Pollination biology of a tree species of Cupania: synchronous dichogamy, generalist phenotype and predominance of stingless bees

Authors

  • Alexandre Tomaz da Fonseca Jardim Botânico do Rio de Janeiro, Rua Pacheco Leão 915, 22460-030, Rio de Janeiro – RJ, Brasil.
  • Leandro Freitas Jardim Botânico do Rio de Janeiro http://orcid.org/0000-0002-4146-2514

DOI:

https://doi.org/10.31055/1851.2372.v57.n2.35857

Keywords:

bees, ecological generalization, Meliponini, monoecious, plant- pollinator interactions, reproductive success, Sapindaceae

Abstract

Background and aims: We know little about the pollination biology of tropical tree species associated with the pollination system by diverse insects (DI). We studied the floral biology, breeding system, and floral visitors of Cupania oblongifolia.

M&M: Experiments and observations were carried out in an area of the Atlantic Forest.

Results: The flowers are small and greenish and produce little nectar. The species is diclinous-monoecious but the anthesis of female and male flowers is temporally separated into the inflorescences, with little or no overlap (i.e., synchronized dichogamy). Fruit set did not differ after cross- and self-pollinations and natural conditions, indicating the absence of both self-incompatibility and pollen limitation. Flowers of C. oblongifolia were visited by 87 species of Hymenoptera, Diptera, Lepidoptera, and Coleoptera. Male flowers were more visited and 20 species visited the two morphs. Floral visitors were mostly rare and about 80% of the visits were made by Hymenoptera, mainly stingless bees. Two species of Scaptotrigona were eudominant.

Conclusions: The floral phenotype fits on the description of DI systems. Many species of insects were recorded but stingless bees predominated. Meliponini constitutes the most abundant anthophilous group in Neotropical forests, thus pollination systems associated with them are expected. Based on our results, it is possible to forecast that some species classified as DI based on floral phenotype and visitor richness may be strongly associated with a certain group of pollinators, denoting a lower degree of generalization

References

GREN, J., T. ELMQVIST & A. TUNLID. 1986. Pollination by deceit, floral sex ratios and seed set in dioecious Rubus chamaemorus L. Oecologia 70: 332-338.

https://doi.org/10.1007/BF00379493

ALVES-DOS-SANTOS, I., C. I. SILVA, M. PINHEIRO & A. M. P. KLEINERT. 2016. Quando um visitante floral é um polinizador? Rodriguésia 67: 295-307.

https://doi.org/10.1590/2175-7860201667202

ARAÚJO, E. D., M. COSTA, J. CHAUD-NETTO & H. G. FOWLER. 2004. Body size and flight distance in stingless bees (Hymenoptera: Meliponini): inference of flight range and possible ecological implications. Braz. J. Biol. 64: 563-568.

https://doi.org/10.1590/S1519-69842004000400003

ARMBRUSTER, W. S. 2017. The specialization continuum in pollination systems: diversity of concepts and implications for ecology, evolution and conservation. Funct. Ecol. 31: 88-100.

https://doi.org/10.1111/1365-2435.12783

ÁVILA JR, R. S. & L. FREITAS. 2011. Frequency of visits and efficiency of pollination by diurnal and nocturnal lepidopterans for the dioecious tree Randia itatiaiae (Rubiaceae). Aust. J. Bot. 59: 176-184.

https://doi.org/10.1071/BT10280

BAKER, H. G. 1976. "Mistake pollination" as a reproductive system with special reference to the Caricaceae. In: BURLEY, J. & B. T. STYLES (eds.), Tropical tree: variation, breeding and conservation, pp. 161-169. Academic Press, London.

BARTOŠ, M., R. TROPEK, L. SPITZER, E. PADYŠÁKOVÁ, P. JANŠTA, J. STRAKA, M. TKOČ & Š. JANEČEK. 2015. Specialization of pollination systems of two co-flowering phenotypically generalized Hypericum species (Hypericaceae) in Cameroon. Arthropod-Plant Interact. 9: 241-252.

https://doi.org/10.1007/s11829-015-9378-8

BAWA, K. S. 1977. The reproductive biology of Cupania guatemalensis Radlk. (Sapindaceae). Evolution 31: 52-63.

https://doi.org/10.1111/j.1558-5646.1977.tb00981.x

BAWA, K. S. 1980. Evolution of dioecy in flowering plants. Ann. Rev. Ecol. Syst. 11: 15-39.

https://doi.org/10.1146/annurev.es.11.110180.000311

BAWA, K. S. 1990. Plant-pollinator interactions in tropical rain forest. Ann. Rev. Ecol. Syst. 21: 399-422.

