EL ROL DE LOS COMPUESTOS ORGÁNICOS VOLÁTILES FLORALES EN LAS INTERACCIONES PLANTA-INSECTO

Autores

  • Mariela Baldelomar Universidad de Talca
  • Matheus Lacerda Viana Universidade Federal de Uberlândia
  • Francismeire Jane Telles Universidade Federal de Uberlândia

DOI:

https://doi.org/10.4257/oeco.2018.2204.02

Palavras-chave:

dishonest signal, floral VOCs, herbivores, honest signal, pollinators

Resumo

Los compuestos orgánicos volátiles (COVs) producidos por plantas son productos secundarios de su metabolismo y están involucrados en una gran variedad de funciones ecológicas. Cuando presentes en las flores, los perfiles de los COVs no sólo están asociados con mutualismos, como la polinización, sino también con procesos antagónicos, como la herbivoría o las señales deshonestas. Su presencia, perfiles y concentraciones en las flores están bajo selección mediada por el compromiso entre supervivencia y reproducción de las plantas, es decir por las interacciones antagonistas y mutualistas mediadas por los COVs. En las interacciones mutualistas, los COVs pueden actuar sinérgicamente con señales visuales asegurando la atención de los polinizadores durante períodos más largos y/o a mayores distancias. A pesar del papel fundamental de las fragancias florales en la biología reproductiva, se han realizado pocos estudios que aborden la evolución de este rasgo floral. Esta revisión destaca la importancia de los volátiles florales en las interacciones ecológicas, principalmente en las interacciones planta-insecto.

 

THE ROLE OF FLORAL VOLATILE ORGANIC COMPOUNDS IN PLANT-INSECT INTERACTIONS. Volatile Organic Compounds (VOCs) produced by plants are secondary products of their metabolism and are related to a wide range of ecological functions. When present in flowers, VOCs profiles are not only associated with mutualisms such as pollination, but also to antagonistic processes such as herbivory or dishonest signaling. Their presence, profiles and concentrations in flowers are under selection mediated by the trade-off between survivorship and reproduction of plants, i.e. antagonist and mutualist interactions mediated by VOCs. In the mutualistic interactions, VOCs can act synergistically with visual signals ensuring the attention of pollinators for longer periods and/or distances. Despite the fundamental role of floral scents on the reproductive biology, few studies addressing the evolution of this floral trait have been reported. This review highlights the importance of floral volatiles on ecological interactions, mainly on plant-insect interactions.

Biografia do Autor

Mariela Baldelomar, Universidad de Talca

Alumna del Magíster en Ecología Aplicada

Referências

Amrad, A., Moser, M., Mandel, T., de Vries, M., Schuurink, R. C., Freitas, L., & Kuhlemeier, C. 2016. Gain and loss of floral scent production through changes in structural genes during pollinator-mediated speciation. Current Biology, 26(24), 3303–3312. DOI: 10.1016/j.cub.2016.10.023

Armbruster, W., & Webster, G. 1979. Pollination of two species of Dalechampia (Euphorbiaceae) in Mexico by Euglossine bees. Biotropica, 11(4), 278–283. DOI: 10.2307/2387919

Balkenius, A., Bisch-Knaden, S., & Hansson, B. 2009. Interaction of visual and odour cues in the mushroom body of the hawkmoth Manduca sexta. Journal of Experimental Biology, 212(4), 535–541. DOI: 10.1242/jeb.021220

Bernhardt, P., Sage, T., Weston, P., Azuma, H., Lam, M., Thien, L., & Bruhl, J. 2003. The pollination of Trimenia moorei (Trimeniaceae): floral volatiles, insect/wind pollen vectors and stigmatic self-incompatibility in a basal Angios-perm. Annals of Botany, 92(3), 445–458. DOI: 10.1093/aob/mcg157

Bestmann, H., Winkler, L., & von Helversen, O. 1997. Headspace analysis of volatile flower scent constituents of bat-pollinated plants. Phyto-chemistry, 46(7), 1169–1172. DOI: 10.1016/S0031-9422(97)00428-7

