Plant Systematics and Evolution

, Volume 213, Issue 1–2, pp 71–90 | Cite as

Floral biology and reproductive ecology ofClusia nemorosa (Clusiaceae) in northeastern Brazil

  • Ariadna Valentina Lopes
  • Isabel Cristina Machado


Between March 1993 and May 1995 the floral biology and the phenology ofClusia nemorosaG. Mey. (Clusiaceae) were studied in two dioecious populations in Pernambuco State, and some observations were made in gynodioecious populations, that were encountered only in Bahia State. The species flowers from June to January/February. The flowers are bowl shaped, and last only one day. The floral reward is resin which is produced by staminodia in all types of flowers. The sex ratio was 1:1 for the studied populations. The pollen viability was approximately 98%. Apomixis was not observed. The rate of fruit set, in hermaphrodite individuals, under natural conditions and the sex ratio of the gynodioecious populations studied suggest that the hermaphrodite individuals may behave as males.Clusia nemorosa is melittophilous and was visited by 16 species of bees. The main pollinators wereEuplusia mussitans, E. iopyhrra, Eulaema cingulata, E. nigrita, Euglossa cordata andEuglossa sp.

Key words

Clusiaceae Clusia Melittophily dioecy gynodioecy polygamodioecy floral resin euglossine bees 


