Testing dose-dependent effects of the nectar alkaloid anabasine on trypanosome parasite loads in adult bumble bees

PLoS ONE

Volumn 10, Issue 11, 2015, Pages

  Anthony, Winston E ^a,d   Palmer Young, Evan C ^a   Leonard, Anne S ^a,e   Irwin, Rebecca E ^b,c   Adler, Lynn S ^a  

^a UNIVERSITY OF MASSACHUSETTS   (United States)

^b Lamont Doherty Earth Observatory   (United States)

^c NORTH CAROLINA STATE UNIVERSITY   (United States)

^d HARVARD MEDICAL SCHOOL   (United States)

^e UNIVERSITY OF NEVADA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANABASINE; NECTAR;

ADULT; ANALYSIS OF VARIANCE; ANIMAL EXPERIMENT; ARTICLE; BUMBLEBEE; CHEMICAL ANALYSIS; CONCENTRATION RESPONSE; CONTROLLED STUDY; CRITHIDIA; CRITHIDIA BOMBI; INOCULATION; NICOTIANA; NONHUMAN; PARASITE LOAD; POLLINATION; SURVIVAL RATE; TRYPANOSOMA; ADMINISTRATION AND DOSAGE; ANIMAL; BEE; CHEMISTRY; DOSE RESPONSE; DRUG EFFECTS; HERBIVORY; HOST PARASITE INTERACTION; MEDICINAL PLANT; NECTAR; PARASITOLOGY; PATHOGENICITY; TOBACCO;

ANABASINE; ANIMALS; BEES; CRITHIDIA; DOSE-RESPONSE RELATIONSHIP, DRUG; HERBIVORY; HOST-PARASITE INTERACTIONS; PARASITE LOAD; PLANT NECTAR; PLANTS, MEDICINAL; TOBACCO;

EID: 84952642384     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0142496     Document Type: Article

References (64)

