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Sapromyiophily in the native orchid, Bulbophyllum variegatum, on Réunion (Mascarene Archipelago, Indian Ocean)

Published online by Cambridge University Press:  30 September 2011

Laurence Humeau ,
Claire Micheneau ,
Hans Jacquemyn ,
Anne Gauvin-Bialecki ,
Jacques Fournel  and
Thierry Pailler
Laurence Humeau*
Affiliation:
Université de La Réunion, UMR Peuplements Végétaux et Bio-Agresseurs en Milieu Tropical, Université de La Réunion, 15 avenue René Cassin, 97715 Saint Denis, La Réunion, France
Claire Micheneau
Affiliation:
Université de La Réunion, UMR Peuplements Végétaux et Bio-Agresseurs en Milieu Tropical, Université de La Réunion, 15 avenue René Cassin, 97715 Saint Denis, La Réunion, France Evolutionary Biology and Ecology Unit CP 160/12, Faculté des Sciences, Université Libre de Bruxelles, Av. F.D. Roosevelt 50, B-1050 Brussels, Belgium
Hans Jacquemyn
Affiliation:
Division of Plant Ecology and Systematics, Biology Department, Katholieke Universiteit Leuven, Kasteelpark Arenberg 31, B-3001 Heverlee, Belgium
Anne Gauvin-Bialecki
Affiliation:
Université de La Réunion, Laboratoire de Chimie des Substances Naturelles et des Sciences des Aliments, Université de La Réunion, 15 avenue René Cassin, 97715 Saint Denis, La Réunion, France
Jacques Fournel
Affiliation:
Université de La Réunion, UMR Peuplements Végétaux et Bio-Agresseurs en Milieu Tropical, Université de La Réunion, 15 avenue René Cassin, 97715 Saint Denis, La Réunion, France Herbier Universitaire de La Réunion, Saint Denis, La Réunion, France
Thierry Pailler
Affiliation:
Université de La Réunion, UMR Peuplements Végétaux et Bio-Agresseurs en Milieu Tropical, Université de La Réunion, 15 avenue René Cassin, 97715 Saint Denis, La Réunion, France
*
1Corresponding author. Email: laurence.humeau@univ-reunion.fr
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Abstract:

Orchid species are well known for their highly specialized pollinator interactions. To better understand the reproductive biology of the tropical epiphytic orchid Bulbophyllum variegatum on Réunion, we investigated the floral morphology, breeding system, pollinator diversity, floral scent profile and fruiting success of about 30 individuals in three natural populations during two consecutive flowering seasons. Controlled hand-pollination experiments in two populations showed that the species is self-compatible, but requires pollinator service to achieve reproduction. Videotape pollinator observations were conducted during two flowering seasons for 56 h and revealed that B. variegatum is pollinated by a single species of fly from the Platystomatidae. This fly seems to be attracted by the unpleasant scent produced by the flowers, and does not receive any reward after achieving pollination. In addition, no egg-laying behaviour was observed. Bulbophyllum variegatum thus exhibits a typical sapromyiophilous pollination syndrome which constitutes the first proven case of sapromyiophily within the genus Bulbophyllum on the Mascarene Archipelago. Hand pollinations further showed that fruit set was not significantly higher for flowers that received outcross pollen than for those that were self-crossed (53% and 44% respectively). Fruit sets under natural conditions were significantly different among populations, ranging from 0.5% to 24.3%. This low fruit production is likely due to infrequent pollinator visits, particularly in disturbed forests where the pollinator has never been observed.

Keywords

floral scentfly-pollinationOrchidaceaeself-compatibility
Type
Research Article
Information
Journal of Tropical Ecology , Volume 27 , Issue 6 , November 2011 , pp. 591 - 599
Copyright
Copyright © Cambridge University Press 2011

