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The perfume flowers ofCyphomandra (Solanaceae): Pollination by euglossine bees, bellows mechanism, osmophores, and volatiles

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Abstract

The perfume syndrome and pollination by fragrance-collecting euglossine bees in the neotropic solanaceous genusCyphomandra was confirmed by field observations. In SE Brazil,C. sciadostylis was visited byEufriesea violaceae, andC. diploconos byEuglossa mandibularis; C. hartwegii was pollinated byEulaema meriana in Costa Rica. The primary attractant, fragrant droplets that ooze from the dorsally bulged connectives, is mopped up by the males with the forebasitarsi. Thereby, the poricidal thecae are inadvertently pushed causing the dry pollen to dust the bee's sternum. The number and direction of the pollen jets are related to pollinator size and stigma structure. The flowers are homogamous, selfsterile, and last three days. The androecium is optically non-contrasting or has cryptic colour. Flowers ofC. sciadostylis andC. diploconos undergo a colour change and an almost three-fold increase in corolla size when scent production and visits cease. The dorsal papillar epidermis of the connective is underlain by a glandular parenchyma typical of osmophores. GC techniques revealed germacrene D as the main component in the mentholic scent ofC. sciadostylis, ipsdienol, heneicosane, and tricosane as dominant in the nutmeg-like scent ofC. diploconos, and benzyl acetate and benzyl alcohol in the sweet fragrance ofC. hartwegii. In all cases, these were accompanied by numerous minor components of heterogeneous chemical nature.—Pollen release by means of a peculiar pneumatic bellows mechanism appears as a necessary and probably ubiquitous feature ofCyphomandra. Even a slight pressure exerted upon the thin, elastic thecal walls blows pollen jets through the pores. Unusual anatomic changes accompany anther maturation. Initially voluminous parenchymatic locular intumescences (placentoids) contract completely during meiosis, then expand once more when the pollen is ripe, pushing the grains against the locular wall, and contract a second time, allowing air to enter the thecae.—Cyphomandra pinetorum was found to be exceptional in exhibiting a pollen flower syndrome, and not cryptical but optically contrasting yellow anthers, as known forSolanum.

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References

  • Ab'saber, A. N., 1977: Os domínios morfoclimáticos na América de Sul. Primeira aproximação. — Geomorfologia52: 1–21.

    Google Scholar 

  • Ackerman, J., 1983: Specificity and mutual dependency of the orchid-euglossine bee interaction. — Biol. J. Linn. Soc.20: 301–314.

    Google Scholar 

  • Barboza, G., 1988: Estudios morfológicos enJaborosa (Solanc.): Análisis comparativo de las estructuras vegetativas y reproductivas relativas a la evolución del género. — Thesis, University of Córdoba, Argentina.

    Google Scholar 

  • Beker, R., Dafni, A., Eisikowitch, D., Ravid, U., 1989: Volatiles of two chemotypes ofMajorana syriaca L. (Labiatae) as olfactory cues for the honeybee. — Oecologia79: 446–451.

    Google Scholar 

  • Bergström, G., 1978: Role of volatile chemicals inOphrys-pollinator interactions. — InHarborne, G., (Ed.): Biochemical aspects of plant and animal coevolution, pp. 107–230. — London, New York: Academic Press.

    Google Scholar 

  • , 1980: Studies on natural odoriferous compounds. XXII. Techniques for the isolation/enrichment of plant volatiles in the analyses ofOphrys orchids (Orchidaceae). — Chem. Scripta16: 173–180.

    Google Scholar 

  • Bernardello, L., 1987: Comparative floral morphology inLycieae (Solanaceae). — Brittonia39: 112–124.

    Google Scholar 

  • Bhandari, N., Sharma, M., 1987: Histochemical and ultrastructural studies during anther development inSolanum nigrum L.: the early ontogeny. — Phytomorphol.37: 249–260.

    Google Scholar 

  • Boch, R., Shearer, D. A., Stone, B. C., 1962: Identification of iso-amyl acetate as an active component in the sting gland pheromone of the honeybee. — Nature195: 1018–1020.

    Google Scholar 

  • Bohs, L., 1986: The biology and taxonomy ofCyphomandra (Solanac.). — Ph. D. Thesis, Harvard University Cambridge, Mass.

