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Diversity, loss, and gain of malaria parasites in a globally invasive bird.

ABSTRACT: Invasive species can displace natives, and thus identifying the traits that make aliens successful is crucial for predicting and preventing biodiversity loss. Pathogens may play an important role in the invasive process, facilitating colonization of their hosts in new continents and islands. According to the Novel Weapon Hypothesis, colonizers may out-compete local native species by bringing with them novel pathogens to which native species are not adapted. In contrast, the Enemy Release Hypothesis suggests that flourishing colonizers are successful because they have left their pathogens behind. To assess the role of avian malaria and related haemosporidian parasites in the global spread of a common invasive bird, we examined the prevalence and genetic diversity of haemosporidian parasites (order Haemosporida, genera Plasmodium and Haemoproteus) infecting house sparrows (Passer domesticus). We sampled house sparrows (N = 1820) from 58 locations on 6 continents. All the samples were tested using PCR-based methods; blood films from the PCR-positive birds were examined microscopically to identify parasite species. The results show that haemosporidian parasites in the house sparrows' native range are replaced by species from local host-generalist parasite fauna in the alien environments of North and South America. Furthermore, sparrows in colonized regions displayed a lower diversity and prevalence of parasite infections. Because the house sparrow lost its native parasites when colonizing the American continents, the release from these natural enemies may have facilitated its invasion in the last two centuries. Our findings therefore reject the Novel Weapon Hypothesis and are concordant with the Enemy Release Hypothesis.

SUBMITTER: Marzal A

PROVIDER: S-EPMC3136938 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:Knowledge about feeding preference of blood-sucking insects is important for the better understanding epidemiology of vector-borne parasitic diseases. Extraction of DNA from blood present in abdomens of engorged insects provides opportunities to identify species of their vertebrate hosts. However, this approach often is insufficiently sensitive due to rapid degeneration of host DNA in midguts. Recent studies indicate that avian malaria parasites (Plasmodium spp.) and related haemosporidians (Haemosporida) belonging to Haemoproteus can persist both in vectors and resistant blood-sucking insects for several weeks after initial blood meals, and these parasites can be readily detected by polymerase chain reaction (PCR)-based methods. Because avian haemosporidians are cosmopolitan, prevalent and strictly specific to birds, the determination of haemosporidian DNA in blood-sucking dipterans can be used as molecular tags in determining bird-biting insects. This hypothesis was tested by investigation of prevalence of natural haemosporidian infections in wild-caught mosquitoes (Culicidae) and biting midges (Ceratopogonidae: Culicoides).Females of mosquitoes (1072 individuals of three species) and biting midges (300 individuals of three species) were collected in wildlife using simple netting. They were identified and tested individually for the presence of both the haemosporidian parasites and the bird blood using PCR-based methods. Seven different Haemoproteus and two Plasmodium lineages were detected, with overall infection prevalence of 1.12 and 1.67 % in mosquitoes and biting midges, respectively. In all, the detection rate of avian haemosporidian parasites was three fold higher compared with the detection of avian blood.Molecular markers of avian malaria parasites and other haemosporidians are recommended for getting additional knowledge about blood-sucking dipterans feeding on bird blood. Many genetic lineages of avian haemosporidians are specific to avian hosts, therefore, the detection of these parasite lineages in blood-sucking insects can indicate their feeding preferences on the level of species or groups of related bird species.

Project description:Diseases can play a role in species decline. Among them, haemosporidian parasites, vector-transmitted protozoan parasites, are known to constitute a risk for different avian species. However, the magnitude of haemosporidian infection in wild columbiform birds, including strongly decreasing European turtle doves, is largely unknown. We examined the prevalence and diversity of haemosporidian parasites Plasmodium, Leucocytozoon and subgenera Haemoproteus and Parahaemoproteus in six species of the order Columbiformes during breeding season and migration by applying nested PCR, one-step multiplex PCR assay and microscopy. We detected infections in 109 of the 259 screened individuals (42%), including 15 distinct haemosporidian mitochondrial cytochrome b lineages, representing five H. (Haemoproteus), two H. (Parahaemoproteus), five Leucocytozoon and three Plasmodium lineages. Five of these lineages have never been described before. We discriminated between single and mixed infections and determined host species-specific prevalence for each parasite genus. Observed differences among sampled host species are discussed with reference to behavioural characteristics, including nesting and migration strategy. Our results support previous suggestions that migratory birds have a higher prevalence and diversity of blood parasites than resident or short-distance migratory species. A phylogenetic reconstruction provided evidence for H. (Haemoproteus) as well as H. (Parahaemoproteus) infections in columbiform birds. Based on microscopic examination, we quantified parasitemia, indicating the probability of negative effects on the host. This study provides a large-scale baseline description of haemosporidian infections of wild birds belonging to the order Columbiformes sampled in the northern hemisphere. The results enable the monitoring of future changes in parasite transmission areas, distribution and diversity associated with global change, posing a potential risk for declining avian species as the European turtle dove.

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Diversity, loss, and gain of malaria parasites in a globally invasive bird.

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