Bohman, B., Phillips, R. D., Menz, M. H. M., Berntsson, B. W., Flematti, G. R., Barrow, R. A., Dixon, K. W., & Peakall, R. 2014. Discovery of pyrazines as pollinator sex pheromones and orchid semiochemicals: implications for the evolution of sexual deception. New Phytologist, 203(3), 939–952. DOI: 10.1111/nph.12800

Brito, V., Telles, F., & Lunau, K. 2014. Ecologia cognitiva da polinizaçao. In: A. Rech, K. Agostini, I. Machado, & P. Oliveira (Eds.), Biologia da Polinizaçao. pp. 417–438. Brasilia: Ministério do Meio Ambiente.

Burkle, L. A., & Runyon, J. B. 2017. The smell of environmental change: using floral scent to explain shifts in pollinator attraction. Applications in Plant Sciences, 5(6), 1600123. DOI: 10.3732/apps.1600123

Campbell, D. R., Waser, N. M., & Melendez-Ackerman, E. J. 1997. Analyzing pollinator-mediated selection in a plant hybrid zone: hummingbird visitation patterns on three spatial scales. The American Naturalist, 149(2), 295–315. DOI: 10.1086/285991

Carlsson, M., & Hansson, B. 2006. Detection and coding of flower volatiles in nectar-foraging insects. In: N. Dudareva & E. Pichersky (Eds.), Biology of Floral Scent. pp. 243–261. Boca Raton: Taylor & Francis Group.

Chen, C., Song, Q., Proffit, M., Bessière, J.-M., Li, Z., & Hossaert-McKey, M. 2009. Private channel: a single unusual compound assures specific pollinator attraction in Ficus semicordata. Functional Ecology, 23(5), 941–950. DOI: 10.1111/j.1365-2435.2009.01622.x

Chen, F., Tholl, D., D’Auria, J. C., Farooq, A., Pichersky, E., & Gershenzon, J. 2003. Biosynthesis and emission of terpenoid volatiles from Arabidopsis flowers. The Plant Cell, 15(2), 481–494. DOI: 10.1105/tpc.007989

Chittka, L., & Raine, N. E. 2006. Recognition of flowers by pollinators. Current Opinion in Plant Biology, 9(4), 428–435. DOI: 10.1016/j.pbi.2006.05.002

Dafni, A. 1992. Pollination ecology: a practical approach. D. Rickwood, & B. D. Hames (Eds.), 1st ed. New York: Oxford University Press: p. 250.

Dobson, H. E. M. 1994. Floral volatiles in insect biology. In: E. A.Bernays (Ed.), Insect-plant Interactions. pp. 47–81. Boca Raton: CRC Press.

Dobson, H. E. M. 2006. Relationship between floral fragrance composition and type of pollinator. In: N. Dudareva, & E. Pichersky (Eds.), Biology of Floral Scent. pp. 147–198. Boca Raton: Taylor & Francis Group.

Dobson, H. E. M., & Bergström, G. 2000. The ecology and evolution of pollen odors. Plant Systematics and Evolution, 222(1/4), 63–87. DOI: 10.1007/BF00984096

Dudareva, N., Klempien, A., Muhlemann, J. K., & Kaplan, I. 2013. Biosynthesis, function and metabolic engineering of plant volatile organic compounds. New Phytologist, 198(1), 16–32. DOI: 10.1111/nph.12145

Dudareva, N., Negre, F., Nagegowda, D. A., & Orlova, I. 2006. Plant volatiles: recent advances and future perspectives. Critical Reviews in Plant Sciences, 25(5), 417–440. DOI: 10.1080/07352680600899973

Dufaÿ, M., Hossaert-McKey, M., & Anstett, M. C. 2003. When leaves act like flowers: how dwarf palms attract their pollinators. Ecology Letters, 6(1), 28–34. DOI: 10.1046/j.1461-0248.2003.00382.x

Effmert, U., Buss, D., Rohrbeck, D., & Birgit, P. 2006. Localization of the synthesis and emission of scent compounds within the flower. In: N. Dudareva & E. Pichersky (Eds.), Biology of Floral Scent. pp. 105–120. Boca Raton: Taylor & Francis Group.