    Google Scholar 

  • , 1987: Species groups inCyphomandra (Solanaceae). — Abstr. Ann. Meeting Bot. Soc. Amer. — Amer. J. Bot.74: 725–726.

    Google Scholar 

  • , 1988: Four new species ofCyphomandra (Solanaceae) from South America. — Syst. Bot.13: 265–275.

    Google Scholar 

  • , 1989:Solanum allophyllum (Miers)Standl. and the generic delimitation ofCyphomandra andSolanum (Solanaceae). — Ann. Missouri Bot. Gard.76: 1129–1140.

    Google Scholar 

  • Borg-Karlson, A.-K., 1987: Chemical basis for the relationship betweenOphrys orchids and their pollinators III. — Chemica Scripta27: 313–325.

    Google Scholar 

  • Buchmann, S., 1983: Buzz pollination in angiosperms. — InJones, C. E., Little, R. J., (Eds): Handbook of experimental pollination biology, pp. 73–113. — New York: Van Nostrand Reinhold.

    Google Scholar 

  • , 1978: A biophysical model for buzz pollination in angiosperms. — J. Theor. Biol.72: 639–657.

    Google Scholar 

  • Buzato, S., Sazima, M., 1990a: Ecologia de polinização de duas espécies simpátricas deMendoncia (Acanthaceae). — Resumos XLV Cong. Nac. Bot. Soc. Bot. do Brasil, p. 369.

  • - - 1990b: Expulsão de polen e anatomia das anteras poricidas em duas espécies deMendoncia (Acanthaceae). — Resumos VIII Cong. Soc. Bot. São Paulo, p. 120.

  • Cane, J. H., 1983: Preliminary chemosystematics of theAndrenidae and exocrine lipid evolution of the short-tongued bees (Hymenoptera: Apoidea). — Syst. Zool.32: 417–430.

    Google Scholar 

  • , 1983: Dufour's gland lipid chemistry of three species ofCentris bees (Hymenoptera: Apoidea, Anthophoridae). — Comp. Biochem. Physiol.76 B: 895–897.

    Google Scholar 

  • Child, A., 1984: Studies inSolanum (and related genera) 3. A provisional conspectus of the genusCyphomandra Mart. exSendtner. — Feddes Repert.95: 283–298.

    Google Scholar 

  • Cocucci, A. A., 1988a: Mecanismos florales en la TribuSolaneae — III. Congr. Mundial Plantas Solanáceas, Bogotá, p. 39.

  • , 1988b: Polinización en Solanáceas neotropicales. — Thesis, University of Córdoba, Argentina.

    Google Scholar 

  • Davis, G., 1966: Systematic embryology of angiosperms. New York: Wiley.

    Google Scholar 

  • D'Arcy, W., D'Arcy, N., Keating, R., 1990: Scented anthers in theSolanaceae. — Rhodora92: 50–53.

    Google Scholar 

  • Delpino, F., 1873: Ulteriori osservazioni e considerazioni sulla dicogamia nel regno vegetale. — Atti Soc. Ital. Sci. Nat.16: 139–140.

    Google Scholar 

  • Dobson, H., Bergström, J., Bergström, G., Groth, I., 1987: Pollen and flower volatiles in twoRosa species. — Phytochemistry26: 3171–3173.

    Google Scholar 

  • , 1990: Differences in fragrance chemistry between flower parts ofRosa rugosa Thunb. (Rosaceae). — Israel J. Bot.39: 143–156.

    Google Scholar 

  • Dressler, R., 1979:Eulaema bombiformis, E. meriana, and müllerian mimicry in related species (Hymen.: Apidae). — Biotropica11: 144–151.

    Google Scholar 

  • , 1982: Biology of the orchid bees (Euglossini). — Ann. Rev. Ecol. Syst.13: 373–394.

    Google Scholar 

  • Eiten, G., 1970: A vegetação do estado de São Paulo. — Bolm. Inst. Bot. (S. Paulo)7: 1–147.

    Google Scholar 

  • Evoy, H., Jones, B. P., 1971: Motor patterns of male euglossine bees evoked by floral fragrances. — Anim. Behav.19: 583–588.

    Google Scholar 

  • Eyde, R. H., Teeri, J. A., 1967: Floral anatomy ofRhexia virginica (Melastomat.). — Rhodora69: 163–178.

    Google Scholar 

  • Gerlach, D., 1984: Botanische Mikrotechnik. 3rd edn. — Stuttgart: Thieme.

