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IntroductionEmerging infectious diseases are increasingly recognized as a global threat to wildlife. Pandemics in amphibians, caused by the fungal pathogen Batrachochytrium dendrobatidis (Bd), have resulted in biodiversity loss at a global scale. Genomic data suggest a complex evolutionary history of Bd lineages that vary in pathogenicity. Africa harbors a significant proportion of global amphibian biodiversity, and multiple Bd lineages are known to occur there; yet, despite the decline of many host species, there are currently no described Bd-epizootics. Here, we describe the historical and recent biogeographical spread of Bd and assess its risk to amphibians across the continent of Africa.MethodsWe provide a 165-year view of host-pathogen interactions by (i) employing a Bd assay to test 4,623 specimens (collected 1908–2013); (ii) compiling 12,297 published Bd records (collected 1852–2017); (iii) comparing the frequency of Bd-infected amphibians through time by both country and region; (iv) genotyping Bd lineages; (v) histologically identifying evidence of chytridiomycosis, and (vi) using a habitat suitability model to assess future Bd risk.ResultsWe found a pattern of Bd emergence beginning largely at the turn of the century. From 1852–1999, we found low Bd prevalence (3.2% overall) and limited geographic spread, but after 2000 we documented a sharp increase in prevalence (18.7% overall), wider geographic spread, and multiple Bd lineages that may be responsible for emergence in different regions. We found that Bd risk to amphibians was highest in much of eastern, central, and western Africa.DiscussionOur study documents a largely overlooked yet significant increase in a fungal pathogen that could pose a threat to amphibians across an entire continent. We emphasize the need to bridge historical and contemporary datasets to better describe and predict host-pathogen dynamics over larger temporal scales.

The emerging fungal pathogen, Batrachochytrium dendrobatidis (Bd), which can cause a fatal disease called chytridiomycosis, is implicated in the collapse of hundreds of host amphibian species. We describe chytridiomycosis dynamics in two co-occurring terrestrial salamander species, the Santa Lucia Mountains slender salamander, Batrachoseps luciae, and the arboreal salamander, Aneides lugubris. We (1) conduct a retrospective Bd-infection survey of specimens collected over the last century, (2) estimate present-day Bd infections in wild populations, (3) use generalized linear models (GLM) to identify biotic and abiotic correlates of infection risk, (4) investigate susceptibility of hosts exposed to Bd in laboratory trials, and (5) examine the ability of host skin bacteria to inhibit Bd in culture. Our historical survey of 2,866 specimens revealed that for most of the early 20th century (~1920–1969), Bd was not detected in either species. By the 1990s the proportion of infected specimens was 29 and 17% (B. luciae and A. lugubris, respectively), and in the 2010s it was 10 and 17%. This was similar to the number of infected samples from contemporary populations (2014–2015) at 10 and 18%. We found that both hosts experience signs of chytridiomycosis and suffered high Bd-caused mortality (88 and 71% for B. luciae and A. lugubris, respectively). Our GLM revealed that Bd-infection probability was positively correlated with intraspecific group size and proximity to heterospecifics but not to abiotic factors such as precipitation, minimum temperature, maximum temperature, mean temperature, and elevation, or to the size of the hosts. Finally, we found that both host species contain symbiotic skin-bacteria that inhibit growth of Bd in laboratory trials. Our results provide new evidence consistent with other studies showing a relatively recent Bd invasion of amphibian host populations in western North America and suggest that the spread of the pathogen may be enabled both through conspecific and heterospecific host interactions. Our results suggest that wildlife disease studies should assess host-pathogen dynamics that consider the interactions and effects of multiple hosts, as well as the historical context of pathogen invasion, establishment, and epizootic to enzootic transitions to better understand and predict disease dynamics.

Batrachochytrium dendrobatidis (Bd), a causal agent of the amphibian fungal skin disease chytridiomycosis, has been implicated in the decline and extinction of over 200 species worldwide since the 1970s. Despite almost two decades of research, the history of Bd and its global spread is not well understood. However, the spread of the Global Panzootic Lineage of Bd (Bd-GPL), the lineage associated with amphibian die-offs, has been linked with the American bullfrog (Rana [Aqurana] catesbeiana) and global trade. Interestingly, R. catesbeiana is native to the eastern U.S., where no Bd-related declines have been observed despite Bd's presence since the late 1800s. In contrast Bd has been found to have emerged in California and Mexico in the 1960s and 1970s, after which epizootics (i.e., epidemics in wildlife) ensued. We hypothesize that Bd-GPL spread from the eastern U.S. with the introduction of R. catesbeiana into the western US, resulting in epizootics and declines of native host species. Using museum records, we investigated the historical relationship between R. catesbeiana and Bd invasion in the western US and found that R. catesbeiana arrived in the same year or prior to Bd in most western watersheds that had data for both species, suggesting that Bd-GPL may have originated in the eastern US and R. catesbeiana may have facilitated Bd invasion in the western US. To predict areas with greatest suitability for Bd, we created a suitability model by integrating habitat suitability and host availability. When we incorporated invasion history with high Bd suitability, we found that watersheds with non-native R. catesbeiana in the mountain ranges of the West Coast have the highest disease risk. These findings shed light on the invasion history and disease dynamics of Bd in North America. Targeted historical surveys using archived specimens in natural history collections and present-day field surveys along with more localized, community-level studies, monitoring, and surveillance are needed to further test this hypothesis and grow our understanding of the disease ecology and host-pathogen dynamics of Bd.