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      Species and abundance of ectoparasitic flies (Diptera) in pied flycatcher nests in Fennoscandia

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          Abstract

          Background

          Birds host several ectoparasitic fly species with negative effects on nestling health and reproductive output, and with the capability of transmitting avian blood parasites. Information on the abundance and distribution of the ectoparasitic fly genera Ornithomya (Hippoboscidae) and Protocalliphora (Calliphoridae) in northern Europe is still generally poor, and we thus explored their geographic range and occurrence of these flies in the nests of a common avian model species, the pied flycatcher Ficedula hypoleuca.

          Methods

          Nests of F. hypoleuca were collected from 21 locations across Fennoscandia in summer 2013, across a latitudinal gradient (between 56 °N – 70 °N) and examined for the presence of fly puparia. Adult specimens of Ornithomya spp. were also collected for species identification. Fly species were identified morphologically and identifications confirmed with DNA barcoding.

          Results

          We found three species: two louse-flies − Ornithomya chloropus and O. avicularia − and one blow-fly, Protocalliphora azurea. The prevalence of O. avicularia was higher in southern latitudes and this species was not encountered beyond 62 °N whereas O. chloropus and P. azurea occurred across the whole range of latitudes. The prevalence of O. chloropus further increased with increasing distance from the coast – a pattern not documented before. The three fly species showed no interspecific associations in their prevalence.

          Conclusions

          Our study revealed relatively high prevalence for all the species ( O. chloropus 59 %, O. avicularia 20 %, P. azurea 32 %), and an interesting spatial pattern in the prevalence of the two louse fly species. Our sample did not indicate any major range shifts towards the north for the southern species as compared to the information from the past. Morphological identification of O. chloropus did not match with the corresponding sequences published in the GenBank and taxonomy of this group calls for further studies.

          Electronic supplementary material

          The online version of this article (doi:10.1186/s13071-015-1267-6) contains supplementary material, which is available to authorized users.

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          Most cited references40

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          Diptera vectors of avian Haemosporidian parasites: untangling parasite life cycles and their taxonomy.

          Haemosporida is a large group of vector-borne intracellular parasites that infect amphibians, reptiles, birds, and mammals. This group includes the different malaria parasites (Plasmodium spp.) that infect humans around the world. Our knowledge on the full life cycle of these parasites is most complete for those parasites that infect humans and, to some extent, birds. However, our current knowledge on haemosporidian life cycles is characterized by a paucity of information concerning the vector species responsible for their transmission among vertebrates. Moreover, our taxonomic and systematic knowledge of haemosporidians is far from complete, in particular because of insufficient sampling in wild vertebrates and in tropical regions. Detailed experimental studies to identify avian haemosporidian vectors are uncommon, with only a few published during the last 25 years. As such, little knowledge has accumulated on haemosporidian life cycles during the last three decades, hindering progress in ecology, evolution, and systematic studies of these avian parasites. Nonetheless, recently developed molecular tools have facilitated advances in haemosporidian research. DNA can now be extracted from vectors' blood meals and the vertebrate host identified; if the blood meal is infected by haemosporidians, the parasite's genetic lineage can also be identified. While this molecular tool should help to identify putative vector species, detailed experimental studies on vector competence are still needed. Furthermore, molecular tools have helped to refine our knowledge on Haemosporida taxonomy and systematics. Herein we review studies conducted on Diptera vectors transmitting avian haemosporidians from the late 1800s to the present. We also review work on Haemosporida taxonomy and systematics since the first application of molecular techniques and provide recommendations and suggest future research directions. Because human encroachment on natural environments brings human populations into contact with novel parasite sources, we stress that the best way to avoid emergent and reemergent diseases is through a program encompassing ecological restoration, environmental education, and enhanced understanding of the value of ecosystem services. © 2012 The Authors. Biological Reviews © 2012 Cambridge Philosophical Society.
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            The blood parasite Haemoproteus reduces survival in a wild bird: a medication experiment.

