Abstract
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.
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Agren, E., Elnquist, T., Tunlid, A., 1986: Pollination by deceit, floral sex ratios, and seed sex in dioeciousRubus chamaemorus L. — Oecologia70: 332–338.
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.
—,Ponzi, R., Pizzolongo, P., 1989: Prime osservazioni sulla biologia della riproduzione inOsyris alba L. — G. Bot. Italiano (Suppl. 1)123: 168.
Arroyo, J., Herrera, J., 1988: Polinizacion y arquitectura floral enEricaceae de Andaluca occidental. — Lagascalia15: 615–623.
Ashton, P. S., 1969: Speciation among tropical forest trees: some deduction in the light of recent evidence. — Biol. J. Linn. Soc.1: 155–196.
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.
—,Baker, I., 1979: Starch in angiosperm pollen grains and its evolutionary significance. — Amer. J. Bot.66: 591–600.
—, —, 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.
—, —, 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.
Barrett, S. C. H., Helernum, K., 1981: Floral sex ratios and life history inAralia nudicaulis (Araliaceae). — Evolution35: 752–762.
Bawa, K. S., 1974: Breeding systems of tree species of a lowland tropical community. — Evolution28: 85–92.
—, 1977: The reproductive biology ofCupania guatemalensis Radlk. (Sapindaceae). — Evolution31: 52–63.
—, 1980a: Mimicry of male by female flowers and intrasexual competition for pollination inJacaratia dolichaula (D. Smith)Woodson (Caricaceae). — Evolution34: 467–474.
—, 1980b: Evolution of dioecy in flowering plants. — Annu. Rev. Evol. Syst.11: 15–39.
—,Opler, P. A., 1975: Dioecism in tropical forest trees. — Evolution29: 167–179.
—,Keegan, C. R., Voss, R. H., 1982: Sexual dimorphism inAralia nudicaulis L. (Araliaceae). — Evolution36: 371–378.
Bosch, J., 1992: Floral biology and pollinators of three co-occurringCistus species (Cistaceae). — Bot. J. Linn. Soc.109: 39–55.
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.
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.
Cox, P. A., 1981: Niche partitioning between sexes of dioecious plants. — Amer. Naturalist117: 295–307.
Currier, H. B., 1957: Callose substance in plant cells. — Amer. J. Bot.44: 478–488.
Dafni, A., 1984: Mimicry and deception in pollination. — Annu. Rev. Ecol. Syst.15: 259–278.
—,Ivri, Y., 1981: The flower biology ofCephalanthera longifolia (Orchidaceae). — Pollen imitation and facultative floral mimicry. — Pl. Syst. Evol.137: 229–240.
Dressler, R. L., 1981: The Orchids—Natural history and classification. — Cambridge, Mass: Harvard University Press.
Freeman, D. C., Klikof, L. G., Harper, K. T., 1976: Differential resource utilization by the sexes of dioecious plants. — Science193: 597–599.
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.
Givnish, T. J., 1980: Ecological constraints on the evolution of breeding systems in seed plants: dioecy and dispersal in gymnosperms. — Evolution34: 959–972.
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.
Guignard, L., 1885: Observations sur les Santalacées. — Ann. Sci. Nat. (Bot.)2: 181–202.
Herrera, C. M., 1982: Breeding systems and dispersal-related maternal reproductive effort of southern spanish bird-dispersed plants. — Evolution36: 1299–1314.
—, 1984: The annual cycle ofOsyris quadripartita, a hemiparasitic dioecious shrub of Mediterranean scrublands. — J. Ecol.72: 1065–1078.
—, 1985: Predispersal reproductive biology of femaleOsyris quadripartita (Santalaceae), a hemiparasitic dioecious shrub of Mediterranean scrublands. — Bot. J. Linn. Soc.90: 113–127.
Herrera, J., 1988: Pollination relationships in southern Spanish Mediterranean scrublands. — J. Ecol.76: 274–287.
—, 1991: The reproductive biology of a riparian Mediterranean shrub,Nerium oleander L. (Apocynaceae). — Bot. J. Linn. Soc.106: 147–172.
—, 1992: Flower variation and breeding systems in theCistaceae. — Pl. Syst. Evol.179: 245–255.
Heslop-Harrison, Y., 1977: The pollen-stigma interaction pollen-tube penetration inCrocus. — Ann. Bot.41: 913–922.
—,Shivanna, K. R., 1977: The receptive surface of the angiosperm stigma. — Ann. Bot.41: 1233–1258.
Heywood, V. H., 1978: Flowering plants of the world. — Oxford: Oxford University Press.
Hilty, S. L., 1980: Flowering and fruiting periodicity in a premontane rain forest in Pacific Colombia. — Biotropica12: 292–306.
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.
Jensen, W. A., 1962: Botanical histochemistry. — San Francisco: Freeman & Co.
Joshi, P. C., 1960: Morphological and embryological studies in the familySantalaceae. — V.Osyris wightiana Woll. — Phytomorphology10: 239–248.
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.
Kerner, A., Oliver, F. W., 1895: The natural history of plants. II, pp. 169–171. — London: Blackie.
Kuijt, J., 1969: The biology of parasitic flowering plants. — Berkeley: University of California Press.
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.
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.
Lloyd, D. G., Webb, G. J., 1977: Secondary sex characters in plants. — Bot. Rev.43: 177–216.
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.
Pasteur, G., 1982: A classificatory review of mimicry systems. — Annu. Rev. Ecol. Syst.13: 169–199.
Pearse, A. G. E., 1972: Histochemistry: theoretical and applied. II. — London, Edinburgh: Churchill Livingstone.
Petanidou, T., Vokou, D., 1990: Pollination and pollen energetics in Mediterranean ecosystems. — Amer. J. Bot.77: 986–992.
Raven, P. H., 1973: Plant biogeography. Introduction. — InDi Castri, F., Mooney, H. A., (Eds): Mediterranean-type ecosystems, pp. 211–212. — Berlin: Springer.
Reitsma, T., 1970: Suggestion towards unification of descriptive terminology of angiosperm pollen grains. — Rev. Paleobot. Palynol.10: 39–60.
Schaeppi, H., Steindl, F., 1937: Blütenmorphologische und embryologische Untersuchungen anOsyris alba L. — Ber. Schweiz. Bot. Ges.47: 369–392.
Schmid, R., 1978: Reproductive anatomy ofActinidia chinensis (Actinidiaceae). — Bot. Jahrb. Syst.100: 149–195.
Thien, L. B., Marcks, B. G., 1972: The floral biology ofArethusa bulbosa, Calopogon tuberosus, andPogania ophioglossoides (Orchidaceae). — Canad. J. Bot.23: 19–25.
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.
—,Dodson, C. H., 1966: Orchid flowers: their pollination and evolution. — Coral Gables, Fl: University of Miami Press.
Van Tieghem, M. P., 1869: Anatomie de la fleur des Santalacées. — Ann. Sci. Nat. Bot.12: 340–346.
Vogel, S., 1975: Mutualismus und Parasitismus in der Nutzung von Pollenträgern. — Verh. Deutsch. Zool. Ges. 1975: 102–110.
—, 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.
Wallace, C. S., Rundel, P. W., 1979: Sexual dimorphism and resource allocation in male and female shrubs ofSimmondsia chinensis. — Oecologia44: 34–39.
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Aronne, G., Wilcock, C.C. & Pizzolongo, P. Pollination biology and sexual differentiation ofOsyris alba (Santalaceae) in the Mediterranean region. Pl Syst Evol 188, 1–16 (1993). https://doi.org/10.1007/BF00937832
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DOI: https://doi.org/10.1007/BF00937832