Fine-scale variation in vector host use and force of infection drive localized patterns of West Nile virus transmission

The influence of host diversity on multi-host pathogen transmission and persistence can be confounded by the large number of species and biological interactions that can characterize many transmission systems. For vector-borne pathogens, the composition of host communities has been hypothesized to affect transmission; however, the specific characteristics of host communities that affect transmission remain largely unknown. We tested the hypothesis that vector host use and force of infection (i.e., the summed number of infectious mosquitoes resulting from feeding upon each vertebrate host within a community of hosts), and not simply host diversity or richness, determine local infection rates of West Nile virus (WNV) in mosquito vectors. In suburban Chicago, Illinois, USA, we estimated community force of infection for West Nile virus using data on Culex pipiens mosquito host selection and WNV vertebrate reservoir competence for each host species in multiple residential and semi-natural study sites. We found host community force of infection interacted with avian diversity to influence WNV infection in Culex mosquitoes across the study area. Two avian species, the American robin (Turdus migratorius) and the house sparrow (Passer domesticus), produced 95.8% of the infectious Cx. pipiens mosquitoes and showed a significant positive association with WNV infection in Culex spp. mosquitoes. Therefore, indices of community structure, such as species diversity or richness, may not be reliable indicators of transmission risk at fine spatial scales in vector-borne disease systems. Rather, robust assessment of local transmission risk should incorporate heterogeneity in vector host feeding and variation in vertebrate reservoir competence at the spatial scale of vector-host interaction.     

Influence of land use and host species on parasite richness,prevalence and co-infection patterns

Tropical forests are experiencing increasing impacts from a multitude of anthropogenic activities such as logging and conversion to agricultural use. These perturbations are expected to have strong impacts on ecological interactions and on the transmission dynamics of infectious diseases. To date, no clear picture of the effects of deforestation on vector-borne disease transmission has emerged. This is associated with the challenge of studying complex systems where many vertebrate hosts and vectors co-exist. To overcome this problem, we focused on an innately simplified system – a small oceanic island (São Tomé, Gulf of Guinea). We analyzed the impacts of human land-use on host-parasite interactions by sampling the bird community (1735 samples from 30 species) in natural and anthropogenic land use at different elevations, and screened individuals for haemosporidian parasites from three genera (Plasmodium, Haemoproteus, Leucocytozoon). Overall, Plasmodium had the highest richness but the lowest prevalence, while Leucocytozoon diversity was the lowest despite having the highest prevalence. Interestingly, co-infections (i.e. intra-host diversity) involved primarily Leucocytozoon lineages (95%). We also found marked differences between bird species and habitats. Some bird species showed low prevalence but harbored high diversity of parasites, while others showed high prevalence but were infected with fewer lineages. These infection dynamics are most likely driven by host specificity of parasites and intrinsic characteristics of hosts. In addition, Plasmodium was more abundant in disturbed habitats and at lower elevations, while Leucocytozoon was more prevalent in forest areas and at higher elevations. These results likely reflect the ecological requirements of their vectors: mosquitoes and black flies, respectively.     

Avian host community structure and prevalence of West Nile virus in Chicago,Illinois

Vertebrate host diversity has been postulated to mediate prevalence of zoonotic, vector-borne diseases, such that as diversity increases, transmission dampens. This “dilution effect” is thought to be caused by distribution of infective bites to incompetent reservoir hosts. We quantified avian species richness, avian seroprevalence for antibodies to West Nile virus (WNV), and infection of WNV in Culex mosquitoes, in the Chicago metropolitan area, Illinois, USA, a region of historically high WNV activity. Results indicated high overall avian seroprevalence and variation in seroprevalence across host species; however, there was no negative correlation between avian richness and Culex infection rate or between richness and infection status in individual birds. Bird species with high seroprevalence, especially northern cardinals and mourning doves, may be important sentinels for WNV in Chicago, since they were common and widespread among all study sites. Overall, our results suggest no net effect of increasing species richness to West Nile virus transmission in Chicago. Other intrinsic and extrinsic factors, such as variation in mosquito host preference, reservoir host competence, temperature, and precipitation, may be more important than host diversity for driving interannual variation in WNV transmission. These results from a fine-scale study call into question the generality of a dilution effect for WNV at coarser spatial scales.     

