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Asymmetric pollen transfer and reproductive success of the hawkmoth-pollinated distylous tree Palicourea tetragona (Rubiaceae) at La Selva, Costa Rica

Published online by Cambridge University Press:  11 September 2013

Silvana Martén-Rodríguez ,
Paola Muñoz-Gamboa ,
Ruth Delgado-Dávila  and
Mauricio Quesada
Silvana Martén-Rodríguez*
Affiliation:
Departamento de Biología Evolutiva, Instituto de Ecología A.C., carretera antigua a Coatepec No. 351, El Haya, Xalapa, Veracruz 91070, México Escuela de Biología, Universidad de Costa Rica, San José, Costa Rica
Paola Muñoz-Gamboa
Affiliation:
Escuela de Biología, Universidad de Costa Rica, San José, Costa Rica
Ruth Delgado-Dávila
Affiliation:
Departamento de Biología Evolutiva, Instituto de Ecología A.C., carretera antigua a Coatepec No. 351, El Haya, Xalapa, Veracruz 91070, México
Mauricio Quesada
Affiliation:
Centro de Investigaciones en Ecosistemas, Universidad Nacional Autónoma de México, Apartado Postal 27-3 (Xangari), Morelia, Michoacán 58089, México
*
1Corresponding author. Email: [email protected]
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Abstract:

Distyly is a floral polymorphism that presumably evolved to facilitate cross-pollination and to prevent sexual interference. However, pollen transfer is often asymmetric, with one floral morph acting as a pollen donor and the other as a pollen recipient. We evaluated the association between floral morphology, pollinator visitation and effectiveness on patterns of pollen transfer in distylous Palicourea tetragona at La Selva Biological Station in Costa Rica. To assess floral variation we measured corolla, pistil and stamen traits from 66 plants. We quantified pollinator visitation and efficiency on 56 individuals and counted pollen loads on stigmas of flowers observed for 1 h. We determined fruit set 2 mo later and assessed between-morph variation in pollen transfer and female reproductive success. Floral variation was mostly consistent with a typical distylous system; however, there was overlap in the stigma heights of pin and thrum individuals in the study population. Primary pollinators were two species of hawkmoths that visited both morphs at a frequency of 2 visits per flower h−1. The mean number of pollen grains deposited on stigmas was 89 for pin and 153 for thrum individuals. However, loads of illegitimate pollen were higher on stigmas of thrum individuals, while loads of legitimate pollen were higher on stigmas of pin individuals. Consistently, fruit set was higher in pin (31%) than in thrum individuals (22%). High deposition of illegitimate pollen, in addition to the lower female reproductive success in the thrum morph reveal that distyly in P. tetragona does not always prevent sexual interference. We suggest that in long and narrow tubular flowers, like those of P. tetragona, stigma clogging by deposition of self- or same-morph pollen may reduce legitimate fertilization of ovules causing the observed asymmetric fruit set.

Keywords

asymmetric pollen transferCosta Ricadistylyhawkmothpollination
Type
Research Article
Information
Journal of Tropical Ecology , Volume 29 , Issue 6 , November 2013 , pp. 501 - 510
Copyright
Copyright © Cambridge University Press 2013 

