Dichogamy and compatibility system in the tropical tree Gymnopodium floribundum (Polygonaceae)

keywords: floral sexual synchrony, compatibility index, inbreeding depression index, sexual expression, tree pollination


Background: Gymnopodium floribundum is a dominant tree in the seasonally tropical dry forests of Yucatan, Mexico. This species shows a large floral display size during short periods, but a very low seed-set has been reported.

Questions: What type of dichogamy does G. floribundum exhibit? What is its compatibility system?

Study species: G. floribundum, a dichogamous tree of importance in beekeeping.

Study sites and dates: Xtmakuil, Yucatan. February-March and November-December 2022. 

Methods: Floral sexual function synchrony and sexual expression was recorded during the flowering season. The compatibility system was evaluated with a hand-pollination experiment.

Results: Intra-floral overlap of sexual functions was low (< 2 %), but relatively high between flowers of different inflorescences (0.48 ± 0.13, Mean ± SD) and between flowers of different trees (0.64 ± 0.11, Mean ± SD). Mature fruit production by hand self-pollination was low (ca. 3 %) and 6 times lower with respect to cross.

Conclusions: G. floribundum shows complete intrafloral dichogamy, but incomplete intra- and interindividual dichogamy. Sexual expression changed throughout flowering, from predominant male bias to female. Although G. floribundum is self-compatible, the results suggest a wide advantage of cross-pollination over self-pollination.


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Dichogamy and compatibility system in the tropical tree <em>Gymnopodium floribundum</em> (Polygonaceae)


Ågren J. Shemske DW. 1993. Outcrossing rate and inbreeding depression in two annual monoecious herbs, Begonia hirsuta and B. semiovata. Evolution 47: 125-135. DOI: https://doi.org/10.11/j.1558-5646.1993.tb01204.x

Albert MJ, Escudero A, Iriondo JM. 2001. Female reproductive success of narrow endemic Erodium paularense in contrasting microhabitats. Ecology 82: 1734-1747. DOI: https://doi.org/10.1890/0012-9658(2001)082[1734:FRSONE]2.0.CO;2

Almeida-Soares S, Polatto LP, Dutra JCS, Torezan-Silingardi HM. 2010. Pollination of Adenocalymma bracteatum (Bignonaceae): floral biology and visitors. Neotropical Entomology 39: 941-948. DOI: https://doi.org/10.1590/S1519-566X2010000600015

Ancona AJJ, Ortiz-Díaz JJ, de Luna E, Tun-Garrido J, Barrientos-Medina RC. 2019. Análisis estadístico de la variación morfológica en el complejo Gymnopodium floribundum (Polygonaceae): definición de tres subespecies. Acta Botanica Mexicana 126: e1517. DOI: https://doi.org/10.21829/abm126.2019.1517

Augspurger CK. 1980. Mass-flowering of a tropical shrub (Hybanthus prunifolius): influence on pollinator attraction and movement. Evolution 34: 475-488. DOI: https://doi.org/10.2307/2408217

Balam N. 2009. ¡Una planta común con varias funciones…aunque usted no lo crea! Posgrado en Ciencias Biológicas. Centro de Investigación Científica de Yucatán, Desde el Herbario 1: 30-31.

Bautista F, Frausto O, Ihl T, Aguilar Y. 2015. Actualización del mapa de suelos del estado de Yucatán México: enfoque geomorfopedológico y WRB. Ecosistemas y Recursos Agropecuarios 2: 303-315.

Bawa KS, Webb CJ. 1984. Flower, fruit and seed abortion in tropical forest trees: implications for the evolution of paternal and maternal reproductive patterns. American Journal of Botany 71: 736-751. DOI: https://doi.org/10.2307/2443371

Becerra JX, Lloyd DG. 1992. Competition-dependent abscission of self-pollinated flowers of Phormium tenax (Agavaceae): a second action of self-incompatibility at the whole flower level? Evolution 46: 2:458-469. DOI: https://doi.org/10.1111/j.1558-5646.1992.tb02051.x

Bell CR. 1971. Breeding systems and floral biology of the Umbelliferae or evidence for specialization in unspecialized flowers. In: Heywood VH. ed. The biology and chemistry of the Umbelliferae. pp. 93-108 New York: Academic Press, ISBN-13 978-0123469403.

