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      Seasonal variation of pollen collected by honey bees ( Apis mellifera) in developed areas across four regions in the United States

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          Abstract

          For honey bees ( Apis mellifera), colony maintenance and growth are highly dependent on worker foragers obtaining sufficient resources from flowering plants year round. Despite the importance of floral diversity for proper bee nutrition, urban development has drastically altered resource availability and diversity for these important pollinators. Therefore, understanding the floral resources foraged by bees in urbanized areas is key to identifying and promoting plants that enhance colony health in those environments. In this study, we identified the pollen foraged by bees in four developed areas of the U.S., and explored whether there were spatial or temporal differences in the types of floral sources of pollen used by honey bees in these landscapes. To do this, pollen was collected every month for up to one year from colonies located in developed (urban and suburban) sites in California, Texas, Florida, and Michigan, except during months of pollen dearth or winter. Homogenized pollen samples were acetolyzed and identified microscopically to the lowest taxonomic level possible. Once identified, each pollen type was classified into a frequency category based on its overall relative abundance. Species richness and diversity indices were also calculated and compared across states and seasons. We identified up to 64 pollen types belonging to 39 plant families in one season (California). Species richness was highest in CA and lowest in TX, and was highest during spring in every state. In particular, “predominant” and “secondary” pollen types belonged to the families Arecaceae, Sapindaceae, Anacardiaceae, Apiaceae, Asteraceae, Brassicaceae, Fabaceae, Fagaceae, Lythraceae, Myrtaceae, Rhamnaceae, Rosaceae, Rutaceae, Saliaceae, and Ulmaceae. This study will help broaden our understanding of honey bee foraging ecology and nutrition in urban environments, and will help promote the use of plants that serve the dual purpose of providing aesthetic value and nutritious forage for honey bee colonies placed in developed landscapes.

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          A mathematical theory of communication

          C. Shannon (2001)
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            Effects of urbanization on species richness: A review of plants and animals

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              Influence of Pollen Nutrition on Honey Bee Health: Do Pollen Quality and Diversity Matter?

              Honey bee colonies are highly dependent upon the availability of floral resources from which they get the nutrients (notably pollen) necessary to their development and survival. However, foraging areas are currently affected by the intensification of agriculture and landscape alteration. Bees are therefore confronted to disparities in time and space of floral resource abundance, type and diversity, which might provide inadequate nutrition and endanger colonies. The beneficial influence of pollen availability on bee health is well-established but whether quality and diversity of pollen diets can modify bee health remains largely unknown. We therefore tested the influence of pollen diet quality (different monofloral pollens) and diversity (polyfloral pollen diet) on the physiology of young nurse bees, which have a distinct nutritional physiology (e.g. hypopharyngeal gland development and vitellogenin level), and on the tolerance to the microsporidian parasite Nosema ceranae by measuring bee survival and the activity of different enzymes potentially involved in bee health and defense response (glutathione-S-transferase (detoxification), phenoloxidase (immunity) and alkaline phosphatase (metabolism)). We found that both nurse bee physiology and the tolerance to the parasite were affected by pollen quality. Pollen diet diversity had no effect on the nurse bee physiology and the survival of healthy bees. However, when parasitized, bees fed with the polyfloral blend lived longer than bees fed with monofloral pollens, excepted for the protein-richest monofloral pollen. Furthermore, the survival was positively correlated to alkaline phosphatase activity in healthy bees and to phenoloxydase activities in infected bees. Our results support the idea that both the quality and diversity (in a specific context) of pollen can shape bee physiology and might help to better understand the influence of agriculture and land-use intensification on bee nutrition and health.
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                Author and article information

                Contributors
                Role: ConceptualizationRole: Data curationRole: Formal analysisRole: InvestigationRole: MethodologyRole: SupervisionRole: VisualizationRole: Writing – original draftRole: Writing – review & editing
                Role: Data curationRole: Formal analysisRole: InvestigationRole: MethodologyRole: ResourcesRole: SupervisionRole: Writing – review & editing
                Role: ConceptualizationRole: Data curationRole: Funding acquisitionRole: InvestigationRole: MethodologyRole: Project administrationRole: ResourcesRole: SoftwareRole: SupervisionRole: ValidationRole: VisualizationRole: Writing – review & editing
                Role: ConceptualizationRole: Data curationRole: Funding acquisitionRole: MethodologyRole: Project administrationRole: ResourcesRole: SupervisionRole: ValidationRole: VisualizationRole: Writing – review & editing
                Role: ConceptualizationRole: Data curationRole: Formal analysisRole: Funding acquisitionRole: InvestigationRole: MethodologyRole: Project administrationRole: ResourcesRole: SoftwareRole: VisualizationRole: Writing – review & editing
                Role: ConceptualizationRole: Data curationRole: InvestigationRole: MethodologyRole: SupervisionRole: Writing – review & editing
                Role: ConceptualizationRole: Funding acquisitionRole: MethodologyRole: Project administrationRole: ResourcesRole: SupervisionRole: VisualizationRole: Writing – review & editing
                Role: ConceptualizationRole: Data curationRole: Formal analysisRole: Funding acquisitionRole: InvestigationRole: MethodologyRole: Project administrationRole: ResourcesRole: SoftwareRole: SupervisionRole: ValidationRole: 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
                12 June 2019
                2019
                : 14
                : 6
                : e0217294
                Affiliations
                [1 ] Department of Entomology, Texas A&M University, Texas, United States of America
                [2 ] Department of Anthropology, Texas A&M University, Texas, United States of America
                [3 ] Entomology and Nematology Department, University of Florida, Gainesville, Florida, United States of America
                [4 ] Department of Entomology, Michigan State University, East Lansing, Michigan, United States of America
                [5 ] Ardea Consulting, Woodland, California, United States of America
                [6 ] Bayer CropScience LP, Crop Science Division, Research Triangle Park, North Carolina, United States of America
                Universitat Leipzig, GERMANY
                Author notes

