A series of terribly unfortunate events: How environment and infection synergized to cause the Kihansi spray toad extinction

Outbreaks of emerging infectious diseases are trained by local biotic and abiotic factors, with host declines occurring when conditions favour the pathogen. Extinction of the Tanzanian Kihansi spray toad (Nectophrynoides asperginis) in 2004 was contemporaneous with the construction of a dam, implicating habitat modification in the loss of this species. However, high burdens of a globally emerging infection, Batrachochytrium dendrobatidis (Bd) were synchronously observed implicating infectious disease in this toads extinction. Here, by shotgun sequencing skin DNA from archived toad mortalities and assembling chytrid mitogenomes, we prove this outbreak was caused by the BdCAPE lineage and not the panzootic lineage BdGPL that is widely associated with global amphibian extinctions. Molecular dating showed an invasion of BdCAPE across Southern Africa overlapping with the timing of the extinction event. However, post-outbreak surveillance of conspecific species inhabiting this mountainous region showed widespread infection by BdCAPE yet no signs of amphibian ill-health or species decline. Our findings show that despite efforts to mitigate the environmental impact caused by dams construction, invasion of the pathogen ultimately led to the loss of the Kihansi spray toad; a synergism between emerging infectious disease and environmental change that likely heralds wider negative impacts on biodiversity in the Anthropocene.

Disease driven extinction in the wild of the Kihansi spray toad (Nectophrynoides asperginis)

The Kihansi spray toad, Nectophrynoides asperginis, became extinct in the wild despite population monitoring and conservation management of its habitat in the Kihansi gorge, Tanzania. Anecdotal evidence has indicated human induced habitat modification, predators, pesticides and disease as possible causes of a rapid population decline and the species extirpation. Here, we systematically investigate the role of disease in the extinction event of the wild toad population. The amphibian chytrid fungus, Batrachochytrium dendrobatidis, was detected in spray toads that died during the extinction event and subsequently in other amphibian species in Kihansi Gorge and the adjacent Udagaji Gorge, but not in any toads collected prior to this. Following the population decline, the remnant spray toad population gradually disappeared over a nine-month period. We demonstrate how demographic and behavioral attributes predisposed the spray toads to chytridiomycosis, due to B. dendrobatidis infection, and how epidemic disease could have been exacerbated by altered environmental conditions in the spray wetlands. Our results show that chytridiomycosis was the proximate cause of extinction in the wild of N. asperginis. This represents the first known case of extinction by disease of an amphibian species in Africa. A captive breeding program in the US and Tanzania ensures the survival of the species and a reintroduction program is underway. However, we caution that chytridiomycosis remains an existing threat that requires a comprehensive mitigation strategy before the desired conservation outcome of an established population of repatriated toads can be achieved.