Bertin RI. 1993. Incidence of monoecy and dichogamy in relation to self-fertilization in angiosperms. American Journal of Botany 80: 557-560. DOI: https://doi.org/10.2307/2445372

Bertin RI, Newman Ch. 1993. Dichogamy in Angiosperms. The Botanical Review 59: 112-152. DOI: https://www.jstor.org/stable/4354205

Bhardwaj M, Eckert ChG. 2001. Functional analysis of synchronous dichogamy in flowering rush, Butomus umbellatus (Butomaceae). American Journal of Botany 88: 2204-2213. DOI: https://doi.org/10.2307/3558382

Bierzychudek P. 1981. Pollinator limitation of plant reproductive effort. The American

Naturalist 117: 838-840. DOI: https://doi.org/10.1086/283773

Bullock SH. 1995. Plant reproduction in neotropical dry forest. In: Bullock SH, Mooney HA, Medina E. Seasonally dry tropical forests. Stanford University, California. Cambridge Cambridge University Press. pp 277-303. ISBN 9780521112840.

Burd M. 1994. Bateman´s principle and plant reproduction: the role of pollen limitation in fruit and seed set. The Botanical Review 60: 83-139. DOI: https://doi.org/10.1007/BF02856594

Campos BSM, Jiménez-Osornio J, Barrientos RM. 2016. Fenología y producción de frutos de plantaciones de siricote (Cordia dodecandra A. DC.) bajo tres tipos de manejo en Xmatkuil, Yucatán, México. Polibotánica 41: 115-131. DOI: https://doi.org/10.18387/polibotanica.41.8

Cawoy V, Deblauwe V, Halbrecq B, Ledent J-F. Kinet JM, Jacquemart A-L. 2006. Morph differences and honeybee morph preference in the distylous species Fagopyrum esculentum Moench. International Journal of Plant Sciences 167: 853-861. DOI: https://doi.org/10.1086/504924

Chemas A, Rico-Gray V. 1991. Apiculture and management of associated vegetation by the maya of Tixcacaltuyub, Yucatán, México. Agroforestry Systems 13: 13-25. DOI: https://doi.org/10.1007/BF00129616

Collevatti RG, Estolano R, García SF, Hay JD. 2009. Seed abortion in the bat pollinated Neotropical tree species, Caryocar brasilense (Caryocaraceae). Botany 87: 1110-1115. DOI: https://doi.org/10.1139/B09-054

Cuevas J, Rallo L, Rapoport HF. 1994. Initial fruit set at high temperature in olive, Olea europaea L. Journal of Horticultural Science 69: 665-672. DOI: https://doi.org/10.1080/14620316.1994.11516498

Dai C, Galloway F. 2010. Do dichogamy and herkogamy reduce sexual interference in a self-incompatible species? Functional Ecology 25: 271-278. DOI: https://doi.org/10.1111/j.1365-2435.2010.01795.x

Flores S. 1990. The flowering periods of Leguminosae in the Yucatan Peninsula in relation to honey flows. Journal of Apicultural Research 29: 82-88. DOI: https://doi.org/10.1080/00218839.1990.11101201

Gallucci M. 2019. GAMLj: General analyses for linear models. https://gamlj.github.io/

Gibbs PE. 2014. Late-acting self-incompatibility - the pariah breeding system in flowering plants. New Phytologist 203: 707-734. DOI: https://doi.org/10.1111/nph.12874

González-Ramírez RM. 2014. Evaluación de Gymnopodium floribundum Rolfe como recurso nectarífero. MSc thesis. Centro de Investigación Científica de Yucatán, AC.

