Bird species with wider geographical ranges have higher blood parasite diversity but not prevalence across the African-Eurasian flyway

Understanding the drivers of broad-scale patterns in parasite infection is vital in predicting alterations in geographical distribution due to global changes, or impacts on hosts through exposure to novel parasites (van Riper III et al., 1986; Goulson et al., 2015). Migratory species may be particularly important in this regard, because changing patterns of migration (Plummer et al., 2015) may either bring migratory species into contact with novel parasites (Morgan et al., 2007, Kubelka et al., 2022), or transfer parasites into novel areas (de Angeli Dutra et al., 2021b). Migratory species tend to host a more diverse range of parasites than their resident counterparts (Figuerola and Green, 2000, Koprivnikar and Leung, 2015, Jenkins et al., 2016, Shaw et al., 2018), although a recent global study found this pattern only for helminth species richness, not haemosporidian species richness (Gutiérrez et al., 2019). However, patterns for parasite prevalence are less consistent (Figuerola and Green, 2000), and can vary markedly between different parasite genera (Fecchio et al., 2021).

Migration is an energetically costly activity (Wikelski et al., 2003), and preparation for migration can cause a decreased investment in non-flight-related functions such as the immune system (Owen and Moore, 2006, Owen and Moore, 2008). Any effects of infection on migratory birds are mixed: Garvin et al. (2006), found negative associations between blood parasite infection and fat scores or body condition in only four of 54 bird species examined. Similarly, Cornelius et al. (2014) found little evidence that haemosporidian infection negatively affects three species of migratory songbirds, finding elevated leucocyte counts in one species, but with no significant effects on cellular immunity, body condition or fat reserves (Cornelius et al., 2014). Other earlier findings suggest that infection does not generally impact preparation for migration or migratory schedules (Santiago-Alarcon et al., 2013, Hahn et al., 2018). However, more recent studies found that juvenile birds infected by certain parasite lineages arrived later on breeding grounds (Ágh et al., 2022), and that birds with higher blood parasite infection intensities delayed the onset of autumn migration (Emmenegger et al., 2021).

Many migratory birds move intercontinentally, likely encountering a wider variety of parasites than resident species on breeding, wintering and stopover grounds, potentially leading to a higher parasite diversity (de Angeli Dutra et al., 2021a). Infection by blood parasites can increase stopover time in migrants (Hegemann et al., 2018), which may potentially increase the likelihood of gaining further infections at stopover sites, although stopover can also allow birds to increase immune function (Eikenaar et al., 2020). Migratory birds may act as reservoirs of blood parasites and introduce them to resident species (Hellgren et al., 2007, Yoshimura et al., 2014, Pulgarín-R et al., 2019). However, parasite lineages have varying levels of host specificity, which may limit the role of migrants in their dispersal (Pulgarín-R et al., 2019, Soares et al., 2020). Indeed, any lineage sharing may strongly depend on the relatedness of migrant and resident species (Clark et al., 2016, Ricklefs et al., 2017). Whilst intercontinental migrants range seasonally over a wide geographic area, many resident species have been introduced beyond their native range, so will be exposed to a wide diversity of locally transmitted parasites across the entirety of their native and introduced range (Clark et al., 2015, Marzal et al., 2018). These species provide an ideal opportunity to test whether it is migratory strategy, or geographic range, that drives patterns of parasite diversity and prevalence at the continental scale.

Haemosporidian genera tend to differ in their degrees of host specialism, and consequently in their abilities to be transmitted between different host species (Hellgren et al., 2009). Within avian blood parasites, Plasmodium lineages tend to be more generalist, with Haemoproteus and Leucocytozoon more specialist (Gupta et al., 2019, Ellis et al., 2020), although there is significant inter-lineage variation within each genus (Moens et al., 2016, Ellis et al., 2020). Each parasite genus has distinct vectors, which may also influence patterns of host distribution, either through vector distribution, vector competence, or vector biting preferences (Valkiūnas, 2005).

Here, we expand on previous studies testing the drivers of large-scale patterns in blood parasite prevalence and diversity (de Angeli Dutra et al., 2021a), testing for the consistency of patterns between the Americas and those found in African-Palaearctic migrants by examining the prevalence and lineage diversity of Plasmodium, Haemoproteus and Leucocytozoon in African-Palaearctic migrants and resident birds. Compared with species found in the Americas, African-Palaearctic migrants tend to have longer migration distances, and migrants and African resident species tend to be more phylogenetically distinct than American species found together on wintering grounds (Ricklefs et al., 2017). The African-Palaearctic dataset also includes species resident across similar geographical ranges to migrant species, allowing us to directly test whether migratory strategy, or range size, might drive any observed differences. We tested two opposing hypotheses: i) migratory birds would have a higher parasite diversity and lineage richness than all three groups of resident species due to a combination of their exposure to infection on breeding, wintering and staging grounds; and ii) species resident on both continents would have similar parasite prevalence and diversity to migratory birds, and both would have higher prevalence and diversity than species resident in either Africa or Europe, due to similar overall geographic range. Furthermore, we predicted that these patterns may differ between parasite genera due to differing vector distributions.

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