    Google Scholar 

  • Gerlach, G., Schill, R., 1989: Fragrance analyses, an aid to taxonomic relationships of the genusCoryanthes (Orchidaceae). — Pl. Syst. Evol.168: 159–165.

    Google Scholar 

  • ,, 1991: Composition of orchid scents attracting euglossine bees. — Bot. Acta104: 379–391.

    Google Scholar 

  • Goebel, K. von, 1893: Sporenaustreibung durch Regentropfen. — Flora80: 480–482.

    Google Scholar 

  • Gregory, P., 1949: The operation of puff-balls mechanism ofLycoperdon perlatum by raindrops shown by ultra-high-speed Sellieren cinematography. — Trans. Brit. Mycol. Soc.32: 11–15.

    Google Scholar 

  • , 1961: The microbiology of the atmosphere. — London, New York: Wiley.

    Google Scholar 

  • Groth, I., Bergström, G., Pellmyr, O., 1987: Floral fragrances inCimicifuga: chemical polymorphism and incipient speciation inCimicifuga simplex. — Biochem. Syst. Ecol.15: 441–444.

    Google Scholar 

  • Harris, A., 1905: The dehiscence of anthers by apical pores. — Ann. Rep. Missouri Bot. Gard.16: 167–257.

    Google Scholar 

  • Hartl, D., 1963: Das Placentoid der Pollensäcke, ein Merkmal der Tubifloren. — Ber. Deutsch. Bot. Ges.76: 71–72.

    Google Scholar 

  • Hefetz, A., Batra, S., Fales, H., 1979: Natural polyesters: Dufour's gland macrocyclic lactones from brood cell laminester inColletes bees. — Science204: 415–417.

    Google Scholar 

  • Huber, A., 1980: Morphologische und entwicklungsgeschichtliche Untersuchungen an Blüten und Blütenständen von Solanaceen undNolana paradoxa (Nolanaceae). — Dissertationes Botanicae55: 1–252.

    Google Scholar 

  • Hueck, K., 1972: As florestas da América do Sul. — São Paulo: Polígono.

    Google Scholar 

  • Ingold, C., 1971: Fungal spores. Their liberation and dispersal. — Oxford: Clarendon.

    Google Scholar 

  • Inouye, D., 1980: The terminology of floral larceny. — Ecology61: 1251–1253.

    Google Scholar 

  • Jagannadham, D., 1988: Embryological studies inNicotiana tabacum andN. rustica. — J. Indian Bot. Soc.67: 115–119.

    Google Scholar 

  • Janzen, D., 1971: Euglossine bees as long-distance pollinators of tropical plants. — Science171: 203–205.

    Google Scholar 

  • Johansen, D., 1940: Plant microtechnique. — New York: McGraw Hill.

    Google Scholar 

  • Joulain, D., 1986: Study of the fragrance given off by certain springtime flowers. — InBurke, E. J., (Ed.): Progress in essential oil research, pp. 57–67. Proceedings Intern. Sympos. Berlin. — Berlin: de Grutyer & Co.

    Google Scholar 

  • Kimsey, L. S., 1982: Systematics of bees of the genusEufriesea (Hymenoptera, Apidae). — Univ. California Publ. Entomol.95: 1–125.

    Google Scholar 

  • Knudsen, J. T., Tollsten, L., 1991: Floral scent and intrafloral scent differentiation inMoneses andPyrola (Pyrolaceae). — Pl. Syst. Evol.177: 81–91.

    Google Scholar 

  • Lagerheim, G., 1899: Über die Bestäubungs- und Aussaugungseinrichtungen vonBrachyotum ledifolium (Desr.)Cogn. — Bot. Not.1899: 105–122.

    Google Scholar 

  • Leggett, W. H., 1881: Fertilization ofRhexia virginica L. — Bull. Torrey Bot. Club8: 102–104.

    Google Scholar 

  • Lewis, J. A., Moore, C. J., Fletcher, M. T., Drew, R. A., Kitching, W., 1988: Volatile compounds from the flowers ofSpathiphyllum cannaefolium. — Phytochemistry27: 2755–2757.

    Google Scholar 

  • Lumer, C., 1980: Rodent pollination ofBlakea (Melastomatac.) in a Costa Rican cloud forest. — Brittonia37: 512–517.

