Plant Systematics and Evolution

, Volume 188, Issue 1–2, pp 1–16 | Cite as

Pollination biology and sexual differentiation ofOsyris alba (Santalaceae) in the Mediterranean region

  • G. Aronne
  • C. C. Wilcock
  • P. Pizzolongo


Osyris alba L. is a widespread dioecious hemiparasitic shrub of S Europe, N Africa, and SW Asia. Male inflorescences are multiflowered whereas each female inflorescence is reduced to a single flower with persistent enlarged bracts. Pollination is a prerequisite for fruit and seed development and wind is unlikely to be an effective means of pollen spread. In southern Italy pollen is transported by small unspecialized flies and beetles. Both male and female flowers produce an indistinguishable sweet odour. Male flowers are produced in large numbers and over a larger period than the females and provide pollen, nectar, and staminal hairs as rewards for pollinators. The presence and function of staminal hairs with tip cells inOsyris alba has been reported for the first time. Female flowers are rewardless, producing neither mature pollen, nectar nor staminal hairs, but possess three modified yellow indehiscent anthers containing no viable pollen which may provide a strong visual feeding stimulus for pollinators. It is suggested that pollinators are attracted by deceit to female flowers by mimicry of the males and the floral mimicry is, therefore, intraspecific and intersexual. The floral characteristics and flowering phenology of male and female plants are consistent with this kind of mimicry. The female flower possesses a tricarpellary ovary with three ovules of which only one develops. The single seed, containing a small embryo and a large, rich endosperm, is borne in a red fleshy bird-dispersed fruit. The reduction in seed number per flower to one highly nutrient-invested seed, together with a reduction of the multiflowered inflorescence to a solitary flower and the sequential production of ripe fruits over an extended fruiting season, suggest that the female function is markedly resource-limited. It is suggested that, although all the reproductive characteristics present inOsyris alba, as well as hemiparasitism, had probably evolved before the end of the tropical Tertiary, they are of adaptive advantage in the nutrient and water-limited environment of the Mediterranean maquis.

Key words

Santalaceae Osyris alba Phenology dioecy floral morphology floral mimicry pollination biology Mediterranean shrublands 


Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.


