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Effects of forest structure on the interaction between avian hosts, dipteran vectors and haemosporidian parasites

ABSTRACT: Background Forest habitats are important biodiversity refuges for a wide variety of bird species. Parasitism may modulate host species presence and abundance, and parasite effects can change according to forest management practices. Such processes are not well studied in vector-borne avian haemosporidians. We analyzed the effects of forest management on bird-dipteran-haemosporidian interactions, using seven common bird species in managed and unmanaged beech forest habitats in northeastern Germany. We assumed that forest structural heterogeneity affects parasite population parameters in avian hosts (i.e., prevalence and parasitemia), through its effect on the condition of the avian host but also through varying vector abundances. Results Parasite prevalence was high (about 80%) and homogeneous across different beech forest categories (i.e., young, old, unmanaged) and for all bird species, except Erithacus rubecula (35%). Parasitemia varied across bird species but not across forest categories within each avian species (lowest parasitemia were found in E. rubecula, Turdus merula, and Turdus philomelos). In our study system, we found that vector abundance was not the main driver of parasite dynamics. We found that forest structure affects parasite infection probability directly and potentially host condition via available resources that have to be used either to combat infections (i.e., high parasitemia) or to maintain a good body condition. Conclusions The effects of each of the predictors were bird species-specific, and we found that Diptera vectors were not the foremost influence in our host-vector-parasite system. Effects of forest habitat variables indicated that for most bird species in this study, habitat regulation of infection probability was more likely (i.e., E. rubecula, Fringilla coelebs, Sylvia atricapilla), whereas for Parus major habitat characteristics impacted first individuals' body condition and subsequently the probability of infection. Our findings emphasize the need of species-specific analyses and to use continuous forest structural parameters (e.g., the proportion of gap, south facing aspect) to better understand habitat and land use effects on host-vector-parasite dynamics.

SUBMITTER: van Hoesel W

PROVIDER: S-EPMC7437053 | biostudies-literature | 2020 Jan

REPOSITORIES: biostudies-literature

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Project description:BackgroundThe order Accipitriformes comprises the largest group of birds of prey with 260 species in four families. So far, 21 haemosporidian parasite species have been described from or reported to occur in accipitriform birds. Only five of these parasite species have been characterized molecular genetically. The first part of this study involved molecular genetic screening of accipitriform raptors from Austria and Bosnia-Herzegovina and the first chromogenic in situ hybridization approach targeting parasites in this host group. The aim of the second part of this study was to summarize the CytB sequence data of haemosporidian parasites from accipitriform raptors and to visualize the geographic and host distribution of the lineages.MethodsBlood and tissue samples of 183 accipitriform raptors from Austria and Bosnia-Herzegovina were screened for Plasmodium, Haemoproteus and Leucocytozoon parasites by nested PCR, and tissue samples of 23 PCR-positive birds were subjected to chromogenic in situ hybridization using genus-specific probes targeting the parasites' 18S rRNAs. All published CytB sequence data from accipitriform raptors were analysed, phylogenetic trees were calculated, and DNA haplotype network analyses were performed with sequences from clades featuring multiple lineages detected in this host group.ResultsOf the 183 raptors from Austria and Bosnia-Herzegovina screened by PCR and sequencing, 80 individuals (44%) were infected with haemosporidian parasites. Among the 39 CytB lineages detected, 18 were found for the first time in the present study. The chromogenic in situ hybridization revealed exo-erythrocytic tissue stages of Leucocytozoon parasites belonging to the Leucocytozoon toddi species group in the kidneys of 14 infected birds. The total number of CytB lineages recorded in accipitriform birds worldwide was 57 for Leucocytozoon, 25 for Plasmodium, and 21 for Haemoproteus.ConclusionThe analysis of the DNA haplotype networks allowed identifying numerous distinct groups of lineages, which have not yet been linked to morphospecies, and many of them likely belong to yet undescribed parasite species. Tissue stages of Leucocytozoon parasites developing in accipitriform raptors were discovered and described. The majority of Leucocytozoon and Haemoproteus lineages are specific to this host group, but most Plasmodium lineages were found in birds of other orders. This might indicate local transmission from birds kept at the same facilities (raptor rescue centres and zoos), likely resulting in abortive infections. To clarify the taxonomic and systematic problems, combined morphological and molecular genetic analyses on a wider range of accipitriform host species are needed.

