Mitigation
Mitigation of Chytridiomycosis has two broad aims: (1) reducing spread and (2) reducing impacts. By the time Bd was recognized widely as the cause of global declines, it had already spread to most areas that contain suitable habitats.
The faster recognition of Bsal, however, has meant that there is potential for biosecurity measures to keep countries disease-free, such as the United States (Martel et al. 2014). However, for both fungi, there is a risk that spread of different strains could lead to dangerous recombinations; hence, reducing movement across already- infected areas is recommended. Long-distance spread is most likely to have occurred due to movement of infected amphibians, particularly through the pet trade but also via accidental movement in produce and in the frog meat industry (although the latter is likely more important for viruses such as ranaviruses, since most frog products are frozen; Kolby et al. 2014). The listing of chytridiomycosis as an internationally notifiable disease by the OIE represents the first disease listed that is solely a biodiversity concern, with the aim to improve trade safety. However, although rigorous quarantine and surveillance protocols are often in place for livestock diseases, improved standards are needed for wildlife (Grogan et al. 2014). Fortunately, the US Fish and Wildlife Service announced restrictions from January 2016 on the importation and interstate movement of salamanders in the United States. In the United States, planning and surveillance for early detection of Bsal incursions and emergency responses is underway (Grant et al. 2016). Ideally, however, all amphibian trade should be restricted. A good example is Australia, where exotic frogs are rarely allowed to be imported and are restricted to biosecured facilities such as zoos or research institutes.Within a region, risk of anthropogenic spread of chytridiomycosis to naive populations, and between infected regions, may be mitigated through containment.
This is a priority for isolated populations such as those on islands or in habitats where natural spread is unlikely to or could not occur (Berger and Skerratt 2012). In moist wilderness areas with abundant wildlife, attempts to stop natural spread appear unlikely to succeed. Control of anthropogenic spread involves restricting access to sites and the use of stringent hygiene protocols on equipment (Murray et al. 2013; Phillott et al. 2010). However, the efficacy of reducing the risk of spread by focusing on humans has not been assessed. Educating the community about basic disease management and the risks of transport of potentially infected amphibians and water is important.Much research has focused on reducing impacts of Bd, which also has high relevance to Bsal where studies have recently commenced. Although small-scale eradication of Bd has been achieved in a specific type of isolated or ephemeral habitat (Bosch et al. 2015), this approach is not broadly applicable. Hence in areas where chytridiomycosis has established, the emphasis is on ensuring the persistence of amphibian populations and species (Skerratt et al. 2016). Extinction has been prevented via establishing amphibian ex situ captive assurance colonies, but methods to ensure self-sustaining wild populations are obviously the goal (McFadden et al. 2013; Scheele et al. 2014; Skerratt et al. 2016).
Currently, reintroductions have had low success, with the continued presence of the pathogen in the environment leading to eventual mortality of reintroduced individuals. Research and trials are currently underway on potential management strategies to improve survival rates in the wild; however these are largely in the experimental phase.
As infected frog populations can thrive in naturally suboptimal habitats for the fungus, which may include warmer, drier or more saline regions (Heard et al. 2015; Puschendorf et al. 2011; Stockwell et al. 2015a, b), eradication of disease is not necessary for successful mitigation.
This also shows the importance of assessing suitability for Batrachochytrium species when choosing habitats to preserve for amphibians. This may lead to conservation of areas that may not have previously been considered prime habitat (Skerratt et al. 2016).Another angle involves altering the environmental suitability for chytridiomycosis. Physical modifications of the environment might be used on a local scale for critically threatened amphibians in situ and may render the habitat less suitable for Bd. These include drying, drainage or alteration of waterflow, provision of shallow warm-water areas, reduction in canopy cover to increase temperature or the addition of basking sites or artificial heat (Scheele et al. 2014). A number of chemical treatments have been proposed or trialled in the field, including the application of salt (Stockwell et al. 2015a, b) and agricultural fungicides (Johnson et al. 2003; Woodhams et al. 2011). Reducing transmission might also be achieved by removal of reservoir hosts or by making habitat less favourable for reservoir species (Scheele et al. 2014; Skerratt et al. 2016).
Other ideas for fighting the pathogen directly include manipulating microbial competition via bioaugmentation of the host or environment with probiotic bacteria that express antifungal metabolites (Becker et al. 2009; Muletz et al. 2012; Vredenburg et al. 2011), augmenting the numbers of Bd predators such as zooplankton (Schmeller et al. 2014) and pathogens such as mycoviruses (Skerratt et al. 2016) and the identification or engineering and release of nonvirulent strains of Bd (Woodhams et al. 2011).
Management strategies aimed at improving host immunity have long-term potential. Manipulation of the host adaptive and innate immune response (via vaccination and assisted selection for disease resistance) is a proven strategy in humans and domestic animals, with potential to reduce the impact of chytridiomycosis in the field. Although adaptive immunity is not heritable and hence immunization may be perceived as a short-term approach, it could assist in providing a population size buffer for the natural evolution of innate immunity, although the artificial maintenance of susceptible genotypes may counter this beneficial effect (Harding et al.
2005). Unfortunately, reinfection trials in the few species examined to date have not demonstrated strong acquired immunity against Bd (Cashins et al. 2013; McMahon et al. 2014).The innate immune system is generally considered responsible for the evolution of inter-generational immunity, and disease resistance or tolerance may be upregulated within a population via assisted selection for less susceptible individuals (Venesky et al. 2012). Comparative techniques (e.g. marker-assisted selection and estimated breeding values) have been widely and successfully used for breeding of disease resistance in plant and domestic animal agriculture (Heringstad et al. 2007; Miedaner and Korzun 2012). This may present a sustainable approach for repatriating the numerous amphibian species that are now extinct in the wild and only persist in ex situ captive programs. Two main approaches that might be feasible in practice for promoting disease resistance include (1) direct selection via exposure of post-metamorphic individuals to Bd, then breeding from those with lower susceptibility, and (2) identifying molecular markers of resistance to advance selection to earlier life stages, removing the need to regularly expose individuals to infection. Some progress has been made towards this latter goal via studies of the major histocompatibility complex (MHC; Bataille et al. 2015; Savage and Zamudio 2011). The increasing longevity of some recovering wild populations suggests evolution of resistance may occur naturally (Newell et al. 2013), although in other species individual annual survival rates remain very low despite a long history of infection (i.e. 15-20 years) (Phillott et al. 2013; Brannelly et al. 2015).
Scheele et al. (2014) present immediately applicable suggestions for bolstering overall population size and recruitment to counteract disease-associated mortality. This strategy is based on the observation of species with high mortality rates persisting via high recruitment (Phillott et al.
2013, Scheele et al. 2015). Interventions may involve removal of other threatening processes from small and declining populations such as improving habitat or excluding competitors and introduced pests (Scheele et al. 2014). Increase of population size can be achieved through reintroductions and minimizing the effect of early predation by head-starting larval stages through metamorphosis in captivity (Hunter et al. 1999; Scheele et al. 2014). An alternative to establishing long-term captive assurance colonies is to rear wild-caught eggs or tadpoles in captivity to ensure higher survival rates before release. Direct translocation to ‘disease refugia' sites could be an efficient way to create sustainable populations (Puschendorf et al. 2011; Skerratt et al. 2016).As disease ecology varies greatly between species and habitats, management will be context-specific; hence research aimed at understanding each situation is needed to devise effective local strategies. A proactive approach is crucial, as many of the most endangered species occur in already protected areas and will not survive without intervention (Skerratt et al. 2016).
Acknowledgements LB was supported by the Australian Research Council (grant FT100100375).