  1. Agren, E., Elnquist, T., Tunlid, A., 1986: Pollination by deceit, floral sex ratios, and seed sex in dioeciousRubus chamaemorus L. — Oecologia70: 332–338.Google Scholar
  2. Aronne, G., Wilcock, C. C., 1992: Reproductive evolution and breeding system in relation to environmental stress in shrubs of the Mediterranean region. — InThanos, A., (Ed.): Plant-animal interactions in Mediterranean type ecosystems, pp. 223–227. — Maleme, Greece: University of Athens Press.Google Scholar
  3. —,Ponzi, R., Pizzolongo, P., 1989: Prime osservazioni sulla biologia della riproduzione inOsyris alba L. — G. Bot. Italiano (Suppl. 1)123: 168.Google Scholar
  4. Arroyo, J., Herrera, J., 1988: Polinizacion y arquitectura floral enEricaceae de Andaluca occidental. — Lagascalia15: 615–623.Google Scholar
  5. Ashton, P. S., 1969: Speciation among tropical forest trees: some deduction in the light of recent evidence. — Biol. J. Linn. Soc.1: 155–196.Google Scholar
  6. Baker, H. G., 1976: “Mistake pollination” as a reproductive system with special reference to theCaricaceae. — InBurley, J., Styles, B. T., (Eds): Tropical trees: variations, breeding and conservation, pp. 161–169. — London: Academic Press.Google Scholar
  7. —,Baker, I., 1979: Starch in angiosperm pollen grains and its evolutionary significance. — Amer. J. Bot.66: 591–600.Google Scholar
  8. —, —, 1983a: Some evolutionary and taxonomic implications of variation in the chemical reserves of pollen. — InMulchay, D. L., Ottaviano, E., (Eds): Pollen: biology and implications for plant breeding, pp. 43–52. — New York: Elsevier.Google Scholar
  9. —, —, 1983b: Floral nectar sugar constituents in relation to pollinator type. — InJones, C. E., Little, R. J., (Eds): Handbook of experimental pollination biology, pp. 117–141. — New York: Scientific & Academic Press.Google Scholar
  10. Barrett, S. C. H., Helernum, K., 1981: Floral sex ratios and life history inAralia nudicaulis (Araliaceae). — Evolution35: 752–762.Google Scholar
  11. Bawa, K. S., 1974: Breeding systems of tree species of a lowland tropical community. — Evolution28: 85–92.Google Scholar
  12. —, 1977: The reproductive biology ofCupania guatemalensis Radlk. (Sapindaceae). — Evolution31: 52–63.Google Scholar
  13. —, 1980a: Mimicry of male by female flowers and intrasexual competition for pollination inJacaratia dolichaula (D. Smith)Woodson (Caricaceae). — Evolution34: 467–474.Google Scholar
  14. —, 1980b: Evolution of dioecy in flowering plants. — Annu. Rev. Evol. Syst.11: 15–39.Google Scholar
  15. —,Opler, P. A., 1975: Dioecism in tropical forest trees. — Evolution29: 167–179.Google Scholar
  16. —,Keegan, C. R., Voss, R. H., 1982: Sexual dimorphism inAralia nudicaulis L. (Araliaceae). — Evolution36: 371–378.Google Scholar
  17. Bosch, J., 1992: Floral biology and pollinators of three co-occurringCistus species (Cistaceae). — Bot. J. Linn. Soc.109: 39–55.Google Scholar
  18. Bullock, S. H., Bawa, K. S., 1981: Sexual dimorphism and the annual flowering pattern inJacaratia dolichaula (D. Smith)Woodson (Caricaceae) in Costa Rican rain forest. — Ecology62: 1494–1504.Google Scholar
  19. Conn, J. S., Blum, U., 1981: Differentiation between the sexes ofRumex hastatulus in net energy allocation, flowering and height. — Bull. Torrey Bot. Club108: 446–455.Google Scholar
  20. Cox, P. A., 1981: Niche partitioning between sexes of dioecious plants. — Amer. Naturalist117: 295–307.Google Scholar
  21. Currier, H. B., 1957: Callose substance in plant cells. — Amer. J. Bot.44: 478–488.Google Scholar
  22. Dafni, A., 1984: Mimicry and deception in pollination. — Annu. Rev. Ecol. Syst.15: 259–278.Google Scholar
  23. —,Ivri, Y., 1981: The flower biology ofCephalanthera longifolia (Orchidaceae). — Pollen imitation and facultative floral mimicry. — Pl. Syst. Evol.137: 229–240.Google Scholar
  24. Dressler, R. L., 1981: The Orchids—Natural history and classification. — Cambridge, Mass: Harvard University Press.Google Scholar
  25. Freeman, D. C., Klikof, L. G., Harper, K. T., 1976: Differential resource utilization by the sexes of dioecious plants. — Science193: 597–599.Google Scholar
  26. Gilbert, L. E., 1975: Ecological consequences of a coevolved mutualism between butterflies and plants. — InGilbert, L. E., Raven, P. H., (Eds): Coevolution of animals and plants, pp. 211–239. — Austin: Texas University Press.Google Scholar
  27. Givnish, T. J., 1980: Ecological constraints on the evolution of breeding systems in seed plants: dioecy and dispersal in gymnosperms. — Evolution34: 959–972.Google Scholar
  28. Goss, G. J., 1977: The reproductive biology of the epiphytic orchids of Florida. 6:Polystachia flavescens (Lindley)J. J. Smith. — Amer. Orchid. Soc. Bull.46: 990–994.Google Scholar
  29. Guignard, L., 1885: Observations sur les Santalacées. — Ann. Sci. Nat. (Bot.)2: 181–202.Google Scholar
  30. Herrera, C. M., 1982: Breeding systems and dispersal-related maternal reproductive effort of southern spanish bird-dispersed plants. — Evolution36: 1299–1314.Google Scholar
  31. —, 1984: The annual cycle ofOsyris quadripartita, a hemiparasitic dioecious shrub of Mediterranean scrublands. — J. Ecol.72: 1065–1078.Google Scholar
  32. —, 1985: Predispersal reproductive biology of femaleOsyris quadripartita (Santalaceae), a hemiparasitic dioecious shrub of Mediterranean scrublands. — Bot. J. Linn. Soc.90: 113–127.Google Scholar
