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      Fragmentation of nest and foraging habitat affects time budgets of solitary bees, their fitness and pollination services, depending on traits: Results from an individual-based model

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          Abstract

          Solitary bees are important but declining wild pollinators. During daily foraging in agricultural landscapes, they encounter a mosaic of patches with nest and foraging habitat and unsuitable matrix. It is insufficiently clear how spatial allocation of nesting and foraging resources and foraging traits of bees affect their daily foraging performance. We investigated potential brood cell construction (as proxy of fitness), number of visited flowers, foraging habitat visitation and foraging distance (pollination proxies) with the model SOLBEE (simulating pollen transport by solitary bees, tested and validated in an earlier study), for landscapes varying in landscape fragmentation and spatial allocation of nesting and foraging resources. Simulated bees varied in body size and nesting preference. We aimed to understand effects of landscape fragmentation and bee traits on bee fitness and the pollination services bees provide, as well as interactions between them, and the general consequences it has to our understanding of the system. This broad scope gives multiple key results. 1) Body size determines fitness more than landscape fragmentation, with large bees building fewer brood cells. High pollen requirements for large bees and the related high time budgets for visiting many flowers may not compensate for faster flight speeds and short handling times on flowers, giving them overall a disadvantage compared to small bees. 2) Nest preference does affect distribution of bees over the landscape, with cavity-nesting bees being restricted to nesting along field edges, which inevitably leads to performance reductions. Fragmentation mitigates this for cavity-nesting bees through increased edge habitat. 3) Landscape fragmentation alone had a relatively small effect on all responses. Instead, the local ratio of nest to foraging habitat affected bee fitness positively through reduced local competition. The spatial coverage of pollination increases steeply in response to this ratio for all bee sizes. The nest to foraging habitat ratio, a strong habitat proxy incorporating fragmentation could be a promising and practical measure for comparing landscape suitability for pollinators. 4) The number of flower visits was hardly affected by resource allocation, but predominantly by bee size. 5) In landscapes with the highest visitation coverage, bees flew least far, suggesting that these pollination proxies are subject to a trade-off between either longer pollen transport distances or a better pollination coverage, linked to how nests are distributed over the landscape rather than being affected by bee size.

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          Confounding factors in the detection of species responses to habitat fragmentation.

          Habitat loss has pervasive and disruptive impacts on biodiversity in habitat remnants. The magnitude of the ecological impacts of habitat loss can be exacerbated by the spatial arrangement -- or fragmentation -- of remaining habitat. Fragmentation per se is a landscape-level phenomenon in which species that survive in habitat remnants are confronted with a modified environment of reduced area, increased isolation and novel ecological boundaries. The implications of this for individual organisms are many and varied, because species with differing life history strategies are differentially affected by habitat fragmentation. Here, we review the extensive literature on species responses to habitat fragmentation, and detail the numerous ways in which confounding factors have either masked the detection, or prevented the manifestation, of predicted fragmentation effects. Large numbers of empirical studies continue to document changes in species richness with decreasing habitat area, with positive, negative and no relationships regularly reported. The debate surrounding such widely contrasting results is beginning to be resolved by findings that the expected positive species-area relationship can be masked by matrix-derived spatial subsidies of resources to fragment-dwelling species and by the invasion of matrix-dwelling species into habitat edges. Significant advances have been made recently in our understanding of how species interactions are altered at habitat edges as a result of these changes. Interestingly, changes in biotic and abiotic parameters at edges also make ecological processes more variable than in habitat interiors. Individuals are more likely to encounter habitat edges in fragments with convoluted shapes, leading to increased turnover and variability in population size than in fragments that are compact in shape. Habitat isolation in both space and time disrupts species distribution patterns, with consequent effects on metapopulation dynamics and the genetic structure of fragment-dwelling populations. Again, the matrix habitat is a strong determinant of fragmentation effects within remnants because of its role in regulating dispersal and dispersal-related mortality, the provision of spatial subsidies and the potential mediation of edge-related microclimatic gradients. We show that confounding factors can mask many fragmentation effects. For instance, there are multiple ways in which species traits like trophic level, dispersal ability and degree of habitat specialisation influence species-level responses. The temporal scale of investigation may have a strong influence on the results of a study, with short-term crowding effects eventually giving way to long-term extinction debts. Moreover, many fragmentation effects like changes in genetic, morphological or behavioural traits of species require time to appear. By contrast, synergistic interactions of fragmentation with climate change, human-altered disturbance regimes, species interactions and other drivers of population decline may magnify the impacts of fragmentation. To conclude, we emphasise that anthropogenic fragmentation is a recent phenomenon in evolutionary time and suggest that the final, long-term impacts of habitat fragmentation may not yet have shown themselves.
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            A global quantitative synthesis of local and landscape effects on wild bee pollinators in agroecosystems.

            Bees provide essential pollination services that are potentially affected both by local farm management and the surrounding landscape. To better understand these different factors, we modelled the relative effects of landscape composition (nesting and floral resources within foraging distances), landscape configuration (patch shape, interpatch connectivity and habitat aggregation) and farm management (organic vs. conventional and local-scale field diversity), and their interactions, on wild bee abundance and richness for 39 crop systems globally. Bee abundance and richness were higher in diversified and organic fields and in landscapes comprising more high-quality habitats; bee richness on conventional fields with low diversity benefited most from high-quality surrounding land cover. Landscape configuration effects were weak. Bee responses varied slightly by biome. Our synthesis reveals that pollinator persistence will depend on both the maintenance of high-quality habitats around farms and on local management practices that may offset impacts of intensive monoculture agriculture. © 2013 Blackwell Publishing Ltd/CNRS.
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              Landscape effects on crop pollination services: are there general patterns?

