The impact of greenhouse tomato (Solanales: Solanaceae) floral volatiles on bumble bee (Hymenoptera: Apidae) pollination

Environmental Entomology

Volumn 41, Issue 4, 2012, Pages 855-864

  Morse, Andrew ^a   Kevan, Peter ^a   Shipp, Les ^b   Khosla, Shalin ^c   McGarvey, Brian ^b  

^a UNIVERSITY OF GUELPH   (Canada)

^b AGRICULTURE AND AGRI FOOD CANADA   (Canada)

^c FOOD AND RURAL AFFAIRS   (Canada)

Author keywords

bumble bee; floral volatile; greenhouse; repellent; tomato

Indexed keywords

ANTIHERBIVORE DEFENSE; BEE; CULTIVAR; FLORISTICS; FLOWER; FORAGING BEHAVIOR; FRUIT; GREENHOUSE ECOSYSTEM; PEST DAMAGE; PLANT-POLLINATOR INTERACTION; VOLATILE ORGANIC COMPOUND;

EID: 84865403141     PISSN: 0046225X     EISSN: None     Source Type: Journal    
DOI: 10.1603/EN11234     Document Type: Article

References (57)

1. Abak, K., and H. Y. Dasgan. 2005. Efficiency of bumblebees as pollinators in unheaded or anti-frost heated hreenhouses, pp. 19-29. In J. M. Guera Sanz, A. Rolda'n Serrano, and A. Mena Granero (eds.), First short course on pollination of horticultural plants, CIFA La Mojonera (IFAPA), Almerõ'a, Spain.
2. Ashman, T. L., M. Bradburn, D. H. Cole, B. H. Blaney, and R. A. Raguso. 2005. The scent of a male: The role of oral volatiles in pollination of a gender dimorphic plant. Ecology 86: 2099-2105. (Pubitemid 41117480)
3. Ashman, T. L., and M. Stanton. 1991. Seasonal-variation in pollination dynamics of sexually dimorphic Sidalcea oregana SSP Spicata (Malvaceae). Ecology 72: 993-1003.
4. Banda, H. J., and R. J. Paxton. 1991. Pollination of greenhouse tomatoes by bees. Acta Hort. 288: 194-198.
5. Biernaskie, J. M., and R. J. Gegear. 2007. Habitat assessment ability of bumble-bees implies frequency-dependent selection on oral rewards and display size. Proc. R. Soc. B. Biol. Sci. 274: 2595-2601. (Pubitemid 47492636)
6. Blarer, A., T. Keasar, and A. Shmida. 2002. Possible mechanisms for the formation of ower size preferences by foraging bumblebees. Ethology 108: 341-351. (Pubitemid 34299793)
7. Buchmann, S. L. 1983. Buzz pollination in angiosperms, pp. 73-113. In C. E. Jones and R. J. Little (eds.), Handbook of experimental pollination biology. Van Nostrand Reinhold Co., New York/Toronto.
8. Buttery, R. G., L. C. Ling, and D. M. Light. 1987. Tomato leaf volatile aroma components. J. Agric. Food Chem. 35: 1039-1042.
9. Cheng, S. S., M. T. Chua, E. H. Chang, C. G. Huang, W. J. Chen, and S. T. Chang. 2009. Variations in insecticidal activity and chemical compositions of leaf essential oils from Cryptomeria japonica at different ages. Bioresour. Technol. 100: 465-470.
10. Dobson, H.E.M. 2005. Pollen odour and its effect on ower visitation by bees, pp. 71-76. In J. M. Guera Sanz, A. Rolda'n Serrano, and A. Mena Granero (eds.), First short course on pollination of horticultural plants. CIFA La Mojonera (IFAPA), Almerõ'a, Spain.
11. Dobson, H.E.M., R. A. Raguso, J. T. Knudsen, and M. Ayasse. 2005. Scent as an attractant, pp. 197-210. In A. Dafni, P. G. Kevan, and B. C. Husband (eds.), Practical pollination biology. Enviroquest, Ltd., Cambridge, Ontario, Canada.
12. Dudareva, N., and E. Pichersky. 2000. Biochemical and molecular genetic aspects of oral scents. Plant Physiol. 122: 627-633.
13. Effmert, U., J. Grosse, U.S.R. Rose, F. Ehrig, R. Kagi, and B. Piechulla. 2005. Volatile composition, emission pattern, and localization of oral scent emission in Mirabilis jalapa (Nyctaginaceae). Am. J. Bot. 92: 2-12. (Pubitemid 40113101)
14. Euler, M., and I. T. Baldwin. 1996. The chemistry of defense and apparency in the corollas of Nicotiana attenuata. Oecologia 107: 102-112.
15. Farag, M. A., and P. W. Pare. 2002. C-6-green leaf volatiles trigger local and systemic VOC emissions in tomato. Phytochemistry 61: 545-554. (Pubitemid 35345861)
16. Fletcher, S. W., and O. I. Gregg. 1907. Pollination of forced tomatoes. Special bulletin of the Michigan agricultural experiment station 39: 294-301.
17. Free, J. B. 1970. Insect pollination of crops. Academic, London, United Kingdom.
