Date Published: July 13, 2017
Publisher: Public Library of Science
Author(s): Mark Blooi, Alexandra E. Laking, An Martel, Freddy Haesebrouck, Merlijn Jocque, Tom Brown, Stephen Green, Miguel Vences, Molly C. Bletz, Frank Pasmans, Louise A. Rollins-Smith.
The fungal pathogen Batrachochytrium dendrobatidis (Bd) drives declines and extinctions in amphibian communities. However, not all regions and species are equally affected. Here, we show that association with amphibian aquatic habitat types (bromeliad phytotelmata versus stream) across Central America results in the odds of being threatened by Bd being five times higher in stream microhabitats. This differential threat of Bd was supported in our study by a significantly lower prevalence of Bd in bromeliad-associated amphibian species compared to riparian species in Honduran cloud forests. Evidence that the bromeliad environment is less favorable for Bd transmission is exemplified by significantly less suitable physicochemical conditions and higher abundance of Bd-ingesting micro-eukaryotes present in bromeliad water. These factors may inhibit aquatic Bd zoospore survival and the development of an environmental reservoir of the pathogen. Bromeliad phytotelmata thus may act as environmental refuges from Bd, which contribute to protecting associated amphibian communities against chytridiomycosis-driven amphibian declines that threaten the nearby riparian communities.
Chytridiomycosis, caused by the chytridiomycete fungus, Batrachochytrium dendrobatidis (Bd) , drives global amphibian declines and extinctions [2–5] and is currently considered the greatest infectious disease threat to biodiversity [6,7]. Although Bd has a worldwide distribution with confirmed presence in over 500 amphibian species from 52 countries [6,8], its most devastating impact is centered on specific regions, such as mountainous regions in Central America [3,9]. In these areas, the cumulative time individuals of a species spend in riparian habitats significantly increases the likelihood of decline [5,9–12]. Therefore, even in these hotspots of chytridiomycosis-driven declines, a proportion of species are less affected [9,13,14], especially those with arboreal, bromeliad-associated habits [15–18]. The reasons for these differential infection and disease dynamics of Bd have been suggested to be multifactorial and dependent on local environmental-, host- and pathogen-associated factors [13,19–24]. Since metamorph mortality disproportionately contributes to chytridiomycosis-driven declines , the habitat of juvenile stages and all associated mechanisms affecting Bd presence, survival and transmission in these habitats is expected to play a major role in Bd-related amphibian declines. Mitchell et al. (2008)  predict that the longer the fungus persists in the aquatic environment, the greater its impact on host populations. Besides abiotic factors such as temperature and pH [22,24,27], the abundance and diversity of aquatic, Bd-ingesting microorganisms (predatory micro-eukaryotes) have recently been shown to dictate the Bd infection and disease dynamics in a European hotspot of chytridiomycosis by driving aquatic pathogen loads .
Within Central America, Bd has had devastating effects on amphibian biodiversity [3,9]. However, within this region, records show that stream-associated anuran species are considerably more likely to be categorized as critically endangered compared to those associated with tank bromeliads (S1 Table; OR of 8.88), and also significantly more threatened by Bd (S1 Table; OR of 4.79). Although the IUCN dataset used for these calculations also include non-peer reviewed literature and expert opinions, it does indicate a clear difference in the conservation status and susceptibility to Bd of bromeliad- and stream-associated amphibians in Central America. This agrees with previous studies suggesting that Central American amphibian species associated with bromeliads may be less affected in Bd outbreaks than riparian species in the same region [15–18]. Within Cusuco National Park (CNP), this same trend is observed: there are three declining riparian amphibian species in which chytridiomycosis is a suspected driver, while no negative population trends are reported for the bromeliad-associated species [18,25]. Here, we also show significantly lower prevalence of Bd in bromeliad species (3.4%) in comparison to stream-associated species (12.4%). Since only two bromeliad-associated amphibian species exist in CNP at the sampled elevation, and account for prevalence of Bd in this microhabitat for this study, differential intrinsic susceptibility of CNP’s amphibian species for Bd could be proposed as the underlying cause for the observed differences in Bd prevalence. However, taking into account all bromeliad- and stream-associated amphibian species of Central America, the same trend in differential effects of Bd on these species is observed, indicating other shared disease-steering factors associated with the aquatic habitat types.