Nocturnal and diurnal pollination in Copaifera coriacea,  a dominant species in sand dunes of the Middle São Francisco  River Basin, Northeastern Brazil

Isys Mascarenhas Souza; Frederic Mendes Hughes; Ligia Silveira Funch; Luciano Paganucci de Queiroz

doi:10.5091/plecevo.2021.1715

Plant Ecology and Evolution 154(2): 207-216, doi: 10.5091/plecevo.2021.1715

Nocturnal and diurnal pollination in Copaifera coriacea, a dominant species in sand dunes of the Middle São Francisco River Basin, Northeastern Brazil

Isys Mascarenhas Souza^‡, Frederic Mendes Hughes^‡, Ligia Silveira Funch^‡, Luciano Paganucci de Queiroz^‡

‡ Universidade Estadual de Feira de Santana, Feira de Santana, Brazil

Corresponding author: Isys Mascarenhas Souza ( isys.souza@gmail.com )

This is an open access article distributed under the terms of the Creative Commons Attribution License (CC BY 4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

Citation: Souza IM, Hughes FM, Funch LS, de Queiroz LP (2021) Nocturnal and diurnal pollination in Copaifera coriacea, a dominant species in sand dunes of the Middle São Francisco River Basin, Northeastern Brazil. Plant Ecology and Evolution 154(2): 207-216. https://doi.org/10.5091/plecevo.2021.1715

Abstract

Background and aims – Copaifera coriacea, a species in the resin-producing clade Detarioideae (Leguminosae), is an endemic and abundant species found in sand dunes in Brazilian Caatinga domain vegetation – a Quaternary paleodesert. We investigated floral traits and aspects of pollination biology, focusing on the pollination system of C. coriacea.

Material and methods – Anthesis duration, stigma receptivity, pollen viability, nectar concentration, and the presence of osmophores and pigments reflecting UV light were assessed. Floral visitors were classified as potential pollinators, occasional pollinators or thieves, based on the time and foraging behaviour and resource collected. Pollination effectiveness were assessed for potential pollinators by the detection of pollen tubes on the stigma or stylar canal by epifluorescence microscopy.

Key results – The species has white and small flowers, with anthesis beginning in the dark (ca 00:30) and the flowers are completely opened approximately 3 h later, when a sweet odour is perceptible. The onset of stigma receptivity and pollen grain viability occurs only after the completion of flower opening, and a concentrated nectar is available during the day. The presence of pollen tubes confirmed the efficiency of the main insects in the transfer of pollen.

Conclusion – Our result demonstrates that C. coriacea has a generalist pollination system mediated mainly by two distinct guilds of insect pollinators: moths (nocturnal, searching for nectar) and bees (diurnal, pollen collectors). This finding can provide more information about diversification in the genus Copaifera.

Keywords

anthesis, floral biology, floral visitors, generalist pollination, Leguminosae, pollen tubes

References

Aguilar-Rodríguez P.A., Krömer T., García-Franco J.G. & MacSwiney M.C.G. 2016. From dusk till dawn: nocturnal and diurnal pollination in the epiphyte Tillandsia heterophylla (Bromeliaceae). Plant Biology 18: 37–45. https://doi.org/10.1111/plb.12319

Alvares C.A., Stape J.L., Sentelhas P.C., Gonçalves J.L. & Sparovek G. 2013. Köppen’s climate classiﬁcation map for Brazil. Meteorologische Zeitschrift 22: 711–728. https://doi.org/10.1127/0941-2948/2013/0507

Amorim F.W., Galetto L. & Sazima M. 2013. Beyond the pollination syndrome: nectar ecology and the role of diurnal and nocturnal pollinators in the reproductive success of Inga sessilis (Fabaceae). Plant Biology 15: 317–327. https://doi.org/10.1111/j.1438-8677.2012.00643.x

Armbruster W.S. 2014. Floral specialization and angiosperm diversity: phenotypic divergence, fitness trade-offs and realized pollination accuracy. Annals of Botany Plants 6: plu003. https://doi.org/10.1093/aobpla/plu003

Armbruster W.S. & Baldwin B.G. 1998. Switch from specialized to generalized pollination. Nature 394: 621. https://doi.org/10.1038/29210

Armbruster W.S., Shi X.-Q. & Huang S.-Q. 2014. Do specialized ﬂowers promote reproductive isolation? Realized pollination accuracy of three sympatric Pedicularis species. Annals of Botany 113: 331–340. https://doi.org/10.1093/aob/mct187

Arroyo M.T.K. 1981. Breeding systems and pollination biology in Leguminosae. In: Polhill R.M. & Raven P.H. (eds) Advances in legume systematics: part 2: 723–769. Royal Botanic Gardens, Kew, Richmond.

