Abstract
Sexual systems play a key role in the ecology and evolution of plant populations. Research on Garcinia L. has shown the occurrence of variations in the sexual systems of this genus, with some authors considering it as dioecious, and for some species as gynodioecious or androdioecious. The population of G. brasiliensis in the restinga of Maricá is dioecious with two individuals characterized as monoecious. Anatomical analysis showed that one has pistillate and sterile staminate flowers, being an unusual female and the other has staminate and perfect flowers (functional pollen grains and ovules), being andromonoecious. In addition, field observations, controlled hand-pollinations, reproductive phenology and anatomical analysis showed no evidence of apomixis in this Neotropical species, different from that provided in the literature for paleotropical species. However, asexual reproduction occurs through ramets suggesting that in this environment of restinga the seedlings are subjected to considerable limitations, and vegetative propagation becomes an important alternative for the occupation of the environment. Flowering episodes occurred throughout the study period, featuring a subannual and long-lasting flowering pattern mainly due to multiple blooms of male plants. The floral characters observed in G. brasiliensis are often associated with a generalist pollination system. Apis mellifera and Trigona spinipes are the effective pollinators of G. brasiliensis flowers. Our findings provide new insights into the reproductive biology of Garcinia.
References
Abe T (2001) Flowering phenology, display size and fruit set in a understory dioecious shrub, Aucuba japonica (Cornaceae). Am J Bot 88:455–461
Armstrong JE (1997) Pollination by deceit in nutmeg (Myristica insipida, Myristicaceae): floral displays and beetle activity at male and female trees. Am J Bot 84:1266–1274
Armstrong JE, Irvine AK (1989) Flowering, sex ratios, pollen-ovule ratios, fruit set, and reproductive effort of a dioecious tree, Myristica insipida (Myristicaceae), in two different rain forest communities. Am J Botany 76:74–85
Ashman TL (2006) The evolution of separate sexes: a focus on the ecological context. In: Harder LD, Barrett SCH (eds) Ecology and evolution of flowers. Oxford University Press, Oxford, pp 204–222
Ashman TL, Swetz J, Shivitz S (2000) Understanding the basis of pollinator selectivity in sexually dimorphic Fragaria virginiana. Oikos 90:347–356
Ashman TL, Knight TM, Steets JA, Amarasekare P, Burd M, Campbell DR, Dudash MR, Johnston MO, Mazer SJ, Mitchell RJ, Morgan MT, Wilson WG (2004) Pollen limitation of plant reproduction: ecological and evolutionary causes and consequences. Ecology 85:2408–2421
Barrett SCH (2002) The evolution of plant sexual diversity. Nat Rev Genet 3:274–284
Barrett SCH (2010) Understanding plant reproductive diversity. Philos Trans R Soc B 365:99–109
Bawa KS (1980) Evolution of dioecy in flowering plants. Annu Rev Ecol Syst 11:15–39
Bawa KS, Opler PA (1975) Dioecism in tropical forest trees. Evolution 29:167–179
Berg ME (1979) Revisão das espécies brasileiras do gênero Rheedia L. (Guttiferae). Acta Amaz 9:43–74
Cavalcante PB (1996) Frutas comestíveis da Amazônia. CNPQ/Museu Paraense Emílio Goeldi, Belém
Cirne P, Scarano FR (2001) Resprouting and growth dynamics after fire of the clonal shrub Andira legalis (Leguminosae) in a sandy coastal plain in southeastern Brazil. J Ecol 89:351–357
Corbet SA (2006) A typology of pollination systems: Implication for crop management and the conservation of wild plants. In: Waser NM, Ollerton J (eds) Plant-pollinator interactions: from specialization to generalization. University of Chicago Press, Chicago, pp 315–340
Dafni A, Keavan PG, Husband BC (2005) Practical pollination biology. Enviroquest, Cambridge
Delouche JC, Still TW, Raspet M, Lienhard M (1976) O teste do tetrazólio para viabilidade da semente. Agiplan, Brasília
Delph LF, Wolf DE (2005) Evolutionary consequences of gender plasticity in genetically dimorphic breeding systems. New Phytol 166:119–128
Faria APG, Matallana G, Wendt T, Scarano FR (2006) Low fruit set in the abundant dioecious tree Clusia hilariana (Clusiaceae) in a Brazilian restinga. Flora 201:606–611
Farwing N, Randrianirina EF, Voigt FA, Kraemer M, Böhning-Gaese K (2004) Pollination ecology of the dioecious tree Commiphora guillauminii in Madagascar. J Trop Ecol 20:307–316
Feder N, O’Brien TP (1968) Plant microtechnique: some principles and new methods. Am J Bot 55:123–142
Fiaschi P, Pirani JR (2009) Review of plant biogeographic studies in Brazil. J Syst Evol 47:477–496
Fournier LA (1974) Un método cuantitativo para la medición de características fenológicas en árboles. Turrialba 24:422–423
Gahan PB (1984) Plant histochemistry and cytochemistry: an introduction. Academic Press, London
