Reproductive systems are fundamental attributes for understanding life cycle and regeneration processes and provide information about seed production and genetic diversity. Analyses of reproductive strategies within communities and their associations with functional groups can indicate how physical and biological characteristics may influence the reproductive ecology of such communities. The main goal was to determine if the reproductive systems and their associated functional groups have particular characteristics related to extreme conditions and disturbance within xerophytic shrubland. Floral morphology analysis and four experimental tests were conducted to determine the reproductive systems of species and their associations with the life form, succulence, carbon metabolism, dispersal syndrome, pollination, and disturbance. Of the 144 plant species studied, 72.9% were hermaphrodite, 22.9% were monoecious, and 4.2% were dioecious. Dioecy was associated with woodiness, frugivory and undisturbed areas, while monoecy was more common in herbs. Adichogamy, protandry and herkogamy were more frequent than dichogamy, protogyny and no herkogamy, respectively. Xenogamous species tend to be woody and grow in undisturbed areas, while partially xenogamous species were mainly herbs occurring in disturbed areas. The majority of species were partially self-incompatible. High levels of outbreeding strategies tended to occur mainly in woody K-strategy species from undisturbed areas, mixed breeding strategies occurred in disturbed areas and overall community, and inbreeding strategies were associated with mostly herbaceous r-strategy primarily in disturbed areas.
References
[1]
Davies, J., Poulsen, L., Schulte-Herbrüggen, B., Mackinnon, K., Crawhall, N., Henwood, W.D., Dudley, N., Smith, J. and Gudka, M. (2012) Conserving Dryland Biodiversity. International Union for Conservation of Nature, Publications Unit, Nairobi, xii +84 p.
[2]
Randriamalala, J.R., Randriarimalala, J., Hervé, D. and Carrière, S.M. (2019) Slow Recovery of Endangered Xerophytic Thickets Vegetation after Slash-and-Burn Cultivation in Madagascar. Biological Conservation, 233, 260-267. https://doi.org/10.1016/j.biocon.2019.03.006
[3]
Ziadat, F.M. and Taimeh, A.Y. (2013) Effect of Rainfall Intensity, Slope, Land Use and Antecedent Soil Moisture on Oil Erosion in an Arid Environment. Land Degradation and Development, 24, 582-590. https://doi.org/10.1002/ldr.2239
[4]
Violle, C., Navas, M.-L., Vile, D., Kazakou, E., Fortunel, C., Hummel, I. and Garnier, E. (2007) Let the Concept of Trait Be Functional! Oikos, 116, 882-892. https://doi.org/10.1111/j.0030-1299.2007.15559.x
[5]
Ramírez, N. and Hokche, O. (2019) Outbreeding and Inbreeding Strategies in Herbaceous-Shrubby Communities in the Venezuelan Gran Sabana Plateau. AoB Plants, 11, plz032. https://doi.org/10.1093/aobpla/plz032
[6]
Ramírez, N. and Briceño, H. (2021) Pollination Types and Plant Reproductive Systems of Two Areas of Venezuelan Cloud Forests. The International Journal of Plant Reproductive Biology, 13, 82-103.
[7]
Ramírez, N. and Briceño, H. (2022) Plant Reproductive Systems in a Secondary Deciduous Forest Remnant in the Caracas Valley, Venezuela. Plant Ecology, 223, 537-557. https://doi.org/10.1007/s11258-022-01226-9
[8]
