ASPECTOS FLORAIS E REPRODUTIVOS DE PSYCHOTRIA CAPITATA RUIZ & PAVON (RUBIACEAE), UM CASO DE DISTILIA TÍPICA NO CERRADO
DOI:
https://doi.org/10.4257/oeco.2021.2503.05Palavras-chave:
heterostyly, pollination, reciprocal herkogamyResumo
A integração fenotípica observada em flores é uma estratégia evolutiva que visa o aumento do fluxo de pólen entre indivíduos, favorecendo o cruzamento e a manutenção da variabilidade genética. Esse sucesso tem relação direta com a estrutura floral, como o hermafroditismo, e com o comportamento dos visitantes, podendo gerar conflitos entre as estruturas florais, sendo selecionadas características que reduzem esse conflito e ampliam o fluxo de pólen, como é o caso da heterostilia. O objetivo do estudo foi descrever as características florais, o sistema reprodutivo, e a polinização em Psychotria capitata Ruiz & Pavon (Rubiaceae). Para tal foram medidas e observadas as estruturas florais, realizados cruzamentos controlados, observados os visitantes florais e avaliado a produção de néctar. Psychotria capitata é uma espécie distílica típica, arbustiva com no máximo 3 metros de altura, com altos índices de hercogamia recíproca entre os morfos florais. Apresenta flores brancas, tubulares, visitadas por uma ampla gama de insetos, incluindo mariposas, abelhas, vespas e moscas. Houve formação maior de frutos em polinização cruzada intermorfo (> 60 %) e menor formação em polinização intramorfo (< 20 %) e autopolinização (< 15 %), caracterizando a auto e intramorfo incompatibilidade. Esses dados foram confirmados pelo não crescimento de tubos polínicos em pistilos autopolinizados e polinizados de forma intramorfo. A floração é anual, e ocorre entre os meses de outubro e janeiro, com pico de floração em novembro e dezembro. Os dados reprodutivos avaliados se mostram similares a outras espécies de Rubiaceae do sub bosque de ambientes florestais do Cerrado. Esses dados enriquecem o conhecimento reprodutivo das espécies de Rubiaceae de sub bosque, tão importantes para a manutenção da fauna em fragmentos florestais.
BREEDING SYSTEMS AND POLLINATION OF THE PSYCHOTRIA CAPITATA RUIZ & PAVON (RUBIACEAE): A CASE THE TYPICAL DISTYLY IN CERRADO: The phenotypic integration observed in flowers is an evolutionary strategy that aims to increase the pollen flow between individuals, favoring the crossing and maintenance of genetic variability. This success is directly related to the floral structure, such as hermaphroditism, and to the behavior of visitors, and can generate conflicts between the floral structures, being selected characteristics that reduce this conflict and amplify the pollen flow, as is the case of heterostyly. The objective of the study was to describe the floral characteristics, the reproductive system, and pollination in Psychotria capitata Ruiz & Pavon (Rubiaceae). For this purpose, the floral structures were measured and observed, controlled crossings were carried out, the floral visitors were observed and the nectar production was evaluated. Psychotria capitata is a typical dystylic species, shrub with a maximum height of 3 meters, with high rates of reciprocal hercogamy between the floral morphs. It has white tubular flowers, visited by a wide range of insects, including moths, bees, wasps and flies. There was higher fruit formation in intermorphic cross-pollination (> 60 %) and lower formation in intramorphic (< 20 %) and self-pollination (< 15 %), characterizing self and intramorphic incompatibility. These data were confirmed by the non growth of pollen tubes in self-pollinated pistils and intramorphic pollinators. Blooming is annual, and occurs between the months of October and January, with peak blooming in November and December. The reproductive data evaluated are similar to other Rubiaceae species in the Cerrado forest sub forest. These data enrich the reproductive knowledge of Rubiaceae's sub-forest species, so important for the maintenance of fauna in forest fragments.
Referências
APG IV Angiosperm Phylogeny Group. 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, 161, 105–121.
Armbruster, W. S., Hansen, T. F., Pélabon, C., Pérez-Barrales, R. & Maad, J. 2009. The adaptive accuracy of flowers - measurement and microevolutionary patterns. Annals of Botany, 103, 1529–1545.