Horn CL (1940) Existence of only one variety of cultivated mangosteen explained by asexually formed “seed”. Science 92:237–238
Kay QON, Lack AJ, Bamber FC, Davies CR (1984) Differences between sexes in floral morphology, nectar production and insect visits in a dioecious species, Silene dioica. New Phytol 98:515–529
Kearns CA, Inouye DW (1993) Techniques for pollination biologists. University Press of Colorado, Boulder
Leal DO, Malafaia C, Cesar R, Pimentel RR, Santiago-Fernandes LDR, Lima HA, Sá-Haiad B (2012) Floral structure of Garcinia brasiliensis in relation to flower biology and evolution. Int J Plant Sci 173:172–183
Lenza E, Oliveira PE (2005) Biologia reprodutiva de Tapirira guianensis Aubl. (Anacardiaceae), uma espécie dióica em mata de galeria do Triângulo Mineiro, Brasil. Rev Bras Bot 28:179–180
Lopes AV, Machado IC (1998) Floral biology and reproductive ecology of Clusia nemerosa (Clusiaceae) in northeastern, Brazil. Plant Syst Evol 213:71–90
Matallana G, Wendt T, Araujo DSD, Scarano FR (2005) High abundance of dioecious plants in a tropical coastal vegetation. Am J Bot 92:1513–1519
Miller S, Venable DL (2003) Floral morphometrics and the evolution of sexual dimorphism in Lycium (Solanaceae). Evolution 57:74–86
Muenchow G, Delesalle V (1994) Pollinator response to male floral display size in two Sagittaria (Alismataceae) species. Am J Bot 81:568–573
Newstrom LE, Frankie GW, Baker HG (1994a) A new classification for plant phenology based on flowering patterns in lowland tropical rain forest trees at La Selva, Costa Rica. Biotropica 26:141–159
Newstrom LE, Frankie GW, Baker HG, Colwell RK (1994b) Diversity of long-term flowering patterns. In: McDade LA, Bawa KS, Hespenheide HA, Hartshorn GS (eds) La Selva: ecology and natural history of a neotropical rain forest. University of Chicago Press, Chicago, pp 142–160
Pangsuban S, Bamroongrugsa N, Kanchanapoom K, Nualsri C (2007) An evaluation of the sexual system of Garcinia atroviridis L. (Clusiaceae), based on reproductive features. Songklanakarin J Sci Technol 29:1457–1468
Radford AE, Dickson WC, Massey JR, Bell CR (1974) Vascular plant systematics. Harper and Row, New York
Ramage CM, Sando L, Peace CP, Carroll BJ, Drew RA (2004) Genetic diversity revealed in the apomictic fruit species Garcinia mangostana L. (mangosteen). Euphytica 136:1–10
Richards AJ (1990a) Studies in Garcinia, dioecious tropical forest trees: agamospermy. Bot J Linn Soci 103:233–250
Richards AJ (1990b) Studies in Garcinia, dioecious tropical forest trees: the phenology, pollination biology and fertilization of G. hombroniana Pierre. Bot J Linn Soc 103:251–261
Richards AJ (2003) Apomixis in flowering plants: an overview. Phil Trans R Soc B 358:1085–1093
Scarano FR (2002) Structure, function and floristic relationships of plant communities in stressful habitats marginal to the Brazilian Atlantic rain forest. Ann Bot 90:517–524
Snow AA (1994) Post-pollination selection and male fitness in plants. Am Nat 144:S69–S83
Stanton ML (1994) Male-male competition during pollination in plant populations. Am Nat 144:40–68
StatSoft Inc (2005) STATISTICA (data analysis software systems), version 7.1. www.Statsoft.com
Sutherland S, Delph L (1984) On the importance of male fitness in plants: patterns of fruit-set. Ecology 65:1093–1104
Sweeney PW (2008) Phylogeny and floral diversity in the genus Garcinia (Clusiaceae) and relatives. Int J Plant Sci 169:1288–1303
Thomas SC (1997) Geographic parthenogenesis in a tropical forest tree. Am J Bot 84:1012–1015
Vaughton G, Ramsey M (1998) Floral display, pollinator visitation and reproductive success in the dioecious perennial herb Wurmbea dioica (Liliaceae). Oecologia 115:93–101
Vaughton G, Ramsey M (2012) Gender plasticity and sexual system stability in Wurmbea. Ann Bot 109:521–530
Acknowledgments
We thank the editor and the anonymous reviewers for their helpful comments, Dr. Marcia Souto Curi and Dr. Favizia Freitas de Oliveira for insect identification and Dr. Janet W. Reid (JWR Associates) for the revision of the English text. This study is part of the Ph.D. thesis of C.R.B. and the M.Sc. theses of D.O.L. and R.C.P.S., which were carried out in the Postgraduate Program in Biological Sciences (Botany) of the Museu Nacional, Universidade Federal do Rio de Janeiro (UFRJ), Rio de Janeiro, Brazil, and were supported by CAPES (Coordenação de Aperfeiçoamento de Pessoal de Nível Superior).
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Leal, D.O., Benevides, C.R., Silva, R.C.P. et al. Garcinia brasiliensis: insights into reproductive phenology and sexual system in a Neotropical environment. Plant Syst Evol 299, 1577–1585 (2013). https://doi.org/10.1007/s00606-013-0833-7
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00606-013-0833-7