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  1. Andrade, V. C., 1987: O gêneroClusia L. (Clusiaceae Lindley) no Estado de Pernambuco (Brasil). — Dissertação de Mestrado, Universidade Federal Rural de Pernambuco, Brasil.Google Scholar
  2. Armbruster, W. S., 1984: The role of resin in Angiosperm pollination: ecological and chemical considerations. — Amer. J. Bot.71: 1149–1160.Google Scholar
  3. , 1986: Reproductive interactions between sympatricDalechampia species: Are natural assemblages “random” or organized? — Ecology67: 522–533.Google Scholar
  4. , 1984: Partitioning and sharing of pollinators by four sympatric species ofDalechampia (Euphorbiaceae) in Panama. — Ann. Missouri Bot. Gard.71: 1–16.Google Scholar
  5. , 1992: Pollination ecology of fourDalechampia species (Euphorbiaceae) in Northern Natal, South Africa. — Amer. J. Bot.79: 306–313.Google Scholar
  6. , 1979: Pollination of two species ofDalechampia (Euphorbiaceae) in Mexico by euglossine bees. — Biotropica11: 278–283.Google Scholar
  7. , 1981: Sistemas de polinização de duas espécies simpátricas deDalechampia (Euphorbiaceae) no Amazonas, Brasil. — Acta Amazon.11: 13–17.Google Scholar
  8. , 1982: Divergent pollination systems in sympatric species of South AmericanDalechampia (Euphorbiaceae). — Amer. Midl. Naturalist.108: 325–337.Google Scholar
  9. , 1992: Pollination of two sympatric species ofDalechampia (Euphorbiaceae) in Suriname by male Euglossine Bees. — Amer. J. Bot.79: 1374–1381.Google Scholar
  10. , 1995: Reproductive significance of indirect pollen-tube growth inDalechampia (Euphorbiaceae). — Amer. J. Bot.82: 51–56.Google Scholar
  11. Armstrong, J. E., Irvine, A. K., 1989: Flowering, sex ratios, pollen-ovule ratios, fruit set, and reproductive effort of a dioecious tree,Myristica insipida (Myristicaceae), in two different rain forest communities. — Amer. J. Bot.76: 74–85.Google Scholar
  12. Arroyo, M. T. K., Raven, P. H., 1975: The evolution of subdioecy in morphologically gynodioecious species ofFuchsia sect.Encliandra (Onagraceae). — Evolution29: 500–511.Google Scholar
  13. Assouad, M. W., Dommée, B., Lumaret, R., Valdeyron, G., 1978: Reproductive capacities in the sexual forms of the gynodioecious speciesThymus vulgaris L. — Bot. J. Linn. Soc.77: 29–39.Google Scholar
  14. Barrett, S. C. H., 1992: Gender variation and the evolution of dioecy inWurmbea dioica (Liliaceae). — J. Evol. Biol.5: 423–444.Google Scholar
  15. Bawa, K. S., 1980a: Mimicry of male by female flowers and intrasexual competition for pollinators inJacaratia dolichaula (D. Smith)Woodson (Caricaceae). — Evolution34: 467–474.Google Scholar
  16. , 1980b: Evolution of dioecy in flowering plants. — Ann. Rev. Ecol. Syst.11: 15–39.Google Scholar
  17. , 1975: Dioecism in tropical forest trees. — Evolution29: 167–179.Google Scholar
  18. Bittrich, V., 1994: Biologia da polinização de algumas espécies deClusia da América do Sul. — Res. XLV Congr. Nac. Bot. São Leopoldo, RS. Brasil, pp. 180–181.Google Scholar
  19. - 1995: Polinização deClusia schomburgkiana eClusia columnaris. — Res. XLVI Congr. Nac. Bot. Ribeirão Preto, SP, Brasil, p. 154.Google Scholar
  20. -Amaral, M. C. E., 1994: O papel dos líquidos apolares na biologia de polinização deClusiaceae. — Res. XLV Congr. Nac. Bot. São Leopoldo, RS, Brasil, p. 258.Google Scholar
  21. , 1996: Flower morphology and pollination biology of someClusia species from the Gran Sabana (Venezuela). — Kew Bull.51: 681–694.Google Scholar
  22. Buchmann, S. L., 1983: Buzz pollination in angiosperms. — InJones, C. E., Little, R. J., (Eds): Handbook of experimental pollination biology, pp. 73–113. — New York: Van Ostrand.Google Scholar
  23. Bullock, S. H., Bawa, K. S., 1981: Sexual dimorphism and the annual flowering pattern inJacaratia dolichaula (D. Smith)Woodson (Caricaceae) in a Costa Rican Rain Forest. — Ecology62: 1494–1504.Google Scholar
  24. Cammerloher, H., 1931: Blütenbiologie I. — Berlin: Borntraeger.Google Scholar
  25. Correia, M. C. R., 1983: Contribuição ao estudo da biologia floral e do sistema de reprodução deClusia fluminensis Pl. & Tr. (Guttiferae). — Dissertação de Mestrado. Universidade Federal do Rio de Janeiro, Brasil.Google Scholar
  26. , 1989: Biologia da reprodução das espécies deClusia da Restinga de Maricá — RJ, Brasil. — Res. XL Congr. Nac. Bot. Cuiabá, MT, Brasil1: 100.Google Scholar
  27. , 1993: Estudo da biologia floral deClusia criuva Camb.: um caso de mimetismo. — Bradea24: 209–219.Google Scholar
