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      Haemoproteus minutus is highly virulent for Australasian and South American parrots

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          Abstract

          Background

          Haemoproteus and Plasmodium species are widespread avian blood parasites. Several Plasmodium species are known for their high virulence and have caused significant declines in naïve bird populations. The impact of closely related Haemoproteus parasites is largely unknown. Recently we reported a lethal disease in two parrot aviaries caused by Haemoproteus parasites.

          Results

          Here we show that the causative pathogen Haemoproteus minutus is responsible for further 17 lethal outbreaks in parrot aviaries in Denmark, Germany and Great Britain. All affected parrots are endemic to Australasia and South America. We sequenced the cytochrome b gene from megalomeront-infected muscle tissue of 21 parrots and identified the two lineages TUPHI01 and TURDUS2 as causative agents, commonly naturally infecting the common blackbird ( Turdus merula) and the song thrush ( Turdus philomelos), respectively, in the Palaearctic. No intraerythrocytic parasite stages were found in any of the parrots. We failed to detect H. minutus in invasive Indian ring-necked parakeets ( Psittacula krameri) in Germany. Together this suggests that abortive infections with two virulent lineages of H. minutus are lethal for naïve parrot species from Australasia and South America. We asked whether we could detect H. minutus in New Zealand, where its Turdus hosts were introduced in the 1800s. We therefore tested invasive blackbirds and song thrushes, and the co-existing endemic red-fronted parakeet ( Cyanoramphus novaezelandiae) population on three New Zealand islands. No Haemoproteus spp. DNA was detected in all blood samples, indicating absence of transmission.

          Conclusions

          The results of this study show that captive parrots in Europe are threatened by two lineages of an otherwise benign parasite of Turdus spp. Aviary collections of parrots should be protected from Culicoides spp. vectors in Europe. Animal trade and climate changes extending the current vector and parasite distribution have to be considered as potential risk factors for the introduction of the disease in naïve parrot populations.

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          Most cited references45

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          Dynamics of mitochondrial DNA evolution in animals: amplification and sequencing with conserved primers.

          With a standard set of primers directed toward conserved regions, we have used the polymerase chain reaction to amplify homologous segments of mtDNA from more than 100 animal species, including mammals, birds, amphibians, fishes, and some invertebrates. Amplification and direct sequencing were possible using unpurified mtDNA from nanogram samples of fresh specimens and microgram amounts of tissues preserved for months in alcohol or decades in the dry state. The bird and fish sequences evolve with the same strong bias toward transitions that holds for mammals. However, because the light strand of birds is deficient in thymine, thymine to cytosine transitions are less common than in other taxa. Amino acid replacement in a segment of the cytochrome b gene is faster in mammals and birds than in fishes and the pattern of replacements fits the structural hypothesis for cytochrome b. The unexpectedly wide taxonomic utility of these primers offers opportunities for phylogenetic and population research.
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            Wildlife disease. Recent introduction of a chytrid fungus endangers Western Palearctic salamanders.

            Emerging infectious diseases are reducing biodiversity on a global scale. Recently, the emergence of the chytrid fungus Batrachochytrium salamandrivorans resulted in rapid declines in populations of European fire salamanders. Here, we screened more than 5000 amphibians from across four continents and combined experimental assessment of pathogenicity with phylogenetic methods to estimate the threat that this infection poses to amphibian diversity. Results show that B. salamandrivorans is restricted to, but highly pathogenic for, salamanders and newts (Urodela). The pathogen likely originated and remained in coexistence with a clade of salamander hosts for millions of years in Asia. As a result of globalization and lack of biosecurity, it has recently been introduced into naïve European amphibian populations, where it is currently causing biodiversity loss. Copyright © 2014, American Association for the Advancement of Science.
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              Population biology of multihost pathogens.

