphibian chytrid fungus Batrachochytrium dendrobatidis (Bd), is a lethal emerging infectious disease that has had profound effects in some amphibian species, but occurs without catastrophic effects in others (Fisher, Garner & Walker, 2009b). Bd affects species differentially. In many cases it is the major threat to animals already stressed by other critical challenges, such as habitat destruction, pollution, invasive species and climate change. In addition to its impact on amphibian populations, the spread and presence of Bd is likely to impact human activities via effects on the pet, bait and food trade (Schloegel et al., 2009, 2010).

Ten years have passed since the formal description of Bd (Longcore, Pessier & Nichols, 1999) and insights gained have been remarkable, both in the quality and quantity of the research. For example, a potential mechanism for death by Bd infection has been identified (Voyles et al., 2009), as have been multiple genotypes of Bd (Morgan et al., 2007; James et al., 2009) that vary in virulence (Retallick & Meira, 2007; Fisher et al., 2009a; Goka et al., 2009). Populations have been extirpated by the disease (Lips, 1999; Schloegel et al., 2006) yet this evidence is juxtaposed by populations that are persisting with disease (Murray et al., 2009; Pilliod et al., 2010). Numerous studies have found that chytrid is broadly distributed geographically; however, the prevalence and intensity of infection varies with season (Kriger & Hero, 2007a), breeding habitat (Kriger & Hero, 2007b), temperature and rainfall (Kriger, Pereoglou & Hero, 2007). While most of the population declines associated with Bd have occurred at higher elevations, the relationship between altitude and chtryid prevalence and intensity remain unclear (Kriger & Hero, 2008). Although reviews have been published (Fisher et al., 2009b; Berger et al., 2010; Kilpatrick, Briggs & Daszak, 2010), there are still significant knowledge gaps and a lack of cohesive direction in the human response to amphibian disease and decline (Garner et al., 2009; Kriger & Hero, 2009) in spite of noteworthy efforts toward that goal (e.g. Amphibian Ark, The Global Amphibian Assessment

The goal of the symposium, Amphibian disease: Where do we go from here?, was to foster discussion of ‘what comes next?’ in the efforts of the global scientific community to combat amphibian decline, specifically in the arena of disease. The symposium included presentations from Australia, Denmark, Ecuador, Spain, Kenya and USA. Topics ranged from laboratory studies to landscape-scale field studies. Although the debate on ‘what comes next’ remains in progress, the symposium prompted discussion and increased international collaborations – including subsequent workshops in Australia and Switzerland. The series of papers from this symposium, featured in this issue, do not provide a roadmap of what comes next, but illustrate the diverse nature of research into amphibian diseases and highlight some of the promising directions being pursued to understand the effects of disease on amphibian populations.

Differences in the scales of these projects (laboratory, local and landscape), emphasize this diversity and the pervasive impacts of amphibian disease at many levels. At the landscape scale, understanding the origin of a disease is an important part of addressing potential control of, and for predicting suitable habitat for, the disease. Such information, in turn, is useful for ameliorating impacts of disease on local amphibians. Kielgast et al. (2010) explores the ‘out of Africa’ hypothesis (Weldon et al., 2004) further with broad scale surveys in Kenya finding widespread infection but little mortality and no apparent declines. A recently published alternative to this hypothesis about origins details the distribution of unique haplotypes of Bd in Japan (Goka et al., 2009) and further highlights the uncertainty of the origin of Bd. The rapid transmission of Bd across the landscape to novel hosts or additional populations within continents is poorly understood but it is a critical aspect of developing protocols for research and management. In this issue, Schloegel et al. (2010) examine the transmission of Bd in Brazil by bullfrogs. Bullfrogs are known carriers of Bd, are little affected by the disease (Daszak et al., 1999; Schlaepfer et al., 2007; Schloegel et al. 2009), and are able to travel long distances overland (Suhre, 2010), making them effective vectors. Schloegel and colleagues conclude bullfrog farms act as reservoirs for Bd and emphasize the importance of understanding vectors and managing their potential to spread disease among amphibians worldwide. The bullfrog data further reveal implications about the origins of Bd in South America, providing an interesting coda to the Kielgast et al. (2010) paper.

The final papers in this series are focused at the level of the population and the level of the individual, respectively. Stockwell, Clulow & Mahony (2010) failed to find any behavioral indicators for predicting infection load in two Australian frogs; however, the response of each species to Bd infection was markedly different: the widespread species, Limnodynastes peronii (Myobatrachidae), was little affected but the species that has declined, Litoria aurea (Hylidae), was impacted by the disease. This finding is challenged by recent work in the US indicating that behavior can affect infection load and that boreal toad juveniles can reduce their infection load when dry resting sites are available (Murphy et al., 2009). Melzer & Bishop (2010) examine skin peptides as defenses against the fungus in New Zealand frogs. They found some skin peptides, while a useful defense in the laboratory, were less effective in combating Bd in the field. Skin bacteria also play an important role in controlling Bd infection (Lam et al., 2010). These studies demonstrate that the complex interactions among temperature, skin bacteria and antimicrobial peptides strongly influence an individual frog's susceptibility and defense against the fungus. Such results highlight the need for field studies to explore these interactions and fungal response within and among populations and species in the field.

Fundamental questions about the origin of Bd, transmission vectors and behavior, molecular details, safe treatments for infected amphibians and the effect of Bd on demographic parameters in wild populations are still unanswered. The papers herein provide only a snapshot of the current research into amphibian disease but highlight the complexities of interactions between disease and host. Taken together, they illustrate that an integration of laboratory knowledge and field results is necessary to successfully address amphibian disease in both wild and captive amphibian populations. While management agencies urgently need answers to the fundamental questions, they also require protocols formulated from the integration of laboratory and field data to address, and perhaps ameliorate, the impacts of amphibian diseases.