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      Avian cholera outbreaks threaten seabird species on Amsterdam Island

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          Abstract

          Infectious diseases may be particularly critical for the conservation of endangered species. A striking example is the recurrent outbreaks that have been occurring in seabirds on Amsterdam Island for the past 30 years, threatening populations of three Endangered seabird species and of the endemic, Critically Endangered Amsterdam albatross Diomedea amsterdamensis. The bacteria Pasteurella multocida (avian cholera causative agent), and to a lesser extent Erysipelothrix rhusiopathiae (erysipelas causative agent), were both suspected to be responsible for these epidemics. Despite this critical situation, demographic trends were not available for these threatened populations, and the occurrence and characterization of potential causative agents of epizootics remain poorly known. The aims of the current study were to (i) provide an update of population trends for four threatened seabird species monitored on Amsterdam Island, (ii) assess the occurrence of P. multocida, and E. rhusiopathiae in live birds from five species, (iii) search for other infectious agents in these samples and, (iv) isolate and genotype the causative agent(s) of epizooties from dead birds. Our study shows that the demographic situation has worsened substantially in three seabird species during the past decade, with extremely low reproductive success and declining populations for Indian yellow-nosed albatrosses Thalassarche carteri, sooty albatrosses Phoebetria fusca, and northern rockhopper penguins Eudyptes moseleyi. Pasteurella multocida or E. rhusiopathiae were detected by PCR in live birds of all five investigated species, while results were negative for eight additional infectious agents. A single strain of P. multocida was repeatedly cultured from dead birds, while no E. rhusiopathiae could be isolated. These results highlight the significance of P. multocida in this particular eco-epidemiological system as the main agent responsible for epizootics. The study stresses the urgent need to implement mitigation measures to alter the course of avian cholera outbreaks threatening the persistence of seabird populations on Amsterdam Island.

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          A new nested polymerase chain reaction method very efficient in detecting Plasmodium and Haemoproteus infections from avian blood.

          Recently, several polymerase chain reaction (PCR)-based methods for detection and genetic identification of haemosporidian parasites in avian blood have been developed. Most of these have considerably higher sensitivity compared with traditional microscope-based examinations of blood smears. These new methods have already had a strong impact on several aspects of research on avian blood parasites. In this study, we present a new nested PCR approach, building on a previously published PCR method, which has significantly improved performance. We compare the new method with some existing assays and show, by sequence-based data, that the higher detection rate is mainly due to superior detection of Plasmodium spp. infections, which often are of low intensity and, therefore, hard to detect with other methods.
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            Mammal invaders on islands: impact, control and control impact.

            The invasion of ecosystems by exotic species is currently viewed as one of the most important sources of biodiversity loss. The largest part of this loss occurs on islands, where indigenous species have often evolved in the absence of strong competition, herbivory, parasitism or predation. As a result, introduced species thrive in those optimal insular ecosystems affecting their plant food, competitors or animal prey. As islands are characterised by a high rate of endemism, the impacted populations often correspond to local subspecies or even unique species. One of the most important taxa concerning biological invasions on islands is mammals. A small number of mammal species is responsible for most of the damage to invaded insular ecosystems: rats, cats, goats, rabbits, pigs and a few others. The effect of alien invasive species may be simple or very complex, especially since a large array of invasive species, mammals and others, can be present simultaneously and interact among themselves as well as with the indigenous species. In most cases, introduced species generally have a strong impact and they often are responsible for the impoverishment of the local flora and fauna. The best response to these effects is almost always to control the alien population, either by regularly reducing their numbers, or better still, by eradicating the population as a whole from the island. Several types of methods are currently used: physical (trapping, shooting), chemical (poisoning) and biological (e.g. directed use of diseases). Each has its own set of advantages and disadvantages, depending on the mammal species targeted. The best strategy is almost always to combine several methods. Whatever the strategy used, its long-term success is critically dependent on solid support from several different areas, including financial support, staff commitment, and public support, to name only a few. In many cases, the elimination of the alien invasive species is followed by a rapid and often spectacular recovery of the impacted local populations. However, in other cases, the removal of the alien is not sufficient for the damaged ecosystem to revert to its former state, and complementary actions, such as species re-introduction, are required. A third situation may be widespread: the sudden removal of the alien species may generate a further disequilibrium, resulting in further or greater damage to the ecosystem. Given the numerous and complex population interactions among island species, it is difficult to predict the outcome of the removal of key species, such as a top predator. This justifies careful pre-control study and preparation prior to initiating the eradication of an alien species, in order to avoid an ecological catastrophe. In addition, long-term monitoring ofthe post-eradication ecosystem is crucial to assess success and prevent reinvasion.
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              Development of PCR assays for species- and type-specific identification of Pasteurella multocida isolates.

              Genomic subtractive hybridization of closely related Pasteurella multocida isolates has generated clones useful in distinguishing hemorrhagic septicemia-causing type B strains from other P. multocida serotypes. Oligonucleotide primers designed during the sequencing of these clones have proved valuable in the development of PCR assays for rapid species- and type-specific detection of P. multocida and of type B:2 in particular. This study demonstrated that the primer pair designed from the sequence of the clone 6b (KTT72 and KTSP61) specifically amplified a DNA fragment from types B:2, B:5, and B:2,5 P. multocida and that the primers KMT1T7 and KMT1SP6 produced an amplification product unique to all P. multocida isolates analyzed. It was also shown that PCR amplification performed directly on bacterial colonies or cultures represents an extremely rapid, sensitive method of P. multocida identification.
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                Author and article information

