Prevalence and diversity patterns of avian blood parasites in degraded African rainforest habitats

Land use changes including deforestation, road construction and agricultural encroachments have been linked to the increased prevalence of several infectious diseases. In order to better understand how deforestation affects the prevalence of vector-borne infectious diseases in wildlife, nine paired sites were sampled (disturbed vs. undisturbed habitats) in Southern Cameroon. We studied the diversity, prevalence and distribution of avian malaria parasites ( Plasmodium spp.) and other related haemosporidians (species of Haemoproteus and Leucocytozoon ) from these sites in two widespread species of African rainforest birds, the yellow-whiskered greenbul ( Andropadus latirostris , Pycnonotidae) and the olive sunbird ( Cyanomitra olivacea , Nectariniidae). Twenty-six mitochondrial cytochrome b lineages were identified: 20 Plasmodium lineages and 6 Haemoproteus lineages. These lineages showed no geographic specificity, nor significant differences in lineage diversity between habitat types. However, we found that the prevalence of Leucocytozoon and Haemoproteus infections were significantly higher in undisturbed than in deforested habitats ( Leucocytozoon spp. 50.3% vs. 35.8%, Haemoproteus spp. 16.3% vs. 10.8%). We also found higher prevalence for all haemosporidian parasites in C. olivacea than in A. latirostris species (70.2% vs. 58.2%). Interestingly, we found one morphospecies of Plasmodium in C. olivacea , as represented by a clade of related lineages, showed increased prevalence at disturbed sites, while another showed a decrease, testifying to different patterns of transmission, even among closely related lineages of avian malaria, in relation to deforestation. Our work demonstrates that anthropogenic habitat change can affect host–parasite systems and result in opposing trends in prevalence of haemosporidian parasites in wild bird populations.     

Temporal dynamics and diversity of avian malaria parasites in a single host species

1. We have used molecular methods to unravel a remarkable diversity of parasite lineages in a long-term population study of great reed warblers Acrocephalus arundinaceus that was not foreseen from traditional microscopic examination of blood smears. This diversity includes eight Haemoproteus and 10 Plasmodium lineages of which most probably represent good biological species. 2. Contrary to expectation, the relative frequency of parasite lineages seemed not to change over the 17-year study period and we found no effects of the parasites on a male secondary sexual ornament (song repertoire size) and two measures of fitness (adult survival and production of recruited offspring). 3. We discuss whether the absence of fitness consequences of the parasites might relate to the fact that we have studied the host at the breeding sites in Europe, whereas the transmission seems to take place at the wintering sites in Africa, where the na?ve birds encounter the parasites for the first time and the resulting primary infections likely make them sicker than during the chronic phase of the infection. 4. The prevalence of the three most common lineages appeared to fluctuate in parallel with a periodicity of approximately 3-4 years. Theoretical models based on intrinsic interactions between parasite antigen and host immune genes cannot explain such dynamics, suggesting that knowledge of extrinsic parameters such as vector distribution and alternative hosts are required to understand these patterns.     

High lineage diversity and host sharing of malarial parasites in a local avian assemblage

Bird populations often have high prevalences of the haemosporidians Haemoproteus spp. and Plasmodium spp., but the extent of host sharing and host switching among these parasite lineages and their avian hosts is not well known. While sampling within a small geographic region in which host individuals are likely to have been exposed to the same potential parasite lineages, we surveyed highly variable mitochondrial DNA from haemosporidians isolated from 14 host taxa representing 4 avian families (Hirundinidae, Parulidae, Emberizidae, and Fringillidae). Analyses of cytochrome b sequences from 83 independent infections identified 29 unique haplotypes, representing 2 well-differentiated Haemoproteus spp. lineages and 6 differentiated Plasmodium spp. lineages. A phylogenetic reconstruction of relationships among these lineages provided evidence against host specificity at the species and family levels, as all haemosporidian lineages recovered from 2 or more host individuals (2 Haemoproteus and 3 Plasmodium lineages) were found in at least 2 host families. We detected a similar high level of host sharing; the 3 most intensively sampled host species each harbored 4 highly differentiated haemosporidian lineages. These results indicate that some Haemoproteus spp. and Plasmodium spp. lineages exhibit a low degree of host specificity, a phenomenon with implications for ecological and evolutionary interactions among these parasites and their hosts.     