Ehrlén, J., Borg-Karlson, A.-K., & Kolb, A. 2012. Selection on plant optical traits and floral scent: Effects via seed development and antagonistic interactions. Basic and Applied Ecology, 13(6), 509–515. DOI: 10.1016/j.baae.2012.08.001

Farré-Armengol, G., Filella, I., Llusia, J., & Peñuelas, J. 2013. Floral volatile organic compounds: between attraction and deterrence of visitors under global change. Perspectives in Plant Ecology, Evolution and Systematics, 15(1), 56–67. DOI: 10.1016/j.ppees.2012.12.002

Farré-Armengol, G., Filella, I., Llusia, J., Primante, C., & Peñuelas, J. 2015. Enhanced emissions of floral volatiles by Diplotaxis erucoides (L.) in response to folivory and florivory by Pieris brassicae (L.). Biochemical Systematics and Ecology, 63, 51–58. DOI: 10.1016/j.bse.2015.09.022

Filella, I., Bosch, J., Llusià, J., Peñuelas, A., & Peñuelas, J. 2011. Chemical cues involved in the attraction of the oligolectic bee Hoplitis adunca to its host plant Echium vulgare. Biochemical Systematics and Ecology, 39(4–6), 498–508. DOI: 10.1016/j.bse.2011.07.008

Friedman, M., Henika, P., & Mandrell, R. 2002. Bactericidal activities of plant essential oils and some of their isolated constituents against Campylobacter jejuni, Escherichia coli, Listeria monocytogenes, and Salmonella enterica. Food Protect, 65(10), 1545–1560. DOI: 10.4315/0362-028X-65.10.1545

Frost, C. J., Appel, H. M., Carlson, J. E., De Moraes, C. M., Mescher, M. C., & Schultz, J. C. 2007. Within-plant signalling via volatiles overcomes vascular constraints on systemic signalling and primes responses against herbivores. Ecology Letters, 10(6), 490–498. DOI: 10.1111/j.1461-0248.2007.01043.x

Galen, C. 1985. Regulation of seed-set in Polemonium viscosum: floral scents, pollina-tion, and resources. Ecology, 66(3), 792–797. DOI: 10.2307/1940540

Gang, D. 2005. Evolution of flavors and scents. Annual Review of Plant Biology, 56(1), 301–325. DOI: 10.1146/annurev.arplant.56.032604.144128

Gervasi, D. D. L., & Schiestl, F. P. 2017. Real-time divergent evolution in plants driven by pollinators. Nature Communications, 8, 14691. DOI: 10.1038/ncomms14691

Gomez, J. M., Bosch, J., Perfectti, F., Fernandez, J. ., Abdelaziz, M., & Camacho, J. 2008. Spatial variation in selection on corolla shape in a generalist plant is promoted by the preference patterns of its local pollinators. Proceedings of the Royal Society B: Biological Sciences, 275(1648), 2241–2249. DOI: 10.1098/rspb.2008.0512

Goyret, J., & Yuan, M. L. 2015. Influence of ambient illumination on the use of olfactory and visual signals by a nocturnal hawkmoth during close-range foraging. Integrative and Comparative Biology, 55(3), 486–494. DOI: 10.1093/icb/icv009

Gregg, K. B. 1983. Variation in floral fragrances and morphology: incipient speciation in Cycnoches? Botanical Gazette, 144(4), 566–576. DOI: 10.1086/337412

Gross, K., Sun, M., & Schiestl, F. P. 2016. Why do floral perfumes become different? Region-specific selection on floral scent in a terrestrial orchid. PLoS ONE, 11(2), e0147975. DOI: 10.1371/journal.pone.0147975

Groth, I., Bergstrom, G., & Pellmyr, O. 1987. Floral fragrances in Cimicifuga: chemical poly-morphism and incipient speciation in Cimicifuga simplex. Biochemical Systematics and Ecology, 15(4), 441–444. DOI: 10.1016/0305-1978(87)90058-5

