Reproductive Biology and Herkogamy of Psychotria elata (Rubiaceae), a Distylous Species of the Tropical Rain Forests of Costa Rica

Abstract

The floral morphology, breeding system and pollinators of four natural populations of Psychotria elata (Rubiaceae), found in tropical rainforests of Costa Rica, were examined. Anisoplethy and distylous morphology were observed in all studied populations. The number of flowers per inflorescence was significantly higher in the most abundant morph (p < 0.005) and the number of open flowers/inflorescence/day was similar between the morphs (p > 0.05). Reciprocal herkogamy was detected in only one of the morphs in one population. Breakdown of the heteromorphic incompatibility system was observed in the populations Tirimbina and Rara Avis. Pollen production was significantly lower in thrum morphs of Tirimbina. Seedless fruits were formed in two of the four populations. One-seeded fruits were formed in all populations and were predominant in thrum morphs of Tirimbina (9.15%) and Zurqui (75%). According to our visitation records, hummingbirds, butterflies and moths are the main pollinators of P. elata flowers.

Share and Cite:

Silva, C. and Segura, J. (2015) Reproductive Biology and Herkogamy of Psychotria elata (Rubiaceae), a Distylous Species of the Tropical Rain Forests of Costa Rica. American Journal of Plant Sciences, 6, 433-444. doi: 10.4236/ajps.2015.63049.

Conflicts of Interest

The authors declare no conflicts of interest.