https://doi.org/10.1146/annurev.es.21.110190.002151

BAWA, K. S. & P. A. OPLER. 1975. Dioecism in tropical forest trees. Evolution 29: 167-179.

https://doi.org/10.1111/j.1558-5646.1975.tb00824.x

BAWA, K. S., S. H. BULLOCK, D. R. PERRY, R. E. COVILLE & M. H. GRAYUM. 1985. Reproductive biology of tropical lowland rain forest trees. II. Pollination systems. Amer. J. Bot. 72: 346-356.

https://doi.org/10.1002/j.1537-2197.1985.tb05358.x

BIESMEIJER, J. C. & E. J. SLAA. 2004. Information flow and organization of stingless bee foraging. Apidologie 35: 143-157.

https://doi.org/10.1051/apido:2004003

BUENO, F. G. B., L. KENDALL, D. A. ALVES, M. L. TAMARA, T. HEARD, T. LATTY & R. GLOAG. 2021. Stingless bee floral visitation in the global tropics and subtropics. bioRxiv 2021.2004.2026.440550.

https://doi.org/10.1101/2021.04.26.440550

CASTILLO, R. A., H. CABALLERO, K. BOEGE, J. FORNONI & C. A. DOMÍNGUEZ. 2012. How to cheat when you cannot lie? Deceit pollination in Begonia gracilis. Oecologia 169: 773-782.

https://doi.org/10.1007/s00442-012-2250-y

CRUDEN, R. W. 1988. Temporal dioecism: systematic breadth, associated traits, and temporal patterns. Bot. Gaz. 149: 1-15.

https://doi.org/10.1086/337684

DAFNI, A. 1984. Mimicry and deception in pollination. Ann. Rev. Ecol. Syst. 15: 259-278.

https://doi.org/10.1146/annurev.es.15.110184.001355

DAFNI, A., P. G. KEVAN & B. C. HUSBAND. 2005. Practical pollination biology. Cambridge, Ontario.

DELLINGER, A. S. 2020. Pollination syndromes in the 21st century: where do we stand and where may we go? New Phytol. 228: 1193-1213.

https://doi.org/10.1111/nph.16793

FAEGRI, K. & L. van der PIJL. 1979. The principles of pollination ecology. 3a ed. Pergamon Press, Oxford.

https://doi.org/10.1016/B978-0-08-023160-0.50020-7

FENSTER, C. B., W. S. ARMBRUSTER, P. WILSON, M. R. DUDASH & J. D. THOMSON. 2004. Pollination syndromes and floral specialization. Ann. Rev. Ecol., Evol., Syst. 35: 375-403.

https://doi.org/10.1146/annurev.ecolsys.34.011802.132347

FERREIRA, D. L. 2009. Interações entre Cupania vernalis Camb. (Sapindaceae) e insetos antófilos em fragmentos florestais no sul do Brasil. Tese de Doutorado, Pontifícia Universidade Católica, Porto Alegre.

FREITAS L. 2018. Precisamos falar sobre o uso impróprio de recursos florais. Rodriguésia 69: 2223-2238.

https://doi.org/10.1590/2175-7860201869446

GUEDES-BRUNI, R. R. 1998. Composição, estrutura e similaridade florística de dossel em seis unidades fisionômicas de Mata Atlântica no Rio de Janeiro. Tese de Doutorado, Universidade de São Paulo, São Paulo.

INOUYE, R. S., G. S. BYERS & J. H. BROWN. 1980. Effects of predation and competition on survivorship, fecundity, and community structure of desert annuals. Ecology 61: 1344-1351.

https://doi.org/10.2307/1939043

JANZEN, D. H. 1975. Ecology of plants in the tropics. Studies in Biology 58. Edward Arnold, Londres.

KEARNS, C. A. & R. S. INOUYE. 1995. Techniques for pollination biologists. Univ. Press Colorado, Niwot.

LARSON, B. M., S. C. BARRETT. 2000. A comparative analysis of pollen limitation in flowering plants. Biol. J. Linn. Soc. 69: 503-520.

https://doi.org/10.1111/j.1095-8312.2000.tb01221.x

LEGENDRE, P. & L. LEGENDRE. 1998. Numerical ecology. 2a ed. Elsevier, Amsterdam.

