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      Quantitative assessment of plant-arthropod interactions in forest canopies: A plot-based approach

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          Abstract

          Research on canopy arthropods has progressed from species inventories to the study of their interactions and networks, enhancing our understanding of how hyper-diverse communities are maintained. Previous studies often focused on sampling individual tree species, individual trees or their parts. We argue that such selective sampling is not ideal when analyzing interaction network structure, and may lead to erroneous conclusions. We developed practical and reproducible sampling guidelines for the plot-based analysis of arthropod interaction networks in forest canopies. Our sampling protocol focused on insect herbivores (leaf-chewing insect larvae, miners and gallers) and non-flying invertebrate predators (spiders and ants). We quantitatively sampled the focal arthropods from felled trees, or from trees accessed by canopy cranes or cherry pickers in 53 0.1 ha forest plots in five biogeographic regions, comprising 6,280 trees in total. All three methods required a similar sampling effort and provided good foliage accessibility. Furthermore, we compared interaction networks derived from plot-based data to interaction networks derived from simulated non-plot-based data focusing either on common tree species or a representative selection of tree families. All types of non-plot-based data showed highly biased network structure towards higher connectance, higher web asymmetry, and higher nestedness temperature when compared with plot-based data. Furthermore, some types of non-plot-based data showed biased diversity of the associated herbivore species and specificity of their interactions. Plot-based sampling thus appears to be the most rigorous approach for reconstructing realistic, quantitative plant-arthropod interaction networks that are comparable across sites and regions. Studies of plant interactions have greatly benefited from a plot-based approach and we argue that studies of arthropod interactions would benefit in the same way. We conclude that plot-based studies on canopy arthropods would yield important insights into the processes of interaction network assembly and dynamics, which could be maximised via a coordinated network of plot-based study sites.

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          Habitat modification alters the structure of tropical host-parasitoid food webs.

          Global conversion of natural habitats to agriculture has led to marked changes in species diversity and composition. However, it is less clear how habitat modification affects interactions among species. Networks of feeding interactions (food webs) describe the underlying structure of ecological communities, and might be crucially linked to their stability and function. Here, we analyse 48 quantitative food webs for cavity-nesting bees, wasps and their parasitoids across five tropical habitat types. We found marked changes in food-web structure across the modification gradient, despite little variation in species richness. The evenness of interaction frequencies declined with habitat modification, with most energy flowing along one or a few pathways in intensively managed agricultural habitats. In modified habitats there was a higher ratio of parasitoid to host species and increased parasitism rates, with implications for the important ecosystem services, such as pollination and biological control, that are performed by host bees and wasps. The most abundant parasitoid species was more specialized in modified habitats, with reduced attack rates on alternative hosts. Conventional community descriptors failed to discriminate adequately among habitats, indicating that perturbation of the structure and function of ecological communities might be overlooked in studies that do not document and quantify species interactions. Altered interaction structure therefore represents an insidious and functionally important hidden effect of habitat modification by humans.
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            Pathogens and insect herbivores drive rainforest plant diversity and composition.

            Tropical forests are important reservoirs of biodiversity, but the processes that maintain this diversity remain poorly understood. The Janzen-Connell hypothesis suggests that specialized natural enemies such as insect herbivores and fungal pathogens maintain high diversity by elevating mortality when plant species occur at high density (negative density dependence; NDD). NDD has been detected widely in tropical forests, but the prediction that NDD caused by insects and pathogens has a community-wide role in maintaining tropical plant diversity remains untested. We show experimentally that changes in plant diversity and species composition are caused by fungal pathogens and insect herbivores. Effective plant species richness increased across the seed-to-seedling transition, corresponding to large changes in species composition. Treating seeds and young seedlings with fungicides significantly reduced the diversity of the seedling assemblage, consistent with the Janzen-Connell hypothesis. Although suppressing insect herbivores using insecticides did not alter species diversity, it greatly increased seedling recruitment and caused a marked shift in seedling species composition. Overall, seedling recruitment was significantly reduced at high conspecific seed densities and this NDD was greatest for the species that were most abundant as seeds. Suppressing fungi reduced the negative effects of density on recruitment, confirming that the diversity-enhancing effect of fungi is mediated by NDD. Our study provides an overall test of the Janzen-Connell hypothesis and demonstrates the crucial role that insects and pathogens have both in structuring tropical plant communities and in maintaining their remarkable diversity.
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              CTFS-ForestGEO: a worldwide network monitoring forests in an era of global change.