Sex-specific associations between reproductive output and hematozoan parasites of American kestrels

Parasites have the potential to decrease reproductive output of hosts by competing for nutrients or forcing hosts to invest in immune function. Conversely, reproductive output may affect parasite loads if hosts allocate resources to reproduction such that allocation to immune function is compromised. Both hypotheses implicitly have a temporal component, so we sampled parasites both before and after egg laying to examine the relationship between reproductive output (indexed using a combined measure of clutch size, egg volume, and initiation date) and blood parasite loads of American kestrels (Falco sparverius). Parasite loads measured prior to egg laying had no adverse effects on subsequent reproductive output. Females that previously had large reproductive outputs subsequently had lower parasite intensities than those whose outputs were smaller, suggesting that females were capable of allocating energy to both forming clutches and reducing parasite loads. Because male kestrels provide most of their mate's energetic needs before, during, and after egg laying, mate choice by females may have consequences for their parasite loads. Females choosing high-quality mates may not only have increased reproductive output, but may also obtain sufficient resources from their mates to enable them to reduce their parasite burdens. Males whose mates had large reproductive outputs were more likely to subsequently be parasitized and have more intense infections. For individual males sampled both before and after egg laying, those whose mates had larger reproductive outputs were also more likely to become parasitized, or remain parasitized, between sampling periods. Increased parasite loads of males may be one mechanism by which the costs of reproduction are paid.     

Host specialization and geographic localization of avian malaria parasites: a regional analysis in the Lesser Antilles

We recovered 26 genetically distinct avian malaria parasite lineages, based on cytochrome b sequences, from a broad survey of terrestrial avifauna of the Lesser Antilles. Here we describe their distributions across host species within a regional biogeographic context. Most parasite lineages were recovered from a few closely related host species. Specialization on one host species and distribution across many hosts were both rare. Geographic patterns of parasite lineages indicated limited dispersal and frequent local extinction. The central islands of the archipelago share similar parasite lineages and patterns of infection. However, the peripheral islands harbor well-differentiated parasite communities, indicating long periods of isolation. Nonetheless, 20 of 26 parasite lineages were recovered from at least one of three other geographic regions, the Greater Antilles, North America, and South America, suggesting rapid dispersal relative to rate of differentiation. Six parasite lineages were restricted to the Lesser Antilles, primarily to endemic host species. Host differences between populations of the same parasite lineage suggest that host preference may evolve more rapidly than mitochondrial gene sequences. Taken together, distributions of avian malarial parasites reveal evidence of coevolution, host switching, extinction, and periodic recolonization events resulting in ecologically dynamic as well as evolutionarily stable patterns of infection.     

Diversity and distribution of avian haematozoan parasites in the western Indian Ocean region: a molecular survey

The genetic diversity of haematozoan parasites in island avifauna has only recently begun to be explored, despite the potential insight that these data can provide into the history of association between hosts and parasites and the possible threat posed to island endemics. We used mitochondrial DNA sequencing to characterize the diversity of 2 genera of vector-mediated parasites (Plasmodium and Haemoproteus) in avian blood samples from the western Indian Ocean region and explored their relationship with parasites from continental Africa. We detected infections in 68 out of 150 (45·3%) individuals and cytochrome b sequences identified 9 genetically distinct lineages of Plasmodium spp. and 7 lineages of Haemoproteus spp. We found considerable heterogeneity in parasite lineage composition across islands, although limited sampling may, in part, be responsible for perceived differences. Two lineages of Plasmodium spp. and 2 lineages of Haemoproteus spp. were shared by hosts in the Indian Ocean and also on mainland Africa, suggesting that these lineages may have arrived relatively recently. Polyphyly of island parasites indicated that these parasites were unlikely to constitute an endemic radiation and instead probably represent multiple colonization events. This study represents the first molecular survey of vector-mediated parasites in the western Indian Ocean, and has uncovered a diversity of parasites. Full understanding of parasite community composition and possible threats to endemic avian hosts will require comprehensive surveys across the avifauna of this region.     