1. Ehrlich PR, Raven PH. Butterflies and plants: a study in coevolution. Evolution. 1964; 18:586-608.
2. Adler LS, Seifert MG, Wink M, Morse GE. Reliance on pollinators predicts defensive chemistry across tobacco species. Ecol Lett. 2012; 15:1140-48. doi: 10.1111/j.1461-0248.2012.01838.x PMID: 22834564
3. Agrawal AA. Macroevolution of plant defense strategies. Trends Ecol Evol. 2007; 22(2):103-9. doi: 10. 1016/j.tree.2006.10.012 WOS:000244169200007. PMID: 17097760
4. Johnson MTJ, Ives AR, Ahern J, Salminen JP. Macroevolution of plant defenses against herbivores in the evening primroses. New Phytol. 2014; 203(1):267-79. doi: 10.1111/nph.12763 WOS:000336970200026. PMID: 24634986
5. Manson JS, Rasmann S, Halitschke R, Thomson JD, Agrawal AA. Cardenolides in nectar may be more than a consequence of allocation to other plant parts: a phylogenetic study of Asclepias. Funct Ecol. 2012; 26(5):1100-10. doi: 10.1111/j.1365-2435.2012.02039.x WOS:000309391500012.
6. Bowers MD, Stamp NE. Chemical variation within and between individuals of Plantago lanceolata (Plantaginaceae). J Chem Ecol. 1992; 18(7):985-95. doi: 10.1007/BF00980057 PMID: 24254142
7. Agrawal AA, Hastings AP, Johnson MTJ, Maron JL, Salminen JP. Insect herbivores drive real-time ecological and evolutionary change in plant populations. Science. 2012; 338(6103):113-6. doi: 10.1126/ science.1225977 WOS:000309457400065. PMID: 23042894
8. Adler LS. The ecological significance of toxic nectar. Oikos. 2000; 91(3):409-20. ISI:000166777500001.
9. Heil M. Nectar: generation, regulation, and ecological functions. Trends Plant Sci. 2011; 16(4):191-200. doi: 10.1016/j.tplants.2011.01.003 WOS:000290508100004. PMID: 21345715
10. Adler LS, Wink M, Distl M, Lentz AJ. Leaf herbivory and nutrients increase nectar alkaloids. Ecol Lett. 2006; 9(8):960-7. ISI:000239510700012. PMID: 16913940
11. Wright GA, Baker DD, Palmer MJ, Stabler D, Mustard JA, Power EF, et al. Caffeine in floral nectar enhances a pollinator's memory of reward. Science. 2013; 339(6124):1202-4. doi: 10.1126/science. 1228806 WOS:000315709900046. PMID: 23471406
12. Thomson JD, Draguleasa MA, Tan MG. Flowers with caffeinated nectar receive more pollination. Arthropod-Plant Interactions. 2015; 9:1-7. doi: 10.1007/s11829-014-9350-z
13. Detzel A, Wink M. Attraction, deterrence or intoxication of bees (Apis mellifera) by plant allelochemicals. Chemoecology. 1993; 4(1):8-18.
14. Singaravelan N, Nee'man G, Inbar M, Izhaki I. Feeding responses of free-flying honeybees to secondary compounds mimicking floral nectars. J Chem Ecol. 2005; 31(12):2791-804. ISI:000234115600003. PMID: 16365705
15. Hare JD. Plant genetic variation in tritrophic interactions. In: Tscharntke T, Hawkins BA, editors. Multitrophic level interactions. Cambridge: Cambridge University Press; 2002. p. 8-43.
16. Thaler JS. Jasmonate-inducible plant defences cause increased parasitism of herbivores. Nature. 1999; 399(6737):686-8. ISI:000080932800059.
17. Price PW, Bouton CE, Gross P, McPheron BA, Thompson JN, Weis AE. Interactions among three trophic levels: influence of plants on interactions between insect herbivores and natural enemies. Annu Rev Ecol Syst. 1980; 11:41-65.
18. Kaplan I, Thaler JS. Plant resistance attenuates the consumptive and non-consumptive impacts of predators on prey. Oikos. 2010; 119(7):1105-13. ISI:000278525800007.
19. Santolamazza-Carbone S, Velasco P, Soengas P, Cartea ME. Bottom-up and top-down herbivore regulation mediated by glucosinolates in Brassica oleracea var. acephala. Oecologia. 2014; 174(3):893-907. doi: 10.1007/s00442-013-2817-2 WOS:000332002300026. PMID: 24352843
20. Manson JS, Otterstatter MC, Thomson JD. Consumption of a nectar alkaloid reduces pathogen load in bumble bees. Oecologia. 2010; 162(1):81-9. ISI:000271736100008. doi: 10.1007/s00442-009-1431-9 PMID: 19711104
21. Richardson LL, Adler LS, Leonard AS, Andicoechea J, Regan KH, Anthony WE, et al. Secondary metabolites in floral nectar reduce parasite infections in bumblebees. Proceedings of the Royal Society B-Biological Sciences. 2015; 282(1803). doi: 10.1098/rspb.2014.2471 WOS:000350349100005.