Matallana, G., Wendtm, T., Araujo, D.S.D. and Scarano, F.R. (2005) High Abundance of Dioecious Plants in a Tropical Coastal Vegetation. American Journal of Botany, 92, 1513-1518. https://doi.org/10.3732/ajb.92.9.1513
[9]
Ramírez, N. (2005) Plant Sexual Systems, Dichogamy, and Herkogamy in the Venezuelan Central Plain. Flora, 200, 30-48. https://doi.org/10.1016/j.flora.2005.01.002
[10]
Puixeu, G., Pickup, M., Field, D.L. and Barrett, S.C.H. (2019) Variation in Sexual Dimorphism in a Wind-Pollinated Plant: The Influence of Geographical Context and Life-Cycle Dynamics. New Phytologist, 224, 1108-1120. https://doi.org/10.1111/nph.16050
[11]
McMullen, C.K. (1987) Breeding Systems of Selected Galapagos Islands Angiosperms. American Journal of Botany, 74, 1694-1705. https://doi.org/10.1002/j.1537-2197.1987.tb08770.x
[12]
Lemus-Jiménez, L. and Ramírez, N. (2005) Sistemas reproductivos de plantas en tres hábitats de la planicie costera de Paraguaná, Venezuela. Revista de Biología Tropical, 53, 415-430. https://doi.org/10.15517/rbt.v53i3-4.14610
[13]
Levin, D.A. (2012) Mating System Shifts on the Trailing Edge. Annals of Botany, 109, 613-620. https://doi.org/10.1093/aob/mcr159
[14]
Karron, J.D., Ivey, C.T., Mitchell, R.J., Whitehead, M.R., Peakall, R. and Case, A.L. (2012) New Perspectives on the Evolution of Plant Mating Systems. Annals of Botany, 109, 493-503. https://doi.org/10.1093/aob/mcr319
[15]
Peng, D.-L., Ou, X.-K., Xu, B., Zhang, Z.-Q., Niu, Y., Li, Z.-M. and Hang, S. (2014) Plant Sexual Systems Correlated with Morphological Traits: Reflecting Reproductive Strategies of Alpine Plants. Journal of Systematics and Evolution, 52, 368-377. https://doi.org/10.1111/jse.12046
[16]
Ramírez, N. and Nassar, J. (2016) Breeding Systems in Angiosperms: Novel Inferences from a New Analytical Approach. Plant Systematics and Evolution, 303, 119-137. https://doi.org/10.1007/s00606-016-1357-8
[17]
Cardoso, J.C.F., Viana, M.L., Matias, R., Furtado, M.T., Caetano, A.P.S., Consolaro, H. and Brito, V.L.G. (2018) Towards a Unified Terminology for Angiosperm Reproductive Systems. Acta Botanica Brasilica, 32, 329-348. https://doi.org/10.1590/0102-33062018abb0124
[18]
Ramírez, N. and Brito, Y. (1990) Reproductive Biology of a Tropical Palm Swamp Community in the Venezuelan Llanos. American Journal of Botany, 77, 1260-1271. https://doi.org/10.1002/j.1537-2197.1990.tb11378.x
[19]
Jaimes, I. and Ramírez, N. (1998) Autoincompatibilidad, autogamia y agamospermia en angiospermas tropicales. Acta Biológica Venezuelica, 18, 59-80.
[20]
Chazdon, R.L., Careaga, S., Webb, C. and Vargas, O. (2003) Community and Phylogenetic Structure of Reproductive Traits of Woody Species in Web Tropical Forests. Ecological Monograph, 73, 331-348. https://doi.org/10.1890/02-4037
[21]
Morales, C.L. and Galetto, L. (2003) Influence of Compatibility System and Life Form on Plant Reproductive Success. Plant Biology, 5, 567-573. https://doi.org/10.1055/s-2003-44794
[22]
Opler, P.A., Baker, H.G. and Frankie, G.W. (1980) Plant Reproductive Characteristics during Secondary Succession in Neotropical Lowland Forest Ecosystems. Biotropica (Suppl.), 12, 40-46. https://doi.org/10.2307/2388155
[23]
Tseng, Y.H., Hsieh, C.F. and Hu, J.M. (2008) Incidences and Ecological Correlates of Dioecious Angiosperms in Taiwan and Its Outlying Orchid Island. Botanical Studies, 49, 261-276.