                Contributors
                Role: ConceptualizationRole: Formal analysisRole: Funding acquisitionRole: InvestigationRole: Writing – original draft
                Role: ConceptualizationRole: InvestigationRole: MethodologyRole: Writing – original draft
                Role: Writing – original draft
                Role: Investigation
                Role: Investigation
                Role: ConceptualizationRole: Resources
                Role: ConceptualizationRole: Funding acquisitionRole: ResourcesRole: Writing – original draft
                Role: Formal analysisRole: InvestigationRole: Resources
                Role: ConceptualizationRole: Formal analysisRole: InvestigationRole: ResourcesRole: Writing – original draft
                Role: ConceptualizationRole: Funding acquisitionRole: Resources
                Role: ConceptualizationRole: Funding acquisitionRole: InvestigationRole: ResourcesRole: Supervision
                Role: ConceptualizationRole: Formal analysisRole: InvestigationRole: MethodologyRole: SupervisionRole: Writing – original draft
                Role: ConceptualizationRole: Funding acquisitionRole: ResourcesRole: Supervision
                Role: Editor
                Journal
                PLoS One
                PLoS ONE
                plos
                plosone
                PLoS ONE
                Public Library of Science (San Francisco, CA USA )
                1932-6203
                30 May 2018
                2018
                : 13
                : 5
                : e0197291
                Affiliations
                [1 ] Université de La Réunion, UMR PIMIT (Processus Infectieux en Milieu Insulaire Tropical), CNRS 9192, INSERM 1187, IRD 249, GIP CYROI, Saint Denis, La Réunion, France
                [2 ] Université de la Réunion, UMR ENTROPIE, UR, IRD, CNRS, Saint Denis, La Réunion, France
                [3 ] Centre de Recherche et de Veille sur les maladies émergentes dans l’Océan Indien, GIP CYROI, Sainte Clotilde, La Réunion, France
                [4 ] Centre d’Ecologie Fonctionnelle et Evolutive, CNRS-Université Montpellier UMR 5175, Montpellier, France
                [5 ] Réserve Naturelle Nationale des Terres Australes Françaises, Terres Australes et Antarctiques Françaises, rue Gabriel Dejean, Saint Pierre, La Réunion, France
                [6 ] Centre d’Etudes Biologiques de Chizé, UMR 7372CNRS – Université de La Rochelle, Villiers en Bois, France
                Peter Doherty Institute for Infection and Immunity, AUSTRALIA
                Author notes

                Competing Interests: The authors have declared that no competing interests exist.

                [¤]

                Current address: National Institute of Polar Research, Tachikawa, Tokyo, Japan

                Author information
                http://orcid.org/0000-0002-5649-0315
                Article
                PONE-D-17-25622
                10.1371/journal.pone.0197291
                5976148
                29847561
                cf6ac23c-41da-49ba-a760-44664b2aeeae
                © 2018 Jaeger et al

                This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

                History
                : 7 July 2017
                : 29 April 2018
                Page count
                Figures: 3, Tables: 2, Pages: 17
                Funding
                Funded by: funder-id http://dx.doi.org/10.13039/501100004796, Institut Polaire Français Paul Emile Victor;
                Award ID: ORNITHOECO-109
                Award Recipient :
                Funded by: Ministère des Outre-Mer
                Award Recipient :
                Funded by: funder-id http://dx.doi.org/10.13039/501100001665, Agence Nationale de la Recherche;
                Award ID: ANR EVEMATA
                Award Recipient :
                Funded by: Terres Australes et Antarctiques Françaises
                Award Recipient :
                Funded by: CeMEBLabEx
                Award Recipient :
                This research was supported by the French Polar Institute (IPEV program ORNITHOECO-109 to HW), le Ministère des Outre-Mer (MOM-2013 to AJ), the French National Research Agency (ANR EVEMATA 11 BSV7 003 to TB), les Terres Australes et Antarctiques Françaises and la Zone Atelier de Recherches sur l’Environnement Antarctique et Subantarctique (CNRS-INEE). VB is supported through a CeMEBLabEx post-doctoral fellowship. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
                Categories
                Research Article
                Biology and Life Sciences
                Microbiology
                Medical Microbiology
                Microbial Pathogens
                Bacterial Pathogens
                Pasteurella Multocida
                Medicine and Health Sciences
                Pathology and Laboratory Medicine
                Pathogens
                Microbial Pathogens
                Bacterial Pathogens
                Pasteurella Multocida
                Earth Sciences
                Geomorphology
                Topography
                Landforms
                Islands
                Biology and Life Sciences
                Organisms
                Eukaryota
                Animals
                Vertebrates
                Amniotes
                Birds
                Seabirds
                Biology and Life Sciences
                Organisms
                Eukaryota
                Animals
                Vertebrates
                Amniotes
                Birds
                Biology and Life Sciences
                Organisms
                Eukaryota
                Animals
                Vertebrates
                Amniotes
                Birds
                Seabirds
                Penguins
                Research and Analysis Methods
                Database and Informatics Methods
                Biological Databases
                Sequence Databases
                Research and Analysis Methods
                Database and Informatics Methods
                Bioinformatics
                Sequence Analysis
                Sequence Databases
                Medicine and Health Sciences
                Infectious Diseases
                Bacterial Diseases
                Cholera
                Medicine and Health Sciences
                Tropical Diseases
                Neglected Tropical Diseases
                Cholera
                Biology and Life Sciences
                Physiology
                Immune Physiology
                Bone Marrow
                Medicine and Health Sciences
                Physiology
                Immune Physiology
                Bone Marrow
                Biology and Life Sciences
                Immunology
                Immune System
                Bone Marrow
                Medicine and Health Sciences
                Immunology
                Immune System
                Bone Marrow
                Custom metadata
                All sequence data are available from the Genbank database (accession numbers MF040795 to MF040801). All other relevant data can be accessed at the following DOI: 10.5281/zenodo.1157302.

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                Uncategorized

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