Prevalence of avian haemosporidian parasites and their host fidelity in the central Philippine islands

We examined the prevalence and host fidelity of avian haemosporidian parasites belonging to the genera Haemoproteus, Leucocytozoon and Plasmodium in the central Philippine islands by sampling 23 bird families (42 species). Using species-specific PCR assays of the mitochondrial cytochrome b gene (471base pairs, bp), we detected infections in 91 of the 215 screened individuals (42%). We also discriminated between single and multiple infections. Thirty-one infected individuals harbored a single Haemoproteus lineage (14%), 18 a single Leucocytozoon lineage (8%) and 12 a single Plasmodium lineage (6%). Of the 215 screened birds, 30 (14%) presented different types of multiple infections. Intrageneric mixed infections were generally more common (18 Haemoproteus/Haemoproteus, 3 Leucocytozoon/Leucocytozoon, and 1 Plasmodium/Plasmodium) than intergeneric mixed infections (7 Haemoproteus/Leucocytozoon and 1 Haemoproteus/Leucocytozoon/Plasmodium). We recovered 81 unique haemosporidian mitochondrial haplotypes. These clustered in three strongly supported monophyletic clades that correspond to the three haemosporidian genera. Related lineages of Haemoproteus and Leucocytozoon were more likely to derive from the same host family than predicted by chance; however, this was not the case for Plasmodium. These results indicate that switches between host families are more likely to occur in Plasmodium. We conclude that Haemoproteus has undergone a recent diversification across well-supported host-family specific clades, while Leucocytozoon shows a longer association with its host(s). This study supports previous evidence of a higher prevalence and stronger host-family specificity of Haemoproteus and Leucocytozoon compared to Plasmodium.     

Specialist versus generalist parasites: the interactions between host diversity,environment and geographic barriers in avian malaria

The specialist versus generalist strategies of hemoparasites in relation to their avian host, as well as environmental factors, can influence their prevalence, diversity and distribution. In this paper we investigated the influence of avian host species, as well as the environmental and geographical factors, on the strategies of Haemoproteus and Plasmodium hemoparasites. We determined prevalence and diversity by targeting their cytochrome b (Cytb) in a total of 2,590 passerine samples from 138 localities of Central and South America, and analysed biogeographic patterns and host-parasite relationships. We found a total prevalence of 23.2%. Haemoproteus presented a higher prevalence (15.3%) than Plasmodium (4.3%), as well as a higher diversity and host specificity. We determined that Plasmodium and Haemoproteus prevalences correlated positively with host diversity (Shannon index) and were significantly influenced by bird diversity, demonstrating a possible “amplification effect”. We found an effect of locality and the avian family for prevalences of Haemoproteus and Plasmodium. These results suggest that Haemoproteus is more specialist than Plasmodium and could be mostly influenced by its avian host and the Andes Mountains.     

Diversification by host switching and dispersal shaped the diversity and distribution of avian malaria parasites in Amazonia

Understanding how pathogens and parasites diversify through time and space is fundamental to predicting emerging infectious diseases. Here, we use biogeographic, coevolutionary and phylogenetic analyses to describe the origin, diversity, and distribution of avian malaria parasites in the most diverse avifauna on Earth. We first performed phylogenetic analyses using the mitochondrial cytochrome b (cyt b) gene to determine relationships among parasite lineages. Then, we estimated divergence times and reconstructed ancestral areas to uncover how landscape evolution has shaped the diversification of Parahaemoproteus and Plasmodium in Amazonia. Finally, we assessed the coevolutionary patterns of diversification in this host–parasite system to determine how coevolution may have influenced the contemporary diversity of avian malaria parasites and their distribution among Amazonian birds. Biogeographic analysis of 324 haemosporidian parasite lineages recovered from 4178 individual birds provided strong evidence that these parasites readily disperse across major Amazonian rivers and this has occurred with increasing frequency over the last five million years. We also recovered many duplication events within areas of endemism in Amazonia. Cophylogenetic analyses of these blood parasites and their avian hosts support a diversification history dominated by host switching. The ability of avian malaria parasites to disperse geographically and shift among avian hosts has played a major role in their radiation and has shaped the current distribution and diversity of these parasites across Amazonia.     