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References

LITERATURE CITED

BAKER, H. G. 1964. Variation in style length in relation to outbreeding in Mirabilis (Nyctaginaceae). Evolution 18:507–509.CrossRefGoogle Scholar
BARRETT, S. C. H. 1990. The evolution and adaptive significance of heterostyly. Trends in Ecology and Evolution 5:144–148.CrossRefGoogle ScholarPubMed
BARRETT, S. C. H. 2002. The evolution of plant sexual diversity. Nature Reviews Genetics 3:274–284.CrossRefGoogle ScholarPubMed
BARRETT, S. C. H. & CRUZAN, M. B. 1994. Incompatibility in heterostylous plants. Pp. 189–219 in Williams, E. G., Clarke, A. E. & Knox, R. B. (eds.). Genetic control of self-incompatibility and reproductive development in flowering plants. Kluwer Academic Publishers, Boston.CrossRefGoogle Scholar
BARRETT, S. C. H. & SHORE, J. S. 2008. New insights on heterostyly: comparative biology, ecology and genetics. Pp. 3–32 in Franlin-Tong, V. E. (ed.). Self-incompatibility in flowering plants. Springer-Verlag, Berlin.CrossRefGoogle Scholar
BAWA, K. S. & BEACH, J. H. 1983. Self-incompatibility systems in the Rubiaceae of a tropical lowland wet forest. American Journal of Botany 70:1281–1288.CrossRefGoogle Scholar
BEACH, J. H. & BAWA, K. S. 1980. Role of pollinators in the evolution of dioecy from distyly. Evolution 34:1138–1142.CrossRefGoogle ScholarPubMed
BERNUCCI VIRILLO, C. B., RAMOS, F. N., CASTRO, C. & SEMIR, J. 2007. Floral biology and breeding system of Psychotria tenuinervis Muell. Arg. (Rubiaceae) in the Atlantic rain forest, SE Brazil. Acta Botanica Brasilica 21:879–884.CrossRefGoogle Scholar
BRYS, R. & JACQUEMYN, H. 2010. Floral display size and spatial distribution of potential mates affect pollen deposition and female reproductive success in distylous Pulmonaria officinalis (Boraginaceae). Plant Biology 12:597–603.Google ScholarPubMed
CRUDEN, R. W. 2009. Pollen grain size, stigma depth, and style length: the relationships revisited. Plant Systematics and Evolution 278:223–238.CrossRefGoogle Scholar
DAFNI, A., KEVAN, P. G. & HUSBAND, B. C. 2005. Practical pollination biology. Enviroquest Ltd., Cambridge. 590 pp.Google Scholar
DARWIN, C. 1877. The different forms of flowers on plants of the same species. John Murray, London. 352 pp.CrossRefGoogle Scholar
DULBERGER, R. 1992. Floral polymorphisms and their functional significance in the heterostylous syndrome. Pp. 41–84 in Barrett, S. C. H. (ed.). Monographs on theoretical and applied genetics. Springer-Verlag, New York.Google Scholar
FAIVRE, A. E. 2002. Variation in pollen tube inhibition sites within and among three heterostylous species of Rubiaceae. International Journal of Plant Sciences 163:783–794.CrossRefGoogle Scholar
FAIVRE, A. E. & MCDADE, L. A. 2001. Population-level variation in the expression of heterostyly in three species of Rubiaceae: does reciprocal placement of anthers and stigmas characterize heterostyly? American Journal of Botany 88:841.CrossRefGoogle ScholarPubMed
FEINSINGER, P. & BUSBY, W. H. 1987. Pollen carryover: experimental comparisons between morphs of Palicourea lasiorrachis (Rubiaceae), a distylous, bird-pollinated, tropical treelet. Oecologia 73:231–235.CrossRefGoogle ScholarPubMed
GANDERS, F. R. 1979. The biology of heterostyly. New Zealand Journal of Botany 17:607–635.CrossRefGoogle Scholar
GARCÍA-ROBLEDO, C. 2008. Asymmetry in pollen flow promotes gender specialization in morphs of the distylous neotropical herb Arcytophyllum lavarum (Rubiaceae). Evolutionary Ecology 22:743–755.CrossRefGoogle Scholar
HAMILTON, C. 1990. Variations on a distylous theme in Mesoamerican Psychotria subgenus Psychotria (Rubiaceae). Memoirs of the New York Botanical Garden 55:62–75.Google Scholar
LAU, P. & BOSQUE, C. 2003. Pollen flow in the distylous Palicourea fendleri (Rubiaceae): An experimental test of the disassortative pollen flow hypothesis. Oecologia 135:593–600.CrossRefGoogle ScholarPubMed
LI, A. M., WU, X. Q., ZHANG, D. X. & BARRETT, S. C. H. 2010. Cryptic dioecy in Mussaenda pubescens (Rubiaceae): a species with stigma-height dimorphism. Annals of Botany 106:521–531.CrossRefGoogle ScholarPubMed