              The majority of pathogens, including many of medical and veterinary importance, can infect more than one species of host. Population biology has yet to explain why perceived evolutionary advantages of pathogen specialization are, in practice, outweighed by those of generalization. Factors that predispose pathogens to generalism include high levels of genetic diversity and abundant opportunities for cross-species transmission, and the taxonomic distributions of generalists and specialists appear to reflect these factors. Generalism also has consequences for the evolution of virulence and for pathogen epidemiology, making both much less predictable. The evolutionary advantages and disadvantages of generalism are so finely balanced that even closely related pathogens can have very different host range sizes.
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                Author and article information

                Contributors
                L.Ortiz-Catedral@massey.ac.nz
                d.h.brunton@massey.ac.nz
                M.Stidworthy@izvg.co.uk
                Hany.Elsheikha@nottingham.ac.uk
                tomp@stdavids-poultryteam.co.uk
                Christoph.Schulze@Landeslabor-bbb.de
                michibraun@gmx.de
                wink@uni-hd.de
                helgerlach@aol.com
                hpendl@pendl-lab.com
                achim.gruber@fu-berlin.de
                John.Ewen@ioz.ac.uk
                jperez@bio.ucm.es
                gedvalk@ekoi.lt
                philipp.olias@vetsuisse.unibe.ch
                Journal
                Parasit Vectors
                Parasit Vectors
                Parasites & Vectors
                BioMed Central (London )
                1756-3305
                17 January 2019
                17 January 2019
                2019
                : 12
                : 40
                Affiliations
                [1 ]ISNI 0000 0001 0696 9806, GRID grid.148374.d, Massey University, Institute of Natural and Mathematical Sciences, Massey University, ; Private Bag 102904, North Shore Mail Centre, Auckland, 0745 New Zealand
                [2 ]International Zoo Veterinary Group, Station House, Parkwood Street, Keighley, BD21 4NQ UK
                [3 ]ISNI 0000 0004 1936 8868, GRID grid.4563.4, University of Nottingham, School of Veterinary Medicine and Science, Sutton Bonington Campus, ; Sutton Bonington, Leicestershire, LE12 5RD UK
                [4 ]Ayr Disease Surveillance Centre, Auchincruive, Ayr, KA6 5AE UK
                [5 ]Berlin-Brandenburg State Laboratory, Gerhard-Neumann-Str. 2, 15236 Frankfurt (Oder), Germany
                [6 ]ISNI 0000 0001 2190 4373, GRID grid.7700.0, Heidelberg University, Institute of Pharmacy and Molecular Biotechnology, ; Im Neuenheimer Feld 364, 69120 Heidelberg, Germany
                [7 ]Gerlach Laboratory, Grosshessloher Strasse 23, 81479 Munich, Germany
                [8 ]Pendl Laboratory, Untere Roostmatt 7, 6300 Zug, Switzerland
                [9 ]ISNI 0000 0000 9116 4836, GRID grid.14095.39, Freie Universität Berlin, Institute of Veterinary Pathology, ; Robert-von-Ostertag-Str. 15, 14163 Berlin, Germany
                [10 ]ISNI 0000 0001 2242 7273, GRID grid.20419.3e, Zoological Society of London, Institute of Zoology, ; Regent’s Park, London, NW1 4RY UK
                [11 ]ISNI 0000 0001 2157 7667, GRID grid.4795.f, Departamento de Biodiversidad, Ecología y Evolución, Facultad de Biología (Planta 9), , Complutense University of Madrid, ; C/ José Antonio Novais, 2. Ciudad Universitaria, 28040 Madrid, Spain
                [12 ]ISNI 0000 0004 0522 3211, GRID grid.435238.b, Institute of Ecology, Nature Research Centre, ; Akademijos str. 2, 08412 Vilnius, Lithuania
                [13 ]ISNI 0000 0001 0726 5157, GRID grid.5734.5, University of Bern, Institute of Animal Pathology, ; Länggassstrasse 122, 3063 Bern, Switzerland
                Author information
                http://orcid.org/0000-0002-7200-2414
                Article
                3255
                10.1186/s13071-018-3255-0
                6337802
                30654841
                74b2399a-c636-45b0-9465-54d3401cfc3d
                © The Author(s). 2019

                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
                : 7 September 2018
                : 4 December 2018
                Categories
                Research
                Custom metadata
                © The Author(s) 2019

                Parasitology
                haemoproteus,plasmodium,malaria,haemosporida,apicomplexa,psittaciformes,parrot,conservation
                Parasitology
                haemoproteus, plasmodium, malaria, haemosporida, apicomplexa, psittaciformes, parrot, conservation

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