  33. Herrera, J., 1988: Pollination relationships in southern Spanish Mediterranean scrublands. — J. Ecol.76: 274–287.Google Scholar
  34. —, 1991: The reproductive biology of a riparian Mediterranean shrub,Nerium oleander L. (Apocynaceae). — Bot. J. Linn. Soc.106: 147–172.Google Scholar
  35. —, 1992: Flower variation and breeding systems in theCistaceae. — Pl. Syst. Evol.179: 245–255.Google Scholar
  36. Heslop-Harrison, Y., 1977: The pollen-stigma interaction pollen-tube penetration inCrocus. — Ann. Bot.41: 913–922.Google Scholar
  37. —,Shivanna, K. R., 1977: The receptive surface of the angiosperm stigma. — Ann. Bot.41: 1233–1258.Google Scholar
  38. Heywood, V. H., 1978: Flowering plants of the world. — Oxford: Oxford University Press.Google Scholar
  39. Hilty, S. L., 1980: Flowering and fruiting periodicity in a premontane rain forest in Pacific Colombia. — Biotropica12: 292–306.Google Scholar
  40. Jacobsen, J. V., Knox, R. B., Pyliotis, N. A., 1971: The structure and composition of aleurone grains in the barley aleurone layer. — Planta101: 189–209.Google Scholar
  41. Jensen, W. A., 1962: Botanical histochemistry. — San Francisco: Freeman & Co.Google Scholar
  42. Joshi, P. C., 1960: Morphological and embryological studies in the familySantalaceae. — V.Osyris wightiana Woll. — Phytomorphology10: 239–248.Google Scholar
  43. Kay, Q. O. N., Lack, A. J., Bomber, F. C., Davies, C. R., 1984: Differences between sexes in floral morphology, nectar production, and insect visits in a dioecious species,Silene dioica. — New Phytol.98: 515–529.Google Scholar
  44. Kerner, A., Oliver, F. W., 1895: The natural history of plants. II, pp. 169–171. — London: Blackie.Google Scholar
  45. Kuijt, J., 1969: The biology of parasitic flowering plants. — Berkeley: University of California Press.Google Scholar
  46. Lamont, B. B., 1983: Strategies for maximizing nutrient uptake in two Mediterranean ecosystems of low nutrient status. — InKruger, F. J., Mitchell, D. T., Jarvis, J. U. M., (Eds): Mediterranean-type ecosystems: the role of nutrients, pp. 246–273. — Ecological studies43. — Berlin: Springer.Google Scholar
  47. Little, R. J., 1983: A review of floral food deception mimicries with comments on floral mutualism. — InJones, C. E., Little, R. J., (Eds): Handbook of experimental pollination biology, pp. 294–309. — New York: Scientific & Academic Press.Google Scholar
  48. Lloyd, D. G., Webb, G. J., 1977: Secondary sex characters in plants. — Bot. Rev.43: 177–216.Google Scholar
  49. Opler, P. A., Frankie, G. W., Baker, H. G., 1980: Comparative phenological studies of treelet and shrub species in tropical wet and dry forests in the lowlands of Costa Rica. — J. Ecol.68: 167–188.Google Scholar
  50. Pasteur, G., 1982: A classificatory review of mimicry systems. — Annu. Rev. Ecol. Syst.13: 169–199.Google Scholar
  51. Pearse, A. G. E., 1972: Histochemistry: theoretical and applied. II. — London, Edinburgh: Churchill Livingstone.Google Scholar
  52. Petanidou, T., Vokou, D., 1990: Pollination and pollen energetics in Mediterranean ecosystems. — Amer. J. Bot.77: 986–992.Google Scholar
  53. Raven, P. H., 1973: Plant biogeography. Introduction. — InDi Castri, F., Mooney, H. A., (Eds): Mediterranean-type ecosystems, pp. 211–212. — Berlin: Springer.Google Scholar
  54. Reitsma, T., 1970: Suggestion towards unification of descriptive terminology of angiosperm pollen grains. — Rev. Paleobot. Palynol.10: 39–60.Google Scholar
  55. Schaeppi, H., Steindl, F., 1937: Blütenmorphologische und embryologische Untersuchungen anOsyris alba L. — Ber. Schweiz. Bot. Ges.47: 369–392.Google Scholar
  56. Schmid, R., 1978: Reproductive anatomy ofActinidia chinensis (Actinidiaceae). — Bot. Jahrb. Syst.100: 149–195.Google Scholar
  57. Thien, L. B., Marcks, B. G., 1972: The floral biology ofArethusa bulbosa, Calopogon tuberosus, andPogania ophioglossoides (Orchidaceae). — Canad. J. Bot.23: 19–25.Google Scholar
  58. Van Der Pijl, L., 1978: Reproductive integration and sexual disharmony in floral functions. — InRichards, A. J., (Ed.): The pollination of flowers by insects, pp. 79–88. — London: Academic Press.Google Scholar
  59. —,Dodson, C. H., 1966: Orchid flowers: their pollination and evolution. — Coral Gables, Fl: University of Miami Press.Google Scholar
  60. Van Tieghem, M. P., 1869: Anatomie de la fleur des Santalacées. — Ann. Sci. Nat. Bot.12: 340–346.Google Scholar
  61. Vogel, S., 1975: Mutualismus und Parasitismus in der Nutzung von Pollenträgern. — Verh. Deutsch. Zool. Ges. 1975: 102–110.Google Scholar
  62. —, 1978: Evolutionary shifts from reward to deception in pollen flowers. — InRichards, A. J., (Ed.): The pollination of flowers by insects, pp. 89–96. — London: Academic Press.Google Scholar
  63. Wallace, C. S., Rundel, P. W., 1979: Sexual dimorphism and resource allocation in male and female shrubs ofSimmondsia chinensis. — Oecologia44: 34–39.Google Scholar

Copyright information

© Springer-Verlag 1993

Authors and Affiliations

  • G. Aronne
    • 1
  • C. C. Wilcock
    • 2
  • P. Pizzolongo
    • 1
  1. 1.Instituto di Botanica, Facoltà di AgrariaUniversità Federico II di NapoliPorticiItaly
  2. 2.Department of Plant and Soil ScienceUniversity of AberdeenAberdeenGreat Britain

Personalised recommendations