    Google Scholar 

  • Mahlberg, P. G., 1985: Trichome morphogenesis on leaves ofCyphomandra betacea Sendt. (Solanaceae). — Israel J. Bot.34: 253–264.

    Google Scholar 

  • Mascré, M., 1921: Recherches sur la développement de l'anthère chez les Solanacées (Contribution à l'étude de l'assise nouricère du pollen). — Thèses presentés à la Faculté de Sciences de Paris.

  • Moscone, E., 1989: Estudios citotaxonómicos en las TribusSolaneae yNicotianeae (Solanaceae) de America del Sur. — Thesis, University of Córdoba, Argentina.

    Google Scholar 

  • Nimer, E., 1977: Clima. In: IBGE, Geografia do Brasil. Região sudeste. 3. — Rio de Janeiro: Sergraf.

    Google Scholar 

  • Prasad, T., Singh, D., 1978: Gametophytes and seed development inNicandra physaloides Gaertn. — J. Indian Bot. Soc.57: 76–83.

    Google Scholar 

  • Pringle, G., Murray, B., 1988: Chromosome size and form in the genusCyphomandra. — III. Congr. Mundial Plantas Solanáceas, Bogotá, p. 92.

  • Renner, S., 1989: A survey of reproductive biology in neotropicalMelastomataceae andMemecylaceae. — Ann. Missouri Bot. Gard.76: 496–518.

    Google Scholar 

  • Roe, K., 1967: Chromosome size inSolanum andCyphomandra: taxonomic and phylogenetic implications. — Amer. Naturalist101: 295–297.

    Google Scholar 

  • Sazima, I., 1992: Natural history of the jararaca pitviper,Bothrops jararaca, in southeastern Brazil. — InCampbell, J., Brodie, E. jr., (Eds): Biology of the pitvipers, pp. 199–216. — Tyler, Texas: Selva Publ.

    Google Scholar 

  • Sazima, M., Vogel, S., 1989:Cyphomandra species (Solanaceae) visited by euglossine bees: floral fragrance as a reward for pollen dispersal. — Abstr. 9. Symposium Morphologie, Anatomie und Systematik Wien 1989, p. 52. — University of Vienna, Institute of Botany.

  • Sendtner, O., 1845: Monographia Cyphomandrae, novi Solanacearum generis. — Flora28: 161–176.

    Google Scholar 

  • Sharma, R., Raghuvanshi, R., Singh, D., 1987: Embryological studies inAtropa andHyoscyamus. — J. Indian Bot. Soc.66: 311–316.

    Google Scholar 

  • Siddiqui, S., Kahn, T., 1988: Ontogeny and dehiscence of anther inSolanaceae. — Bull. Soc. Bot. France132: 101–109.

    Google Scholar 

  • Smith, L. B., Downs, R. J., 1966: Solanáceas. — InReitz, P. R., (Ed.): Flora ilustrada Catarinense 1 fasc. sola, pp. 1–321. — Itajaí: Tip. Livr. Blŭmenavense S. A.

    Google Scholar 

  • Smith, B., Roubik, D., 1983: Mandibular glands of stingless bees (Hymenoptera: Apidae). — J. Chem. Ecol.9: 1465–1472.

    Google Scholar 

  • Soares, A. A., de Campos, O., Viera, M. F., de Melo, G. R., 1989: Relações entreEuglossa (Euglossella)mandibularis Friese 1899 (Hymen. Apidae, Euglossini) eCyphomandra calycina (Solanaceae). — Ciênc. Cult.41: 903–905.

    Google Scholar 

  • Staedtler, G., 1923: Über Reduktionserscheinungen im Bau der Antherenwand von Angiospermen-Blüten. — Flora116: 85–108.

    Google Scholar 

  • Suhende, S., 1974: Studies inGasteromycetes I: Notes on spore liberation and spore dispersal inGeastrum. — Svensk Bot. Tidskr.68: 329–343.

    Google Scholar 

  • Tengö, J., Bergström, G., 1977: Comparative analyses of complex secretions from heads ofAndrena bees (Hym., Apoidea). — Comp. Biochem. Physiol.57 B: 197–202.

    Google Scholar 

  • Thiagarajan, P., 1986: Prefertilization development in theSolanaceae, an overview. — J. Indian Bot. Soc. (Suppl.)65: 72.

    Google Scholar 

  • Thien, L. B., 1974: Floral odors and quantitative taxonomy ofMagnolia andLiriodendron. — Taxon24: 557–568.

