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      Rapid population decline in migratory shorebirds relying on Yellow Sea tidal mudflats as stopover sites

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          Abstract

          Migratory animals are threatened by human-induced global change. However, little is known about how stopover habitat, essential for refuelling during migration, affects the population dynamics of migratory species. Using 20 years of continent-wide citizen science data, we assess population trends of ten shorebird taxa that refuel on Yellow Sea tidal mudflats, a threatened ecosystem that has shrunk by >65% in recent decades. Seven of the taxa declined at rates of up to 8% per year. Taxa with the greatest reliance on the Yellow Sea as a stopover site showed the greatest declines, whereas those that stop primarily in other regions had slowly declining or stable populations. Decline rate was unaffected by shared evolutionary history among taxa and was not predicted by migration distance, breeding range size, non-breeding location, generation time or body size. These results suggest that changes in stopover habitat can severely limit migratory populations.

          Abstract

          Stopover sites are crucial to migratory birds, but the influence of this habitat on population dynamics has not been quantified. Here, Studds et al. show that, among ten migratory species, the degree of reliance on disappearing stopover habitat in the Yellow Sea tidal flats predicts the extent of recent population declines.

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          Most cited references42

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          Regional forest fragmentation and the nesting success of migratory birds.

          Forest fragmentation, the disruption in the continuity of forest habitat, is hypothesized to be a major cause of population decline for some species of forest birds because fragmentation reduces nesting (reproductive) success. Nest predation and parasitism by cowbirds increased with forest fragmentation in nine midwestern (United States) landscapes that varied from 6 to 95 percent forest cover within a 10-kilometer radius of the study areas. Observed reproductive rates were low enough for some species in the most fragmented landscapes to suggest that their populations are sinks that depend for perpetuation on immigration from reproductive source populations in landscapes with more extensive forest cover. Conservation strategies should consider preservation and restoration of large, unfragmented "core" areas in each region.
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            Migratory connectivity magnifies the consequences of habitat loss from sea-level rise for shorebird populations.

            Sea-level rise (SLR) will greatly alter littoral ecosystems, causing habitat change and loss for coastal species. Habitat loss is widely used as a measurement of the risk of extinction, but because many coastal species are migratory, the impact of habitat loss will depend not only on its extent, but also on where it occurs. Here, we develop a novel graph-theoretic approach to measure the vulnerability of a migratory network to the impact of habitat loss from SLR based on population flow through the network. We show that reductions in population flow far exceed the proportion of habitat lost for 10 long-distance migrant shorebirds using the East Asian-Australasian Flyway. We estimate that SLR will inundate 23-40% of intertidal habitat area along their migration routes, but cause a reduction in population flow of up to 72 per cent across the taxa. This magnifying effect was particularly strong for taxa whose migration routes contain bottlenecks-sites through which a large fraction of the population travels. We develop the bottleneck index, a new network metric that positively correlates with the predicted impacts of habitat loss on overall population flow. Our results indicate that migratory species are at greater risk than previously realized.
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              Unravelling the annual cycle in a migratory animal: breeding-season habitat loss drives population declines of monarch butterflies.

              Threats to migratory animals can occur at multiple periods of the annual cycle that are separated by thousands of kilometres and span international borders. Populations of the iconic monarch butterfly (Danaus plexippus) of eastern North America have declined over the last 21 years. Three hypotheses have been posed to explain the decline: habitat loss on the overwintering grounds in Mexico, habitat loss on the breeding grounds in the United States and Canada, and extreme weather events. Our objectives were to assess population viability, determine which life stage, season and geographical region are contributing the most to population dynamics and test the three hypotheses that explain the observed population decline. We developed a spatially structured, stochastic and density-dependent periodic projection matrix model that integrates patterns of migratory connectivity and demographic vital rates across the annual cycle. We used perturbation analysis to determine the sensitivity of population abundance to changes in vital rate among life stages, seasons and geographical regions. Next, we compared the singular effects of each threat to the full model where all factors operate concurrently. Finally, we generated predictions to assess the risk of host plant loss as a result of genetically modified crops on current and future monarch butterfly population size and extinction probability. Our year-round population model predicted population declines of 14% and a quasi-extinction probability ( 5% within a century. Monarch abundance was more than four times more sensitive to perturbations of vital rates on the breeding grounds than on the wintering grounds. Simulations that considered only forest loss or climate change in Mexico predicted higher population sizes compared to milkweed declines on the breeding grounds. Our model predictions also suggest that mitigating the negative effects of genetically modified crops results in higher population size and lower extinction risk. Recent population declines stem from reduction in milkweed host plants in the United States that arise from increasing adoption of genetically modified crops and land-use change, not from climate change or degradation of forest habitats in Mexico. Therefore, reducing the negative effects of host plant loss on the breeding grounds is the top conservation priority to slow or halt future population declines of monarch butterflies in North America.
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                Author and article information

                Journal
                Nat Commun
                Nat Commun
                Nature Communications
                Nature Publishing Group
                2041-1723
                13 April 2017
                2017
                : 8
                : 14895
                Affiliations
                [1 ]School of Biological Sciences, University of Queensland , St. Lucia, 4072 Queensland, Australia
                [2 ]Department of Geography and Environmental Systems, University of Maryland, Baltimore County , Baltimore, Maryland 21250, USA
                [3 ]Migratory Bird Centre, Smithsonian Conservation Biology Institute , Washington, District Of Columbia 20008, USA
                [4 ]Bren School of Environmental Science & Management, University of California , Santa Barbara, California 93106, USA
                [5 ]Centre for Ecosystem Science, School of Biological, Earth and Environmental Sciences, University of New South Wales , Sydney, 2052 New South Wales, Australia
                [6 ]Arthur Rylah Institute for Environmental Research , Heidelberg, 3034 Victoria, Australia
                [7 ]Victorian Wader Study Group , 165 Dalgetty Rd., Beaumaris, 3193 Victoria, Australia
                [8 ]Global Flyway Network , PO Box 3089, Broome, 6725 Western Australia, Australia
                [9 ]Phillip Island Nature Park , PO Box 97 Cowes, 3922 Victoria, Australia
                [10 ]Ornithological Society of New Zealand , 1261 Dovedale Road, RD 2 Wakefield, Nelson 7096, New Zealand
                [11 ]Queensland Wader Study Group, c/o CSIRO Oceans and Atmosphere , PO Box 2583, Brisbane, 4001 Queensland, Australia
                [12 ]Department of Life Sciences, Imperial College London, Silwood Park , Ascot SL5 7PY, UK
                [13 ]Ornithological Society of New Zealand , 231 Forest Hill Road, Waiatarua, Auckland 0612, New Zealand
                [14 ]Avifauna Research and Services Pty Ltd , PO Box 2006, Rockdale, 2216 New South Wales, Australia
                [15 ]Institute for Marine and Antarctic Studies, University of Tasmania , Sandy Bay, 7001 Tasmania, Australia
                Author notes
                Author information
                http://orcid.org/0000-0003-1782-8106
                http://orcid.org/0000-0001-9468-9678
                Article
                ncomms14895
                10.1038/ncomms14895
                5399291
                28406155
                f4907f2a-7618-4251-b41b-dbc804b1af1b
                Copyright © 2017, The Author(s)

                This work is licensed under a Creative Commons Attribution 4.0 International License. The images or other third party material in this article are included in the article's Creative Commons license, unless indicated otherwise in the credit line; if the material is not included under the Creative Commons license, users will need to obtain permission from the license holder to reproduce the material. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/

                History
                : 12 April 2016
                : 09 February 2017
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