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      Immune function and blood parasite infections impact stopover ecology in passerine birds

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          Abstract

          Stopovers play a crucial role for the success of migrating animals and are key to optimal migration theory. Variation in refuelling rates, stopover duration and departure decisions among individuals has been related to several external factors. The physiological mechanisms shaping stopover ecology are, however, less well understood. Here, we explore how immune function and blood parasite infections relate to several aspects of stopover behaviour in autumn migrating short- and long-distance migrating songbirds. We blood sampled individuals of six species and used an automated radio-telemetry system in the stopover area to subsequently quantify stopover duration, ‘bush-level’ activity patterns (~ 0.1–30 m), landscape movements (~ 30–6000 m), departure direction and departure time. We show that complement activity, the acute phase protein haptoglobin and blood parasite infections were related to prolonged stopover duration. Complement activity (i.e., lysis) and total immunoglobulins were negatively correlated with bush-level activity patterns. The differences partly depended on whether birds were long-distance or short-distance migrants. Birds infected with avian malaria-like parasites showed longer landscape movements during the stopover than uninfected individuals, and birds with double blood parasite infections departed more than 2.5 h later after sunset/sunrise suggesting shorter flight bouts. We conclude that variation in baseline immune function and blood parasite infection status affects stopover ecology and helps explain individual variation in stopover behaviour. These differences affect overall migration speed, and thus can have significant impact on migration success and induce carry-over effects on other annual-cycle stages. Immune function and blood parasites should, therefore, be considered as important factors when applying optimal migration theory.

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          Most cited references77

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          Ecological immunology: costly parasite defences and trade-offs in evolutionary ecology

          In the face of continuous threats from parasites, hosts have evolved an elaborate series of preventative and controlling measures - the immune system - in order to reduce the fitness costs of parasitism. However, these measures do have associated costs. Viewing an individual's immune response to parasites as being subject to optimization in the face of other demands offers potential insights into mechanisms of life history trade-offs, sexual selection, parasite-mediated selection and population dynamics. We discuss some recent results that have been obtained by practitioners of this approach in natural and semi-natural populations, and suggest some ways in which this field may progress in the near future.
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            Carry-over effects as drivers of fitness differences in animals.

            1. Carry-over effects occur when processes in one season influence the success of an individual in the following season. This phenomenon has the potential to explain a large amount of variation in individual fitness, but so far has only been described in a limited number of species. This is largely due to difficulties associated with tracking individuals between periods of the annual cycle, but also because of a lack of research specifically designed to examine hypotheses related to carry-over effects. 2. We review the known mechanisms that drive carry-over effects, most notably macronutrient supply, and highlight the types of life histories and ecological situations where we would expect them to most often occur. We also identify a number of other potential mechanisms that require investigation, including micronutrients such as antioxidants. 3. We propose a series of experiments designed to estimate the relative contributions of extrinsic and intrinsic quality effects in the pre-breeding season, which in turn will allow an accurate estimation of the magnitude of carry-over effects. To date this has proven immensely difficult, and we hope that the experimental frameworks described here will stimulate new avenues of research vital to advancing our understanding of how carry-over effects can shape animal life histories. 4. We also explore the potential of state-dependent modelling as a tool for investigating carry-over effects, most notably for its ability to calculate optimal rates of acquisition of a multitude of resources over the course of the annual cycle, and also because it allows us to vary the strength of density-dependent relationships which can alter the magnitude of carry-over effects in either a synergistic or agonistic fashion. 5. In conclusion carry-over effects are likely to be far more widespread than currently indicated, and they are likely to be driven by a multitude of factors including both macro- and micronutrients. For this reason they could feasibly be responsible for a large amount of the observed variation in performance among individuals, and consequently warrant a wealth of new research designed specifically to decompose components of variation in fitness attributes related to processes across and within seasons. © 2010 The Authors. Journal compilation © 2010 British Ecological Society.
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              Optimum fuel loads in migratory birds: distinguishing between time and energy minimization

              By combining the potential flight range of fuel with different migration policies, the optimum departure fuel load for migratory birds can be calculated. We evaluate the optimum departure fuel loads associated with minimization of three different currencies: (1) overall time of migration, (2) energy cost of transport and (3) total energy coast of migration. Predicted departure loads are highest for (1), lowest for (2) and intermediate for (3). Further, currencies (1) and (3) show departure loads dependent on the fuel accumulation rate at stopovers, while (2) is not affected by variation in the rate of fuel accumulation. Furthermore, fuel loads optimized with respect to currency (3) will differ depending on the size (body mass) of the bird and the energy density of the fuel. We review ecological situations in which the various currencies may apply, and suggest how a combination of stopover decisions and observations of flight speed may be used to decide among the three cases of migration policies. Finally, we calculate that the total energy cost of migration is roughly divided between flight and stopover as 1:2. The total time of migration is similarly divided between flight and stopover as 1:7, probably with a relatively longer stopover time in larger species. Hence, we may expect strong selection pressures to optimize the fuel accumulation strategies during stopover episodes.Copyright 1997 Academic Press Limited Copyright 1997 Academic Press Limited
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                Author and article information

                Contributors
                arne.hegemann@biol.lu.se
                Journal
                Oecologia
                Oecologia
                Oecologia
                Springer Berlin Heidelberg (Berlin/Heidelberg )
                0029-8549
                1432-1939
                1 November 2018
                1 November 2018
                2018
                : 188
                : 4
                : 1011-1024
                Affiliations
                [1 ]ISNI 0000 0001 0930 2361, GRID grid.4514.4, Department of Biology, , Lund University, ; Ecology Building, 223 62 Lund, Sweden
                [2 ]ISNI 0000 0001 0674 042X, GRID grid.5254.6, Center for Macroecology, Evolution and Climate, Natural History Museum of Denmark, , University of Copenhagen, ; Universitetsparken 15, 2100 Copenhagen, Denmark
                Author notes

                Communicated by Kevin D Matson.

                Author information
                http://orcid.org/0000-0002-3309-9866
                Article
                4291
                10.1007/s00442-018-4291-3
                6244813
                30386941
                476624e3-de90-4492-87fe-1245b94e0d63
                © The Author(s) 2018

                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.

                History
                : 14 March 2018
                : 22 October 2018
                Funding
                Funded by: FundRef http://dx.doi.org/10.13039/501100003246, Nederlandse Organisatie voor Wetenschappelijk Onderzoek;
                Award ID: 825.13.022
                Award Recipient :
                Funded by: Royal Physiographic Society of Lund
                Funded by: FundRef http://dx.doi.org/10.13039/501100004359, Vetenskapsrådet;
                Award ID: 621-2013-4357
                Award ID: 2016-04391
                Award ID: 621-2013-4386
                Award ID: 349-2007-8690
                Award Recipient :
                Categories
                Physiological Ecology - Original Research
                Custom metadata
                © Springer-Verlag GmbH Germany, part of Springer Nature 2018

                Ecology
                avian migration,eco-immunology,eco-physiology,optimal migration
                Ecology
                avian migration, eco-immunology, eco-physiology, optimal migration

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