                Competing Interests: We have the following interests: This study was funded in part by Bayer Crop Science and Syngenta Crop Protection LLC and by the Texas Beekeepers Association. Daniel R. Schmehl and Ana R. Cabrera are employed by Bayer CropScience LP. Joseph Sullivan is employed by Ardea Consulting. There are no patents, products in development or marketed products to declare. This does not alter our adherence to all the PLOS ONE policies on sharing data and materials.

                Author information
                http://orcid.org/0000-0002-0586-9245
                Article
                PONE-D-19-01652
                10.1371/journal.pone.0217294
                6561680
                31188840
                51e20133-4de2-4767-abed-c2feb984f350
                © 2019 Lau 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
                : 17 January 2019
                : 8 May 2019
                Page count
                Figures: 9, Tables: 1, Pages: 24
                Funding
                Funded by: funder-id http://dx.doi.org/10.13039/100008791, Bayer CropScience;
                Award ID: 00115707
                Award Recipient :
                Funded by: funder-id http://dx.doi.org/10.13039/100008791, Bayer CropScience;
                Award ID: 1005822 – UF
                Award Recipient :
                Funded by: National Institute of Food and Agriculture (US)
                Award ID: 2015-67013-23170
                Award Recipient :
                Funded by: funder-id http://dx.doi.org/10.13039/100007904, Texas A and M University;
                Award ID: TEX09557
                Award Recipient :
                Funded by: Texas Beekeepers Association
                Award ID: Student Research Grant
                Award Recipient :
                Funded by: funder-id http://dx.doi.org/10.13039/100007904, Texas A and M University;
                Award ID: Herb Dean ’40 Endowed Scholarship
                Award Recipient :
                This study was funded in part by a grant to JR (award number M1402691), JDE (award number 00115707), and ZYH (award number NSNTN015) by Bayer Crop Science and Syngenta Crop Protection LLC (1005822 – UF), JR’s Texas AgriLife Research Hatch Project TEX09557, and a USDA National Institute of Food and Agriculture Multistate Project (2015-67013-23170). We would also like to thank the Herb Dean ’40 Endowed Scholarship and the Texas Beekeepers Association for their financial support to PL. These funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. Joseph Sullivan is employed by Ardea Consulting. Ardea Consulting provided support in the form of salary for author JS, but did not have any additional role in the study design, data collection and analysis, decision to publish, or preparation of the manuscript. The specific role of this author is articulated in the ‘author contributions’ section. Daniel R. Schmehl and Ana R. Cabrera are employed by Bayer CropScience LP. Bayer CropScience LP provided support in the form of salaries for authors DRS and ARC, but did not have any additional role in the study design, data collection and analysis, decision to publish, or preparation of the manuscript. The specific roles of these authors are articulated in the ‘author contributions’ section.
                Categories
                Research Article
                Biology and Life Sciences
                Plant Science
                Plant Anatomy
                Pollen
                Biology and Life Sciences
                Ecology
                Ecological Metrics
                Species Diversity
                Shannon Index
                Ecology and Environmental Sciences
                Ecology
                Ecological Metrics
                Species Diversity
                Shannon Index
                Biology and Life Sciences
                Organisms
                Eukaryota
                Animals
                Invertebrates
                Arthropoda
                Insects
                Hymenoptera
                Bees
                Honey Bees
                Biology and Life Sciences
                Ecology
                Ecological Metrics
                Species Diversity
                Ecology and Environmental Sciences
                Ecology
                Ecological Metrics
                Species Diversity
                Earth Sciences
                Seasons
                Spring
                Biology and Life Sciences
                Plant Science
                Plant Taxonomy
                Biology and Life Sciences
                Taxonomy
                Plant Taxonomy
                Computer and Information Sciences
                Data Management
                Taxonomy
                Plant Taxonomy
                Ecology and Environmental Sciences
                Terrestrial Environments
                Urban Environments
                Biology and Life Sciences
                Organisms
                Eukaryota
                Plants
                Shrubs
                Custom metadata
                All relevant data are within the manuscript and its Supporting Information files.

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