Goodwillie C, Kalisz S, Eckert ChG. 2005. The evolutionary enigma of mixed mating system in plants: occurrence, theoretical explanations, and empirical evidence. Annual Review of Ecology, Evolution and Systematics 36: 47-79. DOI: https://doi.org/10.1146/annurev.ecolsys.36.091704.175539

Groeneveld JH, Tscharntke T, Moser G, Clough Y. 2010. Experimental evidence for stronger cacao yield limitation by pollination than by plant resources. Perspectives in Plant Ecology, Evolution and Systematics 12: 183-191. DOI: https://doi.org/10.1016/j.ppees.2010.02.005

Harder LD, Aizen MA. 2004. The functional significance of synchronous protandry in Alstromeria aurea. Functional Ecology 18: 467-474. DOI: https://doi.org/10.1111/j.0269--8463.2004.00859.x

Hedges LV, Olkin I. 1985. Statistical Methods for Metaanalysis. New York, EUA: Academic Press. ISBN: 9780123363800

Horovitz A. 1978. Is the hermaphrodite flowering plant equisexual? American Journal of Botany 65: 485-486. DOI: https://doi.org/10.1002/j.1537-2197.1978.tb06097.x

Hossaert-Mckey M, Bronstein JL. 2001. Self-pollination and its costs in a monoecious fig (Ficus aurea, Moraceae) in a highly seasonal subtropical environment. American Journal of Botany, 88: 685-692. DOI: https://doi.org/10.2307/2657069

Instituto Nacional de Estadística y Geografía. 2010. Compendio de información geográfica municipal 2010. Mérida, Yucatán: Instituto Nacional de Estadística y Geografía https://www.inegi.org.mx/contenidos/app/mexicocifras/datos_geograficos/31/31050.pdf(Accessed May 15, 2023)

Interián-Ku VM, Valdéz-Hernández JI, Cázares-Sánchez E, González-Rodríguez J. 2018. Impacto de variables ambientales en la fenología de Caesalpinia gaumeri Grenm. y Gymnopodium floribundum Rolfe del sur de Yucatán, México. Polibotánica 45: 115-129. DOI: https://doi.org/10.18387/polibotanica.45.9

Jackson EE, Wright SJ, Calderón O, Bullock JM, Oliver T, Gripenberg S. 2022. Pre-dispersal seed predation could help explain premature fruit drop in a tropical forest. Journal of Ecology 110: 751-761. DOI: https://doi.org/10.1111/1365-2745.13867

Jacquemyn H, Honnay O. 2008. Mating system evolution under strong clonality: towards self-compatibility or self-incompatibility. Evolutionary Ecology 22: 483-486. DOI: https://doi.org/10.1007/s10682-007-9207-3

Kato E, Hiura T. 1999. Fruit set in Styrax obassia (Styracaceae): the effect of light availability, display size, and local floral density. American Journal of Botany 86: 495-501. DOI: doi.org/10.2307/2656810

Kearns CA, Inouye DW. 1993. Techniques for pollination biologists. Niwot, Colorado: University Press of Colorado. ISBN: 978-0-87081-281-1

Klein AM, Steffan-Dewenter I, Tscharntke T. 2003 Bee pollination and fruit set of Coffea arabica and C. canephora (Rubiaceae). American Journal of Botany 90: 153-157. DOI: https://doi.org/10.3732/ajb.90.1.153

Knight TM, Steets JA, Vamosi JC, Mazer SJ, Burd M, Campbell DR, Dudash MR, Johnston MO, Mitchell R, Ashman T-L. 2005. Pollen limitation of plant reproduction: pattern and process. Annual Review of Ecology, Evolution and Systematics 36: 467-497. DOI: https://doi.org/10.1146/annurev.ecolsys.36.102403.115320

