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.     

MalAvi: a public database of malaria parasites and related haemosporidians in avian hosts based on mitochondrial cytochrome b lineages

Research in avian blood parasites has seen a remarkable increase since the introduction of polymerase chain reaction-based methods for parasite identification. New data are revealing complex multihost-multiparasite systems which are difficult to understand without good knowledge of the host range and geographical distribution of the parasite lineages. However, such information is currently difficult to obtain from the literature, or from general repositories such as GenBank, mainly because (i) different research groups use different parasite lineage names, (ii) GenBank entries frequently refer only to the first host and locality at which each parasite was sampled, and (iii) different researchers use different gene fragments to identify parasite lineages. We propose a unified database of avian blood parasites of the genera Plasmodium, Haemoproteus and Leucocytozoon identified by a partial region of their cytochrome b sequences. The database uses a standardized nomenclature to remove synonymy, and concentrates all available information about each parasite in a public reference site, thereby facilitating access to all researchers. Initial data include a list of host species and localities, as well as genetic markers that can be used for phylogenetical analyses. The database is free to download and will be regularly updated by the authors. Prior to publication of new lineages, we encourage researchers to assign names to match the existing database. We anticipate that the value of the database as a source for determining host range and geographical distribution of the parasites will grow with its size and substantially enhance the understanding of this remarkably diverse group of parasites.     

The occurrence of haemosporidian parasites in the Fennoscandian bluethroat ( Luscinia svecica) population

A total of 86 adult bluethroats (Luscinia svecica) from nine different localities, covering the full length of the Fennoscandian mountain range, were screened for blood parasites of the three genera Haemoproteus, Plasmodium and Leucocytozoon using a recently developed polymerase chain reaction method. The overall occurrence of infection was 59.3%. Prevalence of Leucocytozoon spp. (47.7%), Plasmodium spp. (23.3%) and Haemoproteus spp. (1.2%) was detected. Of the infected birds, 15.1% carried mixed infections. Five different mitochondrial DNA-lineages of Leucocytozoon spp., eight lineages of Plasmodium spp. and one lineage of Haemoproteus spp. were found. Due to large sequence divergence these corresponded to at least five different species, but with the possibility of all 14 being independent evolutionary units with the potential of evolving different effects on the host. Of the lineages of Leucocytozoon spp., the most common was found throughout the range. The occurrence of the second most common lineage of Leucocytozoon spp. showed significant variation in prevalence between sites. The data also showed molecular evidence of one lineage of Leucocytozoon sp. existing in more than one species of avian host, thus challenging the use of host taxon as a taxonomic character when distinguishing between different species leucocytozoids.Communicated by F. Bairlein     

Blood Protozoa of Imported Birds

SYNOPSIS. Large numbers of birds, until recently, were brought into the United States each year. Countries of origin were varied, and included those of Australasia, Africa, South America, and the Caribbean Islands, as well as other places. With them of course come their parasites, some of which may be potential pathogens to domestic avifauna. In part for this reason, a survey was undertaken of blood parasites of birds from pet shops and importers. So far a total of 1234 birds belonging to 186 species has been examined. Several new species and subspecies of avian Plasmodium have been found in the course of this study, including P. octamerium Manwell, 1968 in a Pintail Whydah, Vidua macoura , from Africa; P. paranucleophilum Manwell & Sessler, 1971 in a South American tanager, Tachyphonus sp.; and P. nucleophilum toucani Manwell & Sessler 1971 in a Swainson's Toucan, Ramphastos s. swainsonii. Plasmodium huffi Muniz, Soares & Battista is undoubtedly a synonym pro parte for the last. Plasmodium tenue Laveran & Marullaz, long thought to be a synonym of Plasmodium vaughani Novy & MacNeal, was rediscovered and found to be a valid species. Plasmodium nucleophilum , infrequently seen in the New World, occurred in many Asian and African birds, and especially in starlings. Infections with other species of Plasmodium were common. Haemoproteus was the commonest blood parasite; Leucocytozoon was very rare as was Atoxoplasma (Lankesterella). The 2 families of birds best represented were the Fringillidae and the Psittacidae, but no blood parasites were seen in the latter. It is clear that imported birds are often infected with blood protozoa, some of which are unknown from native birds.     

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.     

Blood Protozoa of Wild Turkeys in Florida*

From 1969 through 1972, 605 wild turkeys (Meleagris gallopavo Linnaeus) from 10 localities in Florida were examined for blood protozoans. The prevalence in turkeys more than a month old was 84% for Haemoproteus meleagridis Levine, 1961 and 72% for Leucocytozoon smithi Laveran and Lucet, 1905. Sixty-three percent of the birds were infected by both parasites. Infections were most prevalent in juveniles 8–12 months of age. No infection of H. meleagridis or L. smithi was found in 111 poults younger than 35 days. Prevalences were similar in both sexes. Haemoproteus meleagridis was more prevalent (87%) in the southern part of the state; L. smithi was more prevalent (75%) in the north. The prevalence of H. meleagridis did not change during the 4 year period, but L. smithi decreased markedly in 1971, a year of low rainfall. None of the 605 blood films was positive for Plasmodium, but 24 (75%) of 32 blood samples were found by subinoculation technics to be positive for a species of Plasmodium morphologically similar to P. durae Herman, 1941. No trypanosomes were seen on the 605 blood films or in bone marrow cultures (saline-neopeptone-blood) made from 11 turkeys.     