Gu, D., Yang, D.-R., Yang, P., Peng, Y.-Q., & Wang, Z.-J. 2016. Work division of floral scent compounds in mediating pollinator behaviours. Chemistry and Ecology, 32(8), 733–741. DOI: 10.1080/02757540.2016.1189538

Heiduk, A., Brake, I., von Tschirnhaus, M., Göhl, M., Jürgens, A., Johnson, S. D., Meve, U., & Dötterl, S. 2016. Ceropegia sandersonii mimics attacked honeybees to attract kleptoparasitic flies for pollination. Current Biology, 26(20), 2787–2793. DOI: 10.1016/j.cub.2016.07.085

Heil, M., & Karban, R. 2010. Explaining evolution of plant communication by airborne signals. Trends in Ecology and Evolution, 25(3), 137–144. DOI: 10.1016/j.tree.2009.09.010

Holopainen, J. K., & Gershenzon, J. 2010. Multiple stress factors and the emission of plant VOCs. Trends in Plant Science, 15(3), 176–184. DOI: 10.1016/j.tplants.2010.01.006

Johnson, S. D., Burgoyne, P. M., Harder, L. D., & Dotterl, S. 2011. Mammal pollinators lured by the scent of a parasitic plant. Proceedings of the Royal Society B: Biological Sciences, 278(1716), 2303–2310. DOI: 10.1098/rspb.2010.2175

Junker, R. R., & Blüthgen, N. 2010. Floral scents repel facultative flower visitors, but attract obligate ones. Annals of Botany, 105(5), 777–782. DOI: 10.1093/aob/mcq045

Jürgens, A., Dötterl, S., & Meve, U. 2006. The chemical nature of fetid floral odours in stapeliads (Apocynaceae, Asclepiadoideae, Ceropegieae). New Phytologist, 172(3), 452–468. DOI: 10.1111/j.1469-8137.2006.01845.x

Kessler, D., Diezel, C., & Baldwin, I. T. 2010. Changing pollinators as a means of escaping herbivores. Current Biology, 20(3), 237–242. DOI: 10.1016/j.cub.2009.11.071

Kessler, D., Diezel, C., Clark, D. G., Colquhoun, T. A., & Baldwin, I. T. 2013. Petunia flowers solve the defence/apparency dilemma of pollinator attraction by deploying complex floral blends. Ecology Letters, 16(3), 299–306. DOI: 10.1111/ele.12038

Knauer, A. C., & Schiestl, F. P. 2015. Bees use honest floral signals as indicators of reward when visiting flowers. Ecology Letters, 18(2), 135–143. DOI: 10.1111/ele.12386

Knudsen, J., Eriksson, R., Gershenzon, J., & Ståhl, B. 2006. Diversity and distribution of floral scent. The Botanical Review, 72(1), 1–120. DOI: 10.1663/0006-8101(2006)72

Knudsen, J. T., & Gershenzon, J. 2006. The chemical diversity of floral scent. In: N. Dudareva & E. Pichersky (Eds.), Biology of Floral Scent. pp. 27–45. Boca Raton: Taylor & Francis Group.

Knudsen, J. T., & Tollsten, L. 1995. Floral scent in bat-pollinated plants: a case of convergent evolution. Botanical Journal of the Linnean Society, 119(1), 45–57. DOI: 10.1111/j.1095-8339.1995.tb00728.x

Knudsen, J. T., Tollsten, L., Groth, I., Bergström, G., & Raguso, R. A. 2004. Trends in floral scent chemistry in pollination syndromes: floral scent composition in hummingbird-pollinated taxa. Botanical Journal of the Linnean Society, 146(2), 191–199. DOI: 10.1111/j.1095-8339.2004.00329.x

Leonard, A. S., & Masek, P. 2014. Multisensory integration of colors and scents: insights from bees and flowers. Journal of Comparative Physiology A, 200(6), 463–474. DOI: 10.1007/s00359-014-0904-4

