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      Variable effects of nicotine, anabasine, and their interactions on parasitized bumble bees

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          Abstract

          Secondary metabolites in floral nectar have been shown to reduce parasite load in two common bumble bee species. Previous studies on the effects of nectar secondary metabolites on parasitized bees have focused on single compounds in isolation; however, in nature, bees are simultaneously exposed to multiple compounds. We tested for interactions between the effects of two alkaloids found in the nectar of Nicotiana spp. plants, nicotine and anabasine, on parasite load and mortality in bumble bees ( Bombus impatiens) infected with the intestinal parasite Crithidia bombi. Adult worker bees inoculated with C. bombi were fed nicotine and anabasine diet treatments in a factorial design, resulting in four nectar treatment combinations:  2 ppm nicotine, 5 ppm anabasine, 2ppm nicotine and 5 ppm anabasine together, or a control alkaloid-free solution. We conducted the experiment twice: first, with bees incubated under variable environmental conditions (‘Variable’; temperatures varied from 10-35°C with ambient lighting); and second, under carefully controlled environmental conditions (‘Stable’; 27°C incubator, constant darkness). In ‘Variable’, each alkaloid alone significantly decreased parasite loads, but this effect was not realized with the alkaloids in combination, suggesting an antagonistic interaction. Nicotine but not anabasine significantly increased mortality, and the two compounds had no interactive effects on mortality. In ‘Stable’, nicotine significantly increased parasite loads, the opposite of its effect in ‘Variable’. While not significant, the relationship between anabasine and parasite loads was also positive. Interactive effects between the two alkaloids on parasite load were non-significant, but the pattern of antagonistic interaction was similar to that in the variable experiment. Neither alkaloid, nor their interaction, significantly affected mortality under controlled conditions. Our results do not indicate synergy between Nicotiana nectar alkaloids; however, they do suggest a complex interaction between secondary metabolites, parasites, and environmental variables, in which secondary metabolites can be either toxic or medicinal depending on context.

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          Most cited references54

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          Interactions between effects of environmental chemicals and natural stressors: a review.

          Ecotoxicological effect studies often expose test organisms under optimal environmental conditions. However, organisms in their natural settings rarely experience optimal conditions. On the contrary, during most of their lifetime they are forced to cope with sub-optimal conditions and occasionally with severe environmental stress. Interactions between the effects of a natural stressor and a toxicant can sometimes result in greater effects than expected from either of the stress types alone. The aim of the present review is to provide a synthesis of existing knowledge on the interactions between effects of "natural" and chemical (anthropogenic) stressors. More than 150 studies were evaluated covering stressors including heat, cold, desiccation, oxygen depletion, pathogens and immunomodulatory factors combined with a variety of environmental pollutants. This evaluation revealed that synergistic interactions between the effects of various natural stressors and toxicants are not uncommon phenomena. Thus, synergistic interactions were reported in more than 50% of the available studies on these interactions. Antagonistic interactions were also detected, but in fewer cases. Interestingly, about 70% of the tested chemicals were found to compromise the immune system of humans as judged from studies on human cell lines. The challenge for future studies will therefore be to include aspects of combined stressors in effect and risk assessment of chemicals in the environment. Copyright 2009 Elsevier B.V. All rights reserved.
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            Plight of the bumble bee: Pathogen spillover from commercial to wild populations

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                Author and article information

                Journal
                F1000Res
                F1000Res
                F1000Research
                F1000Research
                F1000Research (London, UK )
                2046-1402
                16 December 2015
                2015
                : 4
                : 880
                Affiliations
                [1 ]Department of Biology, University of Massachusetts at Amherst, Amherst, Massachusetts, USA
                [2 ]Department of Biology, Dartmouth College Hanover, New Hampshire, USA
                [3 ]Department of Applied Ecology, North Carolina State University, Raleigh, North Carolina, USA
                [1 ]Honey Bee Breeding, Genetics, and Physiology Research, USDA Agricultural Research Service, Baton Rouge, LA, USA
                [2 ]Department of Entomology, North Carolina State University, Raleigh, NC, USA
                [1 ]School of Biological and Chemical Sciences, Queen Mary, University of London, London, UK
                [1 ]School of Biological and Chemical Sciences, Queen Mary, University of London, London, UK
                Univ of Massachusetts, USA
                [1 ]Honey Bee Breeding, Genetics, and Physiology Research, USDA Agricultural Research Service, Baton Rouge, LA, USA
                [2 ]Department of Entomology, North Carolina State University, Raleigh, NC, USA
                Univ of Massachusetts, USA
                Author notes

                All authors conceived the study. ECPY and LPT designed and conducted the experiments using methods developed by REI. ECPY analyzed the data. LPT and ECPY prepared the first draft of the manuscript. All authors revised the manuscript and have agreed upon the final content.

                Competing interests: No competing interests were disclosed.

                Competing interests: No competing interests were disclosed.

                Competing interests: I am one of the authors of a paper that is cited prominently by Thorburn et al.

                Competing interests: No competing interests were disclosed.

                Competing interests: I am an author on the article being refereed

                Competing interests: No competing interests were disclosed.

                Competing interests: I am an author of the manuscript being reviewed

                Article
                10.12688/f1000research.6870.2
                4786900
                26998225
                b85a14f6-94df-4b31-98e1-cbfcdf91a4bb
                Copyright: © 2015 Thorburn LP et al.

                This is an open access article distributed under the terms of the Creative Commons Attribution Licence, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

                History
                : 11 December 2015
                Funding
                Funded by: National Science Foundation
                Award ID: NSFDEB-1258096
                Award ID: NSF GRFP (Grant DGE-0907995)
                Award ID: NSF DDIG (Grant NSFDEB-1501907)
                Funded by: CSREES
                Award ID: USDA-AFRI 2013-02536
                This research was funded by the National Science Foundation under NSFDEB-1258096, NSF GRFP (Grant DGE-0907995 to ECPY), and NSF DDIG (Grant NSFDEB-1501907 to ECPY and LSA); by the National Research Initiative (NRI) Arthropod and Nematode Biology and Management Program of the USDA Cooperative State Research, Education, and Extension Service (CSREES) Grant no. USDA-AFRI 2013-02536; and by the Garden Club of America Centennial Pollinator Fellowship (ECPY).
                I confirm that the funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
                Categories
                Research Article
                Articles
                Behavioral Ecology
                Plant-Biotic Interactions

                bumble bee,bombus impatiens,parasites,crithidia bombi,plant secondary metabolites,nicotine,alkaloids,tritrophic interactions

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