              Pollination by bees and other animals increases the size, quality, or stability of harvests for 70% of leading global crops. Because native species pollinate many of these crops effectively, conserving habitats for wild pollinators within agricultural landscapes can help maintain pollination services. Using hierarchical Bayesian techniques, we synthesize the results of 23 studies - representing 16 crops on five continents - to estimate the general relationship between pollination services and distance from natural or semi-natural habitats. We find strong exponential declines in both pollinator richness and native visitation rate. Visitation rate declines more steeply, dropping to half of its maximum at 0.6 km from natural habitat, compared to 1.5 km for richness. Evidence of general decline in fruit and seed set - variables that directly affect yields - is less clear. Visitation rate drops more steeply in tropical compared with temperate regions, and slightly more steeply for social compared with solitary bees. Tropical crops pollinated primarily by social bees may therefore be most susceptible to pollination failure from habitat loss. Quantifying these general relationships can help predict consequences of land use change on pollinator communities and crop productivity, and can inform landscape conservation efforts that balance the needs of native species and people.
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                Author and article information

                Contributors
                Role: ConceptualizationRole: Data curationRole: Formal analysisRole: InvestigationRole: MethodologyRole: Project administrationRole: ResourcesRole: SoftwareRole: ValidationRole: VisualizationRole: Writing – original draftRole: Writing – review & editing
                Role: ConceptualizationRole: Funding acquisitionRole: ResourcesRole: SupervisionRole: Writing – review & editing
                Role: ConceptualizationRole: Formal analysisRole: Funding acquisitionRole: MethodologyRole: Project administrationRole: ResourcesRole: SupervisionRole: ValidationRole: Writing – review & editing
                Role: Editor
                Journal
                PLoS One
                PLoS ONE
                plos
                plosone
                PLoS ONE
                Public Library of Science (San Francisco, CA USA )
                1932-6203
                14 February 2018
                2018
                : 13
                : 2
                : e0188269
                Affiliations
                [1 ] Department of Computational Landscape Ecology, Helmholtz Centre for Environmental Research - UFZ, Leipzig, Germany
                [2 ] Department of Ecological Modelling, Helmholtz Centre for Environmental Research - UFZ, Leipzig, Germany
                [3 ] Department of Community Ecology, Helmholtz Centre for Environmental Research - UFZ, Halle, Germany
                RMIT University, AUSTRALIA
                Author notes

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

                [¤a]

                Current address: Department of Community Ecology, Helmholtz Centre for Environmental Research—UFZ, Halle, Germany

                [¤b]

                Current address: Spatial Interaction Ecology, German Centre for Integrative Biodiversity Research (iDiv) Halle-Jena-Leipzig, Leipzig, Germany

                [¤c]

                Current address: Institute of Biological Sciences, University of the Philippines, Los Baños, Philippines

                [¤d]

                Current address: Biometry and Environmental System Analysis, University of Freiburg, Freiburg, Germany

                Author information
                http://orcid.org/0000-0001-8569-7377
                Article
                PONE-D-17-19163
                10.1371/journal.pone.0188269
                5812554
                29444076
                7d8e5073-6584-4ad0-a60f-ffe8fe52dc53
                © 2018 Everaars 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 May 2017
                : 3 November 2017
                Page count
                Figures: 4, Tables: 5, Pages: 28
                Funding
                Funded by: funder-id http://dx.doi.org/10.13039/501100004813, Helmholtz-Zentrum für Umweltforschung;
                Award Recipient :
                Funded by: funder-id http://dx.doi.org/10.13039/100011103, Sixth Framework Programme;
                Award ID: GOCE-CT-2003-506675
                Award Recipient :
                Funded by: funder-id http://dx.doi.org/10.13039/100011103, Sixth Framework Programme;
                Award ID: GOCE-CT-2003-506675
                Award Recipient :
                Funded by: funder-id http://dx.doi.org/10.13039/100011103, Sixth Framework Programme;
                Award ID: GOCE-CT-2003-506675
                Award Recipient :
                Funded by: funder-id http://dx.doi.org/10.13039/501100004813, Helmholtz-Zentrum für Umweltforschung;
                Award Recipient :
                Funded by: funder-id http://dx.doi.org/10.13039/501100004813, Helmholtz-Zentrum für Umweltforschung;
                Award Recipient :
                JE, CFD and JS were funded during the study by the European Commission within FP 6 Integrated Project ALARM: Assessing LArge scale environmental Risks with tested Methods, grant number GOCE-CT-2003-506675, url: www.alarmproject.net, the Helmholtz Association (VH-NG 247), and the Helmholtz Impulse and Networking Fund through HIGRADE. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
                Categories
                Research Article
                Biology and Life Sciences
                Organisms
                Eukaryota
                Animals
                Invertebrates
                Arthropoda
                Insects
                Hymenoptera
                Bees
                Biology and Life Sciences
                Behavior
                Animal Behavior
                Foraging
                Biology and Life Sciences
                Zoology
                Animal Behavior
                Foraging
                Biology and Life Sciences
                Plant Science
                Plant Anatomy
                Flowers
                Biology and Life Sciences
                Plant Science
                Plant Anatomy
                Pollen
                Ecology and Environmental Sciences
                Habitats
                Biology and Life Sciences
                Plant Science
                Plant Physiology
                Pollination
                Biology and Life Sciences
                Physiology
                Physiological Parameters
                Medicine and Health Sciences
                Physiology
                Physiological Parameters
                Biology and Life Sciences
                Agriculture
                Crop Science
                Crops
                Custom metadata
                All relevant data are within the paper and its Supporting Information files.

                Uncategorized
                Uncategorized

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