18. Gabel, B., D. Thiery, V. Suchy, F. Marionpoll, P. Hradsky, and P. Farkas. 1992. Floral volatiles of Tanacetum vulgare L. attractive to Lobesia botrana Den. et-Schiff. females. J. Chem. Ecol. 18: 693-701.
19. Heinrich, B. 2004. Bumblebee economics. Harvard University Press, Cambridge, MA.
20. Ishii, H. S. 2006. Floral display size inuences subsequent plant choice by bumble bees. Funct. Ecol. 20: 233-238. (Pubitemid 43725624)
21. Jakobsen, H. B., and C. E. Olsen. 1994. Inuence of climatic factors on emission of ower volatiles in-situ. Planta 192: 365-371. (Pubitemid 2015249)
22. Janmaat, A. F., W. J. de Kogel, and E. J. Woltering. 2002. Enhanced fumigant toxicity of p-cymene against Frankliniella occidentalis by simultaneous application of elevated levels of carbon dioxide. Pest Manag. Sci 58: 167-173. (Pubitemid 34111252)
23. Kevan, P. G., W. A. Straver, M. Offer, and T. M. Laverty. 1991. Pollination of greenhouse tomatoes by bumble bees in Ontario. Proc. Entomol. Soc. Ont. 122: 15-19.
24. Kevan, P. G., E. Cooper, A. Morse, J. P. Kapongo, L. Shipp, and S. Khosla. 2009. Measuring foraging activity in bumblebee nests: A simple nest-entrance trip recorder. J. Appl. Entomol. 133: 222-228.
25. Kulahci, I. G., A. Dornhaus, and D. R. Papaj. 2008. Multimodal signals enhance decision making in foraging bumble-bees. Proc. R. Soc. B. 275: 797-802. (Pubitemid 351252808)
26. Kunze, J., and A. Gumbert. 2001. The combined effect of color and odor on ower choice behavior of bumble bees in ower mimicry systems. Behav. Ecol. 12: 447-456. (Pubitemid 32632083)
27. Kwon, Y. J., and S. Saeed. 2003. Effect of temperature on the foraging activity of Bombus terrestris L. (Hymenoptera: Apidae) on greenhouse hot pepper (Capsicum annuum L.). Appl. Entomol. Zool. 38: 275-280. (Pubitemid 37365074)
28. Laloi, D., and M. H. Pham-Delegue. 2004. Bumble bees show asymmetrical discrimination between two odors in a classical conditioning procedure. J. Insect Behav. 17: 385-396. (Pubitemid 38871861)
29. Lucia, A., S. Licastro, E. Zerba, and H. Masuh. 2008. Yield, chemical composition, and bioactivity of essential oils from 12 species of Eucalyptus on Aedes aegypti larvae. Entomol. Exp. Appl. 129: 107-114.
30. Lunau, K. 1992. Innate recognition of owers by bumble bees -Orientation of antennae to visual stamen signals. Can. J. Zool. 70: 2139-2144. (Pubitemid 23400463)
31. Maes, K., and P. C. Debergh. 2003. Volatiles emitted from in-vitro grown tomato shoots during abiotic and biotic stress. Plant Cell Tissue Organ Cult. 75: 73-78. (Pubitemid 36946806)
32. Morandin, L. A., T. M. Laverty, and P. G. Kevan. 2001a. Bumble bee (Hymenoptera: Apidae) activity and pollination levels in commercial tomato greenhouses. J. Econ. Entomol. 94: 462-467. (Pubitemid 33749936)
33. Morandin, L. A., T. M. Laverty, P. G. Kevan, S. Khosla, and L. Shipp. 2001b. Bumble bee (Hymenoptera: Apidae) activity and loss in commercial tomato greenhouses. Can. Entomol. 133: 883-893. (Pubitemid 34067568)
34. Muhlemann, J. K., M. O. Waelti, A. Widmer, and F. P. Schiestl. 2006. Postpollination changes in oral odor in Silene latifolia: Adaptive mechanisms for seed-predator avoidance? J. Chem. Ecol. 32: 1855-1860. (Pubitemid 44221422)
35. Ndiege, I. O., W. J. Budenberg, D. O. Otieno, and A. Hassanali. 1996. 1,8-cineole: An attractant for the banana weevil, Cosmopolites sordidus. Phytochemistry 42: 369-371. (Pubitemid 126655034)
36. Negre, F., C. M. Kish, J. Boatright, B. Underwood, K. Shibuya, C. Wagner, D. G. Clark, and N. Dudareva. 2003. Regulation of methylbenzoate emission after pollination in snapdragon and petunia owers. Plant Cell. 15: 2992-3006. (Pubitemid 37546266)
37. Ngoh, S. P., L.E.W. Choo, F. Y. Pang, Y. Huang, M. R. Kini, and S. H. Ho. 1998. Insecticidal and repellent properties of nine volatile constituents of essential oils against the American cockroach, Periplaneta americana (L.). Pestic. Sci. 54: 261-268. (Pubitemid 28504258)
38. [OMAFRA]Ontario Ministry of Agriculture Food and Rural Affairs. 1998. Growing greenhouse vegetables. Ministry of Agriculture Food and Rural Affairs, Toronto, Canada.