References

[1] Barrett, S.C.H. (2002) The Evolution of Plant Sexual Diversity. Nature Reviews Genetic, 3, 274-284.
http://dx.doi.org/10.1038/nrg776
[2] Lloyd, D.G. and Webb, C.J. (1992) The Selection of Heterostyly. In: Barrett, S.C.H., Ed., Evolution and Function of Heterostyly, Springer-Verlag, Berlin, 179-207.
http://dx.doi.org/10.1007/978-3-642-86656-2_7
[3] Lewis, D. and Jones, D.A. (1992) The Genetics of Heterostyly. In: Barrett, S.C.H., Ed., Evolution and Function of Heterostyly, Springer-Verlag, Berlin, 129-130.
http://dx.doi.org/10.1007/978-3-642-86656-2_5
[4] Charlesworth, D. and Charlesworth, B. (1979) A Model for Evolution of Heterostyly. American Naturalist, 114, 467-498. http://dx.doi.org/10.1086/283496
[5] Weller, S.G., Domínguez, C.A., Molina-Freaner, F.E., Foroni, J. and Le Buhn, G. (2007) The Evolution of Distyly from Tristyly in Populations of Oxalis alpina (Oxalidaceae) in the Sky Islands of the Sonoran Desert. American Journal of Botany, 94, 972-985.
http://www.amjbot.org/content/94/6/972.full.pdf+html
http://dx.doi.org/10.3732/ajb.94.6.972
[6] Pérez-Barrales, R., Arroyo, J. and Armbruster, W.S. (2007) Differences in Pollinator Faunas May Generate Geographic Differences in Floral Morphology and Integration in Narcissus papyraceus (Amaryllidaceae). Oikos, 116, 1904-1918.
http://dx.doi.org/10.1111/j.0030-1299.2007.15994.x
[7] Pérez-Barrales, R. and Arroyo, J. (2010) Pollinator Shifts and the Loss of Style Polymorphism in Narcissus papyraceus (Amaryllidaceae). Journal Evolution Biology, 23, 1117-1128.
http://dx.doi.org/10.1111/j.1420-9101.2010.01988.x
[8] Barrett, S.C.H., Harder, L.D. and Cole, W. (2004) Correlated Evolution of Floral Morphology and Mating-Type Frequencies in a Sexually Polymorphic Plant. Evolution, 58, 964-975.
http://www.jstor.org/discover/10.2307/3449192
http://dx.doi.org/10.1111/j.0014-3820.2004.tb00431.x
[9] Hodgins, K.A. and Barrett, S.C.H. (2008) Geographical Variation and Style-Morph Rtios in a Sexually Polymorphic Daffodil. American Journal of Botany, 95, 185-195.
http://www.amjbot.org/10.3732/ajb.95.2.185
http://dx.doi.org/10.3732/ajb.95.2.185
[10] Hodgins, K.A. and Barrett, S.C.H. (2006) Female Reproductive Success and the Evolution of Mating-Type Fequencies in Tristylous Populations. New Phytologist, 171, 569-580.
http://onlinelibrary.wiley.com/doi/10.1111/j.1469-8137.2006.01800.x
[11] Schvinn, T.A., Miranda, A.F. and Silva, C.A. (2014) Reproductive Biology of Amasonia obovata Gleason (Laminaceae). Acta Amazonica, 44, 427-434.
[12] Dart, S.R., Samir, K.E., Austen, E. and Eckert, C.G. (2012) Broad Geographic Covariation between Floral Traits and the Mating System in Camissoniopsis cheiranthifolia (Onagraceae): Multiple Stable Mixed Mating Systems across the Species Range? Annals of Botany, 109, 599-611.
http://dx.doi.org/10.1093/aob/mcr266
[13] Brunet, J. and Eckert, C.G. (1998) Effects of Floral Morphology and Display on Outcrossing in Blue Columbine, Aquilegia caerulea (Ranunculaceae). Functional Ecology, 12, 596-606.
http://dx.doi.org/10.1046/j.1365-2435.1998.00231.x
[14] Herlihy, C.R. and Eckert, C.G. (2007) Evolutionary Analysis of a Key Floral Trait in Aquilegia canadensis (Ranunculaceae): Genetic Variation in Herkogamy and Its Effect on the Mating System. Evolution, 61, 1661-1674.
http://dx.doi.org/10.1111/j.1558-5646.2007.00137.x
[15] Gargiullo, M.B., Magnuson, B. and Kinball, L. (2008) A Field Guide to Plants of Costa Rica. Zona Tropical Publication, Oxford.
[16] Burger, W. and Taylor, C.M. (1993) Family #202 Rubiaceae. In: Burger, W., Ed., Flora Costaricensis, Field Museum of Natural History, Chicago.
[17] Brys, R., Jacquemyn, H., Endels, P., Van Rossum, F., Hermy, M., Triest, L., Bruyn, L. and Blust, G.D.E. (2004) Reduced Reproductive Success in Small Populations of the Self-Incompatible Primula vulgaris. Journal of Ecology, 92, 5-14.
[18] Brys, R., Jacquemyn, H. and Beeckman, T. (2008) Morph-Ratio Variation, Population Size and Female Reproductive Success in Distylous Pulmonaria officinalis (Boraginaceae). Journal of Evolutionary Biology, 21, 1281-1289.
http://dx.doi.org/10.1111/j.1420-9101.2008.01569.x
[19] Kock, A.K., Silva, P.C. and Silva, C.A. (2010) Biologia Reprodutiva de Psychotria carthagenensis (Rubiaceae), Espécie Distílica de Fragmento Florestal de Mata Ciliar, Centro-Oeste do Brasil. Rodriguésia, 61, 551-558.
[20] Radford, A.E., Dickson, W.C., Massey, J.R. and Bell, C.R. (1974) Vascular Plant Systematics. Harper and Row, New York.
[21] Richards, J.H. and Koptur, S. (1993) Floral Variation and Distyly in Guettarda scabra (Rubiaceae). American Journal of Botany, 80, 31-40. http://dx.doi.org/10.2307/2445117
[22] Massinga, P.H., Johnson, S.D. and Harder, L.D. (2005) Heteromorphic Incompatibility and Efficiency of Pollination in Two Distylous Pentanisia Species (Rubiaceae). Annals of Botany, 95, 389-399.
http://dx.doi.org/10.1093/aob/mci040
[23] Keller, B., Vos, J.M. and Cont, E. (2012) Decrease of Sexual Organ Reciprocity between Heterostylous Primrose Species, with Possible Functional and Evolutionary Implications. Annals of Botany, 110, 1233-1244.
http://dx.doi.org/10.1093/aob/mcs199
