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      Phenological responses to climate change based on a hundred years of herbarium collections of tropical Melastomataceae

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          Abstract

          Changes in phenological events have been vastly documented in face of recent global climate change. These studies are concentrated on temperate plants, and the responses of tropical species are still little understood, likely due to the lack of long-term phenological records in the tropics. In this case, the use of herbarium specimens to gather phenological data over long periods and wide geographic areas has emerged as a powerful tool. Here, we used four Melastomataceae species endemic to the Brazilian Atlantic Forest to evaluate phenological patterns and alterations as responses to recent climate changes. Phenological data were gathered from Reflora Virtual Herbarium specimens collected between 1920 and 2018, and analyzed with circular statistics applied to the intervals 1920–1979, 1980–1999, and 2000–2018. The effects of temperature range, average temperature, precipitation, and photoperiod on flowering and fruiting of each species were tested using multiple linear regressions. Through circular statistics, we detected changes, mostly delays, in the flowering of Miconia quinquedentata, Pleroma clavatum and P. trichopodum, and in the fruiting of M. acutiflora, P. clavatum and P. trichopodum. We also found that flowering and fruiting occurrence were related to local climatic conditions from months prior to the collections. We found marked phenological variations over the decades and also that these variations are associated to global climate change, adding up to the large body of evidence from higher latitudes. Our results also support herbarium collections as an important source for long-term tropical phenological studies. The lack of consistent patterns of responses among the four species (e.g. fruiting delayed two months in P. clavatum and advanced one month in M. acutiflora) suggests that climate change has unequal effects across tropical forests. This highlights the urgent need for further research to understand and forecast the ecological implications of these changes in global ecosystems processes.

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          Climatologies at high resolution for the earth’s land surface areas

          High-resolution information on climatic conditions is essential to many applications in environmental and ecological sciences. Here we present the CHELSA (Climatologies at high resolution for the earth’s land surface areas) data of downscaled model output temperature and precipitation estimates of the ERA-Interim climatic reanalysis to a high resolution of 30 arc sec. The temperature algorithm is based on statistical downscaling of atmospheric temperatures. The precipitation algorithm incorporates orographic predictors including wind fields, valley exposition, and boundary layer height, with a subsequent bias correction. The resulting data consist of a monthly temperature and precipitation climatology for the years 1979–2013. We compare the data derived from the CHELSA algorithm with other standard gridded products and station data from the Global Historical Climate Network. We compare the performance of the new climatologies in species distribution modelling and show that we can increase the accuracy of species range predictions. We further show that CHELSA climatological data has a similar accuracy as other products for temperature, but that its predictions of precipitation patterns are better.
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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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              Phenological sensitivity to climate across taxa and trophic levels.

              Differences in phenological responses to climate change among species can desynchronise ecological interactions and thereby threaten ecosystem function. To assess these threats, we must quantify the relative impact of climate change on species at different trophic levels. Here, we apply a Climate Sensitivity Profile approach to 10,003 terrestrial and aquatic phenological data sets, spatially matched to temperature and precipitation data, to quantify variation in climate sensitivity. The direction, magnitude and timing of climate sensitivity varied markedly among organisms within taxonomic and trophic groups. Despite this variability, we detected systematic variation in the direction and magnitude of phenological climate sensitivity. Secondary consumers showed consistently lower climate sensitivity than other groups. We used mid-century climate change projections to estimate that the timing of phenological events could change more for primary consumers than for species in other trophic levels (6.2 versus 2.5-2.9 days earlier on average), with substantial taxonomic variation (1.1-14.8 days earlier on average).
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                Author and article information

                Contributors
                Role: ConceptualizationRole: Data curationRole: InvestigationRole: ValidationRole: VisualizationRole: Writing – original draftRole: Writing – review & editing
                Role: Formal analysisRole: InvestigationRole: MethodologyRole: ValidationRole: Writing – original draftRole: Writing – review & editing
                Role: Data curationRole: Writing – review & editing
                Role: ConceptualizationRole: Funding acquisitionRole: SupervisionRole: Writing – review & editing
                Role: ConceptualizationRole: Writing – review & editing
                Role: ConceptualizationRole: InvestigationRole: MethodologyRole: ValidationRole: VisualizationRole: Writing – review & editing
                Role: Editor
                Journal
                PLoS One
                PLoS One
                plos
                plosone
                PLoS ONE
                Public Library of Science (San Francisco, CA USA )
                1932-6203
                7 May 2021
                2021
                : 16
                : 5
                : e0251360
                Affiliations
                [1 ] Jardim Botânico do Rio de Janeiro, Rio de Janeiro, Brazil
                [2 ] Departamento de Botânica, Universidade Federal do Paraná, Curitiba, Paraná, Brazil
                Universite du Quebec a Chicoutimi, CANADA
                Author notes