Koptur S. 1983. Flowering phenology and floral biology of Inga (Fabaceae: Mimosoideae). Systematic Botany 8: 354-368. DOI: https://doi.org/10.2307/2418355

Larson BMH, Barrett SCH. 2000. A comparative analysis of pollen limitation in flowering plants. Biological Journal of the Linnean Society 69: 503-520. DOI: https://doi.org/10.1006/bijl.1999.0372

Lloyd DG, Webb CJ. 1986. The avoidance of interference between the presentation of pollen and stigmas in angiosperms. I. Dichogamy. New Zealand Journal of Botany 24: 135-162. DOI: https://doi.org/10.1080/0028825X.1986.10409725

Machado IC, Bezerra LMI. 2000. Fly pollination and pollinator sharing in two synchronopatric species: Cordia multispicata (Boraginaceae) and Borreria alata (Rubiaceae). Brazilian Journal of Botany 23. DOI: https://doi.org/10.1590/S0100-84042000000300006

Narbona E, Ortiz PL, Arista M. 2011. Linking self-incompatibility, dichogamy, and flowering synchrony in two Euphorbia species: alternative mechanisms for avoiding self-fertilization? Plos One 6. DOI: https://doi.org/10.1371/journal.pone.0020668

Orellana LR, Espadas MC, Nava MF. 2010. Contexto físico. Climas. In: Durán R, Méndez M., eds. Biodiversidad y Desarrollo Humano en Yucatán.Yucatán, México: Centro de Investigación Científica de Yucatán, Programa de Pequeñas Donaciones del Fondo para el Medio Ambiente Mundial, Comisión Nacional para el Conocimiento y Uso de la Biodiversidad, , Secretaría de Desarrollo Urbano y Medio Ambiente pp. 10-11. ISBN 978-607-7823-08-7.

Ortiz-Díaz JJ. 1994. Etnoflora yucatanense. Polygonacea. Fascículo 10. Mérida, Yucatán, México: Universidad Autónoma de Yucatán. ISBN 9686843280.

Parra-Tabla V, Bullock SH. 1998. Factors limiting fecundity in the tropical tree Ipomoea wolcottiana (Convolvulaceae) in a Mexican tropical dry forest. Journal of Tropical Ecology 14: 615-628. DOI: https://doi.org/10.1017/S0266467498000431

Parra-Tabla V, Bullock SH. 2002. La polinización en la selva de Chamela. In: F. Noguera JH, Vega AN, García-Aldrete, Quezada M. eds. Historia Natural de Chamela. México: Universidad Nacional Autónoma de México. pp. 499-515. ISBN 970-32-0520-8.

Pinto CE, Oliveira R, Schlinwein, C. 2008. Do consecutive flower visits within a crown diminish fruit set in a mass-flowering Hancornia speciosa (Apocynaceae)? Plant Biology 10: 408-412. DOI: https://doi.org/10.1111/j.1438-8677.2008.00045.x

R Core Team. 2021. R: A Language and environment for statistical computing. (Version 4.1). https://www.R-project.org

Ramalho M. 2004. Stingless bees and mass flowering trees in the canopy of Atlantic Forest: a tight relationship. Acta Botanica Brasilica 18: 37-47. DOI: https://doi.org/10.1590/S0102-33062004000100005

Ramírez N. 1993. Producción y costo de frutos y semillas entre formas de vida. Biotropica 25, 46-60. DOI: https://doi.org/10.2307/2388978

Rico-Gray V., García-Franco JG. 1991. The Maya and the vegetation of the Yucatan peninsula. Journal of Ethnobiology 11:135-142. https://ethnobiology.org/sites/default/files/pdfs/JoE/11-1/Rico-Gray.pdf. (Accessed April 10, 2023).

Rico-Gray V, García-Franco JG. 1992. Vegetation and soil seed bank of successional stages in tropical deciduous forest. Journal of Vegetation Science 3: 617-624. DOI: https://doi.org/10.2307/3235828

Rico-Gray V, García-Franco JG, Puch A, Simá P. 1988. Composition and structure of a tropical dry forest in Yucatan, Mexico. International Journal of Ecology and Environmental Sciences 14: 21-29.