[24] Martin, F.W. (1959) Staining and Observing Pollen Tubes in the Style by Means of Fluorescence. Biotechnic & Histochemistry, 34, 125-128.
[25] Kearns, C.A. and Inouye, D.W. (1993) Techniques for Pollination Biologists. University Press of Colorado, Niwot.
[26] StatSoft, Inc. (2010) STATISTICS: Methods and Applications. StatSoft, Tulsa.
[27] Barrett, S.C.H. (1990) The Evolution and Adaptive Significance of Heterostyly. Trends in Ecology and Evolution, 5, 144-148.
http://dx.doi.org/10.1016/0169-5347(90)90220-8
[28] Faivre, A.E. and Mc Dade, 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, 841-853.
http://dx.doi.org/10.2307/2657036
[29] Webb, C.J. and 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.
http://dx.doi.org/10.1080/0028825X.1986.10409726
[30] Brys, R. and Jacquemyn, H. (2011) Variation in the Functioning of Autonomous Self-Pollination, Pollinator Services and Floral Traits in Three Centaurium Species. Annals of Botany, 107, 917-925.
http://dx.doi.org/10.1093/aob/mcr032
[31] Ganders, F.R. (1979) The Biology of Heterostyly. New Zealand Journal of Botany, 17, 607-635.
http://dx.doi.org/10.1080/0028825X.1979.10432574
[32] Sampson, D.A. and Krebs, R.A. (2012) Quantitative Evaluation of Reciprocal Herkogamy in the Distylous Species, Hedyotis caerulea (Rubiaeceae). Plant Systematics and Evolution, 298, 1361-1370.
http://dx.doi.org/10.1007/s00606-012-0642-4
[33] Thompson, J.D., Cesaro, A. and Arroyo, J. (2012) Morph Ratio Variation and Sex Organ Reciprocity in Style-Dimorphic Narcissus assoanus. International Journal of Plant Sciences, 173, 885-893.
http://dx.doi.org/10.1086/667231
[34] Morgan, M.T. and Wilson, W.G. (2005) Self-Fertilization and the Escape from Pollen Limitation in Variable Pollination Environments. Evolution, 59, 1143-1148.
http://dx.doi.org/10.1111/j.0014-3820.2005.tb01050.x
[35] Byers, D.L. and Meagher, T.R. (1992) Mate Availability in Small Populations of Plant-Species with Homomorphic Sporophytic Self-Incompatibility. Heredity, 68, 353-359.
http://dx.doi.org/10.1038/hdy.1992.50
[36] Baker, A.M., Thompson, J.D. and Barrett, S.C.H. (2000) Evolution and Maintenance of Stigma-Height Dimorphism in Narcissus. I. Floral Variation and Style-Morph Ratios. Heredity, 84, 502-513.
http://dx.doi.org/10.1046/j.1365-2540.2000.00651.x
[37] Sakai, S. and 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.
http://dx.doi.org/10.1111/j.1095-8312.2007.00890.x
[38] Silva, C.A., Vieira, M.F. and Amaral, C.H. (2010) Floral Attributes, Ornithophily and Reproductive Success of Palicourea longepedunculata (Rubiaceae), a Distylous Shrub in Southeastern Brazil. Revista Brasileira de Botanica, 33, 207-213.
[39] Silva, C.A. and Vieira, M.F. (2013) Sucesso Reprodutivo de Espécies Distílicas de Psychotria (Rubiaceae) em Sub-bosque de Floresta Atlantica. Revista árvore, 37, 289-297.
http://dx.doi.org/10.1590/S0100-67622013000200010
[40] Feinsinger, P., Busby, W., Murray, K.G., Beach, J.H., Pounds, W.Z. and Linhart, Y.B. (1988) Mixed Support for Spatial Heterogeneity in Species Interactions: Hummingbirds in a Tropical Disturbance Mosaic. American Naturalist, 131, 33-57.
http://dx.doi.org/10.1086/284772
[41] Castro, C.C. and Araujo, C.A. (2004) Distyly and Sequential Pollinators of Psychotria nuda (Rubiaceae) in the Atlantic Rain Forest, Brazil. Plant Systematics and Evolution, 244, 131-139.
http://dx.doi.org/10.1007/s00606-003-0036-8
[42] Coelho, C.P. and Barbosa, A.A. (2003) Biologia Reprodutiva de Palicourea macrobotrys Ruiz & Pavon (Rubiaceae): Um Possível Caso de Homostilia no Gênero Palicourea Aubl. Revista Brasileira de Botanica, 26, 403-413.
[43] Watanabe, K., Shimizu, A. and Sugawara, T. (2014) Dioecy Derived from Distyly and Pollination in Psychotria rubra (Rubiaceae) Occurring in the Ryukyu Islands, Japan. Plant Species Biology, 29, 181-191.
[44] Consolaro, H., Toledo, R.D.P., Ferreguti, R.L., Hay, J. and Oliveira, P.E. (2009) Distilia e Homostilia em Espécies de Palicourea Aubl. (Rubiaceae) do Cerrado do Brasil Central. Revista Brasileira de Botanica, 32, 677-689.
[45] Ramos, F.N. and Santos, F.A.M. (2006) Floral Visitors and Pollination of Psychotria tenuinervis (Rubiaceae): Distance from the Anthropogenic and Natural Edges of an Atlantic Forest Fragment. Biotropica, 38, 383-389.
http://dx.doi.org/10.1111/j.1744-7429.2006.00152.x
[46] Barrett, S.C.H., Jesson, L.K. and Baker, A.M. (2000) The Evolution and Function of Stylar Polymorphisms in Flowering Plants. Annals of Botany, 85, 253-265.
http://dx.doi.org/10.1006/anbo.1999.1067
[47] Alves dos Santos, I. (2002) Flower-Visiting Bees and the Breakdown of the Tristylous Breeding System of Eichhornia azurea (Swartz) Kunth (Pontederiaceae). Biological Journal of the Linnean Society, 77, 499-507.
http://dx.doi.org/10.1046/j.1095-8312.2002.00122.x
[48] Alves dos Santos, I. and Wittmann, D. (2000) Legitimate Pollination of the Trimorphic Flowers of Eichhornia azurea (Pontederiaceae) by Ancyloscelis gigas Bees (Anthophoridae, Apoidae). Plant Systematics and Evolution, 223, 127-137.
http://dx.doi.org/10.1007/BF00985274

Copyright © 2023 by authors and Scientific Research Publishing Inc.

Creative Commons License

This work and the related PDF file are licensed under a Creative Commons Attribution 4.0 International License.