Prevalence and lineage diversity of avian haemosporidians from three distinct cerrado habitats in Brazil

Habitat alteration can disrupt host-parasite interactions and lead to the emergence of new diseases in wild populations. The cerrado habitat of Brazil is being fragmented and degraded rapidly by agriculture and urbanization. We screened 676 wild birds from three habitats (intact cerrado, disturbed cerrado and transition area Amazonian rainforest-cerrado) for the presence of haemosporidian parasites (Plasmodium and Haemoproteus) to determine whether different habitats were associated with differences in the prevalence and diversity of infectious diseases in natural populations. Twenty one mitochondrial lineages, including 11 from Plasmodium and 10 from Haemoproteus were identified. Neither prevalence nor diversity of infections by Plasmodium spp. or Haemoproteus spp. differed significantly among the three habitats. However, 15 of the parasite lineages had not been previously described and might be restricted to these habitats or to the region. Six haemosporidian lineages previously known from other regions, particularly the Caribbean Basin, comprised 50-80% of the infections in each of the samples, indicating a regional relationship between parasite distribution and abundance.     

Detecting shifts of transmission areas in avian blood parasites: a phylogenetic approach

We investigated the degree of geographical shifts of transmission areas of vector-borne avian blood parasites (Plasmodium, Haemoproteus and Leucocytozoon) over ecological and evolutionary timescales. Of 259 different parasite lineages obtained from 5886 screened birds sampled in Europe and Africa, only two lineages were confirmed to have current transmission in resident bird species in both geographical areas. We used a phylogenetic approach to show that parasites belonging to the genera Haemoproteus and Leucocytozoon rarely change transmission area and that these parasites are restricted to one resident bird fauna over a long evolutionary time span and are not freely spread between the continents with the help of migratory birds. Lineages of the genus Plasmodium seem more freely spread between the continents. We suggest that such a reduced transmission barrier of Plasmodium parasites is caused by their higher tendency to infect migratory bird species, which might facilitate shifting of transmission area. Although vector-borne parasites of these genera apparently can shift between a tropical and a temperate transmission area and these areas are linked with an immense amount of annual bird migration, our data suggest that novel introductions of these parasites into resident bird faunas are rather rare evolutionary events.     

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.     

Diversification and host switching in avian malaria parasites

The switching of parasitic organisms to novel hosts, in which they may cause the emergence of new diseases, is of great concern to human health and the management of wild and domesticated populations of animals. We used a phylogenetic approach to develop a better statistical assessment of host switching in a large sample of vector-borne malaria parasites of birds (Plasmodium and Haemoproteus) over their history of parasite-host relations. Even with sparse sampling, the number of parasite lineages was almost equal to the number of avian hosts. We found that strongly supported sister lineages of parasites, averaging 1.2% sequence divergence, exhibited highly significant host and geographical fidelity. Event-based matching of host and parasite phylogenetic trees revealed significant cospeciation. However, the accumulated effects of host switching and long distance dispersal cause these signals to disappear before 4% sequence divergence is achieved. Mitochondrial DNA nucleotide substitution appears to occur about three times faster in hosts than in parasites, contrary to findings on other parasite-host systems. Using this mutual calibration, the phylogenies of the parasites and their hosts appear to be similar in age, suggesting that avian malaria parasites diversified along with their modern avian hosts. Although host switching has been a prominent feature over the evolutionary history of avian malaria parasites, it is infrequent and unpredictable on time scales germane to public health and wildlife management.     

Hidden diversity: parasites of stream arthropods

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Prevalence of blood parasites in seabirds - a review

Introduction

While blood parasites are common in many birds in the wild, some groups seem to be much less affected. Seabirds, in particular, have often been reported free from blood parasites, even in the presence of potential vectors.

Results

From a literature review of hemosporidian prevalence in seabirds, we collated a dataset of 60 species, in which at least 15 individuals had been examined. These data were included in phylogenetically controlled statistical analyses of hemosporidian prevalence in relation to ecological and life-history parameters. Haemoproteus parasites were common in frigatebirds and gulls, while Hepatozoon occurred in albatrosses and storm petrels, and Plasmodium mainly in penguins. The prevalence of Haemoproteus showed a geographical signal, being lower in species with distribution towards polar environments. Interspecific differences in Plasmodium prevalence were explained by variables that relate to the exposure to parasites, suggesting that prevalence is higher in burrow nesters with long fledgling periods. Measures of Plasmodium, but not Haemoproteus prevalences were influenced by the method, with PCR-based data resulting in higher prevalence estimates.

