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

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          Abstract

          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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          Most cited references53

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          Drosophila intestinal response to bacterial infection: activation of host defense and stem cell proliferation.

          Although Drosophila systemic immunity is extensively studied, little is known about the fly's intestine-specific responses to bacterial infection. Global gene expression analysis of Drosophila intestinal tissue to oral infection with the Gram-negative bacterium Erwinia carotovora revealed that immune responses in the gut are regulated by the Imd and JAK-STAT pathways, but not the Toll pathway. Ingestion of bacteria had a dramatic impact on the physiology of the gut that included modulation of stress response and increased stem cell proliferation and epithelial renewal. Our data suggest that gut homeostasis is maintained through a balance between cell damage due to the collateral effects of bacteria killing and epithelial repair by stem cell division. The Drosophila gut provides a powerful model to study the integration of stress and immunity with pathways associated with stem cell control, and this study should prove to be a useful resource for such further studies.
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            Nutrition and health in honey bees

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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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                Author and article information

                Contributors
                Role: Editor
                Journal
                PLoS One
                PLoS ONE
                plos
                plosone
                PLoS ONE
                Public Library of Science (San Francisco, USA )
                1932-6203
                2013
                5 August 2013
                : 8
                : 8
                : e72016
                Affiliations
                [1 ]UMT, Protection des Abeilles dans l’Environnement, CS 40509, Avignon, France
                [2 ]ACTA, Site Agroparc, Avignon, France
                [3 ]INRA, UR 406 Abeilles et Environnement, CS 40509, Avignon, France
                [4 ]INRA, UR 546 Biostatistique et Processus Spatiaux, CS 40509, Avignon, France
                [5 ]Université d’Avignon et des pays du Vaucluse, UMR 7263 Institut Méditerranéen de Biodiversité et d’Ecologie, Pôle Agrosciences, Avignon, France
                The Australian National University, Australia
                Author notes

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

                Conceived and designed the experiments: GDP YLC LPB AD CA. Performed the experiments: GDP MS SS CA. Analyzed the data: GDP AK JLB CA. Contributed reagents/materials/analysis tools: YLC LPB AD. Wrote the manuscript: GDP CA.

                Article
                PONE-D-13-12232
                10.1371/journal.pone.0072016
                3733843
                23940803
                f04686a3-fec2-4de0-bc13-3a2129df0e63
                Copyright @ 2013

                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
                : 25 March 2013
                : 4 July 2013
                Funding
                This work was funded by a grant from the European Agricultural Guarantee Fund (797/2004). GDP was supported by a Conventions Industrielles de Formation par la REcherche fellowship (ANRT). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
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