Rosas-Guerrero V, Hernández D, Cuevas E. 2017. Influence of pollen limitation and inbreeding depression in the maintenance of incomplete dichogamy in Salvia elegans. Ecology and Evolution 7: 4120-4134. DOI: https://doi.org/10.1002/ece3.2827

Ross MD. 1977. Frequency-dependent fitness and differential outcrossing in hermaphrodite populations. The American Naturalist 111: 200-202. DOI: https://doi.org/10.1086/283154

Salinas-Peba L, Parra-Tabla V. 2007. Phenology and pollination of Manilkara zapota in forest and homegardens. Forest Ecology and Management 248: 136-142. DOI: https://doi.org/10.1016/j.foreco.2007.04.046

Sargent RD, Mandegar MA, Otto SP. 2006. A model of the evolution of dichogamy incorporating sex-ratio selection, anther-stigma interference, and inbreeding depression. Evolution 60: 934-944. DOI: https://doi.org/10.1111/j.0014-3820.2006.tb01172.x

Souza-Novelo N. 1981. Plantas melíferas y poliníferas que viven en Yucatán. Mérida, Yucatán, México: Fondo Editorial de Yucatán.

Standley PC, Steyemark JA. 1946. Flora of Guatemala. Fieldiana Botany 24: Part IV. USA: Chicago Natural History Museum. https://www.biodiversitylibrary.org/item/19662#page/11/mode/1up (Accessed April, 11 2023).

Stephenson AG. 1981. Flower and fruit abortion: proximate causes and ultimate functions. Annual Review of Ecology and Systematics 12: 25-279. DOI: https://doi.org/10.1146/annurev.es.12.110181.001345

The jamovi project. 2022. jamovi. (Version 2.3). Accesado de https://www.jamovi.org/

Trueman SJ, Turnbull CGN. 1994. Fruit set abscission and dry matter accumulation on girdled branches of macadamia. Annals of Botany 74: 667-674. DOI: https://doi.org/10.1006/anbo.1994.1169

Valdez-Hernández M, Andrade JL, Jackson PC, Rebolledo-Vieyra M. 2010. Phenology of five tree species of a tropical dry forest in Yucatan, Mexico: effects of environmental and physiological factors. Plant Soil 329: 155-177. DOI: https://doi.org/10.1007/s11104-009-0142-7

Valle RR, Almeida AA-F, de O Leite RM. 1990. Energy cost of flowering, fruiting and cherelle wilt in cacao. Tree Physiology 6: 329-336. DOI: https://doi.org/10.1093/treephys/6.3.329

Vicario-Mejía E, Echazarreta CM. 1999. Gymnopodium floribundum: a major honey plant for beekeepers in Yucatan, Mexico. Bee World 80: 145-147. DOI: https://doi.org/10.1080/0005772X.1999.11099444

Voigt FA, Jung S, Farwig N, Böhning-Gaese K. 2005. Low fruit set in a dioecious tree: pollination ecology of Commiphora harveyi in South Africa. Journal of Tropical Ecology 21:179-188. DOI: https://doi.org/10.1017/S026646740400210X

Zhao Z, Hou M, Wang Y, Du G. 2020. Phenological variation of flower longevity and duration of sex phases in a protandrous alpine plant: potential causes and fitness significance. BMC Plant Biology 20: 137. DOI: https://doi.org/10.1186/s12870-020-02356-w

How to Cite
Paquini-Rodríguez, S. L., Meléndez-Ramírez, V., Tun-Garrido, J., & Parra-Tabla, V. (2023). Dichogamy and compatibility system in the tropical tree Gymnopodium floribundum (Polygonaceae). Botanical Sciences, 102(1), 54-67. https://doi.org/10.17129/botsci.3366