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      Macronutrient ratios in pollen shape bumble bee ( Bombus impatiens) foraging strategies and floral preferences

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          Significance

          Bees pollinate the majority of flowering plant species, including agricultural crops. The pollen they obtain is their main protein and lipid source that fuels development and reproduction. Bee populations are declining globally, in large part because of landscape-level loss of host-plant species contributing to a nutritional shortage. To mitigate declines, we must understand how the nutritional requirements of bees influence foraging behavior. We demonstrate that bumble bees selectively collect pollen from host-plant species based on the protein:lipid ratios of pollen. Our research indicates that bees evaluate pollen quality and adjust foraging decisions to meet their nutritional needs. To be effective, conservation initiatives must include host-plant species that provide pollen that satisfies the nutritional demands of bees to support their populations.

          Abstract

          To fuel their activities and rear their offspring, foraging bees must obtain a sufficient quality and quantity of nutritional resources from a diverse plant community. Pollen is the primary source of proteins and lipids for bees, and the concentrations of these nutrients in pollen can vary widely among host-plant species. Therefore we hypothesized that foraging decisions of bumble bees are driven by both the protein and lipid content of pollen. By successively reducing environmental and floral cues, we analyzed pollen-foraging preferences of Bombus impatiens in ( i) host-plant species, ( ii) pollen isolated from these host-plant species, and ( iii) nutritionally modified single-source pollen diets encompassing a range of protein and lipid concentrations. In our semifield experiments, B. impatiens foragers exponentially increased their foraging rates of pollen from plant species with high protein:lipid (P:L) ratios; the most preferred plant species had the highest ratio (∼4.6:1). These preferences were confirmed in cage studies where, in pairwise comparisons in the absence of other floral cues, B. impatiens workers still preferred pollen with higher P:L ratios. Finally, when presented with nutritionally modified pollen, workers were most attracted to pollen with P:L ratios of 5:1 and 10:1, but increasing the protein or lipid concentration (while leaving ratios intact) reduced attraction. Thus, macronutritional ratios appear to be a primary factor driving bee pollen-foraging behavior and may explain observed patterns of host-plant visitation across the landscape. The nutritional quality of pollen resources should be taken into consideration when designing conservation habitats supporting bee populations.

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          Most cited references58

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          Decline and conservation of bumble bees.

          Declines in bumble bee species in the past 60 years are well documented in Europe, where they are driven primarily by habitat loss and declines in floral abundance and diversity resulting from agricultural intensification. Impacts of habitat degradation and fragmentation are likely to be compounded by the social nature of bumble bees and their largely monogamous breeding system, which renders their effective population size low. Hence, populations are susceptible to stochastic extinction events and inbreeding. In North America, catastrophic declines of some bumble bee species since the 1990s are probably attributable to the accidental introduction of a nonnative parasite from Europe, a result of global trade in domesticated bumble bee colonies used for pollination of greenhouse crops. Given the importance of bumble bees as pollinators of crops and wildflowers, steps must be taken to prevent further declines. Suggested measures include tight regulation of commercial bumble bee use and targeted use of environmentally comparable schemes to enhance floristic diversity in agricultural landscapes.
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            Is Open Access

            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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              Nutrition and health in honey bees

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                Author and article information

                Journal
                Proc Natl Acad Sci U S A
                Proc. Natl. Acad. Sci. U.S.A
                pnas
                pnas
                PNAS
                Proceedings of the National Academy of Sciences of the United States of America
                National Academy of Sciences
                0027-8424
                1091-6490
                12 July 2016
                28 June 2016
                : 113
                : 28
                : E4035-E4042
                Affiliations
                [1] aDepartment of Entomology, Center for Pollinator Research, The Pennsylvania State University , University Park, PA 16802;
                [2] bDepartment of Plant Science, Center for Pollinator Research, The Pennsylvania State University , University Park, PA 16802
                Author notes
                1To whom correspondence should be addressed. Email: adv124@ 123456psu.edu .

                Edited by John G. Hildebrand, University of Arizona, Tucson, AZ, and approved June 1, 2016 (received for review April 19, 2016)

                Author contributions: A.D.V., H.M.P., D.A.M., J.F.T., and C.M.G. designed research; A.D.V. performed research; A.D.V. contributed new reagents/analytic tools; A.D.V., J.F.T., and C.M.G. analyzed data; and A.D.V., J.F.T., and C.M.G. wrote the paper.

                Article
                PMC4948365 PMC4948365 4948365 201606101
                10.1073/pnas.1606101113
                4948365
                27357683
                df8f9e49-e93e-4c70-8f47-50776dd83e19
                History
                Page count
                Pages: 8
                Funding
                Funded by: USDA | National Institute of Food and Agriculture (NIFA) 100005825
                Award ID: 2009-05207
                Funded by: USDA | National Institute of Food and Agriculture (NIFA) 100005825
                Award ID: 10359159
                Categories
                PNAS Plus
                Biological Sciences
                Ecology
                PNAS Plus

                foraging behavior,nutritional ecology,pollen,pollinator,preferences

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