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

                [¤]

                Current address: Programa de Pós-Graduação em Biologia de Fungos, Algas e Plantas, Universidade Federal de Santa Catarina, Florianópolis, Santa Catarina, Brazil

                ‡ These authors also contributed equally to this work.

                Author information
                https://orcid.org/0000-0003-4240-9077
                https://orcid.org/0000-0002-4146-2514
                Article
                PONE-D-20-28944
                10.1371/journal.pone.0251360
                8104365
                33961684
                e29dd5b9-9974-4118-930e-49298ae2fcf8
                © 2021 Lima 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
                : 14 September 2020
                : 23 April 2021
                Page count
                Figures: 3, Tables: 3, Pages: 19
                Funding
                Funded by: funder-id http://dx.doi.org/10.13039/501100003593, Conselho Nacional de Desenvolvimento Científico e Tecnológico;
                Award ID: 55225/2018-9
                Award Recipient :
                Funded by: Conselho Nacional de Desenvolvimento Científico e Tecnológico (BR)
                Award ID: 15246/2019-0
                Award Recipient :
                Funded by: Conselho Nacional de Desenvolvimento Científico e Tecnológico (BR)
                Award ID: 303420/2016-2
                Award Recipient :
                Funded by: Conselho Nacional de Desenvolvimento Científico e Tecnológico (BR)
                Award ID: 308065/2017-4
                Award Recipient :
                Funded by: funder-id http://dx.doi.org/10.13039/501100003593, Conselho Nacional de Desenvolvimento Científico e Tecnológico;
                Award ID: 304794/2018-0
                Award Recipient :
                Funded by: funder-id http://dx.doi.org/10.13039/501100004586, Fundação Carlos Chagas Filho de Amparo à Pesquisa do Estado do Rio de Janeiro;
                Award ID: E-26/202.775/2018
                Award Recipient :
                Funded by: funder-id http://dx.doi.org/10.13039/501100004586, Fundação Carlos Chagas Filho de Amparo à Pesquisa do Estado do Rio de Janeiro;
                Award ID: E-26/202.778/2018
                Award Recipient :
                Funded by: Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (BR)
                Award ID: Finance Code 001
                DFL (#55225/2018-9) and JHFM (#15246/2019-0) received post-doc fellowships, ITL received scientific initiation scholarship, and RCF (#303420/2016-2), RG (#308065/2017-4) and LF (#304794/2018-0) received research productivity grants from Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq, Brazil). RCF (#E-26/202.775/2018) and LF (#E-26/202.778/2018) also received additional funding from Fundação de Amparo à Pesquisa do Estado do Rio de Janeiro (FAPERJ, Brazil, “Programa Cientistas do Nosso Estado”). This work was supported by funds from Natura Cosméticos S/A, and financed in part by Coordernação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES, Brazil) - Finance Code 001. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
                Categories
                Research Article
                Earth Sciences
                Atmospheric Science
                Climatology
                Climate Change
                Biology and Life Sciences
                Ecology
                Ecosystems
                Forests
                Ecology and Environmental Sciences
                Ecology
                Ecosystems
                Forests
                Ecology and Environmental Sciences
                Terrestrial Environments
                Forests
                Biology and Life Sciences
                Organisms
                Eukaryota
                Plants
                Flowering Plants
                People and places
                Geographical locations
                South America
                Brazil
                Biology and Life Sciences
                Organisms
                Eukaryota
                Plants
                Fruits
                Biology and Life Sciences
                Ecology
                Ecosystems
                Ecology and Environmental Sciences
                Ecology
                Ecosystems
                Biology and Life Sciences
                Developmental Biology
                Life Cycles
                Earth Sciences
                Seasons
                Custom metadata
                All data are available from the Figshare database (doi: 10.6084/m9.figshare.13366235).

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