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      Diversity and distribution of avian malaria and related haemosporidian parasites in captive birds from a Brazilian megalopolis

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          Abstract

          Background

          The role of zoos in conservation programmes has increased significantly in last decades, and the health of captive animals is essential to guarantee success of such programmes. However, zoo birds suffer from parasitic infections, which often are caused by malaria parasites and related haemosporidians. Studies determining the occurrence and diversity of these parasites, aiming better understanding infection influence on fitness of captive birds, are limited.

          Methods

          In 2011–2015, the prevalence and diversity of Plasmodium spp. and Haemoproteus spp. was examined in blood samples of 677 captive birds from the São Paulo Zoo, the largest zoo in Latin America. Molecular and microscopic diagnostic methods were used in parallel to detect and identify these infections.

          Results

          The overall prevalence of haemosporidians was 12.6%. Parasites were mostly detected by the molecular diagnosis, indicating that many birds harbour subclinical or abortive infections. In this project, birds of 17 orders (almost half of all the orders currently accepted in taxonomy of birds), 29 families, and 122 species, were tested, detecting positive individuals in 27% of bird species. Birds from the Anatidae were the most prevalently infected (64.7% of all infected animals). In all, infections with parasites of the genus Plasmodium (overall prevalence 97.6%) predominated when compared to those of the genus Haemoproteus (2.4%). In total, 14 cytochrome b ( cytb) lineages of Plasmodium spp. and 2 cytb lineages of Haemoproteus spp. were recorded. Eight lineages were new. One of the reported lineages was broad generalist while others were reported in single or a few species of birds. Molecular characterization of Haemoproteus ortalidum was developed.

          Conclusion

          This study shows that many species of birds are at risk in captivity. It is difficult to stop haemosporidian parasite transmission in zoos, but is possible to reduce the infection rate by treating the infected animals or/and while keeping them in facilities free from mosquitoes. Protocols of quarantine should be implemented whenever an animal is transferred between bird maintaining institutions. This is the first survey of haemosporidians in captive birds from different orders maintained in zoos. It is worth emphasizing the necessity of applying practices to control these parasites in management and husbandry of animals in captivity.

          Electronic supplementary material

          The online version of this article (doi:10.1186/s12936-017-1729-8) contains supplementary material, which is available to authorized users.

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          Most cited references58

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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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            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.
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              Plasmodium relictum (lineage P-SGS1): effects on experimentally infected passerine birds.

              We evaluated the effects of Plasmodium relictum (lineage P-SGS1), which is a host generalist, to five species of passerine birds. Light infection of P. relictum was isolated from a naturally infected adult reed warbler Acrocephalus scirpaceus. The parasites were inoculated to naive juveniles of the chaffinch Fringilla coelebs, common crossbill Loxia curvirostra, house sparrow Passer domesticus, siskin Spinus spinus and starling Sturnus vulgaris. Susceptibility of these birds to the infection of P. relictum was markedly different. This parasite developed in birds belonging to the Fringillidae and Passeridae but the starlings (Sturnidae) were resistant. Only 50% of experimental house sparrows were susceptible to the infection. The intensity of parasitemia varied markedly inside and between different susceptible bird species. There were no effects of the infection on body mass or temperature of experimentally infected birds. Infection of P. relictum leads to the significant decrease of haematocrit value and hypertrophy of spleen and liver in heavily infected common crossbills and siskins. This study shows that infection of the same lineage of P. relictum causes diseases of different severity in different avian hosts; that might have different evolutionary consequences and should be taken in consideration in conservation projects.
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                Author and article information

                Contributors
                crfchagas@gmail.com
                gedvalk@ekoi.lt
                lilianguima@gmail.com
                eliana@biologia.bio.br
                fe_jvaz@yahoo.com.br
                rosefsimoes@gmail.com
                priscilatihara@usp.br
                eluna@usp.br
                karink@usp.br
                Journal
                Malar J
                Malar. J
                Malaria Journal
                BioMed Central (London )
                1475-2875
                17 February 2017
                17 February 2017
                2017
                : 16
                : 83
                Affiliations
                [1 ]São Paulo Zoo Foundation, Av. Miguel Estéfano 4241, São Paulo, SP 04301-905 Brazil
                [2 ]ISNI 0000 0004 0522 3211, GRID grid.435238.b, , Nature Research Centre, ; Akademijos 2, Vilnius, 08412 Lithuania
                [3 ]ISNI 0000 0004 1937 0722, GRID grid.11899.38, Malaria Research Center, Superintendence for Endemic Disease Control, São Paulo, Institute of Tropical Medicine, , University of São Paulo, ; Av. Dr. Enéas de Carvalho, Aguiar 470, São Paulo, SP 05403-000 Brazil
                [4 ]ISNI 0000 0004 1937 0722, GRID grid.11899.38, Department of Parasitology, Institute of Biomedical Sciences, , University of São Paulo, ; Av. Prof. Lineu Prestes 1374, São Paulo, SP 05508-900 Brazil
                [5 ]ISNI 0000 0004 1937 0722, GRID grid.11899.38, Virology Laboratory, Institute of Tropical Medicine, , University of São Paulo, ; Av. Dr. Enéas de Carvalho Aguiar 470, São Paulo, SP 05403-000 Brazil
                Article
                1729
                10.1186/s12936-017-1729-8
                5316177
                28212654
                0770a4fb-b50b-4d14-a10f-62a73a0cba4c
                © The Author(s) 2017

                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
                : 24 December 2016
                : 8 February 2017
                Funding
                Funded by: FAPESP
                Award ID: 2012/51427-1
                Award Recipient :
                Categories
                Research
                Custom metadata
                © The Author(s) 2017

                Infectious disease & Microbiology
                avian malaria,plasmodium,haemoproteus,captive birds,zoo,conservation
                Infectious disease & Microbiology
                avian malaria, plasmodium, haemoproteus, captive birds, zoo, conservation

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