Does facilitating pollinator learning impede deceptive orchid attractiveness? A multi-approach test of avoidance learning

Plant Biology

Volumn 13, Issue 4, 2011, Pages 570-575

  Juillet, N ^a,b   Salzmann, C C ^c   Scopece, G ^a  

^a UNIVERSITY OF NAPLES FEDERICO II   (Italy)

^b Office de l'Environnement de la Corse ^*  (France)

^c ETH ZURICH   (Switzerland)

Author keywords

Anisaldehyde; Floral trait polymorphism; Food deception; Pollinator behaviour; Relaxed selection; Scent addition

Indexed keywords

4 ANISALDEHYDE; 4-ANISALDEHYDE; BENZALDEHYDE DERIVATIVE;

AVOIDANCE REACTION; BEE; BEHAVIORAL ECOLOGY; FLORAL TRAIT; MONOCOTYLEDON; NECTAR; ORGANIC COMPOUND; POLLINATOR; POLYMORPHISM; REPRODUCTIVE SUCCESS;

ANIMAL; ANIMAL BEHAVIOR; ARTICLE; AVOIDANCE BEHAVIOR; BEE; DECEPTION; INFLORESCENCE; ODOR; ORCHIDACEAE; PHENOTYPE; PHYSIOLOGY; POLLINATION; REPRODUCTION;

ANIMALS; AVOIDANCE LEARNING; BEES; BEHAVIOR, ANIMAL; BENZALDEHYDES; DECEPTION; INFLORESCENCE; ODORS; ORCHIDACEAE; PHENOTYPE; POLLINATION; REPRODUCTION;

ANACAMPTIS CORIOPHORA; ANACAMPTIS MORIO; ORCHIDACEAE;

EID: 79958839762     PISSN: 14358603     EISSN: 14388677     Source Type: Journal    
DOI: 10.1111/j.1438-8677.2010.00421.x     Document Type: Article

References (45)

