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      A clue on bee glue: New insight into the sources and factors driving resin intake in honeybees ( Apis mellifera)

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          Abstract

          Honeybees ( Apis mellifera) are threatened by numerous pathogens and parasites. To prevent infections they apply cooperative behavioral defenses, such as allo-grooming and hygiene, or they use antimicrobial plant resin. Resin is a chemically complex and highly variable mixture of many bioactive compounds. Bees collect the sticky material from different plant species and use it for nest construction and protection. Despite its importance for colony health, comparatively little is known about the precise origins and variability in resin spectra collected by honeybees. To identify the botanical resin sources of A. mellifera in Western Europe we chemically compared resin loads of individual foragers and tree resins. We further examined the resin intake of 25 colonies from five different apiaries to assess the effect of location on variation in the spectra of collected resin. Across all colonies and apiaries, seven distinct resin types were categorized according to their color and chemical composition. Matches between bee-collected resin and tree resin indicated that bees used poplar ( Populus balsamifera, P. x canadensis), birch ( Betula alba), horse chestnut ( Aesculus hippocastanum) and coniferous trees (either Picea abies or Pinus sylvestris) as resin sources. Our data reveal that honeybees collect a comparatively broad and variable spectrum of resin sources, thus assuring protection against a variety of antagonists sensitive to different resins and/or compounds. We further unravel distinct preferences for specific resins and resin chemotypes, indicating that honeybees selectively search for bioactive resin compounds.

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          Social immunity.

          Social insect colonies have evolved collective immune defences against parasites. These 'social immune systems' result from the cooperation of the individual group members to combat the increased risk of disease transmission that arises from sociality and group living. In this review we illustrate the pathways that parasites can take to infect a social insect colony and use these pathways as a framework to predict colony defence mechanisms and present the existing evidence. We find that the collective defences can be both prophylactic and activated on demand and consist of behavioural, physiological and organisational adaptations of the colony that prevent parasite entrance, establishment and spread. We discuss the regulation of collective immunity, which requires complex integration of information about both the parasites and the internal status of the insect colony. Our review concludes with an examination of the evolution of social immunity, which is based on the consequences of selection at both the individual and the colony level.
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            Diet effects on honeybee immunocompetence.

            The maintenance of the immune system can be costly, and a lack of dietary protein can increase the susceptibility of organisms to disease. However, few studies have investigated the relationship between protein nutrition and immunity in insects. Here, we tested in honeybees (Apis mellifera) whether dietary protein quantity (monofloral pollen) and diet diversity (polyfloral pollen) can shape baseline immunocompetence (IC) by measuring parameters of individual immunity (haemocyte concentration, fat body content and phenoloxidase activity) and glucose oxidase (GOX) activity, which enables bees to sterilize colony and brood food, as a parameter of social immunity. Protein feeding modified both individual and social IC but increases in dietary protein quantity did not enhance IC. However, diet diversity increased IC levels. In particular, polyfloral diets induced higher GOX activity compared with monofloral diets, including protein-richer diets. These results suggest a link between protein nutrition and immunity in honeybees and underscore the critical role of resource availability on pollinator health.
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              RNA Viruses in Hymenopteran Pollinators: Evidence of Inter-Taxa Virus Transmission via Pollen and Potential Impact on Non-Apis Hymenopteran Species

