Look and touch: Multimodal sensory control of flower inspection movements in the nocturnal hawkmoth Manduca sexta

Journal of Experimental Biology

Volumn 213, Issue 21, 2010, Pages 3676-3682

  Goyret, Joaquín ^a  

^a LUND UNIVERSITY   (Sweden)

Author keywords

Flower handling; Lepidoptera; Mechanoreception; Nectar guides; Pollinator; Sensory ecology

Indexed keywords

ANIMAL; ARTICLE; BIOLOGICAL MODEL; DARKNESS; FEEDING BEHAVIOR; FEMALE; FLOWER; HISTOLOGY; LEPIDOPTERA; MALE; MOVEMENT (PHYSIOLOGY); PHYSIOLOGY; SENSE ORGAN; TIME; TOUCH; VISION;

ANIMALS; DARKNESS; FEEDING BEHAVIOR; FEMALE; FLOWERS; MALE; MANDUCA; MODELS, BIOLOGICAL; MOVEMENT; SENSE ORGANS; TIME FACTORS; TOUCH; VISUAL PERCEPTION;

HEXAPODA; LEPIDOPTERA; MANDUCA SEXTA;

EID: 78149336349     PISSN: 00220949     EISSN: None     Source Type: Journal    
DOI: 10.1242/jeb.045831     Document Type: Article

References (49)