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References

LITERATURE CITED

ADAMS, R. P. 2001. Identification of essential oil components by gas chromatography/quadrupole mass spectroscopy. Allured Publishing Corporation, Carol Stream. 455 pp.Google Scholar
ARCTANDER, S. 1994. Perfume and flavor chemicals. Volumes I & II. Allured Publishing Corporation, Carol Stream.Google Scholar
BARTAREAU, T. 1994. Pollination of Bulbophyllum macphersonii Rupp by a midge fly (Forcipomyia sauteri). The Orchadian 11:255–258.Google Scholar
BORBA, E. L. & SEMIR, J. 1998. Wind-assisted fly pollination in three Bulbophyllum (Orchidaceae) species occurring in the Brazilian campos rupestres. Lindleyana 13:203–218.Google Scholar
CATLING, P. M. 1990. Auto-pollination in the Orchidaceae. Pp. 121–158 in Arditti, J. (ed.). Orchid biology, reviews and perspectives. V. Timber Press, Portland.Google Scholar
CHEKE, A. S. 1987. An ecological history of the Mascarene Islands, with particular reference to extinctions and introductions of land vertebrates. Pp. 5–89 in Diamond, A. W. (ed.) Studies of Mascarene Island birds. Cambridge University Press, Cambridge.Google Scholar
DA SILVA, U. F., BORBA, E. L., SEMIR, J. & MARSAIOLI, A. J. 1999. A simple solid injection device for the analyses of Bulbophyllum (Orchidaceae) volatiles. Phytochemistry 50:31–34.Google Scholar
DAMON, A. & VALLE-MORA, J. 2008. Retrospective spatial analysis of the pollination of two miniature epiphytic orchids with different pollination strategies in a coffee plantation in Soconusco, Chiapas, Mexico. Biological Journal of the Linnean Society 158:448–459.Google Scholar
DOBSON, H. E. M. 2006. Relationship between floral fragrances composition and type of pollinator. Pp. 147–198 in Dudareva, N. & Pichersky, E. (ed.). Biology of floral scent. CRC Press, Boca Raton.Google Scholar
DRESSLER, R. 1981. The orchids. Natural history and classification. Harvard University Press, Cambridge. 332 pp.Google Scholar
DRESSLER, R. L. 1993. Phylogeny and classification of the orchid family. Dioscorides Press, Portland. 314 pp.Google Scholar
FEINSTEIN, J., PURZYCKI, K., MORI, S., HEQUET, V. & BERKOV, A. 2008. Neotropical soldier flies (Stratiomyidae) reared from Lecythis poiteaui in French Guiana: do bat-pollinated flowers attract saprophiles? Journal of the Torrey Botanical Society 135:200–207.CrossRefGoogle Scholar
FISCHER, G. A., GRAVENDEEL, B., SIEDER, A., ANDRIANTIANA, J., HEISELMAYER, P., CRIBB, P. J., SMIDT, E. DE C., SAMUEL, R. & KIEHN, M. 2007. Evolution of resupination in Malagasy species of Bulbophyllum (Orchidaceae). Molecular Phylogenetics and Evolution 45:358–376.Google Scholar
GIBERNAU, M. 2003. Pollinators and visitors of aroid inflorescences. Aroideana 26:66–83.Google Scholar
HAVENS, K. 1999. Pollination biology: implications for restoring rare plants. Ecological Restoration 17:217–219.Google Scholar
JACQUEMYN, H., MICHENEAU, C., ROBERTS, D. L. & PAILLER, T. 2005. Elevational gradients of species diversity, breeding system and floral traits of orchid species on Réunion Island. Journal of Biogeography 32:1751–1761.Google Scholar
JERSÁKOVÁ, J., JOHNSON, S. & KINDLMANN, P. 2006. Mechanisms and evolution of deceptive pollination in orchids. Biological Reviews 81:219–235.Google Scholar
JOHNSON, S., PETER, C., NILSSON, L. & AGREN, J. 2003. Pollination success in a deceptive orchid is enhanced by co-occurring rewarding magnet plants. Ecology 84:2919–2927.Google Scholar
KEARNS, C., INOUYE, D. & WASER, N. 1998. Endangered mutualisms: the conservation of plant–pollinator interactions. Annual Review of Ecology and Systematics 29:83–112.Google Scholar
KOVATS, E. 1965. Gas chromatographic characterization of organic substances in the Retention Index System. Pp. 1–229 in Giddings, J. C. & Keller, R. A.Advances in chromatography. Marcel Dekker, New York.Google Scholar
KNUDSEN, J. T., ERIKSSON, R., GERSHENZON, J. & STAHL, B. 2006. Diversity and distribution of floral scent. The Botanical Review 72:1–120.Google Scholar
LANCASTER, N. 2004. A study of the distribution of orchids in the Mascarene Islands. M.Sc. Plant Diversity, Reading University. 115 pp.Google Scholar
LUMER, C. & YOST, S. 1995. The reproductive biology of Vincetoxicum nigrum (L.) Moench (Asclepiadaceae), a Mediterranean weed in New York State. Bulletin of the Torrey Botanical Club 122:15–23.CrossRefGoogle Scholar