22. Baracchi D, Brown MJF, Chittka L. Behavioural evidence for self-medication in bumblebees? [v2; ref status: indexed, http://f1000r.es/5ep]. F1000Research. 2015; 4(73):1-15. doi: 10.12688/ f1000research.6262.2
23. Costa C, Lodesani M, Maistrello L. Effect of thymol and resveratrol administered with candy or syrup on the development of Nosema ceranae and on the longevity of honeybees (Apis mellifera L.) in laboratory conditions. Apidologie. 2010; 41(2):141-50.
24. Gherman BI, Denner A, Bobis O, Dezmirean DS, Marghitas LA, Schlüns H, et al. Pathogen-associated self-medication behavior in the honeybee Apis mellifera. Behav Ecol Sociobiol. 2014; 68(11):1777-84. doi: 10.1007/s00265-014-1786-8
25. Tadmor-Melamed H, Markman S, Arieli A, Distl M, Wink M, Izhaki I. Limited ability of Palestine sunbirds (Nectarinia osea) to cope with pyridine alkaloids in nectar of tree tobacco, Nicotiana glauca. Funct Ecol. 2004; 18(6):844-50. ISI:000225617200011.
26. Kaczorowski RL, Koplovich A, Sporer F, Wink M, Markman S. Immediate effects of nectar robbing by Palestine sunbirds (Nectarinia osea) on nectar alkaloid concentrations in tree tobacco (Nicotiana glauca). J Chem Ecol. 2014; 40(4):325-30. doi: 10.1007/s10886-014-0411-7 WOS:000335656800011. PMID: 24692053
27. Losey JE, Vaughan M. The economic value of ecological services provided by insects. Bioscience. 2006; 56(4):311-23.
28. Cameron SA, Lozier JD, Strange JP, Koch JB, Cordes N, Solter LF, et al. Patterns of widespread decline in North American bumble bees. Proceedings of the National Academy of Sciences. 2011; 108 (2):662-7.
29. Goulson D, Nicholls E, Botías C, Rotheray EL. Bee declines driven by combined stress from parasites, pesticides, and lack of flowers. Science. 2015; 2010(February):1-16.
30. Cordes N, Huang W-F, Strange JP, Cameron SA, Griswold TL, Lozier JD, et al. Interspecific geographic distribution and variation of the pathogens Nosema bombi and Crithidia species in United States bumble bee populations. J Invertebr Pathol. 2012; 109(2):209-16. doi: 10.1016/j.jip.2011.11.005 PMID: 22119631
31. Heinrich B. Bumblebee Economics: Revised Edition: Harvard University Press; 2004.
32. Williams P, Thorp R, Richardson L, Colla S. Bumble bees of North America. Princeton and Oxford: Princeton University Press; 2014. 208 p.
33. Popp M, Erler S, Lattorff HMG. Seasonal variability of prevalence and occurrence of multiple infections shape the population structure of Crithidia bombi, an intestinal parasite of bumblebees (Bombus spp.). Microbiologyopen. 2012; 1(4):362-72. doi: 10.1002/Mbo3.35 ISI:000209077800002. PMID: 23233373
34. Gillespie S. Factors affecting parasite prevalence among wild bumblebees. Ecol Entomol. 2010; 35 (6):737-47. doi: 10.1111/j.1365-2311.2010.01234.x ISI:000284170200009.
35. Shykoff JA, Schmid-Hempel P. Incidence and effects of four parasites in natural populations of bumble bees in Switzerland Apidologie. 1991; 22(2):117-25. WOS:A1991FP08900004.
36. Schmid-Hempel P. On the evolutionary ecology of host-parasite interactions: addressing the question with regard to bumblebees and their parasites. Naturwissenschaften. 2001; 88(4):147-58. doi: 10. 1007/s001140100222 PMID: 11480702
37. Durrer S, Schmid-Hempel P. Shared use of flowers leads to horizontal pathogen transmission. Proceedings of the Royal Society of London Series B: Biological Sciences. 1994; 258(1353):299-302.
38. Salathé RM, Schmid-Hempel P. The genotypic structure of a multi-host bumblebee parasite suggests a role for ecological niche overlap. PloS one. 2011; 6(8):e22054. doi: 10.1371/journal.pone.0022054 PMID: 21853023
39. Brown MJ, Schmid-Hempel R, Schmid-Hempel P. Strong context-dependent virulence in a host-parasite system: reconciling genetic evidence with theory. J Anim Ecol. 2003; 72(6):994-1002.
40. Liersch S, Schmid-Hempel P. Genetic variation within social insect colonies reduces parasite load. Proceedings of the Royal Society of London Series B: Biological Sciences. 1998; 265(1392):221-5.
41. Whitehorn PR, Tinsley MC, Brown MJ, Darvill B, Goulson D. Genetic diversity, parasite prevalence and immunity in wild bumblebees. Proceedings of the Royal Society B: Biological Sciences. 2011; 278 (1709):1195-202. doi: 10.1098/rspb.2010.1550 PMID: 20926436
