Variation in highbush blueberry floral volatile profiles as a function of pollination status, cultivar, time of day and flower part: Implications for flower visitation by bees

Annals of Botany

Volumn 107, Issue 8, 2011, Pages 1377-1390

  Rodriguez Saona, Cesar ^a   Parra, Leonardo ^b   Quiroz, Andrés ^b   Isaacs, Rufus ^c  

^a RUTGERS UNIVERSITY   (United States)

^b UNIVERSIDAD DE LA FRONTERA   (Chile)

^c MICHIGAN STATE UNIVERSITY   (United States)

Author keywords

bumble bees; diurnal rhythm; honey bees; nectar production; site of emission; Vaccinium corymbosum; volatile organic compounds

Indexed keywords

CINNAMYL ALCOHOL; PROPANOL; VOLATILE ORGANIC COMPOUND;

CROP PRODUCTION; CULTIVAR; DICOTYLEDON; DIURNAL ACTIVITY; FLOWER VISITING; HONEYBEE; NECTAR; POLLINATION; POLLINATOR; VOLATILE ORGANIC COMPOUND;

ANIMAL; ANIMAL BEHAVIOR; ARTICLE; BEE; BIOSYNTHESIS; BLUEBERRY; CHEMISTRY; CIRCADIAN RHYTHM; FLOWER; HISTOLOGY; METABOLISM; NECTAR; ODOR; PHYSIOLOGY; POLLINATION; PRINCIPAL COMPONENT ANALYSIS;

ANIMALS; BEES; BEHAVIOR, ANIMAL; BLUEBERRY PLANT; CIRCADIAN RHYTHM; FLOWERS; ODORS; PLANT NECTAR; POLLINATION; PRINCIPAL COMPONENT ANALYSIS; PROPANOLS; VOLATILE ORGANIC COMPOUNDS;

APIS MELLIFERA; APOIDEA; BOMBUS (GENUS); VACCINIUM; VACCINIUM CORYMBOSUM;

EID: 79957826738     PISSN: 03057364     EISSN: 10958290     Source Type: Journal    
DOI: 10.1093/aob/mcr077     Document Type: Article

References (61)

