Introduction
Land-use change is hypothesized to be a key driver of the emergence of
infectious disease (Foley et al., 2005; Lambin et al., 2010; Norris,
2004; Patz et al., 2000). Deforestation and the expansion of human
activity into forests can alter ecological communities and interactions
(Aguirrea & Taborb, 2008; Roque & Jansen, 2014) and thus potentially
increase the risk of infectious disease emergence from wildlife
reservoirs and vectors (Lambin et al., 2010; T. Lima et al., 2017;
McCauley et al., 2015; Vanwambeke et al., 2007). However, there is
debate on whether there is a generalizable effect of land-use patterns
and consequently changes in biodiversity on increased disease risk (Levi
et al., 2016; Ostfeld, 2013; Ostfeld & Keesing, 2013; Randolph &
Dobson, 2012; Wood et al., 2014; Wood & Lafferty, 2013). The question
of whether dilution, amplification, or neutralizing effects predominate
for particular infectious diseases (or entire suites of pathogens)
across gradients of disturbance and biodiversity is a challenging
empirical problem as the mechanisms are rarely clear and often
non-linear. This is particularly the case for vector-borne pathogens,
which land-use change can influence by modifying the composition,
density, and transmission traits of the hosts, vectors, and pathogens
(Burkett-Cadena & Vittor, 2018; Kocher et al., 2022).
Improved mechanistic understanding of how land-use change influences
host, vector, and pathogen networks is particularly critical in tropical
forests where anthropogenic impacts are rapidly altering landscapes and
the burden of disease is disproportionately high. Large-scale
deforestation and/or forest fragmentation can influence biodiversity by
several mechanisms that likely influence pathogen dynamics and
ultimately disease risk. For example, vertebrates at lower trophic
levels can become hyperabundant in fragmented forest due to energy-rich
subsidies from forest edges and the agricultural matrix (Luskin et al.,
2017; Marczak et al., 2007; Wilcox & Gubler, 2005), and due to
ecological release when habitat loss and/or fragmentation leads to the
decline of larger-bodied competitors and predators (Debinski & Holt,
2000; Nupp & Swihart, 1998; Ripple et al., 2014; Wilmers & Levi,
2013). These mechanisms are supported by field surveys in the southern
Amazon showing a strong negative association between the abundance of
common reservoir species and forest patch size, and the extirpation of
apex predators and other large-bodied taxa in the smallest forest
fragments (Michalski & Peres, 2007). However, as the context of
tropical deforestation changes from agricultural expansion by many
smallholders to large-scale agribusiness monocultures, the impacts of
this change on vertebrate community composition may disrupt the patterns
of forest loss and/or fragmentation on biodiversity witnessed thus far.
While disturbance-tolerant vertebrate reservoir hosts are likely to play
a key role in influencing disease prevalence and emergence as tropical
forest systems are fragmented (Johnson et al., 2013), this mechanism
alone is not sufficient to predict how disease risk changes as tropical
forests are degraded given how the intricate ecological network between
hosts, vectors, and pathogens can respond to forest loss in complex
ways. For vector-borne pathogens, even if forest edge increases the
abundance of reservoir hosts in tropical forests, pathogen reproduction
will be stymied if vector populations decline in edge habitats, if there
is spatial mismatch between hosts and vectors, or if vectors feed
disproportionately on species that are not competent reservoirs. While
studies have demonstrated some of the effects of land-use change on host
species (Guo et al., 2019; LoGiudice et al., 2003), little work has been
done to simultaneously examine the effects of deforestation on vectors,
hosts, and pathogens.
To tease apart the effects of large-scale land-use change on host and
vector communities, and consequently disease risk, we implemented a
multifaceted, landscape epidemiology approach using field surveys and
DNA metabarcoding of sandfly vectors and their bloodmeals to disentangle
the complex relationships between Leishmania parasites, the known
sandfly vectors, and the potential wildlife hosts (see Fig. 1) in
response to rapid deforestation across the Amazonian ‘Arc of
Deforestation’. Numerous Leishmania species cause cutaneous and
visceral leishmaniasis (Akhoundi et al., 2016), neglected tropical
diseases that are associated with both intact tropical forest (Jones et
al., 1987; Lainson, 1983; Travi et al., 1998) and forest fragments (De
Luca et al., 2003; Jones et al., 1987). The natural mammalian hosts are
diverse, but small mammals and armadillos (Dasypus spp.) are
thought to be strongly associated with Leishmania transmission
(Lainson et al., 1979; Lainson & Shaw, 1989; B. S. Lima et al., 2013;
Travi et al., 1994, 1998, 2002). Domesticated species, particularly dogs
(Canis lupus familiaris ), are also important hosts (Courtenay et
al., 2002; Gramiccia & Gradoni, 2005; Quinnell & Courtenay, 2009), and
may play a key role as conduits of disease transmission if forest
fragmentation leads to increased interactions between sylvatic and
domesticated species. Given that many Leishmania species that
cause leishmaniasis in humans are multi-host parasites (Roque & Jansen,
2014), their prevalent transmission pathways in deforested landscapes
remain an open question. Kocher et al. (2022) recently found that mammal
diversity, which declined with greater human footprint, was correlated
with lower reservoir host abundance, lower prevalence ofLeishmania spp. in sandflies, but high sandfly abundance. The
context for this work was the intrusion of small landholders into
otherwise vast, continuous tropical forest across 19 forest sites in
French Guiana. Here, we use a similar landscape epidemiology approach
but, in contrast to Kocher et al. (2022), we sampled a gradient of
forest loss and fragmentation that represents the most typical
deforestation pattern witnessed across much of the Amazon and other
tropical forest ecosystems worldwide, where >70% of all
remaining forests is now within 1 km of a forest edge (Haddad et al.,
2015) primarily due to agricultural expansion (Geist & Lambin, 2002).
Within this context, we ask how large-scale deforestation influencesLeishmania hosts, vectors, their interactions, and pathogen
prevalence. Specifically, we hypothesized that deforestation would be
associated with increased bloodmeals derived from competent hosts that
proliferate due to matrix subsidies and relaxed top-down control, and
that sandfly vector abundance may increase as a result of higher host
density in degraded forests.