LEÓN, A., C. ARIAS-CASTRO, M. A. RODRÍGUEZ-MENDIOLA, R. MEZA-GORDILLO, F. A. GUTIÉRREZ-MICELI, & J. C. NIEH. 2015. Colony foraging allocation is finely tuned to food distance and sweetness even close to a bee colony. Entomol. Exp. Appl. 155: 47-53.

https://doi.org/10.1111/eea.12283

LEONHARDT, S.D. 2017. Chemical ecology of stingless bees. J. Chem. Ecol. 43: 385-402.

https://doi.org/10.1007/s10886-017-0837-9

LIMA, H., G. SOMNER & A. GIULIETTI. 2016. Duodichogamy and sex lability in Sapindaceae: the case of Paullinia weinmanniifolia. Pl. Syst. Evol. 302: 109-120.

https://doi.org/10.1007/s00606-015-1247-5

LLOYD, D. G. & C. J. WEBB. 1986. The avoidance of interference between the presentation of pollen and stigmas in angiosperms. I. Dichogamy. New Zeal. J. Bot. 24: 135-162.

https://doi.org/10.1080/0028825X.1986.10409725

LORENZI, H. 1998. Árvores Brasileiras: manual de identificação e cultivo de plantas arbóreas nativas. Instituto Plantarum, Nova Odessa.

MARTINS, C. & L. FREITAS. 2018. Functional specialization and phenotypic generalization in the pollination system of an epiphytic cactus. Acta Bot. Bras. 32: 359-366.

https://doi.org/10.1590/0102-33062017abb0335

MARTINS, C., M. REGINATO, J. M. GÓMEZ & L. FREITAS. 2022. Phylogenetic conservation and shifts of pollination niche in generalist epiphytic cacti. Persp. Pl. Ecol. Evol. Syst. 54: 125650.

https://doi.org/10.1016/j.ppees.2021.125650

MOMOSE K., T. YUMOTO, T. NAGAMITSU, M. KATO, H. NAGAMASU, S. SAKAI, R. HARRISON, T. ITIOKA, A. HAMID & T. INOUE. 1998. Pollination biology in a lowland dipterocarp forest in Sarawak, Malaysia. I. Characteristics of the plant-pollinator community in a lowland dipterocarp forest. Amer. J. Bot. 85:1477-1501.

https://doi.org/10.2307/2446404

MONTEIRO, D. & M. RAMALHO. 2010. Abelhas generalistas (Meliponina) e o sucesso reprodutivo de Stryphnodendron pulcherrimum (Fabales: Mimosaceae) com florada em massa na Mata Atlântica, BA. Neotrop. Entomol. 39: 519-526.

https://doi.org/10.1590/S1519-566X2010000400009

MOREIRA, M. M. & L. FREITAS. 2020. Review of the pollination system by small diverse insects. Neotrop. Entomol. 49: 472-481.

https://doi.org/10.1007/s13744-020-00779-6

MURPHY, C. M. & M. D. BREED. 2008. Nectar and resin robbing in stingless bees. Amer. Entomol. 54: 36-44.

https://doi.org/10.1093/ae/54.1.36

NARBONA, E. & R. DIRZO. 2010. A reassessment of the function of floral nectar in Croton suberosus (Euphorbiaceae): a reward for plant defenders and pollinators. Amer. J. Bot. 97: 672 - 679.

https://doi.org/10.3732/ajb.0900259

NIEH, J. 2004 Recruitment communication in stingless bees (Hymenoptera, Apidae, Meliponini). Apidologie 35: 159-182.

https://doi.org/10.1051/apido:2004007

NIEMIRSKI, R. & M. ZYCH. 2011. Fly pollination of dichogamous Angelica sylvestris (Apiaceae): how (functionally) specialized can a (morphologically) generalized plant be? Pl. Syst. Evol. 294: 147-158.

https://doi.org/10.1007/s00606-011-0454-y

OLLERTON, J., A. KILLICK, E. LAMBORN, S. WATTS, & M. WHISTON. 2007. Multiple meanings and modes: on the many ways to be a generalist flower. Taxon 56: 717-728.

https://doi.org/10.2307/25065855

PIRES, J. P. A. & L. FREITAS. 2008. Reproductive biology of two tree species of Leguminosae in Montane Rain Forest in southeastern Brazil. Flora 203: 491-498.

https://doi.org/10.1016/j.flora.2007.10.002

RAMALHO, M. 1990. Foraging by stingless bees of the genus Scaptotrigona (Apidae, Meliponinae). J. Apic. Res. 29: 61-67.

https://doi.org/10.1080/00218839.1990.11101198

RAMALHO, M. 2004. Stingless bees and mass flowering trees in the canopy of Atlantic Forest: a tight relationship. Acta Bot. Bras. 18: 37-47.