              Global change is impacting forests worldwide, threatening biodiversity and ecosystem services including climate regulation. Understanding how forests respond is critical to forest conservation and climate protection. This review describes an international network of 59 long-term forest dynamics research sites (CTFS-ForestGEO) useful for characterizing forest responses to global change. Within very large plots (median size 25 ha), all stems ≥ 1 cm diameter are identified to species, mapped, and regularly recensused according to standardized protocols. CTFS-ForestGEO spans 25 °S-61 °N latitude, is generally representative of the range of bioclimatic, edaphic, and topographic conditions experienced by forests worldwide, and is the only forest monitoring network that applies a standardized protocol to each of the world's major forest biomes. Supplementary standardized measurements at subsets of the sites provide additional information on plants, animals, and ecosystem and environmental variables. CTFS-ForestGEO sites are experiencing multifaceted anthropogenic global change pressures including warming (average 0.61 °C), changes in precipitation (up to ± 30% change), atmospheric deposition of nitrogen and sulfur compounds (up to 3.8 g N m(-2) yr(-1) and 3.1 g S m(-2) yr(-1)), and forest fragmentation in the surrounding landscape (up to 88% reduced tree cover within 5 km). The broad suite of measurements made at CTFS-ForestGEO sites makes it possible to investigate the complex ways in which global change is impacting forest dynamics. Ongoing research across the CTFS-ForestGEO network is yielding insights into how and why the forests are changing, and continued monitoring will provide vital contributions to understanding worldwide forest diversity and dynamics in an era of global change.
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                Author and article information