Armbruster, W. S., Bolstad, G. H., Hansen, T. F., Keller, B., Conti, E. 2017. Methods the measure and mismeasure of reciprocity in heterostylous flowers. New Phytologist, 215, 906–917. https://doi.org/10.1111/nph.14604.
Barrett, S. C. H., Jesson, L. K. & Baker, A. M. 2000. The evolution and function of stylar polymorphisms in flowering plants. Annals of Botany, 85, 253–265.
Barrett, S. C. H. 2002. The evolution of plant sexual diversity. Nature reviews. Genetics, 3(4), 274–84. DOI:10.1038/nrg776.
Barrett, S. C. H. 2019. A most complex marriage arrangement’: recent advances on heterostyly and unresolved questions. New Phytologist, 224, 1051–1067. DOI: 10.1111/nph.16026.
Barrett, S. C. H. & Shore, J.S. 1987. Variation and evolution of breeding systems in Turnera ulmifolia L. complex (Turneraceae). Evolution, 41(2), 340–354. https://doi.org/10.1111/j.1558-5646.1987.tb05802.x
Barrett S. C. H. & Shore J. S. 2008. New insights on heterostyly: Comparative biology, ecology and genetics. In: V. Franklin-Tong, ed. Self-incompatibility in flowering plants: Evolution, diversity and Mechanisms. pp. 3–32. Springer-Verlag. Berlin, GER.
Barrett, S. C. H., Jesson, L. K. & Baker, A. M. 2000. The evolution and function of stylar polymorphisms in flowering plants. Annals of Botany, 85(A), 253–265. DOI:l0.1006/anbo.1999.1067.
Bawa, K. S. & Beach, J. H. 1983. Self-Incompatibility systems in the Rubiaceae of a Tropical Lowland set sorest. American Journal of Botany, 70(9), 1281–1288. DOI: 10.2307/2443418.
Bell, G. 1985. On the Function of Flowers. Proceedings of the Royal Society B: Biological Sciences, 224(1235), 223–265.
Bullock, S. H. 1985. Breeding systems in the flora of a tropical decidous forest. Biotropica, 17(4),287–301.DOI: 10.2307/2388591.
Castro, C. C. & Oliveira, P. E. 2002. Pollination biology of distylous Rubiaceae in the Atlantic Rain Forest, SE Brazil. Plant Biology, 4(5), 640–646. DOI: 10.1055/s-2002-35433.
Castro, C. C. & Araújo, A. C. 2004. Distyly and sequential pollinators of Psychotria nuda (Rubiaceae) in the Atlantic rain forest, Brazil. Plant Systematics and Evolution, 244, 131–139. DOI: 10.1007/s00606-003-0036-8.
Castro, C. C., Oliveira, P. E. & Alves, M. C. 2004. Breeding system and floral morphometry of distylous Psychotria L. species in the Atlantic Rain Forest, SE Brazil. Plant Biology, 6(6), 755–760. DOI: 10.1055/s-2004-830349.
Coelho, C. P. & Barbosa, A. A. 2003. Biologia reprodutiva de Palicourea macrobotrys Ruiz & Pavon (Rubiaceae): um possível caso de homostilia no gênero Palicourea Aubl. Revista Brasileira de Botânica, 26(3), 403–413.DOI:10.1590/S0100-84042003000300013.
Coelho, C. P. & Barbosa, A. A. 2004. Biologia reprodutiva de Psychotria poeppigiana Mull. Arg. (Rubiaceae), em mata de galeria. Acta Botanica Brasilica, 18(3),481–489. DOI: 10.1590/S0102-33062004000300008.
Consolaro, H. 2008. A distilia em espécies de Rubiaceae do bioma cerrado. Doctoral thesis. Universidade de Brasília, Programa de Pós-graduação em Ecologia, p. 161.
Consolaro, H. Toledo, R. D. P., Ferreguti, R. L., Hay, J. & Oliveira, P. E. 2009. Distilia e homostilia em espécies de Palicourea Aubl. (Rubiaceae) do Cerrado do Brasil Central. Revista Brasileira de Botânica, 32(4),677–689.DOI:10.1590/S0100-84042009000400007.