Conclusions

Our analyses suggest that, as in other avian taxa, phylogenetic, ecological and life-history parameters determine the prevalence of hemosporidian parasites in seabirds. We discuss how these relationships should be further explored in future studies.

     

Individual genetic diversity and probability of infection by avian malaria parasites in blue tits (Cyanistes caeruleus)

Understanding the importance of host genetic diversity for coping with parasites and infectious diseases is a long‐standing goal in evolutionary biology. Here, we study the association between probability of infection by avian malaria (Plasmodium relictum) and individual genetic diversity in three blue tit (Cyanistes caeruleus) populations that strongly differ in prevalence of this parasite. For this purpose, we screened avian malaria infections and genotyped 789 blue tits across 26 microsatellite markers. We used two different arrays of markers: 14 loci classified as neutral and 12 loci classified as putatively functional. We found a significant relationship between probability of infection and host genetic diversity estimated at the subset of neutral markers that was not explained by strong local effects and did not differ among the studied populations. This relationship was not linear, and probability of infection increased up to values of homozygosity by locus (HL) around 0.15, reached a plateau at values of HL from 0.15 to 0.40 and finally declined among a small proportion of highly homozygous individuals (HL > 0.4). We did not find evidence for significant identity disequilibrium, which may have resulted from a low variance of inbreeding in the study populations and/or the small power of our set of markers to detect it. A combination of subtle positive and negative local effects and/or a saturation threshold in the association between probability of infection and host genetic diversity in combination with increased resistance to parasites in highly homozygous individuals may explain the observed negative quadratic relationship. Overall, our study highlights that parasites play an important role in shaping host genetic variation and suggests that the use of large sets of neutral markers may be more appropriate for the study of heterozygosity–fitness correlations.     

Resource predictability and specialization in avian malaria parasites

We tested the hypothesis that avian haemosporidian (malaria) parasites specialize on hosts that can be characterized as predictable resources at a site in Amazonian Ecuador. We incorporated host phylogenetic relationship and relative abundance in assessing parasite specialization, and we examined associations between parasite specialization and three host characteristics – abundance, mass and longevity – using quantile regression, phylogenetic logistic regression and t‐tests. Hosts of specialist malaria parasite lineages were on average more abundant than hosts of generalist parasite lineages, but the relationship between host abundance and parasite specialization was not consistent across analyses. We also found support for a positive association between parasite specialization and host longevity, but this also was not consistent across analyses. Nonetheless, our findings suggest that the predictability of a host resource may play a role in the evolution of specialization. However, we also discuss two alternative explanations to the resource predictability hypothesis for specialization: (i) that interspecific interactions among the parasites themselves might constrain some parasites to a specialist strategy, and (ii) that frequent encounters with multiple host species, mediated by blood‐sucking insects, might promote generalization within this system.     

Mitochondrial genome diversity in parasites

Mitochondrial genomes have been sequenced from a wide variety of organisms, including an increasing number of parasites. They maintain some characteristics in common across the spectrum of life-a common core of genes related to mitochondrial respiration being most prominent-but have also developed a great diversity of gene content, organisation, and expression machineries. The characteristics of mitochondrial genomes vary widely among the different groups of protozoan parasites, from the minute genomes of the apicomplexans to amoebae with 20 times as many genes. Kinetoplastid protozoa have a similar number of genes to metazoans, but the details of gene organisation and expression in kinetoplastids require extraordinary mechanisms. Mitochondrial genes in nematodes and trematodes appear quite sedate in comparison, but a closer look shows a strong tendency to unusual tRNA structure and alternative initiation codons among these groups. Mitochondrial genes are increasingly coming into play as aids to phylogenetic and epidemiologic analyses, and mitochondrial functions are being recognised as potential drug targets. In addition, examination of mitochondrial genomes is producing further insights into the diversity of the wide-ranging group of organisms comprising the general category of parasites.