Habitat fragmentation, not habitat loss, drives the prevalence of blood parasites in a Caribbean passerine

Abstract

Habitat destruction due to human land-use activities is well recognized as a central threat to biodiversity. However, there is still debate about the relative influence of its two components, habitat loss and habitat fragmentation, mostly because few studies have been able to disentangle their respective effects. We studied mechanisms by which habitat destruction might influence the prevalence of vector-transmitted haemosporidian blood parasites of the genera Plasmodium and Haemoproteus infecting the Lesser Antillean bullfinch Loxigilla noctis on the Caribbean islands of Guadeloupe and Martinique. Starting from a large set of environmental descriptors (including metrics reflecting habitat loss, habitat fragmentation and landscape heterogeneity; as well as other variables not linked to habitat destruction, such as climatic conditions), we used PLS regression analyses to determine which variables were driving parasite prevalence on the islands. Our results showed that variables related to forest destruction were much more influential than other factors for all parasites analyzed on both islands. Remarkably, the effects documented were almost exclusively due to forest fragmentation, as opposed to habitat loss. This positive effect of forest fragmentation on blood parasite prevalence is proposed to happen through its effects on insect vectors and/or host biology. Increased understanding of the role of habitat fragmentation as a driver of parasitic diseases can help limiting the risk of emergence and proliferation of wildlife pathogenic outbreaks and zoonosis through informed landscape planning.

Correlates of blood parasitism in a threatened marshland passerine: infection by kinetoplastids of the genus Trypanosoma is related to landscape metrics of habitat edge

“…Using QGIS software (QGIS Development Team, 2018) and ellipsoidal (GRS 1980) measurement, for each patch and/or capture point, we calculated biologically informative metrics characterizing the proximity, amount and complexity of edge in the breeding habitat (Table 1). These metrics are commonly applied in landscape ecology, also in the context of blood parasitism and vector occurrence (McGarigal et al ., 2012; Li et al ., 2016; Pérez-Rodríguez et al ., 2018). To ease interpretation of the effects of the metrics on infection status, we provide their correlation matrix, alongside with the total length of edge and the area of a patch (Table S1).…”

“…The diversity and prevalence of blood parasites within an avian host species are explained by a range of factors, of which potent ones are landscape features (Sehgal, 2015; Ferraguti et al ., 2018; Pérez-Rodríguez et al ., 2018). Prevalence is related to, for instance, the altitude and distance to water course or water body, as well as habitat degradation (van Riper et al ., 1986; Wood et al ., 2007; Bonneaud et al ., 2009; Loiseau et al ., 2010; Belo et al ., 2011; Knowles et al ., 2011; Gonzalez-Quevedo et al ., 2014; Krama et al ., 2015; Reinoso-Pérez et al ., 2016).…”

“…Also, habitat fragmentation and heterogeneity are expected to affect parasite infection in birds, through increased edge effects and the introduction of new parasite lineages by species occupying ecotones and areas between fragments (Loye and Carroll, 1995; Holmes, 1996). However, studies that addressed the relationship between habitat fragmentation/edge and blood parasite infection in birds are scarce, focused solely on forest habitats and only two of them involved intraspecific comparisons (Sebaio et al ., 2010; Laurance et al ., 2013; Gudex-Cross et al ., 2015; Pérez-Rodríguez et al ., 2018). For example, in a forest passerine, the Antillean Bullfinch ( Loxigilla noctis ), prevalence of two hemosporidian lineages is positively related to variables describing habitat fragmentation and amount of edge (Pérez-Rodríguez et al ., 2018).…”

“…However, studies that addressed the relationship between habitat fragmentation/edge and blood parasite infection in birds are scarce, focused solely on forest habitats and only two of them involved intraspecific comparisons (Sebaio et al ., 2010; Laurance et al ., 2013; Gudex-Cross et al ., 2015; Pérez-Rodríguez et al ., 2018). For example, in a forest passerine, the Antillean Bullfinch ( Loxigilla noctis ), prevalence of two hemosporidian lineages is positively related to variables describing habitat fragmentation and amount of edge (Pérez-Rodríguez et al ., 2018). To our knowledge, treeless habitats have not been studied in this respect, while a similar pattern could be expected due to negative edge effects on parasitism in some animal taxa (Ries et al ., 2004).…”

The importance of core habitat for a threatened species in changing landscapes

“…Habitat area independent of fragmentation does not always explain animals’ responses to landscape structure adequately (Ewers & Didham, ; Rybicki & Hanski, ). For example, fragmentation can increase the edge‐to‐area ratio of habitat patches beyond that resulting from habitat loss alone, further reducing the amount of interior or core habitat to buffer sensitive species from negative edge effects such as increased predation risk, interspecific competition, and/or parasitism (Pérez‐Rodríguez et al., ; Ries, Fletcher, Battin, & Sisk, ; Tscharntke et al., ). Moreover, core habitat availability may depend on characteristics of the landscape matrix, which can influence the abundance of predators, competitors, and/or parasites (Driscoll, Banks, Barton, Lindenmayer, & Smith, ; Ries et al., ).…”