Consolaro, H. Silva, S. C. S. & Oliveira, P. E. 2011. Breakdown of distyly and pin-monomorphism in Psychottria carthagenensis Jacq. (Rubiaceae). Plant Species Biology, 26(1), 24–32. DOI:10.1111/j.1442-1984.2010.00300.x.
Dafni, A., Kevan P. G. & Husband B. C. (Eds.). 2005. Practical Pollination Biology. Enviroquest, Ltd. Cambridge, Ontario, Canada. p. 590.
Eckert, C. G. & Herlihy, C. R. 2004. Using a cost–benefit approach to understand the evolution of self-fertilization in plants- the perplexing case of Aquilegia canadensis (Ranunculaceae). Plant Species Biology, 19, 159–173.
Endress, P. K. 1994. Diversity and evolutionary biology of tropical flowers. Cambridge University Press, Cambridge. p. 420.
Faegri, K. & Pijl, L. 1979. The principles of pollination ecology. London, Pergamon Press. p. 244.
Faivre, A. M. & Mcdade, L. A. 2001. Population-level variation in the expression ofheterostyly in three species of Rubiaceae: does reciprocal placement of anthers and stigmas carachterize heterostyly? American Journal of Botany, 88(5),841–853. https://pubmed.ncbi.nlm.nih.gov/11353709/.
Ganders, F. R. 1979. The biology of heterostyly. New Zealand Journal of Botany, 17,607–635. doi/pdf/10.1080/0028825X.1979.10432574.
Gibbs, P. E. & Bianchi, M. B. 1999. Does Late-acting self-incompatibility (LSI) Show family Clustering? Two more species of Bignoniaceae with LSI: Dolichandra cynanchoides and Tabebuia nodosa. Annals of Botany, London, 84, 449–457.
Hamilton, C. W. 1990. Variations on a distylous theme in Mesoamerican Psychotria subgenus Psychotria (Rubiaceae). Memoirs of the New York Botanical Garden, 55, 65–75.
Harder, L. D. & Barrett, S. C. H. 1995. Mating cost of large floral displays in hermaphrodite plants. Nature, 373, 512–515.
Harder L. D. & Barrett, S. C. H. 2006. Ecology and evolution of flowers. Oxford: Oxford University Press. p. 384.
Jacquemyn, H., Gielen, M. & Brys R. 2018. Is sexual organ reciprocity related to legitimate pollen deposition in distylous Pulmonaria (Boraginaceae)? Oikos, 127(8), 1216–1224. DOI: 10.1111/oik.05122.
Köppen, W.1948. Climatologia: con un estudio de los climas de la Tierra. México: Fundo de Cultura Economica. p. 478.
Lloyd, D. G. & Webb, C. J. 1986. The avoidance of interference between the presentation of pollen and stigmas in angiosperms I. Dichogamy of pollen and stigmas in angiosperms. New Zealand Journal of Botany, 24, 135–162.
Lloyd D. G. & Webb C. J. 1992 The evolution of heterostyly. In: Barrett S. C. H. (Ed.). Evolution and Function of Heterostyly. pp. 151–178. Springer-Verlag, Berlin.
Martin, F. N. 1959. Staining and observing pollen tubes in the style by means of fluorescence. Stain technology, 34, 125–128. DOI: 10.3109/10520295909114663.
Matias, R., Pérez-Barrales, R. & Consolaro. H. 2020. Patterns of variation in distylous traits and reproductive consequences in Erythroxylum species and populations. American Journal of Botany 107(6), 1–13. DOI: 10.1002/ajb2.1478
Naiki, A. 2012. Heterostyly and the possibility of its breakdown by polyploidization. Plant Species Biology, 27(1), 3–29. DOI: 10.1111/j.1442-1984.2011.00363.x.
Oliveira, A. S. 2008. Fenologia e biologia reprodutiva de cinco espécies de Psychotria L. (Rubiaceae) em um remanescente florestal urbano, Araguari, MG. Master Thesis. Programa de Pós-Graduação da Universidade Estadual de Campinas. p. 64.
Opler, P.A. 1983. Nectar production in a tropical ecosystem. In: Bentley, B. & Elias, T. (Eds.) The biology of nectaries. pp. 30–79. Columbia University Press, New York.