Levin, R. A., Raguso, R. A., & McDade, L. A. 2001. Fragrance chemistry and pollinator affinities in Nyctaginaceae. Phytochemistry, 58(3), 429–440. DOI: 10.1016/S0031-9422(01)00257-6

Li, P., Luo, Y. B., Bernhardt, P., Yang, X. Q., & Kou, Y. 2006. Deceptive pollination of the Lady’s Slipper Cypripedium tibeticum (Orchidaceae). Plant Systematics and Evolution, 262(1–2), 53–63. DOI: 10.1007/s00606-006-0456-3

Maad, J. 2000. Phenotypic selection in hawkmoth-pollinated Platanthera bifolia: targets and fitness surfaces. Evolution, 54(1), 112–123. DOI: 10.1111/j.0014-3820.2000.tb00012.x

Maffei, M. E. 2010. Sites of synthesis, biochemistry and functional role of plant volatiles. South African Journal of Botany, 76(4), 612–631. DOI: 10.1016/j.sajb.2010.03.003

Mant, J., Peakall, R., & Schiestl, F. 2005. Does selection on floral odor promote differentiation among populations and species of the sexually deceptive orchid genus Ophrys? Evolution, 59(7), 1449–1463. DOI: 10.1111/j.0014-3820.2005.tb01795.x

Moré, M., Cocucci, A. A., & Raguso, R. A. 2013. The importance of oligosulfides in the attraction of fly pollinators to the brood-site deceptive species Jaborosa rotacea (Solanaceae). Interna-tional Journal of Plant Sciences, 174(6), 863–876. DOI: 10.1086/670367

Muhlemann, J. K., Klempien, A., & Dudareva, N. 2014. Floral volatiles: from biosynthesis to function. Plant, Cell and Environment, 37(8), 1936–1949. DOI: 10.1111/pce.12314

Ollerton, J., Winfree, R., & Tarrant, S. 2011. How many flowering plants are pollinated by animals? Oikos, 120(3), 321–326. DOI: 10.1111/j.1600-0706.2010.18644.x

Parachnowitsch, A. L., Raguso, R. A., & Kessler, A. 2012. Phenotypic selection to increase floral scent emission, but not flower size or colour in bee-pollinated Penstemon digitalis. New Phytologist, 195(3), 667–675. DOI: 10.1111/j.1469-8137.2012.04188.x

Patiny, S. 2012. Evolution of plant-pollinator relationships.Cambridge: Cambridge University Press: p. 469.

Patt, J. M., French, J. C., Schal, C., Lech, J., & Hartman, T. G. 1995. The pollination biology of Tuckahoe, Peltandra virginica (Araceae). Ame-rican Journal of Botany, 82(10), 1230–1240. DOI: 10.2307/2446245

Pellmyr, O. 2003. Yuccas, yucca moths, and coevolution: a review. Annals of the Missouri Botanical Garden, 90(1), 35–55. DOI: 10.2307/3298524

Pichersky, E., & Gershenzon, J. 2002. The formation and function of plant volatiles: perfu-mes for pollinator attraction and defense. Current Opinion in Plant Biology, 5(3), 237–243. DOI: 10.1016/S1369-5266(02)00251-0

Price, P. 2011. Multitrophic interactions. In: P. Price, R. Denno, M. Eubanks, D. Finke, & I. Kaplan (Eds.), Insect ecology: behaviour, populations and communities. pp. 489–534. Cambridge: Cambridge University Press.

Proctor, M., Yeo, P., & Lack, A. 1996. The natural history of pollination. S. A. Corbet S. M. Walters R. West D. Streeter & D. A. Ratcliffe (Eds.), London: Timber Press: p. 646.

Raguso, R. A. 2001. Floral scent, olfaction, and scent-driven foraging behavior. In: L. Chittka & J. Thomson (Eds.), Cognitive ecology of pollination. pp. 83–105. Cambridge: Cambridge University Press.