1. Andrews ES, Theis N, Adler LS. 2007. Pollinator and herbivore attraction to Cucurbita floral volatiles. Journal of Chemical Ecology 33: 1682-1691. (Pubitemid 47414536)
2. Attri LK, Nayyar H, Bhanwra RK, Vij SP. 2007. Post-pollination related biochemical changes in floral organs of Rhynchostylis retusa (L.) Bl. and Aerides multiflora Roxb. (Orchidaceae). Journal of Plant Biology 50: 548-556. (Pubitemid 350189184)
3. Ayasse M. 2006. Floral scent and pollinator attraction in sexually deceptive orchids. In: Dudareva N, Pichersky E. eds. Biology of floral scent. Boca Raton, FL: CRC Press, 219-241.
4. Bergström G, Dobson HEM, Groth I. 1995. Spatial fragrance patterns within the flowers of Ranunculus acris (Ranunculaceae). Plant Systematics and Evolution 195: 221-242.
5. Blight MM, Le Métayer M, Pham Delegue M-H, Pickett JA, Marion-Poll F, Wadhams LJ. 1997. Identification of floral volatiles involved in recognition of oilseed rape flowers, Brassica napus, by honeybees, Apis mel-lifera. Journal of Chemical Ecology 23: 1715-1727. (Pubitemid 27347640)
6. Buchmann SL. 1983. Buzz pollination in angiosperms. In: Jones CE, Little RJ. eds. Handbook of experimental pollination biology. New York, NY: Scientific and Academic Editions, 73-113.
7. Burger H, Dötterl S, Ayasse M. 2010. Host-plant finding and recognition by visual and olfactory floral cues in an oligolectic bee. Functional Ecology 24: 1234-1240.
8. Chang JF, Benedict JH, Payne TL, Camp BJ. 1988. Volatile monoterpenes collected from the air surrounding flower buds of seven cotton genotypes. Crop Science 28: 685-688.
9. Dobson HEM. 2006. Relationship between floral fragrance and type of pollinator. In: Dudareva N, Pichersky E. eds. Biology of floral scent. Boca Raton, FL: CRC Press, 147-198.
10. Dobson HE, Bergström G, Groth I. 1990. Difference in fragrance chemistry between flower parts of Rosa rugosa Thunb. (Rosaceae). Israel Journal of Botany 39: 143-156.
11. Dobson HE, Groth I, Bergström G. 1996. Pollen advertisement: chemical contrasts between whole-flower and pollen odors. American Journal of Botany 83: 877-885. (Pubitemid 26311499)
12. Dötterl S, Vereecken NJ. 2010. The chemical ecology and evolution of bee- flower interactions: a review and perspectives. Canadian Journal of Zoology 88: 668-697.
13. Dudareva N, Pichersky E. 2006. Floral scent metabolic pathways: their regulation and evolution. In: Dudareva N, Pichersky E. eds. Biology of floral scent. Boca Raton, FL: CRC Press, 55-78.
14. Dudareva N, Murfitt LM, Mann CJ, et al. 2000. Developmental regulation of methyl benzoate biosynthesis and emission in snapdragon flowers. The Plant Cell 12: 949-961. (Pubitemid 30458039)
15. Effmert U, Grosse J, Röse USR, Ehrig F, Kägi R, Piechulla B. 2005. Volatile composition, emission pattern, and localization of floral scent emission in Mirabilis jalapa (Nyctaginaceae). American Journal of Botany 92: 2-12. (Pubitemid 40113101)
16. Giurfa M, Núñez JA. 1992. Honeybees mark with scent and reject recently visited flowers. Oecologia 89: 113-117.
17. Gori D. 1983. Post-pollination phenomena and adaptive floral changes. In: Jones CE, Little RJ. eds. Handbook of experimental pollination biology. New York, NY: Scientific and Academic Editions, 31-49.
18. Goulson D, Chapman JW, Hughes WHO. 2001. Discrimination of unrewarding flowers by bees: direct detection of rewards and use of repellent scent marks. Journal of Insect Behavior 14: 669-677.
19. Harder LD. 1990. Behavioral responses by bumblebees to variation in pollen availability. Oecologia 85: 41-47.
20. Hare JD. 2011. Ecological role of volatiles produced by plants in response to damage by herbivorous insects. Annual Review of Entomology 56: 161-180.
21. Hoballah ME, Stuurman J, Turlings TCJ, Guerin PM, Connétable S, Kuhlemeier C. 2005. The composition and timing of flower odour emission by wild Petunia axillaris coincide with the antennal perception and nocturnal activity of the pollinator Manduca sexta. Planta 222: 141-150. (Pubitemid 41429410)
22. Howell A, Alarcón R. 2007. Osmia bees (Hymenoptera: Megachilidae) can detect nectar-rewarding flowers using olfactory cues. Animal Behaviour 74: 199-205. (Pubitemid 47247636)
23. Isaacs R, Kirk AK. 2010. Pollination services provided to small and large highbush blueberry fields by wild and managed bees. Journal of Applied Ecology 47: 841-849.
24. Kessler A, Halitschke R. 2009. Testing the potential for conflicting selection on floral chemical traits by pollinators and herbivores: predictions and case study. Functional Ecology 23: 901-912.
25. Knudsen JT, Gershenzon J. 2006. The chemical diversity of floral scent. In: Dudareva N, Pichersky E. eds. Biology of floral scent. Boca Raton, FL: CRC Press, 27-52.
26. Knudsen JT, Eriksson R, Gershenzon J, Sta?hl B. 2006. Diversity and distribution of floral scent. The Botanical Review 72: 1-120.
27. Komischke BM, Guirfa M, Lachnit H, Malun D. 2002. Successive olfactory reversal learning in honeybees. Learning and Memory 9: 122-129. (Pubitemid 34666084)
28. Loughrin JH, Hamilton-Kemp TR, Andersen RA, Hildebrand DF. 1990. Volatiles from flowers of Nicotiana sylvestris, N. otophora and Malus×domestica: headspace components and day/night changes in their relative concentrations. Phytochemistry 29: 2473-2477.
29. Luyt R, Johnson SD. 2002. Postpollination nectar reabsorption and its implications for fruit quality in an epiphytic orchid. Biotropica 34: 442-446. (Pubitemid 36171639)