    Google Scholar 

  • Tollsten, L., Bergström, J., 1989: Variation and postpollination changes in floral odours released byPlatanthera bifolia (Orchid.). — Nordic J. Bot.9: 359–362.

    Google Scholar 

  • Ule, E., 1895: Über die Blüteneinrichtungen vonPurpurella cleistopetala, einer neuen Melastomatacee. — Ber. Deutsch. Bot. Ges.14: 169–178.

    Google Scholar 

  • Vogel, S., 1962: Duftdrüsen im Dienste der Bestäubung. — Abh. Akademie Wiss. Lit., math.-nat. Kl. Mainz10: 1–165.

    Google Scholar 

  • , 1966: Parfümsammelnde Bienen als Bestäuber von Orchideen undGloxinia. — Österr. Bot. Z.113: 302–361.

    Google Scholar 

  • , 1978: Evolutionary shifts from reward to deception in pollen flowers. — InRichards, A., (Ed.): The pollination of flowers by insects. — Linn. Soc. Symp. Bot. Ser.6: 89–96. — London: Academic Press.

    Google Scholar 

  • , 1990: The role of scent glands in pollination. — English translation, ed. byRenner, S. — Washington: Smithsonian Institution Libraries, New Delhi: Amerind Publ. Comp. Ltd.

    Google Scholar 

  • Whitten, W., Williams, N., Armbruster, W., Battiste, M., Strekowski, L., Lindquist, N., 1986: Carvone epoxide: an example of convergent evolution in euglossine pollinated plants. — Syst. Bot.11: 222–228.

    Google Scholar 

  • , 1988: Occurrence of ipsdienol in floral fragrances. — Phytochemistry27: 2759–2760.

    Google Scholar 

  • , 1989: Function of glandular secretions in fragrance collection by male euglossine bees (Apidae, Euglossini). — J. Chem. Ecol.15: 1285–1296.

    Google Scholar 

  • Williams, N., 1982: The biology of orchids and euglossine bees. — InArditti, J., (Ed.): Orchid biology: reviews and perspectives II, pp. 119–171. — Ithaca, N. Y.: Cornell University Press.

    Google Scholar 

  • , 1976: Euglossine pollination ofSpathiphyllum (Araceae). — Selbyana (Sarasota, Florida)1: 349–356.

    Google Scholar 

  • , 1983: Orchid floral fragrances and male euglossine bees: methods and advances in the last sesquidecade. — Biol. Bull.164: 355–395.

    Google Scholar 

  • Witasek, J., 1931:Solanaceae. — Denkschr. Akad. Wiss. Wien, math.-nat. Kl.79: 313–375.

    Google Scholar 

  • Wittmann, D., Hoffmann, W., Scholz, E., 1988: Southern distributional limits of euglossine bees in Brazil linked to habitats of the Atlantic and subtropical rain forest (Hymenoptera: Apidae: Euglossini). — Entomol. Generalis14: 53–60.

    Google Scholar 

  • Zeisler, M., 1938: Über die Abgrenzung der eigentlichen Narbenfläche mit Hilfe von Reaktionen. — Beih. Bot. Centralbl., Sect. A,58: 308–318.

    Google Scholar 

  • Ziegler, A., 1925: Beiträge zur Kenntnis des Androeceums und der Samenentwicklung einiger Melastomataceen. — Bot. Archiv9: 398–467.

    Google Scholar 

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Authors and Affiliations

  1. Departmento de Botânica, Universidade Estadual de Campinas, Postal 6109, 13081-970, Caixa, Campinas, S.P., Brazil

    Marlies Sazima

  2. Institut für Spezielle Botanik, Johannes Gutenberg-Universität Mainz, Postfach 3980, D-55099, Mainz, Germany

    Stefan Vogel & Gerlinde Hausner

  3. Instituto Multidisciplinario de Biología Vegetal, Universidad de Córdoba, Casilla de Correo 495, 5000, Córdoba, Argentina

    Andrea Cocucci

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  1. Marlies Sazima
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Sazima, M., Vogel, S., Cocucci, A. et al. The perfume flowers ofCyphomandra (Solanaceae): Pollination by euglossine bees, bellows mechanism, osmophores, and volatiles. Pl Syst Evol 187, 51–88 (1993). https://doi.org/10.1007/BF00994091

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