Vector host-feeding preferences drive transmission of multi-host pathogens: West Nile virus as a model system

Seasonal epizootics of vector-borne pathogens infecting multiple species are ecologically complex and difficult to forecast. Pathogen transmission potential within the host community is determined by the relative abilities of host species to maintain and transmit the pathogen and by ecological factors influencing contact rates between hosts and vectors. Increasing evidence of strong feeding preferences by a number of vectors suggests that the host community experienced by the pathogen may be very different from the local host community. We developed an empirically informed transmission model for West Nile virus (WNV) in four sites using one vector species (Culex pipiens) and preferred and non-preferred avian hosts. We measured strong feeding preferences for American robins (Turdus migratorius) by Cx. pipiens, quantified as the proportion of Cx. pipiens blood meals from robins in relation to their abundance (feeding index). The model accurately predicted WNV prevalence in Cx. pipiens at three of four sites. Sensitivity analysis revealed feeding preference was the most influential parameter on intensity and timing of peak WNV infection in Cx. pipiens and a threshold feeding index for transmission was identified. Our findings indicate host preference-induced contact heterogeneity is a key mediator of vector-borne pathogen epizootics in multi-species host communities, and should be incorporated into multi-host transmission models.     

Loss of forest cover and host functional diversity increases prevalence of avian malaria parasites in the Atlantic Forest

Host phylogenetic relatedness and ecological similarity are thought to contribute to parasite community assembly and infection rates. However, recent landscape level anthropogenic changes may disrupt host-parasite systems by impacting functional and phylogenetic diversity of host communities. We examined whether changes in host functional and phylogenetic diversity, forest cover, and minimum temperature influence the prevalence, diversity, and distributions of avian haemosporidian parasites (genera Haemoproteus and Plasmodium) across 18 avian communities in the Atlantic Forest. To explore spatial patterns in avian haemosporidian prevalence and taxonomic and phylogenetic diversity, we surveyed 2241 individuals belonging to 233 avian species across a deforestation gradient. Mean prevalence and parasite diversity varied considerably across avian communities and parasites responded differently to host attributes and anthropogenic changes. Avian malaria prevalence (termed herein as an infection caused by Plasmodium parasites) was higher in deforested sites, and both Plasmodium prevalence and taxonomic diversity were negatively related to host functional diversity. Increased diversity of avian hosts increased local taxonomic diversity of Plasmodium lineages but decreased phylogenetic diversity of this parasite genus. Temperature and host phylogenetic diversity did not influence prevalence and diversity of haemosporidian parasites. Variation in the diversity of avian host traits that promote parasite encounter and vector exposure (host functional diversity) partially explained the variation in avian malaria prevalence and diversity. Recent anthropogenic landscape transformation (reduced proportion of native forest cover) had a major influence on avian malaria occurrence across the Atlantic Forest. This suggests that, for Plasmodium, host phylogenetic diversity was not a biotic filter to parasite transmission as prevalence was largely explained by host ecological attributes and recent anthropogenic factors. Our results demonstrate that, similar to human malaria and other vector-transmitted pathogens, prevalence of avian malaria parasites will likely increase with deforestation.     

