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      Pollination in a new climate: Assessing the potential influence of flower temperature variation on insect pollinator behaviour

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          Abstract

          Climate change has the potential to enhance or disrupt biological systems, but currently, little is known about how organism plasticity may facilitate adaptation to localised climate variation. The bee-flower relationship is an exemplar signal-receiver system that may provide important insights into the complexity of ecological interactions in situations like this. For example, several studies on bee temperature preferences show that bees prefer to collect warm nectar from flowers at low ambient temperatures, but switch their preferences to cooler flowers at ambient temperatures above about 30° C. We used temperature sensor thermal probes to measure the temperature of outdoor flowers of 30 plant species in the Southern regions of the Australian mainland, to understand how different species could modulate petal temperature in response to changes in ambient temperature and, potentially, influence the decision-making of bees in the flowering plant’s favour. We found that flower petal temperatures respond in different ways to changing ambient temperature: linearly increasing or decreasing relative to the ambient temperature, dynamically changing in a non-linear manner, or varying their temperature along with the ambient conditions. For example, our investigation of the difference between ambient temperature and petal temperature ( ΔT), and ambient temperature, revealed a non-linear relationship for Erysimum linifolium and Polygala grandiflora that seems suited to bee temperature preferences. The temperature profiles of species like Hibertia vestita and H. obtusifolia appear to indicate that they do not have a cooling mechanism. These species may therefore be less attractive to bee pollinators in changing climatic conditions with ambient temperatures increasingly above 30° C. This may be to the species’ detriment when insect-pollinator mediated selection is considered. However, we found no evidence that flower visual characteristics used by bees to identify flowers at close range, such as colour or shape, were straightforward modulators of floral temperature. We could not identify any clear link to phylogenetic history and temperature modulation either. Mapping our test flower distribution on the Australian continent however, indicates a potential clustering that suggests different flower responses may constitute adaptations to local conditions. Our study proposes a framework for modelling the potential effects of climate change and floral temperature on flower pollination dynamics at local and global scales.

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          Most cited references70

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          Ecological and Evolutionary Responses to Recent Climate Change

          Ecological changes in the phenology and distribution of plants and animals are occurring in all well-studied marine, freshwater, and terrestrial groups. These observed changes are heavily biased in the directions predicted from global warming and have been linked to local or regional climate change through correlations between climate and biological variation, field and laboratory experiments, and physiological research. Range-restricted species, particularly polar and mountaintop species, show severe range contractions and have been the first groups in which entire species have gone extinct due to recent climate change. Tropical coral reefs and amphibians have been most negatively affected. Predator-prey and plant-insect interactions have been disrupted when interacting species have responded differently to warming. Evolutionary adaptations to warmer conditions have occurred in the interiors of species' ranges, and resource use and dispersal have evolved rapidly at expanding range margins. Observed genetic shifts modulate local effects of climate change, but there is little evidence that they will mitigate negative effects at the species level.
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            Shifts in phenology due to global climate change: the need for a yardstick.

            Climate change has led to shifts in phenology in many species distributed widely across taxonomic groups. It is, however, unclear how we should interpret these shifts without some sort of a yardstick: a measure that will reflect how much a species should be shifting to match the change in its environment caused by climate change. Here, we assume that the shift in the phenology of a species' food abundance is, by a first approximation, an appropriate yardstick. We review the few examples that are available, ranging from birds to marine plankton. In almost all of these examples, the phenology of the focal species shifts either too little (five out of 11) or too much (three out of 11) compared to the yardstick. Thus, many species are becoming mistimed due to climate change. We urge researchers with long-term datasets on phenology to link their data with those that may serve as a yardstick, because documentation of the incidence of climate change-induced mistiming is crucial in assessing the impact of global climate change on the natural world.
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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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                Author and article information

                Contributors
                Role: ConceptualizationRole: Data curationRole: Formal analysisRole: InvestigationRole: MethodologyRole: VisualizationRole: Writing – original draftRole: Writing – review & editing
                Role: ConceptualizationRole: Data curationRole: Formal analysisRole: MethodologyRole: VisualizationRole: Writing – original draftRole: Writing – review & editing
                Role: Data curationRole: Formal analysisRole: MethodologyRole: VisualizationRole: Writing – review & editing
                Role: ConceptualizationRole: Data curationRole: Formal analysisRole: Funding acquisitionRole: InvestigationRole: MethodologyRole: Project administrationRole: ResourcesRole: SupervisionRole: VisualizationRole: Writing – review & editing
                Role: ConceptualizationRole: Data curationRole: Formal analysisRole: Funding acquisitionRole: InvestigationRole: MethodologyRole: Project administrationRole: ResourcesRole: SupervisionRole: VisualizationRole: Writing – original draftRole: Writing – review & editing
                Role: Editor
                Journal
                PLoS One
                PLoS ONE
                plos
                plosone
                PLoS ONE
                Public Library of Science (San Francisco, CA USA )
                1932-6203
                1 August 2018
                2018
                : 13
                : 8
                : e0200549
                Affiliations
                [1 ] School of Media and Communication, RMIT University, Melbourne, Australia
                [2 ] Faculty of Information Technology, Monash University, Melbourne, Australia
                [3 ] Department of Physiology, Monash University, Melbourne, Australia
                Indian Institute of Science, INDIA
                Author notes

                Competing Interests: Adrian G Dyer wishes to disclose that he is an editor for PLoS ONE. The authors declare that they have no conflict of interest involving the work reported here.

                Author information
                http://orcid.org/0000-0002-6165-8418
                http://orcid.org/0000-0002-5456-4835
                Article
                PONE-D-18-05392
                10.1371/journal.pone.0200549
                6070230
                30067757
                05ec1565-d83a-402b-8472-87559f6f5d67
                © 2018 Shrestha 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 February 2018
                : 28 June 2018
                Page count
                Figures: 11, Tables: 2, Pages: 24
                Funding
                Funded by: Australian Research Council (AU)
                Award ID: DP130100015
                Award Recipient :
                Funded by: Australian Research Council (AU)
                Award ID: DP130100015
                Award Recipient :
                Funded by: Australian Research Council (AU)
                Award ID: DP160100161
                Award Recipient :
                Funded by: Australian Research Council (AU)
                Award ID: DP160100161
                Award Recipient :
                This research was supported under Australian Research Council's Discovery Projects funding scheme (Project numbers DP130100015, DP160100161). The funder 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
                Plant Science
                Plant Anatomy
                Flowers
                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
                Physiology
                Physiological Parameters
                Body Temperature
                Medicine and Health Sciences
                Physiology
                Physiological Parameters
                Body Temperature
                Biology and Life Sciences
                Plant Science
                Plant Anatomy
                Flower Anatomy
                Petals
                Earth Sciences
                Atmospheric Science
                Climatology
                Climate Change
                Biology and Life Sciences
                Organisms
                Eukaryota
                Plants
                Biology and Life Sciences
                Organisms
                Eukaryota
                Animals
                Invertebrates
                Arthropoda
                Insects
                Custom metadata
                All relevant data are within the paper and its Supporting Information file.

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                Uncategorized

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