  28. Costich, D. E., Galán, F., 1988: The ecology of monoecious and dioecious subspecies ofEcballium elaterium (L.)Richard (Cucurbitaceae). I. Geographic distribution and relationship to climate conditions in Spain. — Lagascalia15: 697–710.Google Scholar
  29. Croat, T. B., 1978: Flora of Barro Colorado island. — Stanford: Stanford University Press.Google Scholar
  30. Dafni, A., 1992: Pollination ecology — a practical approach. — Oxford: Oxford University Press.Google Scholar
  31. Dommée, B., Assouad, M. W., Valdeyron, G., 1978: Natural selection and gynodioecy inThymus vulgaris L. — Bot. J. Linn. Soc.77: 17–28.Google Scholar
  32. Endress, P. K., 1994: Diversity and evolutionary biology of tropical flowers. — Cambridge: Cambridge University Press.Google Scholar
  33. Erdtman, G., 1966: Pollen morphology and plant taxonomy — angiosperms. — New York: Hafner.Google Scholar
  34. Faegri, K., Pijl, L., van der, 1979: The principles of pollination ecology. — London: Pergamon Press.Google Scholar
  35. Frankie, G. W., Harber, W. A., Opler, P. A., Bawa, K. S., 1983: Characteristics and organisation of the large bee pollination system in the Costa Rican dry forest. — InJones, C. E., Little, R. J., (Eds): Handbook of experimental pollination biology, pp. 411–447. — New York: Van Nostrand.Google Scholar
  36. Galen, C., Plowright, R. C., 1987: Testing the accuracy of using peroxidase activity to indicate stigma receptivity. — Canad. J. Bot.65: 107–111.Google Scholar
  37. Gentry, A. H., 1974: Flowering phenology and diversity in tropicalBignoniaceae. — Biotropica6: 64–68.Google Scholar
  38. Gottsberger, G., Amaral, A., Jr., 1984: Pollination strategies in BrazilianPhilodendron species. — Ber. Deutsch. Bot. Ges.97: 391–410.Google Scholar
  39. Herrera, C. M., 1988: Variation in mutualisms: the spatio-temporal mosaic of a pollinator assemblage. — Biol. J. Linn. Soc.35: 95–125.Google Scholar
  40. Horovitz, A., Galil, J., 1972: Gynodioecism in East MediterraneanHirschfeldia incana. Cruciferae. — Bot. Gaz.133: 127–131.Google Scholar
  41. Hutchinson, J., 1969: Evolution and phylogeny of flowering plants — Dicotyledons: facts and theory. — London: Academic Press.Google Scholar
  42. Janzen, D. H., 1971: Euglossine bees as long distance pollinators of tropical plants. — Science171: 203–205.Google Scholar
  43. Kohn, J. R., 1988: Why be female? — Nature335: 431–433.Google Scholar
  44. Lloyd, D. G., 1972: Breeding systems inCotula L. (Compositae, Anthemideae). I. The array of monoclinous and diclinous systems. — New Phytol.71: 1181–1194.Google Scholar
  45. , 1975: The maintenance of gynodioecy and androdioecy in angiosperms. — Genetica45: 325–339.Google Scholar
  46. , 1976: The transmission of genes via pollen and ovules in gynodioecious angiosperms. — Theor. Populat. Biol.9: 229–316.Google Scholar
  47. , 1977: Secondary sex characters in plants. — Bot. Rev.43: 177–216.Google Scholar
  48. Lopes, A. V. F., Machado, I. C. S., 1996: Biologia floral deSwartzia pickelii (Leguminosae-Papilionoideae) e sua polinização porEulaema spp. (Apidae-Euglossini). — Revista Brasil. Bot.19: 17–24.Google Scholar
  49. Maguire, B., 1966: The genusClusia (Clusiaceae) in Suriname. — Acta Bot. Neerl.15: 63–75.Google Scholar
  50. , 1976: Apomixis in the genusClusia (Clusiaceae). A preliminary report. — Taxon25: 241–244.Google Scholar
  51. , 1978: Notes on theClusiaceae — chiefly of Panama. III. — Phitologia39: 65–77.Google Scholar
  52. , 1961: The botany of the Guayana Highland. Part IV. — Mem. New York Bot. Gard.10: 1–87.Google Scholar
  53. Mariz, G., 1974: Chaves para as espécies deClusia nativas no Brasil. — Mem. Inst. Bioc. Univ. Fed. PE, Brasil.1: 249–314.Google Scholar
  54. Mayo, S. J., 1986: Systematics ofPhilodendron Schott (Araceae) with special reference to inflorescence characters. — Ph.D. Thesis, University of Reading, UK.Google Scholar
  55. , 1991: A revision ofPhilodendron subgenusMeconostigma (Araceae). — Kew Bull.46: 601–681.Google Scholar
  56. Mesquita, R. C. G., Franciscon, C. H., 1995: Flower visitors ofClusia nemorosa G. F. W. Meyer (Clusiaceae) in an Amazonian white-sand Campina. — Biotropica27: 254–257.Google Scholar
  57. Morellato, L. P. C., Leitã-Filho, H. F., Rodrigues, R. R., Joly, C. A., 1990: Estratégias fenológicas de espécies arbóreas em floresta de altitude na Serra do Japi, Jundiaí, São Paulo. — Revista Brasil. Biol.50: 149–162.Google Scholar
