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      Native habitat mitigates feast–famine conditions faced by honey bees in an agricultural landscape

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          Industrial-scale production of crops through monocultures has resulted in “green deserts” of reduced biodiversity in many areas worldwide. Such simplified landscapes may impact ecosystem services such as pollination. Here, we present a large-scale, longitudinal study of managed honey bee colonies in the context of corn and soybean monocultures. Our results reveal a brief burst of colony growth during soybean bloom, followed by a longer period of forage dearth, resulting in decline in several aspects of honey bee health at both colony and individual levels. We demonstrate this decline is reversible when honey bees have access to native, perennial plants (i.e., prairie). Our results suggest sustainable pollinator management in landscapes dominated by monocultures can be achieved through reintegration of native biodiversity.

          Abstract

          Intensive agriculture can contribute to pollinator decline, exemplified by alarmingly high annual losses of honey bee colonies in regions dominated by annual crops (e.g., midwestern United States). As more natural or seminatural landscapes are transformed into monocultures, there is growing concern over current and future impacts on pollinators. To forecast how landscape simplification can affect bees, we conducted a replicated, longitudinal assessment of honey bee colony growth and nutritional health in an intensively farmed region where much of the landscape is devoted to production of corn and soybeans. Surprisingly, colonies adjacent to soybean fields surrounded by more cultivated land grew more during midseason than those in areas of lower cultivation. Regardless of the landscape surrounding the colonies, all experienced a precipitous decline in colony weight beginning in August and ended the season with reduced fat stores in individual bees, both predictors of colony overwintering failure. Patterns of forage availability and colony nutritional state suggest that late-season declines were caused by food scarcity during a period of extremely limited forage. To test if habitat enhancements could ameliorate this response, we performed a separate experiment in which colonies provided access to native perennials (i.e., prairie) were rescued from both weight loss and reduced fat stores, suggesting the rapid decline observed in these agricultural landscapes is not inevitable. Overall, these results show that intensively farmed areas can provide a short-term feast that cannot sustain the long-term nutritional health of colonies; reintegration of biodiversity into such landscapes may provide relief from nutritional stress.

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          Crop pollination from native bees at risk from agricultural intensification.

          Ecosystem services are critical to human survival; in selected cases, maintaining these services provides a powerful argument for conserving biodiversity. Yet, the ecological and economic underpinnings of most services are poorly understood, impeding their conservation and management. For centuries, farmers have imported colonies of European honey bees (Apis mellifera) to fields and orchards for pollination services. These colonies are becoming increasingly scarce, however, because of diseases, pesticides, and other impacts. Native bee communities also provide pollination services, but the amount they provide and how this varies with land management practices are unknown. Here, we document the individual species and aggregate community contributions of native bees to crop pollination, on farms that varied both in their proximity to natural habitat and management type (organic versus conventional). On organic farms near natural habitat, we found that native bee communities could provide full pollination services even for a crop with heavy pollination requirements (e.g., watermelon, Citrullus lanatus), without the intervention of managed honey bees. All other farms, however, experienced greatly reduced diversity and abundance of native bees, resulting in insufficient pollination services from native bees alone. We found that diversity was essential for sustaining the service, because of year-to-year variation in community composition. Continued degradation of the agro-natural landscape will destroy this "free" service, but conservation and restoration of bee habitat are potentially viable economic alternatives for reducing dependence on managed honey bees.
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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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              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
                10 December 2019
                25 November 2019
                25 November 2019
                : 116
                : 50
                : 25147-25155
                Affiliations
                [1] aDepartment of Entomology, University of Illinois Urbana–Champaign , Urbana, IL 61801;
                [2] bDepartment of Ecology and Evolutionary Biology, Iowa State University , Ames, IA 50011;
                [3] cDepartment of Entomology, Iowa State University , Ames, IA 50011
                Author notes
                2To whom correspondence may be addressed. Email: adolezal@ 123456illinois.edu .

                Edited by David L. Denlinger, The Ohio State University, Columbus, OH, and approved October 25, 2019 (received for review July 24, 2019)

                Author contributions: A.G.D., A.L.S.C., G.Z., A.L.T., and M.E.O. designed research; A.G.D., A.L.S.C., and G.Z. performed research; A.L.S.C. analyzed data; and A.G.D., A.L.S.C., A.L.T., and M.E.O. wrote the paper.

                1A.G.D. and A.L.S.C. contributed equally to this work.

                Author information
                http://orcid.org/0000-0001-6164-1344
                Article
                201912801
                10.1073/pnas.1912801116
                6911205
                31767769
                89a1fd0f-fe34-461c-acbd-43b92a8b7d3e
                Copyright © 2019 the Author(s). Published by PNAS.

                This open access article is distributed under Creative Commons Attribution-NonCommercial-NoDerivatives License 4.0 (CC BY-NC-ND).

                History
                Page count
                Pages: 9
                Funding
                Funded by: United Soybean Board
                Award ID: 1520-732-7225
                Award Recipient : Adam G Dolezal Award Recipient : Amy L Toth Award Recipient : Matthew E. O'Neal
                Funded by: Hatch Act
                Award ID: n/a
                Award Recipient : Adam G Dolezal Award Recipient : Amy L Toth Award Recipient : Matthew E. O'Neal
                Categories
                Biological Sciences
                Ecology
                From the Cover

                honey bee,apis mellifera,land use,agriculture,pollinators
                honey bee, apis mellifera, land use, agriculture, pollinators

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