1. Ackerman J.D. (1986) Mechanisms and evolution of food-deceptive pollination systems in orchids. Lindleyana, 1, 108-113.
2. Ackerman J.D., Galarza-Pérez M. (1991) Patterns and maintenance of extraordinary variation in the Caribbean orchid, Tolumnia (Oncidium) variegata. Systematic Botany, 16, 182-194.
3. Aragón S., Ackerman J.D. (2004) Does flower colour variation matter in deception pollinated Psychilis monensis (Orchidaceae)? Oecologia, 138, 332-338.
4. Bateman R.M., Hollingsworth P.M., Preston J., Yi-Bo L., Pridgeon A.M., Chase M.W. (2003) Molecular phylogenetics and evolution of Orchidinae and selected Habenariinae (Orchidaceae). Botanical Journal of the Linnean Society, 142, 1-40.
5. Chase M.W., Freudenstein J.F., Cameron K.M. (2003) DNA data and Orchidaceae systematics: a new phylogenetic classification. In: Dixon K.W., Kell S.P., Barrett R.L., Cribb P.J. (Eds), Orchid conservation. Natural History Publications, Kota Kinabalu, Sabah, pp. 69-89.
6. Chittka L., Thomson J.D. (2001) Cognitive ecology of pollination. Animal behaviour and floral evolution. Cambridge University Press, Cambridge, UK.
7. van der Cingel N.A. (1995) An atlas of orchid pollination: European orchids. A.A. Balkema, Rotterdam, The Netherlands.
8. Cozzolino S., Schiestl F.P., Müller A., De Castro O., Nardella A.M., Widmer A. (2005) Evidence for pollinator sharing in Mediterranean nectar-mimic orchids: Absence of premating barriers? Proceedings of the Royal Society B-Biological Sciences, 272, 1271-1278.
9. Cunningham J.P., Moore C.J., Zalucki M.P., West S.A. (2004) Learning, odour preferences and flower foraging in moths. Journal of Experimental Biology, 207, 87-94.
10. Dafni A. (1987) Pollination in Orchis and related genera: Evolution from reward to deception. In: Arditti J. (Ed), Orchid biology: reviews and perspectives, Vol. IV. Cornell University Press, Ithaca, NY, USA, pp. 80-104.
11. Dafni A., Ivri Y. (1979) Pollination ecology of, and hybridization between, Orchis coriophora L. and O. collina Sol. Ex Russ. (Orchidaceae) in Israel. New Phytologist, 83, 181-187.
12. Delforge P. (2001) Guide des Orchidées d'Europe, d'Afrique du Nord et du Proche-Orient, 2ème édn. Delachaux et Niestlé, Lausanne, Switzerland.
13. Dukas R., Real L.A. (1993) Learning constraints and floral choice behaviour in bumble bees. Animal Behaviour, 46, 637-644.
14. Gumbert A. (2000) Color choices by bumble bees (Bombus terrestris): innate preferences and generalization after learning. Behavioral Ecology and Sociobiology, 48, 36-43.
15. Heinrich B. (1975) Bee flowers: a hypothesis on flower variety and blooming times. Evolution, 29, 325-334.
16. Heinrich B. (1979) "Majoring" and "minoring" by foraging bumblebees, Bombus vagans: an experimental analysis. Ecology, 60, 245-255.
17. Jersáková J., Johnson S.D., Kindlmann P. (2006) Mechanisms and evolution of deceptive pollination in orchids. Biological Reviews, 81, 219-235.
18. Johnson S.D., Nilsson L.A. (1999) Pollen carryover, geitonogamy, and the evolution of deceptive pollination systems in orchids. Ecology, 80, 2607-2619.
19. Johnson S.D., Peter C.I., Ågren J. (2004) The effects of nectar addition on pollen removal and geitonogamy in the non-rewarding orchid Anacamptis morio. Proceedings of the Royal Society B-Biological Sciences, 271, 803-809.
20. Juillet N., Scopece G. (2010) Does floral trait variability enhance reproductive success in deceptive orchids? Perspectives in Plant Ecology, Evolution and Systematics, 12, 317-322.
21. Manly B.F.J. (1997) Randomization, bootstrap and Monte Carlo methods in biology. Chapman & Hall, London, UK.
22. Menzel R., Greggers U. (1992) Temporal dynamics and foraging behaviour in honeybees. In: Billen J. (Ed), Biology and evolution of social insects. Leuven University Press, Leuven, Belgium, pp. 303-318.
23. Moccia M.D., Widmer A., Cozzolino S. (2007) The strength of reproductive isolation in two food deceptive orchids species. Molecular Ecology, 16, 2855-2866.
24. Moya S., Ackerman J.D. (1993) Variation in the floral fragrance of Epidendrum ciliare (Orchidaceae). Nordic Journal of Botany, 13, 41-47.
25. Nilsson L.A. (1980) The pollination ecology of Dactylorhiza sambucina (Orchidaceae). Botaniska Notiser, 133, 367-385.
26. Nilsson L.A. (1984) Anthecology of Orchis morio at its outpost in the north. Nova acta Regiae Societatis Scientiarum Upsaliensis, 5, 167-179.
27. Nilsson L.A. (1992) Orchid pollination biology. Trends in Ecology and Evolution, 7, 255-259.
28. R Development Core Team (2005) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. []
29. Raguso R.A. (2008) Wake up and smell the roses: the ecology and evolution of floral scent. Annual Reviews in Evolution, Ecology and Systematics, 39, 49-69.
30. Raine N.E., Chittka L. (2007) Flower constancy and memory dynamics in bumblebees (Hymenoptera: Apidae: Bombus). Entomologia Generalis, 29, 179-199.
31. Renner S.S. (2006) Rewardless flowers in the Angiosperms and the role of insect cognition in their evolution. In: Waser N.M., Ollerton J. (Eds), Plant-pollinator interactions: from specialization to generalization. University of Chicago Press, Chicago, USA, pp. 123-144.
32. Renner M.A., Nieh J.C. (2008) Bumblebee olfactory information flow and contact-based foraging activation. Insectes Sociaux, 55, 417-424.
33. Riveros A.J., Gronenberg W. (2009) Olfactory learning and memory in the bumblebee Bombus occidentalis. Naturwissenschaften, 96, 851-856.
34. Salzmann C.C., Cozzolino S., Schiestl F.P. (2007a) Floral scent in food-deceptive orchids: species specificity and sources of variability. Plant Biology, 9, 720-729.
35. Salzmann C.C., Nardella A.M., Cozzolino S., Schiestl F.P. (2007b) Variability in floral scent in rewarding and deceptive orchids: the signature of pollinator-imposed selection? Annals of Botany, 100, 757-765.
36. Scopece G., Juillet N., Müller A., Schiestl F.P., Cozzolino S. (2009) Pollinator attraction in Anacamptis papilionacea (Orchidaceae): a food or a sex promise? Plant Species Biology, 24, 109-114.
37. Smithson A. (2002) The consequences of rewardlessness in orchids: reward-supplementation experiments with Anacamptis morio (Orchidaceae). American Journal of Botany, 89, 1579-1587.
38. Smithson A., Gigord L.D.B. (2003) The evolution of empty flowers revisited. American Naturalist, 161, 537-552.
39. Smithson A., Macnair M.R. (1997) Negative frequency-dependent selection by pollinators on artificial flowers without rewards. Evolution, 51, 715-723.
40. Smithson A., Juillet N., Macnair M.R., Gigord L.D.B. (2007) Do rewardless orchids show a positive relationship between phenotypic diversity and reproductive success? Ecology, 88, 434-442.
41. Sprengel C.K. (1793) Das Entdeckte Geheimnis in der Natur im Bau und in der Befruchtung der Blumen. Bei Friedrich Vieweg dem aeltern, Berlin, Germany.
42. Tremblay R.L., Ackerman J.D., Zimmerman J.K., Calvo R.N. (2005) Variation in sexual reproduction in orchids: a spasmodic journey to diversification. Biological Journal of the Linnean Society, 84, 1-54.
43. Waser N.M. (1986) Flower constancy: definition, cause, and measurement. American Naturalist, 127, 593-603.
44. Wright G.A., Schiestl F.P. (2009) The evolution of floral scent: the influence of olfactory learning by insect pollinators on the honest signalling of floral rewards. Functional Ecology, 23, 841-851.
45. Yokoi T., Fujisaki K. (2009) Recognition of scent marks in solitary bees to avoid previously visited flowers. Ecological Research, 24, 803-809.