https://doi.org/10.1590/S0102-33062004000100005

RENNER, S. S. & J. P. FEIL. 1993. Pollinators of tropical dioecious angiosperms. Amer. J. Bot. 80: 1100-1107.

https://doi.org/10.1002/j.1537-2197.1993.tb15337.x

ROSAS-GUERRERO, V., R. AGUILAR, S. MARTÉN-RODRÍGUEZ, L. ASHWORTH, M. LOPEZARAIZA-MIKEL, J. M. BASTIDA & M. QUESADA. 2014. A quantitative review of pollination syndromes: do floral traits predict effective pollinators? Ecol. Lett. 17: 388-400.

https://doi.org/10.1111/ele.12224

ROUBIK, D. W. 1989. Ecology and natural history of tropical bees. Cambridge Tropical Biology Series. Cambridge Univ. Press, Cambridge.

https://doi.org/10.1017/CBO9780511574641

ROUBIK, D. W. & M. ALUJA. 1983. Flight ranges of Melipona and Trigona in tropical forest. J. Kansas Entomol. Soc. 56: 217-222.

SEGADAS-VIANNA, F. & L. DAU. 1965. Ecology of Itatiaia range, southeastern Brazil. II. Climates and altitudinal climatic zonation. Arq. Mus. Nac. (Rio de J.) 53: 31-53.

SOMNER, G. & M. S. FERRUCCI. 2009. Sapindaceae. In: WANDERLEY, M. G. L., G. J. SHEPHERD, T. S. MELHEM, A. M. GIULIETTI & S. E. MARTINS (eds.), Flora Fanerogâmica do Estado de São Paulo, vol. 6, pp. 195-256. Instituto de Botânica, São Paulo.

SOMNER, G.V., M. S. FERRUCCI, P. ACEVEDO-RODRÍGUEZ, R. O. PERDIZ, R. L. G. COELHO & H. MEDEIROS. 2015. Sapindaceae in Lista de Espécies da Flora do Brasil. [online]. Disponível em: http://floradobrasil.jbrj.gov.br/jabot/floradobrasil/FB216. [Acesso: 05 Novembro 2019].

STEBBINS, G. L. 1970. Adaptative radiation of reproductive characteristics in angiosperms, I: Pollination mechanisms. Ann. Rev. Ecol. Syst. 1: 307-326.

https://doi.org/10.1146/annurev.es.01.110170.001515

STEVENS, P. F. 2001 (onwards). Angiosperm Phylogeny Website - Version 14 [online]. Disponível em: http://www.mobot.org/MOBOT/research/APweb/ [Acesso: 20 Outubro 2021].

THORP, R. W. 2000. The collection of pollen by bees. Pl. Syst. Evol. 222: 211-223.

https://doi.org/10.1007/978-3-7091-6306-1_11

WARDHAUGH C. W. 2015. How many species of arthropods visit flowers? Arthropod-Plant Interact. 9: 547-565.

https://doi.org/10.1007/s11829-015-9398-4

WASER, N. M., L. CHITTKA, M. V. PRICE, N. M. WILLIAMS & J. OLLERTON. 1996. Generalization in pollination systems, and why it matters. Ecology 77: 1043-1060.

https://doi.org/10.2307/2265575

YADAV, N., A. K. PANDEY & A. K. BHATNAGAR. 2020. Pollination biology and breeding system of maple species Acer oblongum Wall. ex DC. (Sapindaceae) showing mixed syndromes of wind and insect pollination. Proc. Natl. Acad. Sci., India, Section B 90: 489-500.

https://doi.org/10.1007/s40011-019-01120-x

ZAMUDIO, F., M. GATTI, N. I. HILGERT, L. J. ÁLVAREZ, P. MULIERI, R. AGUILAR & L. ASHWORTH. 2021. Insects or Wind? New findings on the pollination system of Euterpe edulis (Arecaceae). Arthropod Plant Interact. 15: 503–516.

https://doi.org/10.1007/s11829-021-09836-2ZAR, J. H. 1999. Biostatistical analysis. 3a ed. Prince-Hall, New Jersey.

Published

2022-06-29

Issue

Section

Biología Reproductiva

How to Cite

“Pollination Biology of a Tree Species of Cupania: Synchronous Dichogamy, Generalist Phenotype and Predominance of Stingless Bees”. 2022. Boletín De La Sociedad Argentina De Botánica (Journal of the Argentine Botanical Society 57 (2). https://doi.org/10.31055/1851.2372.v57.n2.35857.

Similar Articles

151-160 of 216

You may also start an advanced similarity search for this article.