                Contributors
                Role: ConceptualizationRole: Data curationRole: InvestigationRole: MethodologyRole: SupervisionRole: VisualizationRole: Writing – original draftRole: Writing – review & editing
                Role: ConceptualizationRole: Data curationRole: InvestigationRole: MethodologyRole: Project administrationRole: SupervisionRole: Writing – review & editing
                Role: ConceptualizationRole: Data curationRole: InvestigationRole: MethodologyRole: Project administrationRole: SupervisionRole: Writing – review & editing
                Role: ConceptualizationRole: Data curationRole: InvestigationRole: MethodologyRole: SupervisionRole: Writing – review & editing
                Role: Data curationRole: InvestigationRole: MethodologyRole: SupervisionRole: Writing – review & editing
                Role: Data curationRole: InvestigationRole: Project administrationRole: Writing – review & editing
                Role: InvestigationRole: Project administrationRole: Writing – review & editing
                Role: Project administrationRole: SupervisionRole: Writing – review & editing
                Role: ConceptualizationRole: MethodologyRole: Project administrationRole: SupervisionRole: Writing – original draft
                Role: Data curationRole: InvestigationRole: Writing – review & editing
                Role: Data curationRole: InvestigationRole: MethodologyRole: SupervisionRole: Writing – review & editing
                Role: ConceptualizationRole: Funding acquisitionRole: InvestigationRole: MethodologyRole: Project administrationRole: SupervisionRole: Writing – review & editing
                Role: InvestigationRole: Project administrationRole: Writing – review & editing
                Role: Data curationRole: InvestigationRole: MethodologyRole: Writing – review & editing
                Role: Project administrationRole: SupervisionRole: Writing – review & editing
                Role: Data curationRole: InvestigationRole: Project administrationRole: Writing – review & editing
                Role: Data curationRole: InvestigationRole: Writing – review & editing
                Role: InvestigationRole: Project administrationRole: Writing – review & editing
                Role: ConceptualizationRole: MethodologyRole: SupervisionRole: Writing – review & editing
                Role: InvestigationRole: Project administrationRole: Writing – review & editing
                Role: Data curationRole: InvestigationRole: Writing – review & editing
                Role: InvestigationRole: Project administrationRole: SupervisionRole: Writing – review & editing
                Role: Project administrationRole: SupervisionRole: Writing – review & editing
                Role: Data curationRole: InvestigationRole: Writing – review & editing
                Role: Data curationRole: InvestigationRole: Writing – review & editing
                Role: Data curationRole: MethodologyRole: Writing – review & editing
                Role: Data curationRole: InvestigationRole: Writing – review & editing
                Role: Data curationRole: InvestigationRole: MethodologyRole: Writing – review & editing
                Role: ConceptualizationRole: Data curationRole: Funding acquisitionRole: InvestigationRole: MethodologyRole: SupervisionRole: Writing – review & editing
                Role: ConceptualizationRole: Data curationRole: Funding acquisitionRole: InvestigationRole: MethodologyRole: Project administrationRole: SupervisionRole: Writing – review & editing
                Role: Editor
                Journal
                PLoS One
                PLoS ONE
                plos
                plosone
                PLoS ONE
                Public Library of Science (San Francisco, CA USA )
                1932-6203
                23 October 2019
                2019
                : 14
                : 10
                : e0222119
                Affiliations
                [1 ] Biology Centre of the Czech Academy of Sciences, Ceske Budejovice, Czech Republic
                [2 ] German Centre for Integrative Biodiversity Research (iDiv) Halle-Jena-Leipzig, Leipzig, Germany
                [3 ] Faculty of Science, University of South Bohemia, Ceske Budejovice, Czech Republic
                [4 ] Faculty of Science, Chiba University, Chiba, Japan
                [5 ] New Guinea Binatang Research Center, Madang, Papua New Guinea
                [6 ] Conservation Ecology Center, Smithsonian Conservation Biology Institute; Front Royal, VA, United States of America
                [7 ] ForestGEO, Smithsonian Tropical Research Institute, Panama City, Panama
                [8 ] Maestria de Entomologia, Universidad de Panama, Panama City, Panama
                [9 ] Faculty of Science, University of Ostrava, Ostrava, Czech Republic
                [10 ] Graduate School of Agricultural and Life Sciences, The University of Tokyo, Furano, Japan
                [11 ] School of Biological Sciences, University of Bristol, Bristol, United Kingdom
                [12 ] National Museum of Natural History, Smithsonian Institution, Washington, DC, United States of America
                [13 ] Tomakomai Experimental Forest, Hokkaido University, Tomakomai, Japan
                [14 ] Institute of Botany, Czech Academy of Sciences, Brno, Czech Republic
                [15 ] Department of Zoology, Fisheries, Hydrobiology and Apiculture, Mendel University in Brno, Brno, Czech Republic
                [16 ] Department of Ecology, Faculty of Science, Charles University, Prague, Czech Republic
                [17 ] Bell Museum and Department of Plant & Microbial Biology, University of Minnesota, Saint Paul, MN, United States of America
                Helmholtz Centre for Environmental Research - UFZ, GERMANY
                Author notes

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

                Author information
                http://orcid.org/0000-0003-4126-3897
                http://orcid.org/0000-0002-1856-6833
                http://orcid.org/0000-0001-8461-9713
                http://orcid.org/0000-0002-5554-6591
                http://orcid.org/0000-0002-4602-8856
                http://orcid.org/0000-0001-8305-6672
                http://orcid.org/0000-0003-0270-1241
                http://orcid.org/0000-0003-3608-8780
                http://orcid.org/0000-0002-9796-5081
                http://orcid.org/0000-0002-3161-1539
                http://orcid.org/0000-0002-3743-7201
                http://orcid.org/0000-0003-4876-9794
                http://orcid.org/0000-0001-7499-6259
                Article
                PONE-D-19-08839
                10.1371/journal.pone.0222119
                6808442
                31644586
                c3bb8601-54ef-4911-935b-ff24db583a30

                This is an open access article, free of all copyright, and may be freely reproduced, distributed, transmitted, modified, built upon, or otherwise used by anyone for any lawful purpose. The work is made available under the Creative Commons CC0 public domain dedication.