              Although overall pollinator populations have declined over the last couple of decades, the honey bee (Apis mellifera) malady, colony collapse disorder (CCD), has caused major concern in the agricultural community. Among honey bee pathogens, RNA viruses are emerging as a serious threat and are suspected as major contributors to CCD. Recent detection of these viral species in bumble bees suggests a possible wider environmental spread of these viruses with potential broader impact. It is therefore vital to study the ecology and epidemiology of these viruses in the hymenopteran pollinator community as a whole. We studied the viral distribution in honey bees, in their pollen loads, and in other non-Apis hymenopteran pollinators collected from flowering plants in Pennsylvania, New York, and Illinois in the United States. Viruses in the samples were detected using reverse transcriptase-PCR and confirmed by sequencing. For the first time, we report the molecular detection of picorna-like RNA viruses (deformed wing virus, sacbrood virus and black queen cell virus) in pollen pellets collected directly from forager bees. Pollen pellets from several uninfected forager bees were detected with virus, indicating that pollen itself may harbor viruses. The viruses in the pollen and honey stored in the hive were demonstrated to be infective, with the queen becoming infected and laying infected eggs after these virus-contaminated foods were given to virus-free colonies. These viruses were detected in eleven other non-Apis hymenopteran species, ranging from many solitary bees to bumble bees and wasps. This finding further expands the viral host range and implies a possible deeper impact on the health of our ecosystem. Phylogenetic analyses support that these viruses are disseminating freely among the pollinators via the flower pollen itself. Notably, in cases where honey bee apiaries affected by CCD harbored honey bees with Israeli Acute Paralysis virus (IAPV), nearby non-Apis hymenopteran pollinators also had IAPV, while those near apiaries without IAPV did not. In containment greenhouse experiments, IAPV moved from infected honey bees to bumble bees and from infected bumble bees to honey bees within a week, demonstrating that the viruses could be transmitted from one species to another. This study adds to our present understanding of virus epidemiology and may help explain bee disease patterns and pollinator population decline in general.
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                Author and article information

                Contributors
                Role: ConceptualizationRole: Data curationRole: Formal analysisRole: Writing – original draft
                Role: Writing – review & editing
                Role: ConceptualizationRole: MethodologyRole: Writing – review & editing
                Role: ConceptualizationRole: Formal analysisRole: Funding acquisitionRole: Project administrationRole: ResourcesRole: 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
                6 February 2019
                2019
                : 14
                : 2
                : e0210594
                Affiliations
                [1 ] Institute of Ecology, Leuphana University of Lüneburg, Lüneburg, Germany
                [2 ] Chair of Nature Conservation and Landscape Ecology, University of Freiburg, Freiburg, Germany
                [3 ] Department of Animal Ecology and Tropical Biology, University of Würzburg, Biocenter—Am Hubland, Würzburg, Germany
                College of Agricultural Sciences, UNITED STATES
                Author notes

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

                Author information
                http://orcid.org/0000-0002-8154-9569
                Article
                PONE-D-18-21433
                10.1371/journal.pone.0210594
                6364881
                30726258
                17c5c37f-42a0-4b53-afbe-1828153a2175
                © 2019 Drescher 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
                : 19 July 2018
                : 28 December 2018
                Page count
                Figures: 7, Tables: 3, Pages: 20
                Funding
                Funded by: funder-id http://dx.doi.org/10.13039/501100001659, Deutsche Forschungsgemeinschaft;
                Award ID: LE 2750/1-1
                Award Recipient :
                Funded by: University of Wuerzburg
                Award ID: Open Access Publishing
                Award Recipient :
                Funding was provided by the Deutsche Forschungsgemeinschaft (DFG project: LE 2750/1-1) to SDL and the University of Würzburg in the funding programme Open Access Publishing to ND. 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
                Insects
                Hymenoptera
                Bees
                Honey Bees
                Biology and Life Sciences
                Organisms
                Eukaryota
                Plants
                Trees
                Poplars
                Biology and Life Sciences
                Organisms
                Eukaryota
                Plants
                Trees
                Biology and Life Sciences
                Ecology
                Ecosystems
                Forests
                Ecology and Environmental Sciences
                Ecology
                Ecosystems
                Forests
                Ecology and Environmental Sciences
                Terrestrial Environments
                Forests
                Physical Sciences
                Chemistry
                Chemical Composition
                Biology and Life Sciences
                Organisms
                Eukaryota
                Animals
                Invertebrates
                Arthropoda
                Insects
                Hymenoptera
                Bees
                Biology and Life Sciences
                Organisms
                Eukaryota
                Plants
                Trees
                Conifers
                Physical Sciences
                Chemistry
                Chemical Compounds
                Phenols
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