            While avian chronic haemoparasite infections induce reproductive costs, infection has not previously been shown to affect survival. Here, we experimentally reduced, through medication, the intensity of infection by Haemoproteus parasites in wild-breeding female blue tits Cyanistes caeruleus. However, this treatment did not reduce the intensity of infection in males or the intensity of infection by Leucocytozoon. Medicated females, but not males, showed increased local survival until the next breeding season compared with control birds. To our knowledge, this is the first empirical evidence showing long-term direct survival costs of chronic Haemoproteus infections in wild birds.
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              The phylogeny and evolution of host choice in the Hippoboscoidea (Diptera) as reconstructed using four molecular markers.

              Hippoboscoidea is a superfamily of Diptera that contains the Glossinidae or tsetse flies, the Hippoboscidae or louse flies, and two families of bat flies, the Streblidae and the Nycteribiidae. We reconstruct the phylogenetic relationships within Hippoboscoidea using maximum parsimony and Bayesian methods based on nucleotide sequences from fragments of four genes: nuclear 28S ribosomal DNA and the CPSase domain of CAD, and mitochondrial 16S rDNA and cytochrome oxidase I. We recover monophyly for most of the presently recognized groups within Hippoboscoidea including the superfamily as a whole, the Hippoboscidae, the Nycteribiidae, the bat flies, and the Pupipara (=Hippoboscidae+Nycteribiidae+Streblidae), as well as several subfamilies within the constituent families. Streblidae appear to be paraphyletic. Our phylogenetic hypothesis is well supported and decisive in that most competing topological hypotheses for the Hippoboscoidea require significantly longer trees. We confirm a single shift from a free-living fly to a blood-feeding ectoparasite of vertebrates and demonstrate that at least two host shifts from mammals to birds have occurred. Wings have been repeatedly lost, but never regained. The hippoboscoid ancestor also evolved adenotrophic viviparity and our cladogram is consistent with a gradual reduction in the motility of the deposited final instar larvae from active burrowing in the soil to true pupiparity where adult females glue the puparium within the confines of bat roosts.
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                Author and article information

                Contributors
                tapio.eeva@utu.fi
                tojajuan@utu.fi
                asa.berglund@emg.umu.se
                jon.brommer@utu.fi
                raimohyvonen@gmail.com
                tero.klemola@utu.fi
                tokrla@utu.fi
                o.loukola@qmul.ac.uk
                chimor@utu.fi
                karainio@utu.fi
                paivi.sirkia@helsinki.fi
                ejvest@utu.fi
                Journal
                Parasit Vectors
                Parasit Vectors
                Parasites & Vectors
                BioMed Central (London )
                1756-3305
                21 December 2015
                21 December 2015
                2015
                : 8
                : 648
                Affiliations
                [ ]Department of Biology, University of Turku, FI-20014 Turku, Finland
                [ ]Kevo Subarctic Research Institute, University of Turku, FI-20014 Turku, Finland
                [ ]Department of Ecology and Environmental Science, Umeå University, Umeå, Sweden
                [ ]Varnankatu 2 D, FI-20320 Turku, Finland
                [ ]Department of Biology, University of Oulu, FI-90014 Oulu, Finland
                [ ]Finnish Natural History Museum, Zoology Unit, University of Helsinki, FI-00014 Helsinki, Finland
                [ ]Department of Agricultural Sciences, Spatial Foodweb Ecology Group, University of Helsinki, FI-00014 Helsinki, Finland
                Article
                1267
                10.1186/s13071-015-1267-6
                4687113
                26691851
                2bd514cf-0361-448f-b698-7a2c8d722b16
                © Eeva et al. 2015

                Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License ( http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver ( http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.

                History
                : 8 October 2015
                : 11 December 2015
                Funding
                Funded by: FundRef http://dx.doi.org/10.13039/501100002341, Suomen Akatemia (FI);
                Award ID: 265859
                Award Recipient :
                Funded by: Turku University Foundation
                Funded by: FundRef http://dx.doi.org/http://dx.doi.org/10.13039/501100003502, Ella ja Georg Ehrnroothin Säätiö (FI);
                Funded by: Emil Aaltonen Foundation
                Categories
                Research
                Custom metadata
                © The Author(s) 2015

                Parasitology
                blood parasites,bird blowflies,ectoparasite prevalence,louse flies,pied flycatcher
                Parasitology
                blood parasites, bird blowflies, ectoparasite prevalence, louse flies, pied flycatcher

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