39. Omura, H., K. Honda, and N. Hayashi. 2000. Floral scent of Osmanthus fragrans discourages foraging behavior of cabbage buttery, Pieris rapae. J. Chem. Ecol. 26: 655-666. (Pubitemid 30176790)
40. Palma, G., J.J.G. Quezada-Eua'n, V. Reyes-Oregel, V. Mele'ndez, and H. Moo-Vale. 2008. Production of greenhouse tomatoes (Lycopersicon esculentum) using Nannotrigona perilampoides, Bombus impatiens and mechanical vibration (Hym.: Apoidea). J. Appl. Entomol. 132: 79-85.
41. Pare, P. W., and J. H. Tumlinson. 1997. De novo biosynthesis of volatiles induced by insect herbivory in cotton plants. Plant Physiol. 114: 1161-1167. (Pubitemid 28382277)
42. Pellmyr, O., and L. B. Thien. 1986. Insect reproduction and oral fragrances: Keys to the evolution of the angiosperms? Taxon 35: 76-85.
43. Pellmyr, O., W. Tang, I. Groth, G. Bergstrom, and L. B. Thien. 1991. Cycad cone and angiosperm oral volatiles: Inferences for the evolution of insect pollination. Biochem. Syst. Ecol. 19: 623-627.
44. Plowright, R. C., and T. M. Laverty. 1987. Bumblebees and crop pollination in Ontario. P. Entomol. Soc. Ont. 118: 155-160.
45. Regnault-Roger, C., and A. Hamraoui. 1995. Fumigant toxic activity and reproductive inhibition induced by monoterpenes on Acanthoscelides obtectus (Say) (Coleoptera), a bruchid of kidney bean (Phaseolus vulgaris L). J. Stored Prod. Res. 31: 291-299.
46. Rodriguez, E., and D. A. Levin. 1976. Biochemical parallelisms of repellents and attractants in higher plants and arthropods, pp. 214-270. In J. W. Wallace and R. L. Mansell (eds.), Biochemical interaction between plants and insects, vol. 10. Plenum, New York.
47. Sabara, H. A., and M. L. Winston. 2003. Managing honey bees (Hymenoptera: Apidae) for greenhouse tomato pollination. J. Econ. Entomol. 96: 547-554. (Pubitemid 37418010)
48. Sagae, M., N. Oyama-Okubo, T. Ando, E. Marchesi, and M. Nakayama. 2008. Effect of temperature on the oral scent emission and endogenous volatile profile of Petunia axillaris. Biosci. Biotechnol. Biochem. 72: 110-115. (Pubitemid 351158946)
49. Sato, S., and M. M. Peet. 2005. Effects of moderately elevated temperature stress on the timing of pollen release and its germination in tomato (Lycopersicon esculentum Mill.). J. Hortic. Sci. Biotech. 80: 23-28.
50. Schearer, W. R. 1984. Components of oil of tansy (Tanacetum vulgare) that repel Colorado potato beetles (Leptinotarsa decemlineata). J. Nat. Prod. 47: 964-969. (Pubitemid 15174357)
51. Schiestl, F. P., M. Ayasse, H. F. Paulus, D. Erdmann, and W. Francke. 1997. Variation of oral scent emission and postpollination changes in individual owers of Ophrys sphegodes subsp. sphegodes. J. Chem. Ecol. 23: 2881-2895. (Pubitemid 28031047)
52. Theis, N., M. Lerdau, and R. A. Raguso. 2007. The challenge of attracting pollinators while evading oral herbivores: Patterns of fragrance emission in Cirsium arvense and Cirsium repandum (Asteraceae). Int. J. Plant Sci. 168: 587-601. (Pubitemid 46849380)
53. Tollsten, L. 1993. A multivariate approach to postpollination changes in the oral scent of Platanthera bifolia (Orchidaceae). Nord. J. Bot. 13: 495-499. (Pubitemid 2015891)
54. Velthuis, H.H.W., and A. van Doorn. 2006. A century of advances in bumblebee domestication and the economic and environmental aspects of its commercialization for pollination. Apidologie 37: 421-451. (Pubitemid 44049578)
55. Werner, R. A. 1995. Toxicity and repellency of 4 allylanisole and monoterpenes from white spruce and tamarack to the spruce beetle and eastern larch beetle (Coleoptera, Scolytidae). Environ. Entomol. 24: 372-379. (Pubitemid 26451617)
56. Whittington, R., and M. L. Winston. 2003. Are bumble bee colonies in tomato greenhouses obtaining adequate nutrition? Can. Entomol. 135: 883-892. (Pubitemid 38192356)
57. Whittington, R., M. L. Winston, C. Tucker, and A. L. Parachnowitsch. 2004. Plant-species identity of pollen collected by bumblebees placed in greenhouses for tomato pollination. Can. J. Plant Sci. 84: 599-602. (Pubitemid 38991570)