42. Gegear RJ, Otterstatter MC, Thomson JD. Does parasitic infection impair the ability of bumblebees to learn flower-handling techniques? Animal Behaviour. 2005; 70(1):209-15.
43. Gegear RJ, Otterstatter MC, Thomson JD. Bumble-bee foragers infected by a gut parasite have an impaired ability to utilize floral information. Proceedings of the Royal Society B: Biological Sciences. 2006; 273(1590):1073-8. PMID: 16600883
44. Pavia C, Pierre A, Nowakowski J. Antimicrobial activity of nicotine against a spectrum of bacterial and fungal pathogens. J Med Microbiol. 2000; 49(7):675. PMID: 10882095
45. Wink M. Interference of alkaloids with neuroreceptors and ion channels. Studies in natural products chemistry. 2000; 21:3-122.
46. Campbell F, Sullivan W, Smith C. The relative toxicity of nicotine, anabasine, methyl anabasine, and lupinine for culicine mosquito larvae. J Econ Entomol. 1933; 26(2):500-9.
47. Yothers MA, Griffin SW. Tests of rotenone, anabasine, nicotine, and other insecticides against the woolly apple aphid and the apple aphid. J Econ Entomol. 1940; 33(5):800-3.
48. Tadmor-Melamed H, Markman S, Arieli A, Distl M, Wink M, Izhaki I. Limited ability of Palestine sunbirds (Nectarinia osea) to cope with pyridine alkaloids in nectar of tree tobacco Nicotiana glauca. FUNCTIONAL ECOLOGY. 2004; 18(6):844-50.
49. Fokt H, Pereira A, Ferreira A, Cunha A, Aguiar C. How do bees prevent hive infections? The antimicrobial properties of propolis. Current Research, Technology and Education Topics in Applied Microbiology and Microbial Biotechnology. 2010; 1:481-4493.
50. Otterstatter M, Thomson J. Within-host dynamics of an intestinal pathogen of bumble bees. Parasitology. 2006; 133(6):749.
51. Richardson LL, Adler LS, Leonard AS, Henry K, Anthony W, Manson JS, et al. Secondary metabolites in floral nectar reduce parasite infections in bumble bees. Proceedings of the Royal Society B: Biological Sciences. 2015; 282:20142471. doi: 10.1098/rspb.2014.2471 PMID: 25694627
52. Müller C, Blackburn T, Schmid-Hempel P. Field evidence that host selection by conopid parasitoids is related to host body size. Insectes Soc. 1996; 43(3):227-33.
53. R Core Team. R: A language and environment for statistical computing. Vienna, Austria: R Foundation for Statistical Computing; 2014.
54. Therneau TM. R package coxme: Mixed effects cox models.: R package version 2.2-5; 2015.
55. Lesnoff M, Lancelot R. R package aod: Analysis of overdispersed data. R package version 1.3; 2012.
56. Tiedeken EJ, Stout JC, Stevenson PC, Wright GA. Bumblebees are not deterred by ecologically relevant concentrations of nectar toxins. The Journal of experimental biology. 2014; 217(9):1620-5.
57. Kessler SC, Tiedeken EJ, Simcock KL, Derveau S, Mitchell J, Softley S, et al. Bees prefer foods containing neonicotinoid pesticides. Nature. 2015; 521:74-6. doi: 10.1038/nature14414 PMID: 25901684
58. Brown M, Loosli R, Schmid-Hempel P. Condition-dependent expression of virulence in a trypanosome infecting bumblebees. Oikos. 2000; 91(3):421-7.
59. Manson JS, Otterstatter MC, Thomson JD. Consumption of a nectar alkaloid reduces pathogen load in bumble bees. Oecologia. 2010; 162(1):81-9. doi: 10.1007/s00442-009-1431-9 PMID: 19711104
60. Baracchi D, Brown MJF, Chittka L. Weak and contradictory effects of self-medication with nectar nicotine by parasitized bumblebees. F1000Research. 2015;(0: ):1-15. doi: 10.12688/f1000research.6262. 1
61. Sadd BM. Food-environment mediates the outcome of specific interactions between a bumblebee and its trypanosome parasite. Evolution. 2011; 65(10):2995-3001. doi: 10.1111/j.1558-5646.2011.01345.x PMID: 21967438
62. Koch H, Schmid-Hempel P. Socially transmitted gut microbiota protect bumble bees against an intestinal parasite. Proceedings of the National Academy of Sciences. 2011; 108(48):19288-92.
63. Li M, Wang B, Zhang M, Rantalainen M, Wang S, Zhou H, et al. Symbiotic gut microbes modulate human metabolic phenotypes. Proceedings of the National Academy of Sciences. 2008; 105(6):2117-22. doi: 10.1073/pnas.0712038105
64. Imdorf A, Bogdanov S, Ochoa R, Ibáñez, Calderone N, W. Use of essential oils for the control of Varroa jacobsoni Oud. in honey bee colonies. Apidologie. 1999; 30(2-3):209-28.