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      An Exception to the Rule: Carry-Over Effects Do Not Accumulate in a Long-Distance Migratory Bird

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          Abstract

          Recent years have seen a growing consensus that events during one part of an animal's annual cycle can detrimentally affect its future fitness. Notably, migratory species have been shown to commonly display such carry-over effects, facing severe time constraints and physiological stresses that can influence events across seasons. However, to date, no study has examined a full annual cycle to determine when these carry-over effects arise and how long they persist within and across years. Understanding when carry-over effects are created and how they persist is critical to identifying those periods and geographic locations that constrain the annual cycle of a population and determining how selection is acting upon individuals throughout the entire year. Using three consecutive years of migration tracks and four consecutive years of breeding success data, we tested whether carry-over effects in the form of timing deviations during one migratory segment of the annual cycle represent fitness costs that persist or accumulate across the annual cycle for a long-distance migratory bird, the Hudsonian godwit, Limosa haemastica. We found that individual godwits could migrate progressively later than population mean over the course of an entire migration period, especially southbound migration, but that these deviations did not accumulate across the entire year and were not consistently detected among individuals across years. Furthermore, neither the accumulation of lateness during previous portions of the annual cycle nor arrival date at the breeding grounds resulted in individuals suffering reductions in their breeding success or survival. Given their extreme life history, such a lack of carry-over effects suggests that strong selection exists on godwits at each stage of the annual cycle and that carry-over effects may not be able to persist in such a system, but also emphasizes that high-quality stopover and wintering sites are critical to the maintenance of long-distance migratory populations.

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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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            Linking winter and summer events in a migratory bird by using stable-carbon isotopes

            For migratory birds, early arrival and physical condition on the breeding grounds are important determinants of reproductive success and fitness. Differences in arrival times often exceed a month, and later arriving individuals are often in poorer condition. Habitat-specific isotopic signatures indicate that the quality of winter habitats occupied by American redstarts (Setophaga ruticilla) determines their physical condition and spring departure dates, which in turn result in variable arrival schedules and condition on temperate breeding grounds. These findings link events in tropical winter grounds with those in temperate breeding areas for a migratory songbird and provide evidence that winter habitats may be limiting.
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              Absolute Consistency: Individual versus Population Variation in Annual-Cycle Schedules of a Long-Distance Migrant Bird

              Flexibility in scheduling varies throughout an organism’s annual cycle, reflecting relative temporal constraints and fitness consequences among life-history stages. Time-selection can act at different scales, either by limiting the range of alternative strategies in the population, or by increasing the precision of individual performance. We tracked individual bar-tailed godwits Limosa lapponica baueri for two full years (including direct observation during non-breeding seasons in New Zealand and geolocator tracking of round-trip migrations to Alaska) to present a full annual-cycle view of molt, breeding, and migration schedules. At both population and individual scales, temporal variation was greater in post-breeding than pre-breeding stages, and greater in molts than in movements, but schedules did not tighten across successive stages of migration toward the breeding grounds. In general, individual godwits were quite consistent in timing of events throughout the year, and repeatability of pre-breeding movements was particularly high (r = 0.82–0.92). However, we demonstrate that r values misrepresent absolute consistency by confounding inter- and intra-individual variation; the biological significance of r values can only be understood when these are considered separately. By doing so, we show that some stages have considerable tolerance for alternative strategies within the population, whereas scheduling of northbound migratory movements was similar for all individuals. How time-selection simultaneously shapes both individual and population variation is central to understanding and predicting adaptive phenological responses to environmental change.
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                Author and article information

                Contributors
                Role: Editor
                Journal
                PLoS One
                PLoS ONE
                plos
                plosone
                PLoS ONE
                Public Library of Science (San Francisco, USA )
                1932-6203
                2014
                11 February 2014
                : 9
                : 2
                : e86588
                Affiliations
                [1 ]Cornell Lab of Ornithology, Cornell University, Ithaca, New York, United States of America
                [2 ]British Antarctic Survey, Cambridge, United Kingdom
                Institute of Ecology, Germany
                Author notes

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

                Conceived and designed the experiments: NRS WMH. Performed the experiments: NRS. Analyzed the data: NRS WMH. Contributed reagents/materials/analysis tools: NRS JWF VA. Wrote the paper: NRS WMH. Developed technology employed in the study: VA JWF.

                [¤a]

                Current Address: Animal Ecology Group, University of Groningen, Groningen, The Netherlands

                [¤b]

                Current address: Migrate Technology Ltd., Coton, Cambridge, United Kingdom

                Article
                PONE-D-13-43687
                10.1371/journal.pone.0086588
                3921144
                24523862
                01bae09d-055d-4d84-8541-079f0a6451e6
                Copyright @ 2014

                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
                : 25 October 2013
                : 16 December 2013
                Page count
                Pages: 11
                Funding
                National Science Foundation (#1110444); David and Lucile Packard Foundation ( www.packard.org); U.S. Fish and Wildlife Service NMBCA (#4474 and 4073); Faucett Family Foundation ( http://faucett-family-foundation.idilogic.aidpage.com/prn-index.htm); Cornell University internal grants; Arctic Audubon Society ( http://www.arcticaudubon.org/grants.html); Ducks Unlimited Canada ( http://www.ducks.ca/our-science/graduate-fellowships/); American Museum of Natural History ( http://www.amnh.org/our-research/vertebrate-zoology/ornithology/grants). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
                Categories
                Research Article
                Biology
                Ecology
                Behavioral Ecology
                Conservation Science
                Evolutionary Ecology
                Global Change Ecology
                Physiological Ecology
                Population Ecology
                Evolutionary Biology
                Animal Behavior
                Behavioral Ecology
                Evolutionary Ecology
                Veterinary Science
                Animal Management
                Animal Behavior

                Uncategorized
                Uncategorized

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