We previously characterized and quantified the influence of land use on survival and productivity of colonies positioned in six apiaries and found that colonies in apiaries surrounded by more land in uncultivated forage experienced greater annual survival, and generally more honey production. Here, detailed metrics of honey bee health were assessed over three years in colonies positioned in the same six apiaries. The colonies were located in North Dakota during the summer months and were transported to California for almond pollination every winter. Our aim was to identify relationships among measures of colony and individual bee health that impacted and predicted overwintering survival of colonies. We tested the hypothesis that colonies in apiaries surrounded by more favorable land use conditions would experience improved health. We modeled colony and individual bee health indices at a critical time point (autumn, prior to overwintering) and related them to eventual spring survival for California almond pollination. Colony measures that predicted overwintering apiary survival included the amount of pollen collected, brood production, and Varroa destructor mite levels. At the individual bee level, expression of vitellogenin, defensin1, and lysozyme2 were important markers of overwinter survival. This study is a novel first step toward identifying pertinent physiological responses in honey bees that result from their positioning near varying landscape features in intensive agricultural environments.

Human reliance on insect pollination services continues to increase even as pollinator populations exhibit global declines. Increased commodity crop prices and federal subsidies for biofuel crops, such as corn and soybeans, have contributed to rapid land-use change in the US Northern Great Plains (NGP), changes that may jeopardize habitat for honey bees in a part of the country that supports >40% of the US colony stock. We investigated changes in biofuel crop production and grassland land covers surrounding ∼18,000 registered commercial apiaries in North and South Dakota from 2006 to 2014. We then developed habitat selection models to identify remotely sensed land-cover and land-use features that influence apiary site selection by Dakota beekeepers. Our study demonstrates a continual increase in biofuel crops, totaling 1.2 Mha, around registered apiary locations in North and South Dakota. Such crops were avoided by commercial beekeepers when selecting apiary sites in this region. Furthermore, our analysis reveals how grasslands that beekeepers target when selecting commercial apiary locations are becoming less common in eastern North and South Dakota, changes that may have lasting impact on pollinator conservation efforts. Our study highlights how land-use change in the NGP is altering the landscape in ways that are seemingly less conducive to beekeeping. Our models can be used to guide future conservation efforts highlighted in the US national pollinator health strategy by identifying areas that support high densities of commercial apiaries and that have exhibited significant land-use changes.apiary selection models | Apis mellifera | land use | land-cover trends | pollinators A nimal pollination service is critical for sustaining ecosystem health and human well-being (1, 2). In many terrestrial systems, plant-pollinator interactions provide the basic framework for all other trophic interactions. Globally, about one-third of crop production depends on animal pollination (3). US agricultural production relies heavily on managed and native insects for pollination services, with an estimated economic value of $15 billion annually (2). Reliance on insects for pollination services is growing even as populations of native and managed pollinators exhibit concurrent declines (4, 5). For example, in 2013−2014, total US honey bee colony losses were 34%, but beekeepers on average lost 51% of their colonies (6). Declines in managed honey bees and native bees put significant pressure on global food supplies, plant-pollinator networks, agricultural producers, and ecosystem function (7,8).Proposed reasons for the declines include parasites, diseases, agro-chemical use, forage availability, and land-use change (9, 10). Much of the research investigating anthropogenic disturbance effects on managed and native pollinators focuses on pesticides and less so on habitat fragmentation, land-use, and loss of forage. Although a paucity of data exists for most parts of the world, recent research indicates that land use influences honey ...

A B S T R A C TThe Northern Great Plains region of the US annually hosts a large portion of commercially managed U.S. honey bee colonies each summer. Changing land use patterns over the last several decades have contributed to declines in the availability of bee forage across the region, and the future sustainability of the region to support honey bee colonies is unclear. We examined the influence of varying land use on the survivorship and productivity of honey bee colonies located in six apiaries within the Northern Great Plains state of North Dakota, an area of intensive agriculture and high density of beekeeping operations. Land use surrounding the apiaries was quantified over three years, 2010-2012, and survival and productivity of honey bee colonies were determined in response to the amount of bee forage land within a 3.2-km radius of each apiary. The area of uncultivated forage land (including pasture, USDA conservation program fields, fallow land, flowering woody plants, grassland, hay land, and roadside ditches) exerted a positive impact on annual apiary survival and honey production. Taxonomic diversity of bee-collected pollen and pesticide residues contained therein varied seasonally among apiaries, but overall were not correlated to large-scale land use patterns or survival and honey production. The predominant flowering plants utilized by honey bee colonies for pollen were volunteer species present in unmanaged (for honey bees), and often ephemeral, lands; thus placing honey bee colonies in a precarious situation for acquiring forage and nutrients over the entire growing season. We discuss the implications for land management, conservation, and beekeeper site selection in the Northern Great Plains to adequately support honey bee colonies and insure long term security for pollinator-dependent crops across the entire country.

Taxonomic identification of pollen has historically been accomplished via light microscopy but requires specialized knowledge and reference collections, particularly when identification to lower taxonomic levels is necessary. Recently, next-generation sequencing technology has been used as a cost-effective alternative for identifying bee-collected pollen; however, this novel approach has not been tested on a spatially or temporally robust number of pollen samples. Here, we compare pollen identification results derived from light microscopy and DNA sequencing techniques with samples collected from honey bee colonies embedded within a gradient of intensive agricultural landscapes in the Northern Great Plains throughout the 2010-2011 growing seasons. We demonstrate that at all taxonomic levels, DNA sequencing was able to discern a greater number of taxa, and was particularly useful for the identification of infrequently detected species. Importantly, substantial phenological overlap did occur for commonly detected taxa using either technique, suggesting that DNA sequencing is an appropriate, and enhancing, substitutive technique for accurately capturing the breadth of bee-collected species of pollen present across agricultural landscapes. We also show that honey bees located in high and low intensity agricultural settings forage on dissimilar plants, though with overlap of the most abundantly collected pollen taxa. We highlight practical applications of utilizing sequencing technology, including addressing ecological issues surrounding land use, climate change, importance of taxa relative to abundance, and evaluating the impact of conservation program habitat enhancement efforts.

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