Ordano, M., Fornoni, J., Boege, K. & Domínguez, C. A. 2008. The adaptive value of phenotypic floral integration. The New phytologist, 179(4), 1183–1192.
Passos, L. & Sazima, M. 1995. Reproductive biology of the distylous Mannetia luteo-rubra (Rubiaceae). Botanica Acta, 108(4), 309–313. DOI: 10.1111/j.1438-8677.1995.tb00499.x.
Pereira, Z. V., Vieira, M. F. & Carvalho-Okano, R. M. 2006. Fenologia da floração, morfologia floral e sistema de incompatibilidade em espécies distílicas de Rubiaceae em fragmento florestal do Sudeste brasileiro. Revista Brasileira de Botânica, 29(3), 471–480. DOI: 10.1590/S0100-84042006000300014.
Proctor, M., Yeo, P. & Lack, A. 1996. The natural history of pollination. Harper Collins Publishers, London. p. 479.
Raupp, P. P., Matias, R., Furtado, M. T. & Consolaro, H. 2020. The role of distyly in pollen flow of the hummingbird-pollinated Palicourea rigida (Rubiaceae). Flora, 271, 151681. DOI: 10.1016/j.flora.2020.151681
Rodrigues, E. B. & Consolaro, H. 2013. Atypical distyly in Psychotria goyazensis Mull. Arg. (Rubiaceae), an intramorph self-compatible species. Acta Botanica Brasilica, 27(1), 155–161. DOI: 10.1590/S0102-33062013000100016.
Ruiz, T.Z. & Arroyo, M.T.K. 1978. Plant reproductive ecology of a secondary deciduous tropical forest. Biotropica, 10(3), 221–230. DOI: 10.2307/2387907.
Sage, T. L., Strumas, F., Cole, W. W. & Barrett, S. C. H. 1999. Differential ovule development following self- and cross-pollination: the basis of self-sterility in Narcissus triandrus (Amaryllidaceae). American Journal of Botany, 86(6), 855–70.
Sakai S. & Wright S. J. 2008. Reproductive ecology of 21 coexisting Psychotria species (Rubiaceae): heterostyly lost? Biological Journal of the Linnean Society, 93(1), 125–134. DOI:10.1111/j.1095-8312.2007.00890.x.
Shore, J. S. & Barrett, S. C. H. 1984. The effect of pollination intensity and incompatible pollen on seed set in Turnera ulmifolia (Turneraceae). Canadian Journal of Botany, 62, 1298–1303. DOI: 10.1139/b84-175.
Sobrevila, C., Ramirez, N. & Enrech, N. X. 1983. Reproductive biology of Palicourea fendleri and P. petiolares (Rubiaceae), heterostylous shrubs of a tropical cloud forest in Venezuela. Biotropica, 15(3), 161–169. DOI: 10.2307/2387824.
Souza, R. T. T. 2019. Inacurácia em espécies distílicas de Rubiaceae. Master Thesis. Programa de Pós-Graduação em Biologia Vegetal da Universidade Federal de Uberlândia. p. 70.
Stehlik, I., Caspersen, J. P. & Barrett, S. C. H. 2006. Spatial ecology of mating success in a sexually polymorphic plant. Proceedings of the Royal Society of London B, Biological Sciences, 273(1585), 387–394. DOI: 10.1098/rspb.2005.3317.
Takebayashi, N. & Morrell, P. L. 2001. Is self-fertilization an evolutionary dead end? Revisiting an old hypothesis with genetic theories and a macroevolutionary approach. American Institute of Biological Science, 88(7), 1143–1150. DOI: 10.2307/3558325.
Teixeira, L. A. G. & Machado, I. C. 2004. Biologia da polinização e sistema reprodutivo de Psychotria barbiflora DC. (Rubiaceae). Acta Botanica Brasilica,18(4),853–862. DOI: 10.1590/S0102-33062004000400016.
Waser, N. M. & Price, M. V. 1991. Outcrossing Distance Effects in Delphinium nelsonii: Pollen Loads, Pollen Tubes, and Seed Set. Ecology, 72(1), 171–179. DOI: 10.2307/1938912.
Washitani, I. 1996. Predicted genetic consequences of strong fertility selection due to pollinator loss in an isolated population of Primula sieboldil. Conservation Biology, 10(1), 59–64.
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.