LIU, Y., LUO, Z., WU, X., BAI, X. & ZHANG, D. 2012. Functional dioecy in Morinda parvifolia (Rubiaceae), a species with stigma-height dimorphism. Plant Systematics and Evolution 298:775–785.CrossRefGoogle Scholar
LLOYD, D. G. 1979. Evolution towards dioecy in heterostylous populations. Plant Systematics and Evolution 131:71–80.CrossRefGoogle Scholar
LLOYD, D. & WEBB, C. 1992. The selection of heterostyly. Pp. 179–207 in Barrett, S. C. H. (ed.). Monographs on theoretical and applied genetics. Springer-Verlag, New York.Google Scholar
MCDADE, L. A. & HARTSHORN, G. S. 1994. La Selva Biological Station. Pp. 6–14 in McDade, L. A., Bawa, K. S., Hespenheide, H. A. & Hartshorn, G. S. (eds.). La Selva: ecology and natural history of a neotropical rain forest. University of Chicago Press, Chicago.Google Scholar
NAIKI, A. & KATO, M. 1999. Pollination system and evolution of dioecy from distyly in Mussaenda parviflora (Rubiaceae). Plant Species Biology 14:217–227.CrossRefGoogle Scholar
ORNELAS, J. F., JIMÉNEZ, L., GONZÁLEZ, C. & HERNÁNDEZ, A. 2004. Reproductive ecology of distylous Palicourea padifolia (Rubiaceae) in a tropical montane cloud forest. I. Hummingbirds’ effectiveness as pollen vectors. American Journal of Botany 91:1052–1060.CrossRefGoogle Scholar
PAILLER, T. & THOMPSON, J. D. 1997. Distyly and variation in heteromorphic incompatibility in Gaertnera vaginata (Rubiaceae) endemic to La Reunion Island. American Journal of Botany 84:315–327.CrossRefGoogle ScholarPubMed
PAILLER, T., HUMEAU, L., FIGIER, J. & THOMPSON, J. D. 1998. Reproductive trait variation in the functionally dioecious and morphologically heterostylous island endemic Chassalia corallioides (Rubiaceae). Biological Journal of the Linnean Society 64:297–313.Google Scholar
PÉREZ-BARRALES, R., VARGAS, P. & ARROYO, J. 2006. New evidence for the Darwinian hypothesis of heterostyly: breeding systems and pollinators in Narcissus sect. Apodanthi. New Phytologist 171:553–567.CrossRefGoogle ScholarPubMed
POSADA, J. M. & SCHUUR, E. A. G. 2011. Relationships among precipitation regime, nutrient availability, and carbon turnover in tropical rain forests. Oecologia 165:783–795.CrossRefGoogle ScholarPubMed
REE, R. H. 1997. Pollen flow, fecundity, and the adaptive significance of heterostyly in Palicourea padifolia (Rubiaceae). Biotropica 29:298–308.CrossRefGoogle Scholar
ROULSTON, T. H., CANE, J. H. & BUCHMANN, S. L. 2000. What governs protein content of pollen: pollinator preferences, pollen–pistil interactions, or phylogeny? Ecological Monographs 70:617–643.Google Scholar
SAKAI, S. & WRIGHT, S. J. 2008. Reproductive ecology of 21 coexisting Psychotria species (Rubiaceae): when is heterostyly lost? Biological Journal of the Linnean Society 93:125–134.CrossRefGoogle Scholar
SÁNCHEZ, J. M., FERRERO, V. & NAVARRO, L. 2013. Quantifying reciprocity in distylous and tristylous populations. Plant Biology 15:616–620.CrossRefGoogle Scholar
STEPHENSON, A. G., TRAVERS, S. E., MENA-ALI, J. I. & WINSOR, J. A. 2003. Pollen performance before and during the autotrophic–heterotrophic transition of pollen tube growth. Philosophical Transactions of the Royal Society of London. Series B: Biological Sciences 358:1009–1018.CrossRefGoogle ScholarPubMed
STONE, J. L. 1995. Pollen donation patterns in a tropical distylous shrub (Psychotria suerrensis; Rubiaceae). American Journal of Botany 82:1390–1398.CrossRefGoogle Scholar
VALOIS-CUESTA, H., SORIANO, P. J. & ORNELAS, J. F. 2011. Asymmetrical legitimate pollination in distylous Palicourea demissa (Rubiaceae): the role of nectar production and pollinator visitation. Journal of Tropical Ecology 27:393–404.CrossRefGoogle Scholar
VUILLEUMIER, B. S. 1967. The origin and evolutionary development of heterostyly in the angiosperms. Evolution 21:210–226.CrossRefGoogle ScholarPubMed
WEBB, C. J. & LLOYD, D. G. 1986. The avoidance of interference between the presentation of pollen and stigmas in angiosperms II. Herkogamy. New Zealand Journal of Botany 24:163–178.CrossRefGoogle Scholar
WOLFF, D. & LIEDE-SCHUMANN, S. 2007. Evolution of flower morphology, pollen dimorphism, and nectar composition in Arcytophyllum, a distylous genus of Rubiaceae. Organisms Diversity and Evolution 7:106–123.CrossRefGoogle Scholar

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