[24]
Hilje, B., Calvo-Alvarado, J., Jiménez-Rodríguez, C. and Sánchez-Azofeifa, A. (2015) Tree Species Composition, Breeding Systems, and Pollination and Dispersal Syndromes in Three Forest Successional Stages in a Tropical Dry Forest in Mesoamerica. Tropical Conservation Science, 8, 76-94. https://doi.org/10.1177/194008291500800109
[25]
Nassar, J., Ramirez, N. and Linares, O. (1997) Comparative Pollination Biology of Venezuelan Columnar Cacti and the Role of Nectar-Feeding Bats in Their Sexual Reproduction. American Journal of Botany, 84, 918-927. https://doi.org/10.2307/2446282
[26]
Nassar, J.M. and Ramírez, N. (2004) Reproductive Biology of the Melon Cactus, Melocactus curvispinus (Cactaceae). Plant Systematics and Evolution, 248, 31-44. https://doi.org/10.1007/s00606-004-0193-4
[27]
Ramírez, N. and Navarro, L. (2010) Trends in the Reproductive Biology of Venezuelan Melochia (Sterculiaceae) Species. Plant Systematics and Evolution, 289, 147-163. https://doi.org/10.1007/s00606-010-0340-z
[28]
Sutherland, S. and Delph, L.F. (1984) On the Importance of Male Fitness in Plants: Patterns of Fruit-Set. Ecology, 65, 1093-104. https://doi.org/10.2307/1938317
[29]
Sutherland, S. (1986) Patterns of Fruit-Set: What Controls Fruit-Flower Ratios in Plants? Evolution, 40, 117-128. https://doi.org/10.1111/j.1558-5646.1986.tb05723.x
[30]
Ramírez, N. and Herrera, A. (2017) Reproductive Efficiency and Photosynthetic Pathway in Seed Plants. Perspectives in Plant Ecology, Evolution and Systematics, 24, 48-60. https://doi.org/10.1016/j.ppees.2016.12.004
[31]
Thomson, J.P. and Brunett, J. (1990) Hypothesis for the Evolution of Dioecy in Seed Plants. Trends in Ecology and Evolution, 5, 11-16. https://doi.org/10.1016/0169-5347(90)90006-Y
[32]
Ewel, J.J., Madriz, A. and Tosi Jr., J.A. (1976) Zonas de Vida de Venezuela. Editorial Sucre, Segunda Edición, Venezuela.
[33]
Huber, O. and Alarcón, C. (1988) Mapa de Vegetación. MARNR, Caracas.
[34]
Castillo, A.C., Gómez, S. and Moreno, O. (1992) Aspectos florísticos y fisionómicos de un ecosistema semiárido del litoral central, Municipio Vargas, Distrito Federal. Acta Biológica Venezuelica, 13, 92-115.
[35]
APG IV (2016) An Update of the Angiosperm Phylogeny Group Classification for the Orders and Families of Flowering Plants: APG IV. Botanical Journal of the Linnean Society, 181, 1-20. https://doi.org/10.1111/boj.12385
[36]
Raduski, A.R., Haney, E.B. and Igic, B. (2012) The Expression of Self-Incompatibility in Angiosperms Is Bimodal. Evolution, 66, 1275-1283. https://doi.org/10.1111/j.1558-5646.2011.01505.x
[37]
Richards, A.J. (1997) Plant Breeding Systems. Second Edition, Chapman and Hall, London. https://doi.org/10.1007/978-1-4899-3043-9
[38]
Richards, A.J. (2003) Apomixis in Flowering Plants: An Overview. Philosophical Transactions of the Royal Society of London Series B, 358, 1058-1093. https://doi.org/10.1098/rstb.2003.1294
[39]
Barrett, S.C.H. (2014) Evolution of Mating Systems: Outcrossing versus Selfing. In: Losos, J., Ed., The Princeton Guide to Evolution, Princeton University Press, Princeton, 356-362.
[40]
Ramírez, N. (2004) Ecology of Pollination in a Tropical Venezuelan Savanna. Plant Ecology, 173, 171-189. https://doi.org/10.1023/B:VEGE.0000029320.34895.7d
[41]
Faegri, K. and van der Pijl, L. (1979) The Principles of Pollination Ecology. Pergamon Press, Oxford. https://doi.org/10.1016/B978-0-08-023160-0.50020-7
[42]
Bawa, K.S. and Krisp, J.E. (1980) Wind-Pollination in the Understorey of a Rain Forest in Costa Rica. Journal of Ecology, 68, 871-976. https://doi.org/10.2307/2259462
[43]
Webb, C.J. and Lloyd, D.G. (1986) The Avoidance of Interference between the Presentation of Pollen and Stigma in Angiosperms II. Herkogamy. New Zealand Journal of Botany, 24, 163-178. https://doi.org/10.1080/0028825X.1986.10409726
[44]
Lloyd, D.G. and Webb, C.J. (1986) The Avoidance of Interference between the Presentation of Pollen and Stigma in Angiosperms I. Dichogamy. New Zealand Journal of Botany, 24, 135-162. https://doi.org/10.1080/0028825X.1986.10409725
[45]
Madriz, R. and Ramírez, N. (1997) Biología Reproductiva de Coccoloba uvifera (L.) Jacq. (Polygonaceae), una especie polígamo-dioica. Revista Biología Tropical, 44-45, 105-115.
[46]
Riveros, M., Humaña, A.M. and Arroyo, M.K. (1996) Sistemas de reproducción en especies del bosque Valdiviano (40° Latitud Sur). ØYTON, 58, 167-176.