                History
                : 27 March 2019
                : 21 August 2019
                Page count
                Figures: 4, Tables: 2, Pages: 20
                Funding
                Funded by: Alexander von Humboldt-Stiftung (DE)
                Award ID: Ref.3.3-CZE-1192673-HFST-P
                Award Recipient :
                Funded by: Grantová Agentura České Republiky (CZ)
                Award ID: 19-15645Y
                Award Recipient :
                Funded by: Ministerstvo Školství, Mládeže a Tělovýchovy (CZ)
                Award ID: LO1208
                Award Recipient :
                Funded by: Institute of Environmental Technologies
                Award ID: CZ.1.05/2.1.00/03.0100
                Award Recipient :
                Funded by: Japan Society for the Promotion of Science
                Award ID: Grant-in-Aid for Challenging Exploratory Research 26550087
                Award Recipient :
                Funded by: funder-id http://dx.doi.org/10.13039/501100004240, Akademie Věd České Republiky;
                Award ID: RVO 67985939
                Award Recipient :
                Funded by: National Science Foundation (US)
                Award ID: DEB-0515678
                Award Recipient :
                Funded by: National Science Foundation (US)
                Award ID: DEB-0841885
                Award Recipient :
                Funded by: European Science Foundation
                Award ID: 669609
                Award Recipient :
                Funded by: Darwin Initiative
                Award ID: 22-002
                Award Recipient :
                Funded by: Grantová Agentura České Republiky (CZ)
                Award ID: 17-23862S
                Award Recipient :
                MV acknowledges funding by Alexander von Humboldt Foundation and the Federal Ministry for Education and Research Ref.3.3-CZE-1192673-HFST-P ( https://www.humboldt-foundation.de). GPAL thanks Grant Agency of the Czech Republic 19-15645Y ( https://gacr.cz) for the support during writing the article. PD and MŠ acknowledge the Ministry of Education, Youth and Sports of the Czech Republic LO1208 ( http://www.msmt.cz), and the Institute of Environmental Technologies CZ.1.05/2.1.00/03.0100 ( http://www.ietech.eu/index.php/iet). NK acknowledges Japan Society for the Promotion of Science (Grant-in-Aid for Challenging Exploratory Research 26550087, https://www.jsps.go.jp). JŠ acknowledges long-term research development project RVO 67985939 from the Czech Academy of Sciences ( https://www.avcr.cz). GDW acknowledges US National Science Foundation grants DEB-0515678 and DEB-0841885. VN acknowledges the European Science Foundation grant 669609 ( www.esf.org), Darwin Initiative project no. 22-002 ( www.darwininitiative.org.uk), and Grant Agency of the Czech Republic 17-23862S ( https://gacr.cz). RT was supported by the Charles University (PRIMUS/17/SCI/8 and UNCE204069). 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
                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
                Trees
                Biology and Life Sciences
                Plant Science
                Plant Anatomy
                Leaves
                Biology and Life Sciences
                Ecology
                Plant Ecology
                Plant-Animal Interactions
                Herbivory
                Ecology and Environmental Sciences
                Ecology
                Plant Ecology
                Plant-Animal Interactions
                Herbivory
                Biology and Life Sciences
                Plant Science
                Plant Ecology
                Plant-Animal Interactions
                Herbivory
                Biology and Life Sciences
                Ecology
                Community Ecology
                Trophic Interactions
                Herbivory
                Ecology and Environmental Sciences
                Ecology
                Community Ecology
                Trophic Interactions
                Herbivory
                Biology and Life Sciences
                Organisms
                Eukaryota
                Plants
                Fruits
                Cherries
                Biology and Life Sciences
                Organisms
                Eukaryota
                Animals
                Invertebrates
                Arthropoda
                Insects
                Hymenoptera
                Ants
                Biology and Life Sciences
                Molecular Biology
                Interaction Networks
                Custom metadata
                We provide the data used in the analyses in S1 Table. The data on Yawan dataset that were used for the comparison of plot-based and non-plot-based analyses of herbivore-plant interaction networks were taken from Redmond et al. 2019 [ 20]. The publicly available sequences on insect DNA barcodes can be accessed from The Barcode of Life Data System ( http://www.boldsystems.org) as DS-LANZMIK (Mikulcice and Lanzhot sites; [ 21]), TLR (Tomakomai), DS-CATS1, DS-SEGAR16, and ASPNA (Wanang; [ 48, 56]), and DS-YAWAN2 (Yawan; [ 23, 57]) datasets.

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