Raguso, R. A. 2004. Why are some floral nectars scented? Ecology, 85(6), 1486–1494. DOI: 10.1890/03-0410

Raguso, R. A. 2009. Floral scent in a whole-plant context: moving beyond pollinator attraction. Functional Ecology, 23(5), 837–840. DOI: 10.1111/j.1365-2435.2009.01643.x

Raguso, R. A., Levin, R. A., Foose, S. E., Holmberg, M. W., & McDade, L. A. 2003. Fragrance chemistry, nocturnal rhythms and pollination “syndromes” in Nicotiana. Phytochemistry, 63(3), 265–284. DOI: 10.1016/S0031-9422(03)00113-4

Raguso, R. A., & Weiss, M. R. 2015. Concerted changes in floral colour and scent, and the importance of spatio-temporal variation in floral volatiles. Journal of the Indian Institute of Science, 95(1), 69–92.

Raguso, R. A., & Willis, M. A. 2002. Synergy between visual and olfactory cues in nectar feeding by wild hawkmoths, Manduca sexta. Animal Behaviour, 69(2), 407–418. DOI: 10.1016/j.anbehav.2004.04.015

Ramya, M., Kwon, O. K., An, H. R., Park, P. M., Baek, Y. S., & Park, P. H. 2017. Floral scent: regulation and role of MYB transcription factors. Phytochemistry Letters, 19, 114–120. DOI: 10.1016/j.phytol.2016.12.015

Renoult, J. P., Thomann, M., Schaefer, H. M., & Cheptou, P. 2013. Selection on quantitative colour variation in Centaurea cyanus: the role of the pollinator’s visual system. Journal of Evolutionary Biology, 26(11), 2415–2427. DOI: 10.1111/jeb.12234

Salzmann, C. C., Cozzolino, S., & Schiestl, F. P. 2007. Floral scent in food-deceptive orchids: species specificity and sources of variability. Plant Biology, 9(6), 720–729. DOI: 10.1055/s-2007-965614

Schiestl, F. P. 2003. The chemistry of sexual deception in an orchid-wasp pollination system. Science, 302(5644), 437–438. DOI: 10.1126/science.1087835

Schiestl, F. P. 2010. The evolution of floral scent and insect chemical communication. Ecology Letters, 13(5), 643–656. DOI: 10.1111/j.1461-028.2010.01451.x

Schiestl, F.P., Dötterl, S., 2012. The evolution of floral scent and olfactory preferences in pollinators: coevolution or pre-existing bias? Evolution, 66(7), 2042–2055. DOI: 10.1111/j.1558-5646.2012.01593.x

Schiestl, F. P. 2015. Ecology and evolution of floral volatile-mediated information transfer in plants. New Phytologist, 206(2), 571–577. DOI: 10.1111/nph.13243

Schiestl, F. P., & Ayasse, M. 2000. Post-mating odor in females of the solitary bee, Andrena nigroaenea (Apoidea, Andrenidae), inhibits male mating behavior. Behavioral Ecology and Sociobiology, 48(4), 303–307. DOI: 10.1007/s002650000241

Schiestl, F. P., Ayasse, M., Paulus, H. F., Löfstedt, C., Hansson, B. S., Ibarra, F., & Francke, W. 2000. Sex pheromone mimicry in the early spider orchid (Ophrys sphegodes): patterns of hydrocarbons as the key mechanism for pollination by sexual deception. Journal of Comparative Physiology A: Sensory, Neural, and Behavioral Physiology, 186(6), 567–574. DOI: 10.1007/s003590000112

Schiestl, F. P., Huber, F. K., & Gomez, J. M. 2011. Phenotypic selection on floral scent: trade-off between attraction and deterrence? Evolutio-nary Ecology, 25(2), 237–248. DOI: 10.1007/s10682-010-9409-y

Schiestl, F. P., & Johnson, S. D. 2013. Pollinator-mediated evolution of floral signals. Trends in Ecology & Evolution, 28(5), 307–315. DOI: 10.1016/j.tree.2013.01.019

Sletvold, N., Grindeland, J. M., & Ågren, J. 2010. Pollinator-mediated selection on floral display, spur length and flowering phenology in the deceptive orchid Dactylorhiza lapponica. New Phytologist, 188(2), 385–392. DOI: 10.1111/j.1469-8137.2010.03296.x

Smith, B., Wright, G., & Daly, K. 2006. Learning-based recognition and discrimination of floral odors. In: N. Dudareva & E. Pichersky (Eds.), Biology of Floral Scent. pp. 263–295. Boca Raton: Taylor & Francis Group.