[47]
Ruiz-Zapata, T. and Arroyo, M.T.K. (1978) Plant Reproductive Ecology of a Secondary Deciduous Forest in Venezuela. Biotropica, 10, 221-230. https://doi.org/10.2307/2387907
[48]
Sobrevila, C. and Arroyo, M.T.K. (1982) Breeding Systems in a Montane Tropical Cloud Forest in Venezuela. Plant Systematics and Evolution, 140, 19-37. https://doi.org/10.1007/BF02409895
[49]
Lloyd, D.G. and Schoen, D.J. (1992) Self-Fertilization and Cross-Fertilization in Plants. 1. Functional Dimensions. International Journal of Plant Science, 153, 358-369. https://doi.org/10.1086/297040
[50]
Sokal, R.R. and Rohlf, F.J. (1998) Biometry. W.H. Freeman and Company, New York.
[51]
Statsoft, Inc. (2007) STATISTICA (Data Analysis Software System). Version 8.0. https://www.statsoft.com
[52]
Legendre, L. and Legendre, P. (1993) Numerical Ecology. Elsevier, Amsterdam.
[53]
Bullock, S.H. (1985) Breeding Systems in the Flora of Tropical Deciduos Forest in Mexico. Biotropica, 17, 287-301. https://doi.org/10.2307/2388591
[54]
Flores, S. and Schemske, D.W. (1984) Dioecy and Monoecy in the Flora of Puerto Rico and Virgin Islands: Ecological Correlates. Biotropica, 16, 132-139. https://doi.org/10.2307/2387845
[55]
Steiner, K.E. (1988) Dioecism and Its Correlated in the Cape Flora of South Africa. American Journal of Botany, 75, 1742-1754. https://doi.org/10.1002/j.1537-2197.1988.tb11250.x
[56]
Ramírez, N. (1993) Reproductive Biology in Tropical Shrub of the Venezuelan Guayana. Journal of Vegetation Science, 4, 5-12. https://doi.org/10.2307/3235727
[57]
Machado, I.C., Lopes, A.V. and Sazima, M. (2006) Plant sexual Systems and a Review of the Breeding System Studies in the Caatinga, a Brazilian Tropical Dry Forest. Annals of Botany, 97, 277-287. https://doi.org/10.1093/aob/mcj029
[58]
Bawa, K.S. and Opler, P.A. (1975) Dioecism in Tropical Forest Trees. Evolution, 29, 167-179. https://doi.org/10.1111/j.1558-5646.1975.tb00824.x
[59]
Bawa, K.S. and Beach, J.H. (1981) Evolution of Sexual Systems in Flowering Plants. The Annals of the Missouri Botanical Garden, 68, 254-274. https://doi.org/10.2307/2398798
[60]
Bawa, K.S., Perry, D.R. and Beach, J.H. (1985) Reproductive Biology of Tropical Lowland Rain Forest Trees. II. Sexual Systems and Incompatibility Mechanisms. American Journal of Botany, 72, 331-345. https://doi.org/10.1002/j.1537-2197.1985.tb05357.x
[61]
Fox, J.F. (1985) Incidence of Dioecy in Relation to Growth Form, Pollination and Dispersal. Oecologia, 67, 244-249. https://doi.org/10.1007/BF00384293
[62]
Givnish, T.J. (1982) Outcrossing versus Ecological Constrains in the Evolution of Dioecy. The American Naturalist, 119, 849-865. https://doi.org/10.1086/283959
[63]
Muenchow, G.E. (1987) Is Dioecy Associated with Fleshy Fruit? American Journal of Botany, 74, 287-293. https://doi.org/10.1002/j.1537-2197.1987.tb08607.x
[64]
Schemske, D.W., Willson, M.F,, Melampy, N.M,, Millar, L.J., Verter, L., Schemske, K.M. and Best, L.B. (1978) Flowering Ecology of Some Spring Woodland Herbs. Ecology, 59, 351-366. https://doi.org/10.2307/1936379
[65]
Willson, M.F. (1983) Plant Reproductive Ecology. Willey, New York.