Host ecology and life-history traits associated with blood parasite species richness in birds

Identifying host traits associated with the number of different parasite species or strains harboured by a particular host species can have important implications for understanding the impact of parasitism on hosts. We investigated associations between host ecology and life history, and parasite richness and prevalence of the four major avian blood parasite genera. We used an extensive data on blood parasite infections and host ecology in 263 bird species from the Western Palearctic, combining species-specific data with a comparative approach to control for similarity in phenotype among host species due to the effects of common phylogenetic descent. Adult survival rate negatively correlated with the number of parasite species infecting a host species when controlling for similarity due to common descent and body mass. In addition, the prevalence of Haemoproteus, Plasmodium and Leucocytozoon was higher in species harbouring a richer parasite assemblage. These results suggest that the impact on host fitness caused by avian haematozoa may be underestimated in natural populations if the exacerbated virulence associated with exposure to multiple parasites is not taken into account.     

Avian Haematozoa: Some Taxonomic and Nomenclatural Problems Arising from the Russian Literature*

SYNOPSIS. It is evident from a survey of the Russian literature that many species of avian haematozoa recorded do not meet the basic criteria required by the International Code of Zoological Nomenclature. Thus 28 species of Haemoproteus and 4 species of Leucocytozoon are considered to be nomina nuda, while 1 species, Leucocytozoon turtur orientalis is a synonym of L. marchouxi.     

LINKAGE BETWEEN NUCLEAR AND MITOCHONDRIAL DNA SEQUENCES IN AVIAN MALARIA PARASITES: MULTIPLE CASES OF CRYPTIC SPECIATION?

Analyses of mitochondrial cytochrome b diversity among avian blood parasites of the genera Haemoproteus and Plasmodium suggest that there might be as many lineages of parasites as there are species of birds. This is in sharp contrast to the approximately 175 parasite species described by traditional methods based on morphology using light microscopy. Until now it has not been clear to what extent parasite mitochondrial DNA lineage diversity reflects intra- or interspecific variation. We have sequenced part of a fast-evolving nuclear gene, dihydrofolate reductase-thymidylate synthase (DHFR-TS), and demonstrate that most of the parasite mitochondrial DNA lineages are associated with unique gene copies at this locus. Although these parasite lineages sometimes coexist in the same host individual, they apparently do not recombine and could therefore be considered as functionally distinct evolutionary entities, with independent evolutionary potential. Studies examining parasite virulence and host immune systems must consider this remarkable diversity of avian malaria parasites.     

No relationship between individual genetic diversity and prevalence of avian malaria in a migratory kestrel

Insight into the genetic basis of malaria resistance is crucial for understanding the consequences of this parasite group on animal populations. Here, we analyse the relationship between genotypic variation at 11 highly variable microsatellite loci and prevalence of three different lineages of avian malaria, two Plasmodium (RTSR1, LK6) and one Haemoproteus (LK2), in a wild population of the endangered lesser kestrel (Falco naumanni). Although we used a large sample size (584 typed individuals), we did not find any significant association between the prevalence of the studied parasite lineages and individual genetic diversity. Although our data set is large, the 11 neutral markers typed may have had low power to detect such association, in part because of the low parasite prevalence observed (less than 5% of infected birds). However, the fact that we have detected previous correlations between genetic diversity and other traits (ectoparasitism risk, fecundity) in the study population using the same panel of neutral markers and lower sample sizes suggests that other factors could underlie the absence of such a similar correlation with avian malaria. Differences in the genetics of the studied traits and in their particular basis of inbreeding depression (dominance vs. overdominance) may have led to malaria prevalence, but not other traits, being uncoupled with individual genetic diversity. Also, we cannot discard the possibility that the absence of association was a consequence of a low pathogenic effect of these particular malaria lineages on our lesser kestrel population, and thus we should not expect the evolution of genetic resistance against these parasites.     

Arthropod-borne disease as a possible factor limiting the distribution of birds

Warner found that arthropod-borne disease in the Hawaiian islands (bird malaria and avian pox in particular) is a factor limiting the distribution of the Drepaniidae. Rowan considers it conceivable that the present distribution of certain African birds (and perhaps some other vertebrates showing similar patterns of occurrence) may have been determined in the same way. This suggestion is supported by the observations of the author in southern Africa in regard to bird malaria and avian pox.