Ecosystem dynamics, biological diversity and emerging infectious diseases

In this article, we summarize the major scientific developments of the last decade on the transmission of infectious agents in multi-host systems. Almost sixty percent of the pathogens that have emerged in humans during the last 30-40 years are of animal origin and about sixty percent of them show an important variety of host species besides humans (3 or more possible host species). In this review, we focus on zoonotic infections with vector-borne transmission and dissect the contrasting effects that a multiplicity of host reservoirs and vectors can have on their disease dynamics. We discuss the effects exerted by host and vector species richness and composition on pathogen prevalence (i.e., reduction, including the dilution effect, or amplification). We emphasize that, in multiple host systems and for vector-borne zoonotic pathogens, host reservoir species and vector species can exert contrasting effect locally. The outcome on disease dynamics (reduced pathogen prevalence in vectors when the host reservoir species is rich and increased pathogen prevalence when the vector species richness increases) may be highly heterogeneous in both space and time. We then ask briefly how a shift towards a more systemic perspective in the study of emerging infectious diseases, which are driven by a multiplicity of hosts, may stimulate further research developments. Finally, we propose some research avenues that take better into account the multi-host species reality in the transmission of the most important emerging infectious diseases, and, particularly, suggest, as a possible orientation, the careful assessment of the life-history characteristics of hosts and vectors in a community ecology-based perspective.     

Risk of Exposure to Eastern Equine Encephalomyelitis Virus Increases with the Density of Northern Cardinals

For a variety of infectious diseases, the richness of the community of potential host species has emerged as an important factor in pathogen transmission, whereby a higher richness of host species is associated with a lowered disease risk. The proposed mechanism driving this pattern is an increased likelihood in species-rich communities that infectious individuals will encounter dead-end hosts. Mosquito-borne pathogen systems potentially are exceptions to such “dilution effects” because mosquitoes vary their rates of use of vertebrate host species as bloodmeal sources relative to host availabilities. Such preferences may violate basic assumptions underlying the hypothesis of a dilution effect in pathogen systems. Here, we describe development of a model to predict exposure risk of sentinel chickens to eastern equine encephalitis virus (EEEV) in Walton County, Florida between 2009 and 2010 using avian species richness as well as densities of individual host species potentially important to EEEV transmission as candidate predictor variables. We found the highest support for the model that included the density of northern cardinals, a highly preferred host of mosquito vectors of EEEV, as a predictor variable. The highest-ranking model also included Culiseta melanura abundance as a predictor variable. These results suggest that mosquito preferences for vertebrate hosts influence pathogen transmission.     

Modelling transmission of vector-borne pathogens shows complex dynamics when vector feeding sites are limited

The relationship between species richness and the prevalence of vector-borne disease has been widely studied with a range of outcomes. Increasing the number of host species for a pathogen may decrease infection prevalence (dilution effect), increase it (amplification), or have no effect. We derive a general model, and a specific implementation, which show that when the number of vector feeding sites on each host is limiting, the effects on pathogen dynamics of host population size are more complex than previously thought. The model examines vector-borne disease in the presence of different host species that are either competent or incompetent (i.e. that cannot transmit the pathogen to vectors) as reservoirs for the pathogen. With a single host species present, the basic reproduction ratio R(0) is a non-monotonic function of the population size of host individuals (H), i.e. a value [Formula: see text] exists that maximises R(0). Surprisingly, if [Formula: see text] a reduction in host population size may actually increase R(0). Extending this model to a two-host species system, incompetent individuals from the second host species can alter the value of [Formula: see text] which may reverse the effect on pathogen prevalence of host population reduction. We argue that when vector-feeding sites on hosts are limiting, the net effect of increasing host diversity might not be correctly predicted using simple frequency-dependent epidemiological models.     

Drivers of community turnover differ between avian hemoparasite genera along a North American latitudinal gradient