[66]
Freeman, D.C., Doust, J.L., El-Keblawy, A., Miglia, K.J. and Mcarthur, E.D. (1997) Sexual Specialization and Inbreeding Avoidance in the Evolution of Dioecy. The Botanical Review, 63, 65-92. https://doi.org/10.1007/BF02857918
[67]
Thompson, D.I. and Edwards, T.J. (2001) Breeding Biology, Resource Partitioning and Reproductive Effort of a Dioecious Shrub, Clutia pulchella L. (Euphorbiaceae). Plant Systematics and Evolution, 226, 13-22. https://doi.org/10.1007/s006060170070
[68]
Medina, E. (2002) Tropical Savannas. In: Mooney, H.A. and Canadell, J.G., Eds., The Earth System: Biological and Ecological Dimensions of Global Environmental Change, Encyclopedia of Global Environmental Change, Vol. 2, John Willey & Sons, Ltd., Chichester, 586-592.
[69]
Bernardello, G., Anderson, G.J., Stuessy, T.F. and Crawford, D.J. (2001) A Survey of Floral Traits, Breeding Systems, Floral Visitors, and Pollination Systems of Angiosperms of the Juan Fernández Islands (Chile). The Botanical Review, 67, 255-308. https://doi.org/10.1007/BF02858097
[70]
Bertin, R.I. (1993) Incidence of Monoecy and Dichogamy in Relation to Self-Fertilization in Angiosperms. American Journal of Botany, 80, 557-560. https://doi.org/10.1002/j.1537-2197.1993.tb13840.x
[71]
Barrett, S.C.H. (2003) Mating Strategies in Flowering Plants: The Outcrossing-Selfing Paradigm and Beyond. Philosophical Transactions of the Royal Society of London Series B, 358, 991-1004. https://doi.org/10.1098/rstb.2003.1301
[72]
Freitas, L. and Sazima, M. (2009) Floral Biology and Mechanisms of Spontaneous Self-Pollination in Five Neotropical Species of Gentianaceae. The Botanical Journal of the Linnean Society, 160, 357-368. https://doi.org/10.1111/j.1095-8339.2009.00989.x
[73]
Firetti, F. (2018) Apomixis in Neotropical Vegetation. In: Sebata, A., Ed., Vegetation, Vol. 7, IntechOpen, London, 129-149. https://doi.org/10.5772/intechopen.69411
[74]
Jaimes, I. and Ramírez, N. (1999) Breeding Systems in a Secondary Deciduous Forest in Venezuela: The Importance of Life Form, Habitat, and Pollination Specificity. Plant Systematics and Evolution, 215, 23-36. https://doi.org/10.1007/BF00984645
[75]
Baker, H.G. (1978) Invasion and Replacement in Californian and Neotropical Grasslands. In: Wilson, J.R., Ed., Plant Relations in Pastures, CSIRO, East Melbourne, 368-384.
[76]
Raffl, C., Marcante, S. and Erschbamer, B. (2007) The Role of Spontaneous Selfing in Pioneer Species Saxifraga aizoides. Flora, 202, 128-132. https://doi.org/10.1016/j.flora.2006.05.002
[77]
Harder, L.D., Richards, S.A. and Routley, M.B. (2007) Effect of Reproductive Compensation, Gamete Discounting and Reproductive Assurance on Mating-System Diversity in Hermaphrodites. Evolution, 62, 157-172. https://doi.org/10.1111/j.1558-5646.2007.00272.x
[78]
Newstrom, L. and Robertson, A. (2005) Progress in Understanding Pollination Systems in New Zealand. New Zealand Journal of Botany, 43, 1-59. https://doi.org/10.1080/0028825X.2005.9512943
[79]
Herrera, I. and Nassar, J.M. (2009) Reproductive and Recruitment Traits as Indicators of the Invasive Potential of Kalanchoe daigremontiana (Crassulaceae) and Stapelia gigantea (Apocynaceae) in a Neotropical Arid Zone. The Journal of Arid Environments, 73, 978-986. https://doi.org/10.1016/j.jaridenv.2009.05.004
[80]
Herrera, I., Ramírez, N. and Nassar, J.M. (2009) La biología reproductiva en la predicción del potencial invasor de plantas exóticas. In: Medel, R., Aizen, M.A. and Zamora, R., Eds., Ecología y Evolución de Interacciones Planta-Animal, Editorial Universitaria, Santiago de Chile, 263-285.
[81]
Busch, J.W. and Delph, L.F. (2012) The Relative Importance of Reproductive Assurance and Automatic Selection as Hypotheses for the Evolution of Self-Fertilization. Annals of Botany, 109, 553-562.
[82]
Medrano, M., Herrera, C.M. and Barrett, S.C.H. (2005) Herkogamy and Mating Patterns in the Self-Compatible Daffodil Narcissus longispathus. Annals of Botany, 95, 1105-1111. https://doi.org/10.1093/aob/mci129