1. Andersson, S. and Dobson, H. E. M. (2003). Behavioral foraging responses by the butterfly Heliconius melpomene to Lantana camara floral scent. J. Chem. Ecol. 29, 2303-2318.
2. Baerends, J. P. (1950). Specializations of organs and movements with releasing function. In Physiological Mechanisms in Animal Behaviour, vol. 4 (eds J. F. Danirelli and R. Brown), pp. 337-360. Academic Press Inc.
3. Baker, H. G. (1961). The adaptation of flowering plants to nocturnal and crepuscular pollinators. Q. Rev. Biol. 36, 64-73.
4. Bell, R. A. and Joachim, F. G. (1976). Techniques for rearing laboratory colonies of tobacco hornworms and pink bollworms Lepidoptera-Sphingidae- Gelechiidae. Ann. Entomol. Soc. Am. 69, 365-373.
5. Benitez-Vieyra, S., Medina, A. M., Glinos, E. and Cocucci, A. A. (2006). Pollinatormediated selection on floral traits and size of floral display in Cyclopogon elatus, a sweat bee-pollinated orchid. Funct. Ecol. 20, 948-957.
6. Bolwig, N. (1954). The role of scent as a nectar guide for honeybees on flowers and an observation of the effect of colour on recruits. Br. J. Anim. Behav. 2, 81-83.
7. Brantjes, N. B. M. (1973). Sphingophilous flowers, function of their scent. In Pollination and Dispersal (ed. N. B. M. Brantjes and H. F. Linskens), pp. 24-46. Nijmegen: Publishing Department Botany.
8. Brantjes, N. B. M. (1976). Senses involved in the visiting of flowers by Cucullia umbratica (Noctuidae, Lepidoptera). Entomol. Exp. Appl. 20, 1-7.
9. Brantjes, N. B. M. (1978). Sensory responses to flowers in night-flying moths. In The Pollination of Flowers by Insects (ed. A. J. Richards), pp. 13-19. London: Academic Press.
10. Campbell, D. R., Waser, N. M. and Pederson, G. T. (2002). Predicting patterns of mating and potential hybridization from pollinator behavior. Am. Nat. 159, 438-450.
11. Craig, W. (1918). Appetites and aversions as constituents of instincts. Biol. Bull. 91-107.
12. Cutler, D. E., Bennett, R. R., Stevenson, R. D. and White, R. H. (1995). Feedingbehavior in the nocturnal moth Manduca Sexta is mediated mainly by blue receptors, but where are they located in the retina. J. Exp. Biol. 198, 1909-1917.
13. Darwin, C. (1876). The Effects of Cross- and Self-fertilization in the Vegetable Kingdom. London: Murray.
14. Daumer, K. (1958). Blumenfarben, wie sie die bienen sehen. Zeitschrift Fur Vergleichende Physiologie 41, 49-110.
15. Free, J. B. (1970). Effect of flower shapes and nectar guides on the behaviour of foraging honeybees. Behaviour 37, 269-285.
16. Gegear, R. J. (2005). Multicomponent floral signals elicit selective foraging in bumblebees. Naturwissenschaften 92, 269-271.
17. Giurfa, M., Vorobyev, M., Kevan, P. and Menzel, R. (1996). Detection of coloured stimuli by honeybees: minimum visual angles and receptor specific contrasts. J. Comp. Physiol. A 178, 699-709.
18. Goyret, J. and Raguso, R. A. (2006). The role of mechanosensory input in flower handling efficiency and learning by Manduca sexta. J. Exp. Biol. 209, 1585-1593.
19. Goyret, J., Markwell, P. M. and Raguso, R. A. (2007). The effect of decoupling olfactory and visual stimuli on the foraging behavior of Manduca sexta. J. Exp. Biol. 210, 1398-1405.
20. Goyret, J., Pfaff, M., Raguso, R. A. and Kelber, A. (2008). Why do Manduca sexta feed from white flowers? Innate and learnt colour preferences in a hawkmoth. Naturwissenschaften 95, 569-576.
21. Goyret, J., Kelber, A., Pfaff, M. and Raguso, R. A. (2009). Flexible responses to visual and olfactory stimuli by foraging Manduca sexta: larval nutrition affects adult behaviour. Proc. R. Soc. Lond. B. Biol. Sci. 276, 2739-2745.
22. Grant, V. (1983). The systematic and geographical-distribution of hawkmoth flowers in the temperate North-American flora. Bot. Gaz. 144, 439-449.
23. Haber, W. A. and Frankie, G. W. (1989). A tropical hawkmoth community - Costa Rican dry forest Sphingidae. Biotropica 21, 155-172.
24. Hebets, E. A. and Papaj, D. R. (2005). Complex signal function: developing a framework of testable hypotheses. Behav. Ecol. Sociobiol. 57, 197-214.
25. Heinrich, B. (1971). Temperature regulation of sphinx moth Manduca sexta. 1. Flight energetics and body temperature during free and tethered flight. J. Exp. Biol. 54, 141-152.
26. Kandori, I. and Ohsaki, N. (1998). Efect of experience on foraging behavior towards artificial nectar guides in the cabbage butterfly, Pieris rapae crucivora (Lepidoptera: Pieridae). Appl. Entomol. Zool. 33, 35-42.
27. Kelber, A. (2002). Pattern discrimination in a hawkmoth: innate preferences, learning performance and ecology. Proc. R. Soc. Lond. B. Biol. Sci. 269, 2573-2577.
28. Kelber, A., Balkenius, A. and Warrant, E. J. (2002). Scotopic colour vision in nocturnal hawkmoths. Nature 419, 922-925.
29. Kevan, P. G. and Lane, M. A. (1985). Flower petal microtexture is a tactile cue for bees. Proc. Natl. Acad. Sci. USA 82, 4750-4752.
30. Lehrer, M., Horridge, G. A., Zhang, S. W. and Gadagkar, R. (1995). Shape vision in bees: innate preferences for flower-like patterns. Philos. Trans. R. Soc. Lond. B. Biol. Sci. 347, 123-137.
31. Lewis, A. C. (1986). Memory constraints and flower choice in Pieris rapae. Science 232, 863-865.
32. Lex, T. (1954). Duftmale und Blüten. Zeitschrift Fur Vergleichende Physiologie 36, 212-234.
33. Lorenz, K. Z. (1973). Behind the Mirror. Orlando, FL: Harcourt Brace Jovanovich.
34. Lunau, K. and Dinkel, T. (2001). How drone flies (Eristalis tenax L., Syrphidae, Diptera) use floral guides to locate food sources. J. Insect Physiol. 47, 1111-1118.
35. Lunau, K., Unseld, K. and Wolter, F. (2009). Visual detection of diminutive floral guides in the bumblebee Bombus terrestris and in the honeybee Apis mellifera. J. Comp. Physiol. A 195, 1121-1130.
36. Mayr, E. (1988). Toward a New Philosophy of Biology: Observations of an Evolutionist. Cambridge, MA: Harvard University Press.
37. Moré, M., Sérsic, A. N. and Cocucci, A. A. (2007). Restriction of pollinator assemblage through flower length and width in three long-tongued hawkmothpollinated species of Mandevilla (Apocynaceae, Apocynoideae). Ann. Mo. Bot. Gard. 94, 485-504.
38. Nattero, J., More, M., Sersic, A. N. and Cocucci, A. A. (2003). Possible tobacco progenitors share long-tongued hawkmoths as pollen vectors. Plant Syst. Evol. 241, 47-54.
39. Nilsson, L. A. (1988). The evolution of flowers with deep corolla tubes. Nature 334, 147-149.
40. Odell, E., Raguso, R. A. and Jones, K. N. (1999). Bumblebee foraging responses to variation in floral scent and color in snapdragons (Antirrhinum: Scrophulariaceae). Am. Midl. Nat. 142, 257-265.
41. Plowright, C. M. S., Simonds, V. M. and Butler, M. A. (2006). How bumblebees first find flowers: Habituation of visual pattern preferences, spontaneous recovery, and dishabituation. Learn. Motiv. 37, 66-78.
42. Raguso, R. A. and Willis, M. A. (2002). Synergy between visual and olfactory cues in nectar feeding by naive hawkmoths Manduca sexta. Anim. Behav. 64, 685-695.
43. Raguso, R. A. and Willis, M. A. (2003). Hawkmoth pollination in Arizona's sonoran desert: behavioral responses to floral traits. In Butterflies: Ecology and Evolution Taking Flight (ed. C. L. Boggs, W. B. Watt and P. R. Ehrlich), pp. 43-66. Chicago: The University of Chicago Press.
44. Raguso, R. A., Henzel, C., Buchmann, S. L. and Nabhan, G. P. (2003). Trumpet flowers of the Sonoran desert: floral biology of Peniocereus cacti and sacred Datura. Int. J. Plant Sci. 164, 877-892.
45. Sokal, R. R. and Rohlf, P. J. (1994). Biometry. San Francisco: Freeman and Company.
46. Sprayberry, J. D. H. and Daniel, T. L. (2007). Flower tracking in hawkmoths: behavior and energetics. J. Exp. Biol. 210, 37-45.
47. Sprengel, C. K. (1793). Das entdeckte Geheimniss der Natur im Bau und in der Befruchtung der Blumen. Berlin: Vieweg. Tinbergen, N. (1950). The hierarchical organization of nervous mechanisms underlying instinctive behaviour. Symp. Soc. Exp. Biol. 4, 305-312.
48. Tinbergen, N. (1958). Curious Naturalists. New York: Basic Books. Wicklein, M. and Strausfeld, N. J. (2000). Organization and significance of neurons that detect change of visual depth in the hawk moth Manduca sexta. J. Comp. Neurol. 424, 356-376.
49. Willis, M. A. and Arbas, E. A. (1991). Odor-modulated upwind flight in Manduca sexta. J. Comp. Physiol. A 169, 427-440.