  58. Newstron, L. E., Frankie, G. W., Baker, H. G., 1994a: A new classification for phenology based on flowering patterns in Lowland Tropical Rain Forest trees at La Selva, Costa Rica. — Biotropica26: 141–159.Google Scholar
  59. , 1994b: Diversity of long-term flowering patterns. — InMcDade, L. A., Bawa, K. S., Hespenheide, H., Hartshorn, G., (Eds): La Selva: ecology and natural history of a neotropical rain forest, pp. 142–160. — Chicago: University of Chicago Press.Google Scholar
  60. Oliveira, P. E. A. M, Sazima, M., 1990: Pollination biology of two species ofKielmeyera (Guttiferae) from Brazilian Cerrado Vegetation. — Pl. Syst. Evol.172: 35–49.Google Scholar
  61. Opler, P. A., Bawa, K. S., 1978: Sex ratio in tropical forest trees. — Evolution32: 812–821.Google Scholar
  62. Pijl, L. van der, 1978: Reproductive integration and sexual disharmony in floral functions. — InRichards, A. J., (Ed.): The pollination of flowers by insects. — Linnean Society Symposium Series6, pp. 79–88. — London: Academic Press.Google Scholar
  63. Radford, A. E., Dickinson, W. C., Massey, J. R., Bell, C. R., 1974: Vascular plant systematics. — New York: Harper & Row.Google Scholar
  64. Ramírez, W. B., Gómez, L. D. P., 1978: Production of nectar and gums by flowers ofMonstera deliciosa (Araceae) and of some species ofClusia (Guttiferae) collected by New WorldTrigona bees. — Brenesia14/15: 407–412.Google Scholar
  65. Renner, S. S., Feil, J. P., 1993: Pollinators of tropical dioecious angiosperms. — Amer. J. Bot.80: 1100–1107.Google Scholar
  66. Richards, A. J., 1986: Plant breeding systems. — London: George Allen & Unwin.Google Scholar
  67. Robertson, J. L., Wyatt, R., 1990: Evidence for pollination ecotypes in the yellow-fringed orchid,Platanthera ciliaris. — Evolution44: 121–133.Google Scholar
  68. Ross, M. D., 1970: Evolution of dioecy from gynodioecy. — Evolution24: 827–828.Google Scholar
  69. , 1982: Five evolutionary pathways to subdioecy. — Amer. Naturalist119: 297–318.Google Scholar
  70. Roubik, D. W., 1992: Ecology and natural history of tropical bees. — Cambridge: Cambridge University Press.Google Scholar
  71. Sazima, M., Sazima, I., Carvalho-Okano, R. M., 1985: Biologia floral deDalechampia stipulacea (Euphorbiaceae) e sua polinização porEuglossa melanotricha (Apidae). — Revista Brasil. Biol.45: 85–93.Google Scholar
  72. Scogin, R., Young, D. A., Jones, C. E., 1977: Anthochlor pigments and pollination biology II. The ultraviolet floral patterns ofCoreopsis gigantea (Asteraceae). — Bull. Torrey Bot. Club104: 155–159.Google Scholar
  73. Simpson, B. B., Neff, J. L., 1981: Floral rewards: alternatives to pollen and nectar. — Ann. Missouri Bot. Gard.68: 301–322.Google Scholar
  74. , 1983: Evolution and diversity of floral rewards. — InJones, C. E., Little, R. J., (Eds): Handbook of experimental pollination biology, pp. 142–159. — New York: Van Nostrand.Google Scholar
  75. Steiner, K. E., Whitehead, V. B., 1991: Resin collection and pollination ofDalechampia capensis (Euphorbiaceae) byPachyanthidium cordatum (Hymenoptera-Megachilidae) in South Africa. — J. Entomol. Soc. S. Africa54: 67–72.Google Scholar
  76. Stephen, N. P., Bohart, G. E., Torchio, P. F., 1969: The biology and external morphology of bees. — Oregon: Oregon State University.Google Scholar
  77. Vogel, S., 1963: Duftdrüsen im Dienste der Bestäubung. Über Bau und Funktion der Osmophoren. — Akad. Wiss. Mainz Abh. Math.-Naturwiss. Kl.10: 600–763.Google Scholar
  78. Willson, M. F., Ågren, J., 1989: Differential floral rewards and pollination by deceit in unisexual flowers. — Oikos55: 23–29.Google Scholar
  79. Zapata, T. R., Arroyo, M. T. K., 1978: Plant reproductive ecology of a secondary deciduous tropical forest in Venezuela. — Biotropica10: 221–230.Google Scholar
  80. Zeisler, M., 1938: Über die Abgrenzung der eigentlichen Narbenfläche mit Hilfe von Reaktionen. — Beih. Bot. Centralbl.58: 308–318.Google Scholar
  81. Zucchi, R., Sakagami, S. F., Camargo, J. M. F., 1969: Biological observations on Neotropical parasocial beeEulaema nigrita, with a review on the biology ofEuglossinae (Hymenoptera, Apidae), A comparative study. — J. Fac. Sci. Hokkaido Univ.17: 271–380.Google Scholar

Copyright information

© Springer-Verlag 1998

Authors and Affiliations

  • Ariadna Valentina Lopes
    • 1
  • Isabel Cristina Machado
    • 1
  1. 1.Departamento de Botânica, Centro de Ciências BiológicasUniversidade Federal de PernambucoRecife, PernambucoBrasil

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