The latitudinal diversity gradient (LDG) is an established macroecological pattern, but is poorly studied in microbial organisms, particularly parasites. In this study, we tested whether latitude, elevation, and host species predicted patterns of prevalence, alpha diversity, and community turnover of hemosporidian parasites. We expected parasite diversity to decrease with latitude, alongside the diversity of their hosts and vectors. Similarly, we expected infection prevalence to decrease with latitude as vector abundances decrease. Lastly, we expected parasite community turnover to increase with latitudinal distance and to be higher between rather than within host species. We tested these hypotheses by screening blood and tissue samples of three closely related avian species in a clade of North American songbirds (Turdidae: Catharus, n = 466) across 17.5° of latitude. We used a nested PCR approach to identify parasites in hemosporidian genera that are transmitted by different dipteran vectors. Then, we implemented linear‐mixed effects and generalized dissimilarity models to evaluate the effects of latitude, elevation, and host species on parasite metrics. We found high diversity of hemosporidian parasites in Catharus thrushes (n = 44 lineages) but no evidence of latitudinal gradients in alpha diversity or prevalence. Parasites in the genus Leucocytozoon were most prevalent and lineage rich in this study system; however, there was limited turnover with latitude and host species. Contrastingly, Plasmodium parasites were less prevalent and diverse than Leucocytozoon parasites, yet communities turned over at a higher rate with latitude and host species. Leucocytozoon communities were skewed by the dominance of one or two highly prevalent lineages with broad latitudinal distributions. The few studies that evaluate the hemosporidian LDG do not find consistent patterns of prevalence and diversity, which makes it challenging to predict how they will respond to global climate change.     

Parasite Prevalence Corresponds to Host Life History in a Diverse Assemblage of Afrotropical Birds and Haemosporidian Parasites

Avian host life history traits have been hypothesized to predict rates of infection by haemosporidian parasites. Using molecular techniques, we tested this hypothesis for parasites from three haemosporidian genera (Plasmodium, Haemoproteus, and Leucocytozoon) collected from a diverse sampling of birds in northern Malawi. We found that host life history traits were significantly associated with parasitism rates by all three parasite genera. Nest type and nest location predicted infection probability for all three parasite genera, whereas flocking behavior is an important predictor of Plasmodium and Haemoproteus infection and habitat is an important predictor of Leucocytozoon infection. Parasite prevalence was 79.1% across all individuals sampled, higher than that reported for comparable studies from any other region of the world. Parasite diversity was also exceptionally high, with 248 parasite cytochrome b lineages identified from 152 host species. A large proportion of Plasmodium, Haemoproteus, and Leucocytozoon parasite DNA sequences identified in this study represent new, previously undocumented lineages (n = 201; 81% of total identified) based on BLAST queries against the avian malaria database, MalAvi.     

Migratory birds have higher prevalence and richness of avian haemosporidian parasites than residents

Individuals of migratory species may be more likely to become infected by parasites because they cross different regions along their route, thereby being exposed to a wider range of parasites during their annual cycle. Conversely, migration may have a protective effect since migratory behaviour allows hosts to escape environments presenting a high risk of infection. Haemosporidians are one of the best studied, most prevalent and diverse groups of avian parasites, however the impact of avian host migration on infection by these parasites remains controversial. We tested whether migratory behaviour influenced the prevalence and richness of avian haemosporidian parasites among South American birds. We used a dataset comprising ~ 11,000 bird blood samples representing 260 bird species from 63 localities and Bayesian multi-level models to test the impact of migratory behaviour on prevalence and lineage richness of two avian haemosporidian genera (Plasmodium and Haemoproteus). We found that fully migratory species present higher parasite prevalence and higher richness of haemosporidian lineages. However, we found no difference between migratory and non-migratory species when evaluating prevalence separately for Plasmodium and Haemoproteus, or for the richness of Plasmodium lineages. Nevertheless, our results indicate that migratory behaviour is associated with an infection cost, namely a higher prevalence and greater variety of haemosporidian parasites.     

