Does deforestation beget disease?: Leishmania host and vector
communities across a gradient of forest loss on the Amazonian
deforestation frontier
Abstract
There is ongoing debate concerning whether there exists a generalizable
effect of land-use change on biodiversity and consequently zoonotic
disease risk. Strong data informing this debate is sparse because
ecological and sampling complexities make it challenging to establish
direct links between vertebrate hosts (and non-hosts), vectors, and
pathogens across landscapes. However, emerging molecular methods using
invertebrate-derived DNA (iDNA) can now measure species diversity and
interactions from vector bloodmeals, which has the potential to improve
mechanistic understanding of the effects of land-use change on zoonotic
disease risk. Here, we used iDNA metabarcoding of vectors and their
bloodmeals to disentangle the complex relationships between Leishmania
parasites, known sandfly vectors, and potential wildlife hosts. We
collected 56,775 sandflies during 3,159 trap nights at 39 forested sites
across the southern Amazon ‘Arc of Deforestation’, which exemplifies
global patterns of deforestation and fragmentation at the borders of
tropical forest ecosystems due to agricultural expansion. We found that
vector community composition was influenced by forest cover and pasture
cover, and the most common vector, Nyssomia spp., was encountered less
frequently in forests surrounded by pasture. Sandflies fed on a
diversity of vertebrates, but the edge-loving nine-banded armadillo,
Dasypus novemcinctus, was overwhelmingly the most prevalent host,
followed by the greater long-nosed armadillo, Dasypus kappleri. The
probability of a host being detected in sandfly bloodmeals was lower at
sites with higher forest cover, which was overwhelmingly due to reduced
bloodmeals arising from D. novemcinctus. Armadillos were also the most
prevalent sylvatic vertebrate taxon in sandfly pools that were positive
for Leishmania, further suggesting that these xenarthrans are a key host
pathway for zoonotic disease transmission.