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      Warmer temperatures advance flowering in a spring plant more strongly than emergence of two solitary spring bee species

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      PLoS ONE
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          Abstract

          Climate warming has the potential to disrupt plant-pollinator interactions or to increase competition of co-flowering plants for pollinators, due to species-specific phenological responses to temperature. However, studies focusing on the effect of temperature on solitary bee emergence and the flowering onset of their food plants under natural conditions are still rare. We studied the effect of temperature on the phenology of the two spring bees Osmia cornuta and Osmia bicornis, by placing bee cocoons on eleven grasslands differing in mean site temperature. On seven grasslands, we additionally studied the effect of temperature on the phenology of the red-list plant Pulsatilla vulgaris, which was the first flowering plant, and of co-flowering plants with later flowering. With a warming of 0.1°C, the abundance-weighted mean emergence of O. cornuta males advanced by 0.4 days. Females of both species did not shift their emergence. Warmer temperatures advanced the abundance-weighted mean flowering of P. vulgaris by 1.3 days per 0.1°C increase, but did not shift flowering onset of co-flowering plants. Competition for pollinators between P. vulgaris and co-flowering plants does not increase within the studied temperature range. We demonstrate that temperature advances plant flowering more strongly than bee emergence suggesting an increased risk of pollinator limitation for the first flowers of P. vulgaris.

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          Global warming and the disruption of plant-pollinator interactions.

          Anthropogenic climate change is widely expected to drive species extinct by hampering individual survival and reproduction, by reducing the amount and accessibility of suitable habitat, or by eliminating other organisms that are essential to the species in question. Less well appreciated is the likelihood that climate change will directly disrupt or eliminate mutually beneficial (mutualistic) ecological interactions between species even before extinctions occur. We explored the potential disruption of a ubiquitous mutualistic interaction of terrestrial habitats, that between plants and their animal pollinators, via climate change. We used a highly resolved empirical network of interactions between 1420 pollinator and 429 plant species to simulate consequences of the phenological shifts that can be expected with a doubling of atmospheric CO(2). Depending on model assumptions, phenological shifts reduced the floral resources available to 17-50% of all pollinator species, causing as much as half of the ancestral activity period of the animals to fall at times when no food plants were available. Reduced overlap between plants and pollinators also decreased diet breadth of the pollinators. The predicted result of these disruptions is the extinction of pollinators, plants and their crucial interactions.
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            How does climate warming affect plant-pollinator interactions?

            Climate warming affects the phenology, local abundance and large-scale distribution of plants and pollinators. Despite this, there is still limited knowledge of how elevated temperatures affect plant-pollinator mutualisms and how changed availability of mutualistic partners influences the persistence of interacting species. Here we review the evidence of climate warming effects on plants and pollinators and discuss how their interactions may be affected by increased temperatures. The onset of flowering in plants and first appearance dates of pollinators in several cases appear to advance linearly in response to recent temperature increases. Phenological responses to climate warming may therefore occur at parallel magnitudes in plants and pollinators, although considerable variation in responses across species should be expected. Despite the overall similarities in responses, a few studies have shown that climate warming may generate temporal mismatches among the mutualistic partners. Mismatches in pollination interactions are still rarely explored and their demographic consequences are largely unknown. Studies on multi-species plant-pollinator assemblages indicate that the overall structure of pollination networks probably are robust against perturbations caused by climate warming. We suggest potential ways of studying warming-caused mismatches and their consequences for plant-pollinator interactions, and highlight the strengths and limitations of such approaches.
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              Foraging ranges of solitary bees

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                Author and article information

                Contributors
                Role: Data curationRole: Formal analysisRole: InvestigationRole: MethodologyRole: ValidationRole: VisualizationRole: Writing – original draftRole: Writing – review & editing
                Role: ConceptualizationRole: 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
                24 June 2019
                2019
                : 14
                : 6
                : e0218824
                Affiliations
                [001]Department of Animal Ecology and Tropical Biology, Biocenter, University of Würzburg, Würzburg, Germany
                Universite du Quebec a Chicoutimi, CANADA
                Author notes

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

                Author information
                http://orcid.org/0000-0001-5345-1866
                Article
                PONE-D-19-05781
                10.1371/journal.pone.0218824
                6590824
                31233540
                9da8c60c-980f-4800-b3b5-a7c2c8d49135
                © 2019 Kehrberger, Holzschuh

                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
                : 27 February 2019
                : 10 June 2019
                Page count
                Figures: 3, Tables: 1, Pages: 15
                Funding
                Funding was provided to AH by the German Research Foundation (DFG), collaborative research centre SFB 1047 ‘Insect timing’. Additional funding for Open Access Publishing was provided by the German Research Foundation (DFG) and the University of Wuerzburg in the funding programme Open Access Publishing. 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
                Plants
                Flowering Plants
                Biology and Life Sciences
                Organisms
                Eukaryota
                Animals
                Invertebrates
                Arthropoda
                Insects
                Hymenoptera
                Bees
                Biology and Life Sciences
                Microbiology
                Medical Microbiology
                Microbial Pathogens
                Bacterial Pathogens
                Proteus Vulgaris
                Medicine and Health Sciences
                Pathology and Laboratory Medicine
                Pathogens
                Microbial Pathogens
                Bacterial Pathogens
                Proteus Vulgaris
                Biology and Life Sciences
                Evolutionary Biology
                Evolutionary Processes
                Evolutionary Emergence
                Biology and Life Sciences
                Organisms
                Eukaryota
                Plants
                Biology and Life Sciences
                Evolutionary Biology
                Evolutionary Processes
                Speciation
                Species Delimitation
                Biology and Life Sciences
                Plant Science
                Plant Anatomy
                Flowers
                Biology and Life Sciences
                Physiology
                Biological Locomotion
                Animal Flight
                Insect Flight
                Medicine and Health Sciences
                Physiology
                Biological Locomotion
                Animal Flight
                Insect Flight
                Custom metadata
                All relevant data are deposited on Dryad at DOI: 10.5061/dryad.5tq5dn6.

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                Uncategorized

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