Local host-tick coextinction in neotropical forest fragments

Ticks are obligatory parasites with complex life cycles that often depend on larger bodied vertebrates as final hosts. These traits make them particularly sensitive to local coextinction with their host. Loss of wildlife abundance and diversity should thus lead to loss of tick abundance and diversity to the point where only generalist tick species remain. However, direct empirical tests of these hypotheses are lacking, despite their relevance to our understanding of tick-borne disease emergence in disturbed environments. Here, we compare vertebrate and tick communities across 12 forest islands and peninsulas in the Panama Canal that ranged 1000-fold in size (2.6–2811.3?ha). We used drag sampling and camera trapping to directly assess the abundance and diversity of communities of questing ticks and vertebrate hosts. We found that the abundance and species richness of ticks were positively related to those of wildlife. Specialist tick species were only present in fragments where their final hosts were found. Further, less diverse tick communities had a higher relative abundance of the generalist tick species Amblyomma oblongoguttatum, a potential vector of spotted fever group rickettsiosis. These findings support the host-parasite coextinction hypothesis, and indicate that loss of wildlife can indeed have cascading effects on tick communities. Our results also imply that opportunities for pathogen transmission via generalist ticks may be higher in habitats with degraded tick communities. If these patterns are general, then tick identities and abundances serve as useful bioindicators of ecosystem health, with low tick diversity reflecting low wildlife diversity and a potentially elevated risk of interspecific disease transmission via remaining host species and generalist ticks.     

Higher infection probability of haemosporidian parasites in Blue-black Grassquits (Volatinia jacarina) inhabiting native vegetation across Brazil

Human induced changes on landscape can alter the biotic and abiotic factors that influence the transmission of vector-borne parasites. To examine how infection rates of vector-transmitted parasites respond to changes on natural landscapes, we captured 330 Blue-black Grassquits (Volatinia jacarina) in Brazilian biomes and assessed the prevalence and diversity of avian haemosporidian parasites (Plasmodium and Haemoproteus) across avian host populations inhabiting environment under different disturbance and climatic conditions. Overall prevalence in Blue-black Grassquits was low (11%) and infection rates exhibited considerable spatial variation, ranging from zero to 39%. Based on genetic divergence of cytochrome b gene, we found two lineages of Haemoproteus (Parahaemoproteus) and 10 of Plasmodium. We showed that Blue-black Grassquit populations inhabiting sites with higher proportion of native vegetation cover were more infected across Brazil. Other landscape metrics (number of water bodies and distance to urban areas) and climatic condition (temperature and precipitation) known to influence vector activity and promote avian malaria transmission did not explain infection probability in Blue-black Grassquit populations. Moreover, breeding season did not explain prevalence across avian host populations. Our findings suggest that avian haemosporidian prevalence and diversity in Blue-black Grassquit populations are determined by recent anthropogenic changes in vegetation cover that may alter microclimate, thus influencing vector activity and parasite transmission.     

Disentangling Vector-Borne Transmission Networks: A Universal DNA Barcoding Method to Identify Vertebrate Hosts from Arthropod Bloodmeals

Emerging infectious diseases represent a challenge for global economies and public health. About one fourth of the last pandemics have been originated by the spread of vector-borne pathogens. In this sense, the advent of modern molecular techniques has enhanced our capabilities to understand vector-host interactions and disease ecology. However, host identification protocols have poorly profited of international DNA barcoding initiatives and/or have focused exclusively on a limited array of vector species. Therefore, ascertaining the potential afforded by DNA barcoding tools in other vector-host systems of human and veterinary importance would represent a major advance in tracking pathogen life cycles and hosts. Here, we show the applicability of a novel and efficient molecular method for the identification of the vertebrate host''s DNA contained in the midgut of blood-feeding arthropods. To this end, we designed a eukaryote-universal forward primer and a vertebrate-specific reverse primer to selectively amplify 758 base pairs (bp) of the vertebrate mitochondrial Cytochrome c Oxidase Subunit I (COI) gene. Our method was validated using both extensive sequence surveys from the public domain and Polymerase Chain Reaction (PCR) experiments carried out over specimens from different Classes of vertebrates (Mammalia, Aves, Reptilia and Amphibia) and invertebrate ectoparasites (Arachnida and Insecta). The analysis of mosquito, culicoid, phlebotomie, sucking bugs, and tick bloodmeals revealed up to 40 vertebrate hosts, including 23 avian, 16 mammalian and one reptilian species. Importantly, the inspection and analysis of direct sequencing electropherograms also assisted the resolving of mixed bloodmeals. We therefore provide a universal and high-throughput diagnostic tool for the study of the ecology of haematophagous invertebrates in relation to their vertebrate hosts. Such information is crucial to support the efficient management of initiatives aimed at reducing epidemiologic risks of arthropod vector-borne pathogens, a priority for public health.     