30. MacKenzie K. 2009. Pollination practices and the use of bees in Vaccinium crops. Acta Horticulturae 810: 527-538.
31. Menzel R. 1993. Associative learning in honey bees. Apidologie 24: 157-168. (Pubitemid 24414929)
32. Menzel R, Müller U. 1996. Learning and memory in honeybees: from behavior to neural substrates. Annual Review of Neuroscience 19: 379-404. (Pubitemid 26080833)
33. Michener CD. 2000. The bees of the world. Baltimore, MD: Johns Hopkins University Press.
34. Moore D, Siegfried D, Wilson R, Rankin MA. 1989. The influence of time of day on the foraging behavior of the honeybee, Apis mellifera. Journal of Biological Rhythms 4: 305-325.
35. Moya S, Ackerman JD. 1993. Variation in the floral fragrance of Epidendrum ciliare (Orchidaceae). Nordic Journal of Botany 13: 41-47.
36. Pham-Delegue MH, Etievant P, Guichard E, Masson C. 1989. Sunflower volatiles involved in honeybee discrimination among genotypes and flowering stages. Journal of Chemical Ecology 15: 329-343.
37. Pichersky E, Gershenzon J. 2002. The formation and function of plant vola-tiles: perfumes for pollinator attraction and defense. Current Opinion in Plant Biology 5: 237-243. (Pubitemid 34452071)
38. Pichersky E, Raguso RA, Lewinsohn E, Croteau R. 1994. Floral scent production in Clarkia (Onagraceae). I. Localization and developmental modulation of monoterpene emission and linalool synthase activity. Plant Physiology 106: 1533-1540. (Pubitemid 24986582)
39. Raguso RA. 2008. Wake up and smell the roses: the ecology and evolution of floral scent. Annual Review of Ecology, Evolution and Systematics 39: 549-569.
40. Rao S, Stephen WP, White L. 2009. Native bee pollinator diversity in Oregon blueberries. Acta Horticulturae 810: 539-548.
41. Rodriguez-Saona C, Rodriguez-Saona L, Frost C. 2009. Herbivore-induced volatiles in the perennial shrub, Vaccinium corymbosum, and their role in inter-branch signaling. Journal of Chemical Ecology 35: 163-175.
42. Scheiner SM. 2001. MANOVA: multiple response variables and multispecies interactions. In: Scheiner SM, Gurevitch J. eds. Design and analysis of ecological experiments, 2nd edn. New York, NY: Oxford University Press, 99-155.
43. Schiestl FP. 2010. The evolution of floral scent and insect chemical communication. Ecology Letters 13: 643-656.
44. Schiestl FP, Ayasse M. 2001. Post-pollination emission of a repellent compound in a sexually deceptive orchid: a new mechanism for maximizing reproductive success? Oecologia 126: 531-534. (Pubitemid 32442691)
45. Schiestl FP, Ayasse M, Paulis HF, Erdmann D, Franke W. 1997. Variation of floral scent emission and postpollination changes in individual flowers of Ophrys sphegodes subsp. sphegodes. Journal of Chemical Ecology 23: 2881-2895. (Pubitemid 28031047)
46. Seeley TD. 1989. Social foraging in honey bees: how nectar foragers assess their colony's nutritional status. Behavioral Ecology and Sociobiology 24: 181-199.
47. Simpson BB, Neff JL. 1983. Evolution and diversity of floral rewards. In: Jones CE, Little RJ. eds. Handbook of experimental pollination biology. New York, NY: Scientific and Academic Editions, 142-159.
48. Smith BH, Getz WM. 1994. Nonpheromonal olfactory processing in insects. Annual Review of Entomology 39: 351-375.
49. Stout JC, Goulson D. 2002. The influence of nectar secretion rates on the responses of bumblebees (Bombus spp.) to previously visited flowers. Behavioral Ecology and Sociobiology 52: 239-246. (Pubitemid 36064233)
50. Strik BC, Yarborough D. 2005. Blueberry production trends in North America, 1992 to 2003, and predictions for growth. HortTechnology 15: 391-398. (Pubitemid 40428662)
51. Szendrei Z, Malo E, Stelinski L, Rodriguez-Saona C. 2009. Response of cranberry weevil (Anthonomus musculus Say, Coleoptera: Curculionidae) to host plant volatiles. Environmental Entomology 38: 861-869.
52. Theis N, Raguso RA. 2005. The effect of pollination on floral fragrance in thistles. Journal of Chemical Ecology 31: 2581-2600. (Pubitemid 41599763)
53. Tholl D, Röse USR. 2006. Detection and identification of floral scent compounds. In: Dudareva N, Pichersky E. eds. Biology of floral scent. Boca Raton, FL: CRC Press, 3-25.
54. Tollsten L. 1993. A multivariate approach to post-pollination changes in the floral scent of Platanthera bifolia (Orchidaceae). Nordic Journal of Botany 13: 495-499. (Pubitemid 2015891)
55. Tollsten L, Bergström J. 1989. Variation and post-pollination changes in floral odours released by Planthera bifolia (Orchidaceae). Nordic Journal of Botany 9: 359-362.
56. Tuell JK, Ascher JS, Isaacs R. 2009. Wild bees (Hymenoptera: Apoidea: Anthophila) of the Michigan highbush blueberry agroecosystem. Annals of the Entomological Society of America 102: 275-287.
57. Weatherwax PB. 1986. Why do honeybees reject certain flowers? Oecologia 69: 567-570.
58. West TP, McCutcheon TW. 2009. Evaluating Osmia cornifrons as pollinators of highbush blueberry. International Journal of Fruit Science 9: 115-125.
59. Williams CS. 1998. The identity of the previous visitor influences flower rejection by nectar-collecting bees. Animal Behaviour 56: 673-681. (Pubitemid 28463575)
60. Willmer P, Stanley DA, Steijven K, Matthews IM, Nuttman CV. 2009. Bidirectional flower color and shape changes allow a second opportunity for pollination. Current Biology 19: 919-923.
61. Wright GA, Smith BH. 2004. Different thresholds for detection and discrimination of odors in the honey bee (Apis mellifera). Chemical Senses 29: 127-135. (Pubitemid 41288979)