Project description:BackgroundPlasmodium species feature only four to eight nuclear ribosomal units on different chromosomes, which are assumed to evolve independently according to a birth-and-death model, in which new variants originate by duplication and others are deleted throughout time. Moreover, distinct ribosomal units were shown to be expressed during different developmental stages in the vertebrate and mosquito hosts. Here, the 18S rDNA sequences of 32 species of avian haemosporidian parasites are reported and compared to those of simian and rodent Plasmodium species.MethodsAlmost the entire 18S rDNAs of avian haemosporidians belonging to the genera Plasmodium (7), Haemoproteus (9), and Leucocytozoon (16) were obtained by PCR, molecular cloning, and sequencing ten clones each. Phylogenetic trees were calculated and sequence patterns were analysed and compared to those of simian and rodent malaria species. A section of the mitochondrial CytB was also sequenced.ResultsSequence patterns in most avian Plasmodium species were similar to those in the mammalian parasites with most species featuring two distinct 18S rDNA sequence clusters. Distinct 18S variants were also found in Haemoproteus tartakovskyi and the three Leucocytozoon species, whereas the other species featured sets of similar haplotypes. The 18S rDNA GC-contents of the Leucocytozoon toddi complex and the subgenus Parahaemoproteus were extremely high with 49.3% and 44.9%, respectively. The 18S sequences of several species from all three genera showed chimeric features, thus indicating recombination.ConclusionGene duplication events leading to two diverged main sequence clusters happened independently in at least six out of seven avian Plasmodium species, thus supporting evolution according to a birth-and-death model like proposed for the ribosomal units of simian and rodent Plasmodium species. Patterns were similar in the 18S rDNAs of the Leucocytozoon toddi complex and Haemoproteus tartakovskyi. However, the 18S rDNAs of the other species seem to evolve in concerted fashion like in most eukaryotes, but the presence of chimeric variants indicates that the ribosomal units rather evolve in a semi-concerted manner. The new data may provide a basis for studies testing whether differential expression of distinct 18S rDNA also occurs in avian Plasmodium species and related haemosporidian parasites.

Project description:BackgroundThe mobility of birds across or between continents exposes them to numerous vectors that have the potential to transmit pathogens and spread them into new regions. A combination of rich species diversity of birds along with the small amount of molecular studies in Iran makes observing the blood parasite distribution in wild avian populations indispensable for further estimation and administration of blood parasites.Methodology/principal findingsIn order to evaluate the infection rate and molecular context of avian blood parasites, bird samples were collected (passerine = 316 and non-passerine = 14) in eight provinces of northern Iran between June to September 2015 and 2016. All bird samples were examined for haematoprotozoan infections by morphological screening using light microscope and mtDNA cytb gene amplification. A total of 115 birds were positive for blood parasites by molecular approach (34.84% overall infection). The infection rate of Haemoproteus, Plasmodium, and Leucocytozoon were 33.03%, 1.21%, and 0.6%, respectively. Sequences analysis has detected 43 lineages in Iranian birds' hosts. Lineages were attributed to three genera Haemoproteus (n = 37), Plasmodium (n = 4), and Leucocytozoon (n = 2), of which 23 lineages fully matched previously recorded sequences in GenBank and MalAvi data reciprocities. Five lineages of ACDUM1, ACDUM2, PARUS1, PYERY01, and SISKIN1 were detected in multiple hosts' species from dissimilar families. In Bayesian tree, all sequences were clustered in three main monophyletic clades as Haemoproteus, Plasmodium, and Leucocytozoon genera.Conclusions/significanceAs the first study outlining the molecular detection of hematozoa of passerines from Iran, the current study has recorded 20 new lineages for three genera of Haemoproteus, Plasmodium, and Leucocytozoon. Additional investigations into these taxa in the avifauna for the other parts of Iran may provide extra information on blood parasites, hosts relationships and distribution patterns.

Project description:BackgroundHaemosporidian parasites are transmitted by dipteran blood-sucking insects but certain vectors remain unidentified for the great majority of described species. Sensitive PCR-based methods are often used for the detection of haemosporidian infection in wild-caught insects. However, this approach alone cannot distinguish between different sporogonic stages and thus is insufficient to demonstrate that the parasites produce the infective stage (sporozoite), which is essential for transmission. To prove that PCR-positive insects could act as vectors, the record of sporozoites is needed. We developed a methodology for the determination of natural vectors of avian Haemoproteus species and other haemosporidians. The essence of this approach is to apply PCR-based and microscopic diagnostic tools in parallel for sporozoite detection in insects.MethodsCulicoides biting midges transmit avian Haemoproteus parasites, but certain insect species, which are involved in transmission, remain insufficiently investigated. Biting midges were collected in the wild and identified; parous females were dissected and preparations of thorax content containing salivary glands were prepared. Remnants of the dissected midges were screened using PCR-based methods. Only thorax preparations of PCR-positive biting midges were examined microscopically.ResultsIn total, 460 parous females belonging to 15 species were collected and dissected. DNA of haemosporidians was detected in 32 (7%) of dissected insects belonging to 7 species. Of the thorax samples PCR-positive for Haemoproteus parasites, two preparations were microscopically positive for sporozoites. Both biting midges were Culicoides kibunensis. Haemoproteus pallidus (hPFC1) was identified, indicating that transmission of this infection occurs at the study site. It was proved that seven species of biting midges take bird blood meals naturally in the wild.ConclusionsCulicoides kibunensis is a new vector species of avian haemoproteids and is a natural vector of H. pallidus. Numerous studies have identified vectors of Haemoproteus parasites experimentally; however, this is the first direct identification of a natural vector of Haemoproteus infection in the Old World. We suggest using the described methodology for vector research of Haemoproteus and other haemosporidians in the wild.

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Effects of forest structure on the interaction between avian hosts, dipteran vectors and haemosporidian parasites

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