Host specificity of avian haemosporidian parasites is unrelated among sister lineages but shows phylogenetic signal across larger clades

Parasites can vary in the number of host species they infect, a trait known as “host specificity”. Here we quantify phylogenetic signal—the tendency for closely related species to resemble each other more than distantly related species—in host specificity of avian haemosporidian parasites (genera Plasmodium, Haemoproteus and Leucocytozoon) using data from MalAvi, the global avian haemosporidian database. We used the genetic data (479 base pairs of cytochrome b) that define parasite lineages to produce genus level phylogenies. Combining host specificity data with those phylogenies revealed significant levels of phylogenetic signal while controlling for sampling effects; phylogenetic signal was higher when the phylogenetic diversity of hosts was taken into account. We then tested for correlations in the host specificity of pairs of sister lineages. Correlations were generally close to zero for all three parasite genera. These results suggest that while the host specificity of parasite sister lineages differ, larger clades may be relatively specialised or generalised.     

Ecological determinants of American crow mortality due to West Nile virus during its North American sweep

We examined the ecological factors influencing population declines in American crows (Corvus brachyrhynchos) as they were initially exposed to West Nile virus (WNV), a pathogen first detected in the US in 1999 that has since become one of North America’s most prevalent vector-borne pathogens. The strongest effects were initial crow population density (denser populations were more likely to suffer declines), avian species diversity (populations in areas with high diversity were less likely to suffer a decline), human population density (populations were more likely to decline in more urban areas), and time since the pathogen’s introduction to the US (populations exposed to the pathogen later in its North American sweep were less likely to suffer declines than those exposed earlier). Variables that played only a minor role included rainfall, mean maximum temperature, and total number of birds, used as a proxy for the overall reservoir competence of the community. These findings indicate that WNV declined in virulence during its rapid 5-year sweep and support the importance of the ‘dilution effect’ whereby a diverse host community dampens pathogen transmission and potentially slows its rate of spread. Results underscore the need for considering the entire community when trying to understand the factors shaping disease risk.     

Cross-Immunity and Community Structure of a Multiple-Strain Pathogen in the Tick Vector

Many vector-borne pathogens consist of multiple strains that circulate in both the vertebrate host and the arthropod vector. Characterization of the community of pathogen strains in the arthropod vector is therefore important for understanding the epidemiology of mixed vector-borne infections. Borrelia afzelii and B. garinii are two species of tick-borne bacteria that cause Lyme disease in humans. These two sympatric pathogens use the same tick, Ixodes ricinus, but are adapted to different classes of vertebrate hosts. Both Borrelia species consist of multiple strains that are classified using the highly polymorphic ospC gene. Vertebrate cross-immunity against the OspC antigen is predicted to structure the community of multiple-strain Borrelia pathogens. Borrelia isolates were cultured from field-collected I. ricinus ticks over a period spanning 11 years. The Borrelia species of each isolate was identified using a reverse line blot (RLB) assay. Deep sequencing was used to characterize the ospC communities of 190 B. afzelii isolates and 193 B. garinii isolates. Infections with multiple ospC strains were common in ticks, but vertebrate cross-immunity did not influence the strain structure in the tick vector. The pattern of genetic variation at the ospC locus suggested that vertebrate cross-immunity exerts strong selection against intermediately divergent ospC alleles. Deep sequencing found that more than 50% of our isolates contained exotic ospC alleles derived from other Borrelia species. Two alternative explanations for these exotic ospC alleles are cryptic coinfections that were not detected by the RLB assay or horizontal transfer of the ospC gene between Borrelia species.     

