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      Detection, prevalence, and transmission of avian hematozoa in waterfowl at the Arctic/sub-Arctic interface: co-infections, viral interactions, and sources of variation

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          Abstract

          Background

          The epidemiology of avian hematozoa at high latitudes is still not well understood, particularly in sub-Arctic and Arctic habitats, where information is limited regarding seasonality and range of transmission, co-infection dynamics with parasitic and viral agents, and possible fitness consequences of infection. Such information is important as climate warming may lead to northward expansion of hematozoa with unknown consequences to northern-breeding avian taxa, particularly populations that may be previously unexposed to blood parasites.

          Methods

          We used molecular methods to screen blood samples and cloacal/oropharyngeal swabs collected from 1347 ducks of five species during May-August 2010, in interior Alaska, for the presence of hematozoa, Influenza A Virus (IAV), and IAV antibodies. Using models to account for imperfect detection of parasites, we estimated seasonal variation in prevalence of three parasite genera ( Haemoproteus, Plasmodium, Leucocytozoon) and investigated how co-infection with parasites and viruses were related to the probability of infection.

          Results

          We detected parasites from each hematozoan genus in adult and juvenile ducks of all species sampled. Seasonal patterns in detection and prevalence varied by parasite genus and species, age, and sex of duck hosts. The probabilities of infection for Haemoproteus and Leucocytozoon parasites were strongly positively correlated, but hematozoa infection was not correlated with IAV infection or serostatus. The probability of Haemoproteus infection was negatively related to body condition in juvenile ducks; relationships between Leucocytozoon infection and body condition varied among host species.

          Conclusions

          We present prevalence estimates for Haemoproteus, Leucocytozoon, and Plasmodium infections in waterfowl at the interface of the sub-Arctic and Arctic and provide evidence for local transmission of all three parasite genera. Variation in prevalence and molecular detection of hematozoa parasites in wild ducks is influenced by seasonal timing and a number of host traits. A positive correlation in co-infection of Leucocytozoon and Haemoproteus suggests that infection probability by parasites in one or both genera is enhanced by infection with the other, or that encounter rates of hosts and genus-specific vectors are correlated. Using size-adjusted mass as an index of host condition, we did not find evidence for strong deleterious consequences of hematozoa infection in wild ducks.

          Electronic supplementary material

          The online version of this article (doi:10.1186/s13071-016-1666-3) contains supplementary material, which is available to authorized users.

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          Most cited references74

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          ESTIMATING ABUNDANCE FROM REPEATED PRESENCE–ABSENCE DATA OR POINT COUNTS

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            Recent warming reverses long-term arctic cooling.

            The temperature history of the first millennium C.E. is sparsely documented, especially in the Arctic. We present a synthesis of decadally resolved proxy temperature records from poleward of 60 degrees N covering the past 2000 years, which indicates that a pervasive cooling in progress 2000 years ago continued through the Middle Ages and into the Little Ice Age. A 2000-year transient climate simulation with the Community Climate System Model shows the same temperature sensitivity to changes in insolation as does our proxy reconstruction, supporting the inference that this long-term trend was caused by the steady orbitally driven reduction in summer insolation. The cooling trend was reversed during the 20th century, with four of the five warmest decades of our 2000-year-long reconstruction occurring between 1950 and 2000.
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              Species interactions in a parasite community drive infection risk in a wildlife population.

              Most hosts, including humans, are simultaneously or sequentially infected with several parasites. A key question is whether patterns of coinfection arise because infection by one parasite species affects susceptibility to others or because of inherent differences between hosts. We used time-series data from individual hosts in natural populations to analyze patterns of infection risk for a microparasite community, detecting large positive and negative effects of other infections. Patterns remain once variations in host susceptibility and exposure are accounted for. Indeed, effects are typically of greater magnitude, and explain more variation in infection risk, than the effects associated with host and environmental factors more commonly considered in disease studies. We highlight the danger of mistaken inference when considering parasite species in isolation rather than parasite communities.
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                Author and article information

                Contributors
                bmeixell@usgs.gov
                arnol065@umn.edu
                mslindberg@alaska.edu
                mmsmith@usgs.gov
                jrun@mit.edu
                aramey@usgs.gov
                Journal
                Parasit Vectors
                Parasit Vectors
                Parasites & Vectors
                BioMed Central (London )
                1756-3305
                7 July 2016
                7 July 2016
                2016
                : 9
                : 390
                Affiliations
                [ ]Department of Fisheries, Wildlife, and Conservation Biology, University of Minnesota, St. Paul, MN 55108 USA
                [ ]U.S. Geological Survey, Alaska Science Center, Anchorage, AK 99508 USA
                [ ]Institute of Arctic Biology and Department of Biology and Wildlife, University of Alaska Fairbanks, Fairbanks, AK 99775 USA
                [ ]Department of Biological Engineering and Division of Comparative Medicine, Massachusetts Institute of Technology, Cambridge, MA 02139 USA
                Article
                1666
                10.1186/s13071-016-1666-3
                4936110
                27387437
                42d6a05a-3dff-4038-8a08-8078cbd13b34
                © The Author(s). 2016

                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
                : 23 March 2016
                : 23 June 2016
                Funding
                Funded by: U.S. Geological Survey (US)
                Funded by: FundRef http://dx.doi.org/http://dx.doi.org/10.13039/100000202, U.S. Fish and Wildlife Service;
                Funded by: Delta Waterfowl Foundation
                Funded by: FundRef http://dx.doi.org/http://dx.doi.org/10.13039/501100005266, Institute for Wetland and Waterfowl Research, Ducks Unlimited Canada;
                Funded by: CRIP (Center for Research on Influenza Pathogenesis)
                Award ID: HHSN272201400008C and HHSN266200700010C
                Award Recipient :
                Categories
                Research
                Custom metadata
                © The Author(s) 2016

                Parasitology
                hematozoa,blood parasites,co-infection,occupancy models,detection probability,haemoproteus,leucocytozoon,plasmodium,influenza a virus,waterfowl

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