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      Sedentary songbirds maintain higher prevalence of haemosporidian parasite infections than migratory conspecifics during seasonal sympatry

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          Abstract

          Long-distance migrations influence the physiology, behavior, and fitness of migratory animals throughout their annual cycles, and fundamentally alter their interactions with parasites. Several hypotheses relating migratory behavior to the likelihood of parasitism have entered the literature, making conflicting, testable predictions. To assess how migratory behavior of hosts is associated with parasitism, we compared haemosporidian parasite infections between two closely related populations of a common North American sparrow, the dark-eyed junco, that co-occur in shared habitats during the non-breeding season. One population is sedentary and winters and breeds in the Appalachian Mountains. The other population is migratory and is found in seasonal sympatry with the sedentary population from October through April, but then flies (≥ 900 km) northwards to breed. The populations were sampled in the wild on the shared montane habitat at the beginning of winter and again after confining them in a captive common environment until the spring. We found significantly higher prevalence of haemosporidian parasite infections in the sedentary population. Among infected juncos, we found no difference in parasite densities (parasitemias) between the sedentary and migrant populations and no evidence for winter dormancy of the parasites. Our results suggest that long-distance migration may reduce the prevalence of parasite infections at the population level. Our results are inconsistent with the migratory exposure hypothesis, which posits that long-distance migration increases exposure of hosts to diverse parasites, and with the migratory susceptibility hypothesis, which posits that trade-offs between immune function and migration increase host susceptibility to parasites. However, our results are consistent with the migratory culling hypothesis, which posits that heavily infected animals are less likely to survive long-distance migration, and with the migratory escape hypothesis, which posits that long-distance migration allows host populations to seasonally escape areas of high infection risk.

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          Social Barriers to Pathogen Transmission in Wild Animal Populations

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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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              Lower predation risk for migratory birds at high latitudes.

              Quantifying the costs and benefits of migration distance is critical to understanding the evolution of long-distance migration. In migratory birds, life history theory predicts that the potential survival costs of migrating longer distances should be balanced by benefits to lifetime reproductive success, yet quantification of these reproductive benefits in a controlled manner along a large geographical gradient is challenging. We measured a controlled effect of predation risk along a 3350-kilometer south-north gradient in the Arctic and found that nest predation risk declined more than twofold along the latitudinal gradient. These results provide evidence that birds migrating farther north may acquire reproductive benefits in the form of lower nest predation risk.
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                Author and article information

                Contributors
                Role: ConceptualizationRole: Formal analysisRole: Funding acquisitionRole: InvestigationRole: MethodologyRole: Writing – original draftRole: Writing – review & editing
                Role: ConceptualizationRole: Formal analysisRole: MethodologyRole: SupervisionRole: Writing – review & editing
                Role: InvestigationRole: MethodologyRole: Writing – review & editing
                Role: InvestigationRole: MethodologyRole: ValidationRole: Writing – review & editing
                Role: InvestigationRole: MethodologyRole: ValidationRole: Writing – review & editing
                Role: SupervisionRole: Writing – review & editing
                Role: ConceptualizationRole: Funding acquisitionRole: SupervisionRole: Writing – review & editing
                Role: ConceptualizationRole: InvestigationRole: MethodologyRole: SupervisionRole: Writing – review & editing
                Role: Editor
                Journal
                PLoS One
                PLoS ONE
                plos
                plosone
                PLoS ONE
                Public Library of Science (San Francisco, CA USA )
                1932-6203
                22 August 2018
                2018
                : 13
                : 8
                : e0201563
                Affiliations
                [1 ] Department of Biology, Indiana University, Bloomington, IN, United States of America
                [2 ] Environmental Resilience Institute, Indiana University, Bloomington, IN, United States of America
                [3 ] School of Natural Sciences, Black Hills State University, Spearfish, SD, United States of America
                [4 ] Zoology Department, Denver Museum of Nature and Science, Denver, CO, United States of America
                Universidade Federal de Minas Gerais, BRAZIL
                Author notes

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

                [¤]

                Current address: Department of Integrative Biology, University of California, Berkeley, CA, United States of America

                Author information
                http://orcid.org/0000-0002-2827-9387
                Article
                PONE-D-18-08287
                10.1371/journal.pone.0201563
                6104930
                30133475
                d52c42ec-e3ce-4812-95be-52b633ad1939
                © 2018 Slowinski 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
                : 18 March 2018
                : 17 July 2018
                Page count
                Figures: 4, Tables: 1, Pages: 18
                Funding
                Funded by: funder-id http://dx.doi.org/10.13039/100000002, National Institutes of Health;
                Award ID: 2 T32 HD049336-11A1
                Award Recipient :
                Funded by: funder-id http://dx.doi.org/10.13039/100000001, National Science Foundation;
                Award ID: IOS-1257474
                Award Recipient :
                Funded by: funder-id http://dx.doi.org/10.13039/100006733, Indiana University;
                Award ID: FRSP
                Award Recipient :
                Funded by: funder-id http://dx.doi.org/10.13039/100000057, National Institute of General Medical Sciences;
                Award ID: P20GM103443
                Award Recipient :
                This work was funded by the National Institute of Health Common Themes in Reproductive Diversity program for a Predoctoral Fellowship to SPS (grant number 2 T32 HD049336-11A1), the National Science Foundation (IOS-1257474 to E.D.K.), a FRSP grant from Indiana University to E.D.K., and by an Institutional Development Award (IDeA) from the National Institute of General Medical Sciences of the National Institutes of Health under grant number P20GM103443 through the South Dakota Biomedical Research Infrastructure Network (SD BRIN) core facilities. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
                Categories
                Research Article
                Medicine and Health Sciences
                Parasitic Diseases
                Biology and Life Sciences
                Behavior
                Animal Behavior
                Animal Migration
                Biology and Life Sciences
                Zoology
                Animal Behavior
                Animal Migration
                Biology and Life Sciences
                Organisms
                Eukaryota
                Animals
                Vertebrates
                Amniotes
                Birds
                Biology and Life Sciences
                Parasitology
                Quantitative Parasitology
                Parasitemia
                Biology and Life Sciences
                Species Interactions
                Parasitism
                Biology and Life Sciences
                Ecology
                Community Ecology
                Trophic Interactions
                Parasitism
                Ecology and Environmental Sciences
                Ecology
                Community Ecology
                Trophic Interactions
                Parasitism
                Medicine and Health Sciences
                Parasitic Diseases
                Protozoan Infections
                Biology and Life Sciences
                Molecular Biology
                Molecular Biology Techniques
                Artificial Gene Amplification and Extension
                Polymerase Chain Reaction
                Research and Analysis Methods
                Molecular Biology Techniques
                Artificial Gene Amplification and Extension
                Polymerase Chain Reaction
                Biology and Life Sciences
                Developmental Biology
                Life Cycles
                Parasitic Life Cycles
                Biology and Life Sciences
                Parasitology
                Parasitic Life Cycles
                Custom metadata
                Data will be archived and made available to readers in the online data repository DRYAD.

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                Uncategorized

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