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      Warming Increases Pollen Lipid Concentration in an Invasive Thistle, with Minor Effects on the Associated Floral-Visitor Community

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          Abstract

          Climate warming is likely to change the ways in which plants interact with their insect mutualists, for example through changes in phytochemistry. In particular, this may have implications for the ways in which we manage noxious weeds, which may spread more quickly if they experience stronger mutualistic interactions. We grew the invasive nodding thistle, Carduus nutans, in two experimental treatments in the field: either passively warmed with open top chambers or at ambient temperatures. We collected pollen from thistles in each treatment and analysed the total protein, lipid, and carbohydrate content. We observed no difference in the pollen protein or carbohydrate content, but the total lipid content of the pollen was significantly higher in warmed plants. We conducted a total of 12.75 h of observations of putatively mutualistic, flower-visiting insects. In addition, we spent 4.17 h collecting bees that visited thistle inflorescences in the treatments, allowing us to identify them to species. We found a significant increase in the abundance of flower-visiting insects in the observations, but not bee abundance in collections. In addition, there was no treatment effect on the number of flower-visiting morphotypes in the observations, or bee species richness in the collections. However, a nonparametric test did identify a significant effect of warming on the composition of flower-visiting morphotypes in observations and bee species in collections. Overall, the warming treatment significantly increased lipid content of the pollen, but had relatively weak effects on insect visitation patterns. However, these effects may be amplified at larger spatial and temporal scales or higher temperatures.

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

              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. 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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                Author and article information

                Journal
                Insects
                Insects
                insects
                Insects
                MDPI
                2075-4450
                25 December 2019
                January 2020
                : 11
                : 1
                : 20
                Affiliations
                [1 ]Department of Entomology and Plant Pathology, University of Tennessee, Institute of Agriculture, Knoxville, TN 37996, USA
                [2 ]Department of Biology, Pennsylvania State University, State College, PA 16802, USA; jak573@ 123456psu.edu (J.K.); k-shea@ 123456psu.edu (K.S.)
                [3 ]Department of Entomology, Center for Pollinator Research, Huck Institutes of the Life Sciences, Pennsylvania State University, University Park, PA 16803, USA; advaudo@ 123456gmail.com (A.D.V.); christina.grozinger@ 123456gmail.com (C.M.G.)
                [4 ]Department of Biology, University of Nevada Reno, Reno, NV 89557, USA
                Author notes
                [* ]Correspondence: lrusso@ 123456utk.edu
                Author information
                https://orcid.org/0000-0002-7343-9837
                Article
                insects-11-00020
                10.3390/insects11010020
                7022432
                31881659
                0964df5c-ddfe-40a3-a332-2c8a335e8d2e
                © 2019 by the authors.

                Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license ( http://creativecommons.org/licenses/by/4.0/).

                History
                : 30 November 2019
                : 20 December 2019
                Categories
                Article

                mutualisms,pollinators,bees,climate change,experimental warming,carduus nutans,pollen nutrition

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