Stokl, J., Brodmann, J., Dafni, A., Ayasse, M., & Hansson, B. S. 2011. Smells like aphids: orchid flowers mimic aphid alarm pheromones to attract hoverflies for pollination. Proceedings of the Royal Society B: Biological Sciences, 278(1709), 1216–1222. DOI: 10.1098/rspb.2010.1770

Taiz, L., Zeiger, E., Møller, I. M., & Murphy, A. 2017. Plant physiology and development. 5th ed. Massachusetts: Sinauer Associates: p. 778.

Theis, N. 2006. Fragance of Canada thistle (Cirsium arvense) attracts both floral herbivores and pollinators. Journal of Chemical Ecology, 32(5), 917–927. DOI: 10.1007/s10886-006-9051-x

Thien, L. B., Azuma, H., & Kawano, S. 2000. New perspectives on the pollination biology of basal angiosperms. International Journal of Plant Sciences, 161(S6), S225–S235. DOI: 10.1086/317575

Urru, I., Stensmyr, M. C., & Hansson, B. S. 2011. Pollination by brood-site deception. Phyto-chemistry, 72(13), 1655–1666. DOI: 10.1016/j.phytochem.2011.02.014

Vazquez, D. P., Bluthgen, N., Cagnolo, L., & Chacoff, N. P. 2009. Uniting pattern and process in plant-animal mutualistic networks: a review. Annals of Botany, 103(9), 1445–1457. DOI: 10.1093/aob/mcp057

Vivaldo, G., Masi, E., Taiti, C., Caldarelli, G., & Mancuso, S. 2017. The network of plants volatile organic compounds. Scientific Reports, 7(1), 1–18. DOI: 10.1038/s41598-017-10975-x

von Helversen, O., Winkler, L., & Bestmann, H. J. 2000. Sulphur-containing “perfumes” attract flower-visiting bats. Journal of Comparative Physiology A, 186(2), 143–153. DOI: 10.1007/s003590050014

Willmer, P. G., Nuttman, C. V, Raine, N. E., Stone, G. N., Pattrick, J. G., Henson, K., Stillman, P., McIlroy, L., Potts, S. G., & Knudsen, J. T. 2009. Floral volatiles controlling ant behaviour. Functional Ecology, 23(5), 888–900. DOI: 10.1111/j.1365-2435.2009.01632.x

Willmer, P. G., & Stone, G. N. 1997. How aggressive ant-guards assist seed-set in Acacia flowers. Nature, 388(6638), 165–167. DOI: 10.1038/40610

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(5), 841–851. DOI: 10.1111/j.1365-2435.2009.01627.x

Yan, J., Wang, G., Sui, Y., Wang, M., & Zhang, L. 2016. Pollinator responses to floral colour change, nectar and scent promote reproductive fitness in Quisqualis indica (Combretaceae). Scientific Reports, 6(1), 24408. DOI: 10.1038/srep24408

Yue, Y., Yu, R., & Fan, Y. 2015. Transcriptome profiling provides new insights into the formation of floral scent in Hedychium coronarium. BMC Genomics, 16(1), 470. DOI: 10.1186/s12864-015-1653-7

Zangerl, A. R., & Berenbaum, M. R. 2009. Effects of florivory on floral volatile emissions and pollination success in the wild parsnip. Arthropod-Plant Interactions, 3(3), 181–191. DOI: 10.1007/s11829-009-9071-x

Zu, P., Blanckenhorn, W. U., & Schiestl, F. P. 2016. Heritability of floral volatiles and pleiotropic responses to artificial selection in Brassica rapa. New Phytologist, 209(3), 1208–1219. DOI: 10.1111/nph.13652

Downloads

Publicado

2018-12-18