Pathogens manipulate the preference of vectors,slowing disease spread in a multi‐host system

The spread of vector‐borne pathogens depends on a complex set of interactions among pathogen, vector, and host. In single‐host systems, pathogens can induce changes in vector preferences for infected vs. healthy hosts. Yet it is unclear if pathogens also induce changes in vector preference among host species, and how changes in vector behaviour alter the ecological dynamics of disease spread. Here, we couple multi‐host preference experiments with a novel model of vector preference general to both single and multi‐host communities. We show that viruliferous aphids exhibit strong preferences for healthy and long‐lived hosts. Coupling experimental results with modelling to account for preference leads to a strong decrease in overall pathogen spread through multi‐host communities due to non‐random sorting of viruliferous vectors between preferred and non‐preferred host species. Our results demonstrate the importance of the interplay between vector behaviour and host diversity as a key mechanism in the spread of vectored‐diseases.     

An Integrative Eco-Epidemiological Analysis of West Nile Virus Transmission

West Nile disease, caused by the West Nile virus (WNV), is a mosquito-borne zoonotic disease affecting humans and horses that involves wild birds as amplifying hosts. The mechanisms of WNV transmission remain unclear in Europe where the occurrence of outbreaks has dramatically increased in recent years. We used a dataset on the competence, distribution, abundance, diversity and dispersal of wild bird hosts and mosquito vectors to test alternative hypotheses concerning the transmission of WNV in Southern France. We modelled the successive processes of introduction, amplification, dispersal and spillover of WNV to incidental hosts based on host–vector contact rates on various land cover types and over four seasons. We evaluated the relative importance of the mechanisms tested using two independent serological datasets of WNV antibodies collected in wild birds and horses. We found that the same transmission processes (seasonal virus introduction by migratory birds, Culex modestus mosquitoes as amplifying vectors, heterogeneity in avian host competence, absence of ‘dilution effect’) best explain the spatial variations in WNV seroprevalence in the two serological datasets. Our results provide new insights on the pathways of WNV introduction, amplification and spillover and the contribution of bird and mosquito species to WNV transmission in Southern France.     

Biogeographical patterns of blood parasite lineage diversity in avian hosts from southern Melanesian islands

Aim (1) To describe the species–area relationships among communities of Plasmodium and Haemoproteus parasites in different island populations of the same host genus (Aves: Zosterops). (2) To compare distance–decay relationships (turnover) between parasite communities and those with potential avian and dipteran hosts, which differ with respect to their movement and potential to disperse parasite species over large distances. Location Two archipelagos in the south‐west Pacific, Vanuatu and New Caledonia (c. 250 km west of Vanuatu) and its Loyalty Islands, with samples collected from a total of 16 islands of varying sizes (328–16,648 km²). Methods We characterized parasite diversity and distribution via polymerase chain reaction (PCR) from avian (Zosterops) blood samples. Bayesian methods were used to reconstruct the parasite phylogeny. In accordance with recent molecular evidence, we treat distinct mitochondrial DNA lineages as equivalent to species in this study. Path analysis and parasite lineage accumulation curves were used to assess the confounding effect of inadequate sampling on the estimation of parasite richness. Species–area and species–distance relationships were assessed using linear regression: distance–decay relationships were assessed using Mantel tests. Results Birds and mosquito species and Plasmodium lineages exhibited significant species–area relationships. However, Plasmodium lineages showed the weakest ‘species–area’ relationship; no relationship was found for Haemoproteus lineages. Avian species richness influenced parasite lineage richness more than mosquito species richness did. Within individual avian host species, the species–area relationship of parasites showed differing patterns. Path analysis indicated that sampling effort was unlikely to have a confounding effect on parasite richness. Distance from mainland (isolation effect) showed no effect on parasite richness. Community similarity decayed significantly with distance for avifauna, mosquito fauna and Plasmodium lineages but not for Haemoproteus lineages. Main conclusions Plasmodium lineages and mosquito species fit the power‐law model with steeper slopes than found for the avian hosts. The lack of species–distance relationship in parasites suggests that other factors, such as the competence of specific vectors and habitat features, may be more important than distance. The decay in similarity with distance suggests that the sampled Plasmodium lineages and their potential hosts were not randomly distributed, but rather exhibited spatially predictable patterns. We discuss these results in the context of the effects that parasite generality may have on distribution patterns.