Discussion
There has been a robust debate about whether there is a generalizable effect of changes in biodiversity (as a consequence of habitat loss and/or fragmentation) on the emergence and prevalence of infectious diseases (Levi et al., 2016; Ostfeld, 2013; Ostfeld & Keesing, 2013; Randolph & Dobson, 2012; Wood et al., 2014; Wood & Lafferty, 2013). This debate has been stymied by a lack of landscape-scale empirical data across land-use gradients and observational approaches that are unable to deduce the mechanistic underpinning to changing disease risk. This can be especially complex for vector-borne pathogens where land-use change can differentially influence hosts, vectors, and pathogens (Burkett-Cadena & Vittor, 2018). We addressed this debate with a landscape scale epidemiology approach across a forest habitat loss gradient within the world’s largest tropical deforestation frontier induced by large-scale agricultural commodity production.
By using DNA metabarcoding of sandflies and their vertebrate bloodmeals, we were able to link medically important hosts and vectors to deforestation at large scales (56,775 sandflies collected from 27 light traps set for 3 days at each of the 39 sites). Metabarcoding allowed us to identify thousands of sandflies at the species or genus level so that the ecology of vectors and non-vectors could be investigated. Species level sandfly data is usually only possible with painstaking morphological identification of sandfly species, which requires rare taxonomic expertise. In contrast, previous research has shown that DNA derived from sandflies are a good measure of the vertebrate diversity in this landscape and requires significantly less resources and identification effort (Massey et al., 2022). Ideally, sample pools would have included fewer individuals, or we would have a larger sample size, so that direct vector to host comparisons and interaction networks could be quantified without data contamination from multiple sandflies sequenced as part of the same pool. However, metabarcoding of sandfly pools allowed for sufficient cost reduction to allow sequencing of over 50,000 individual sandflies to taxonomically identify both sandfly species and any vertebrate bloodmeal remnants.
Fundamentally, sandfly responses to deforestation reported here were nuanced. Although total sandfly abundance did not vary with deforestation, the relative abundance of vector species ordinated in the direction of greater forest cover with the most significant positive response to forest cover found with Psychodopygus davisi , a known vector of Leishmania braziliensis (Fig. 4). Further, the probability of a sandfly pool containing any vector or the dominant sandfly vector genus, Nyssomyia spp., was higher at sites surrounded by less cattle pasture (Fig. 4). Psychodopygus davisiand Nyssomyia spp. are vectors known for transmitting species ofLeishmania responsible for cutaneous leishmaniasis in Brazil, which while treatable, causes disfiguring and painful skin lesions. We found no significant positive responses of sandfly density or the probability of finding a vector species to increasing deforestation which runs counter to the hypothesis that vector amplification (as a consequence of increased host density) occurs in response to deforestation.
However, disease risk is a product of both vector and host ecology. Despite the heavily deforested nature of this region, we found that this landscape supports a large diversity of terrestrial and arboreal vertebrate species. The majority of sylvatic vertebrate taxa we detected using sandflies as a source of iDNA are known host species forLeishmania parasites. The responses of sylvatic vertebrate taxa in sandfly bloodmeals were driven by the high prevalence of armadillos in the genus Dasypus, particularly the disturbance-tolerant nine-banded armadillo, D. novemcinctus , which was by far the most common source of bloodmeals (Fig. 3). These data suggest that sandflies strongly select for armadillos, which are among the most important hosts for Leishmania spp., which cause leishmaniasis in humans (Christensen et al., 1982; Kocher et al., 2017; Lainson & Shaw, 1989). Armadillos were the only prevalent vertebrate taxa to show a significant relationship to the deforestation gradient with increased probability of finding D. novemcinctus in sandfly bloodmeals as forest cover decreased (Fig. 4). Bipartite networks, which directly measured sandfly × vertebrate interactions, and the Leishmania -positive samples suggest that armadillos drive the feeding ecology of sandflies andLeishmania transmission dynamics across a degraded forest landscape. However, we excluded domesticated species from our analyses because (i) we were primarily concerned with how land use change influences wild vertebrate communities, and (ii) possible routine lab contamination. Even with conservative read thresholds, we found that domestic dog (Canis lupus familiaris ) occurred in just over 20% of the sandfly samples and was ubiquitous across the landscape (Appendix SI: Fig. S1), including in some samples that also containedDasypus (Appendix SI: Fig. S3). Given that pathogen spillover to humans increases when domesticated species are in close proximity to sylvatic hosts, domestic dogs may play a key role in peridomestic transmission of Leishmania to humans. Our findings support this potential mechanism of zoonotic disease transmission primarily through the observed pattern of armadillo and dog co-occurrences from sample pools across the study area.
While our sampling scheme allowed us to sample across a landscape-scale deforestation gradient, it is important to note that we did not sample the extremes of vast tracts of continuous, undisturbed forests (compared with Kocher et al. 2022) nor entirely deforested landscapes lacking forest remnants. Consequently, while there was a gradient of deforestation across our study region, it is likely that the current forest landscape structure has not resulted in the same level of extirpation of vertebrate species as other studies have documented. Instead, our study system represents a landscape-scale deforestation gradient resulting from rapid and recent forest conversion into seed crop agriculture. As discussed previously, this expansion of human activity into tropical forests can alter ecological communities and species interactions particularly at transition zones between forests and peri-urban areas (Aguirrea & Taborb, 2008; Roque & Jansen, 2014), thereby potentially increasing the risk of infectious disease emergence from wildlife reservoirs and vectors into domestic vertebrate hosts and/or humans (Lambin et al., 2010; T. Lima et al., 2017; McCauley et al., 2015; Vanwambeke et al., 2007). Our findings support this given the high diversity of vertebrate hosts and sandfly vectors found across the landscape and the lack of localized extinctions at even the most forest degraded sites.
In summary, we found that it was most important to examine the responses of individual species even when investigating the generality of biodiversity and disease risk to land-use change. While overall sandfly abundance (including non-vectors) was unrelated to deforestation, sandfly vectors were more strongly associated with more intact forest landscapes (either more forest or less pasture), which was largely driven by the response of the dominant vector taxa (Nyssomyiaspp. ). Likewise, changes in the relative abundance of sylvatic hosts (namely armadillos) were apparent despite no significant response of the aggregate vertebrate host community across the deforestation gradient. Additionally, samples that tested positive for the presence ofLeishmania species also failed to show any response to forest cover, pasture cover, or distance to the urban center, suggesting thatLeishmania transmission can occur across both intact and degraded forests in this system. In conclusion, the complex combined responses of vectors and hosts within the context of partly deforested landscapes did not support the generality of the ‘dilution effect’ hypothesis. However, patterns of individual species responses to deforestation and vector × host interactions across the deforestation gradient show disease risk consequences of forest conversion and increased human encroachment into Amazonian primary forest.