MICHENEAU, C., FOURNEL, J., GAUVIN-BIALECKI, A. & PAILLER, T. 2008. Auto-pollination in a long-spurred endemic orchid (Jumellea stenophylla) on Reunion Island (Mascarene Archipelago, Indian Ocean). Plant Systematics and Evolution 272:11–22.CrossRefGoogle Scholar
MITTERMEIER, R. A., GIL, P. R., HOFFMAN, M., PILGRIM, J., BROOKS, T., MITTERMEIER, C. G., LAMOREUX, J. & DA FONSECA, G. A. B. 2005. Hotspots revisited: Earth's biologically richest and most endangered terrestrial ecoregions. Cemex, Conservation International and Agrupacion Sierra Madre, Monterrey, Mexico. 392 pp.Google Scholar
MYERS, N., MITTERMEIER, R. A., MITTERMEIER, C.G., DA FONSECA, G. A. B. & KENT, J. 2000. Biodiversity hotspots for conservation priorities. Nature 403:853–858.Google Scholar
NEILAND, M. R. M. & WILCOCK, C. C. 1998. Fruit set, nectar rewards, and rarity in the Orchidaceae. American Journal of Botany 85:1657–1671.Google Scholar
NISHIDA, R., TAN, K. H., WEE, S. L., HEE, A. K. W. & TOONG, Y. C. 2004. Phenylpropanoids in the fragrance of the fruit fly orchid, Bulbophyllum cheiri, and their relationship to the pollinator, Bactrocera papayae. Biochemical Systematics and Ecology 32:245–252.Google Scholar
RENNER, S. 2006. Rewardless flowers in the angiosperms and the role of insect cognition in their evolution. Pp. 123–144 in Waser, N. M. & Ollerton, J.Plant–pollinator interactions: from specialization to generalization. University of Chicago Press, Chicago.Google Scholar
ROBERTS, D. L. 2001. Reproductive biology and conservation of the orchids of Mauritius. Ph.D. thesis, University of Aberdeen, UK.Google Scholar
STRAHM, W. A. 1993. The conservation and restoration of the flora of Mauritius and Rodrigues. Ph.D. thesis, University of Reading, UK. 240 pp.Google Scholar
STRASBERG, D., ROUGET, M., RICHARDSON, D. M., BARET, S., DUPONT, J. & COWLING, R. 2005. An assessment of habitat diversity and transformation on La Réunion Island (Mascarene Islands, Indian Ocean) as a basis for identifying broad-scale conservation priorities. Biodiversity Conservation 14:3015–3032.Google Scholar
TAN, K. & NISHIDA, R. 2000. Mutual reproductive benefits between a wild orchid, Bulbophyllum patens, and Bactrocera fruit flies via a floral synomone. Journal of Chemical Ecology 26:533–546.Google Scholar
TAN, K. & NISHIDA, R. 2007. Zingerone in the floral synomone of Bulbophyllum baileyi (Orchidaceae) attracts Bactrocera fruit flies during pollination. Biochemical Systematics and Ecology 35:334–341.CrossRefGoogle Scholar
TAN, K., NISHIDA, R. & TOONG, Y. 2002. Floral synomone of a wild orchid, Bulbophyllum cheiri, lures Bactrocera fruit flies for pollination. Journal of Chemical Ecology 28:1161–1172.Google Scholar
TAN, K. H. & RITSUO, N. 2005. Synomone or kairomone? – Bulbophyllum apertum flower releases raspberry ketone to attract Bactrocera fruit flies. Journal of Chemical Ecology 31:497–507.Google Scholar
TAN, K. H., TAN, L. T. & NISHIDA, R. 2006. Floral phenylpropanoid cocktail and architecture of Bulbophyllum vinaceum orchid in attracting fruit flies for pollination. Journal of Chemical Ecology 32:2429–2441.Google Scholar
TEIXEIRA, S. D. P., BORBA, E. L. & SEMIR, J. 2004. Lip anatomy and its implications for the pollination mechanisms of Bulbophyllum species (Orchidaceae). Annals of Botany 93:499–505.Google Scholar
TREMBLAY, R. L. & ACKERMAN, J. D. 2007. Floral color patterns in a tropical orchid: are they associated with reproductive success? Plant Species Biology 22:95–105.Google Scholar
TREMBLAY, R. L., ACKERMAN, J. D., ZIMMERMAN, J. K. & CALVO, R. N. 2005. Variation in sexual reproduction in orchids and its evolutionary consequences: a spasmodic journey to diversification. Biological Journal of the Linnean Society 84:1–54.Google Scholar
VAN DER CINGEL, N. A. 1995. An atlas of orchid pollination: European orchids. A.A. Balkema Publishers, Rotterdam. 192 pp.Google Scholar
VAN DER CINGEL, N. A. 2001. An atlas of orchid pollination. America, Africa, Asia and Australia. A.A. Balkema Publishers, Rotterdam. 308 pp.Google Scholar
VAN DER PIJL, L. & DODSON, C. 1966. Orchid flowers, their pollination and evolution. University of Miami Press, Florida. 214 pp.Google Scholar
ZANG, Z. & PAWLISZYN, J. 1993. Headspace solid-phase microextraction. Analytical Chemistry 65:1843–1852.Google Scholar