Avila Jr. R.S. & Freitas L. 2011. Frequency of visits and efﬁciency of pollination by diurnal and nocturnal lepidopterans for the dioecious tree Randia itatiaiae (Rubiaceae). Australian Journal of Botany 59: 176–184. https://doi.org/10.1071/bt10280

Avila Jr. R., Pinheiro M. & Sazima M. 2015. The generalist Inga subnuda subsp. luschnathiana (Fabaceae): negative effect of floral visitors on reproductive success? Plant Biology 17: 728–733. https://doi.org/10.1111/plb.12291

Costa J.A.S. 2007. Estudos taxonômicos, biossistemáticos e filogenéticos em Copaifera L. (Leguminosae-Detarieae) com ênfase nas espécies do Brasil Extra-Amazônico. PhD thesis, Universidade Estadual de Feira de Santana, Brazil.

Costa J.A.S. 2020. Copaifera. In: Flora do Brasil 2020, under construction. Jardim Botânico do Rio de Janeiro. Available from http://floradobrasil.jbrj.gov.br/ [accessed 9 Dec. 2019].

Costa A.C.G. & Machado I.C. 2017. Pin-monomorphism in Palicourea crocea (SW.) Roem. & Schult. (Rubiaceae): reproductive traits and role of ﬂoral visitors. Brazilian Journal of Botany 40: 1063–1070. https://doi.org/10.1007/s40415-017-0406-z

Dafni A., Kevan P.G. & Husband B.C. 2005. Practical pollination biology. Enviroquest Ltd., Cambridge, Ontario, Canada.

Dar S., Arizmendi M.D.C. & Valiente-Banuet A. 2006. Diurnal and nocturnal pollination of Marginatocereus marginatus (Pachycereeae: Cactaceae) in Central Mexico. Annals of Botany 97: 423–427. https://doi.org/10.1093/aob/mcj045

de la Estrella M., Forest F., Klitgard B., et al. 2018. A new phylogeny-based tribal classification of subfamily Detarioideae, an early branching clade of florally diverse tropical arborescent legumes. Scientific Reports 8: 6884. https://doi.org/10.1038/s41598-018-24687-3

Faegri K. & van der Pijl L. 1979. The principles of pollination ecology. Fourth edition. Pergamon Press, Oxford, New York, USA.

Feldman T.S. 2006. Pollinator aggregative and functional responses to flower density: does pollinator response to patches of plants accelerate at low-densities? Oikos 115: 128–140. https://doi.org/10.1111/j.2006.0030-1299.14493.x

Fenster C.B., Armbruster W.S., Wilson P., Dudash M.R. & Thomson J.T. 2004. Pollination syndromes and ﬂoral specialization. Annual Review of Ecology, Evolution, and Systematics 35: 375–403. https://doi.org/10.1146/annurev.ecolsys.34.011802.132347

Fougère-Danezan M., Herendeen P.S., Maumont S. & Bruneau A. 2010. Morphological evolution in the variable resin-producing Detarieae (Fabaceae): do morphological characters retain a phylogenetic signal? Annals of Botany 105: 311–325. https://doi.org/10.1093/aob/mcp280

Freitas C.V. & Oliveira P.E. 2002. Biologia reprodutiva de Copaifera langsdorffii Desf. (Leguminosae, Caesalpinioideae). Brazilian Journal of Botany 25: 311–321. https://doi.org/10.1590/S0100-84042002000300007

Glover B.J. & Whitney H. 2010. Iridescence and structural colour in plants – the poorly studied relatives of pigment colour. Annals of Botany 105: 505–511. https://doi.org/10.1093/aob/mcq007

Gómez J.M., Perfectti F., Abdelaziz M., Lorite J., Muñoz-Pajares A.J. & Valverde J. 2014. Evolution of pollination niches in a generalist plant clade. New Phytologist 205: 440–453. https://doi.org/10.1111/nph.13016

Grant V. 1949. Pollination systems as isolating mechanisms in angiosperms. Evolution 3: 82–97. https://www.jstor.org/stable/2405454

Grant V. 1994. Modes and origins of mechanical and ethological isolation in angiosperms. Proceedings of the National Academy of Sciences of the United States of America 91: 3–10. https://doi.org/10.1073/pnas.91.1.3

Gronquist M., Bezzerides A., Attygalle A., Meinwal J., Eisner M. & Eisner T. 2001. Attractive and defensive functions of the ultraviolet pigments of a flower (Hypericum calycinum). Proceedings of the National Academy of Sciences of the United States of America 98: 13745–13750. https://doi.org/10.1073/pnas.231471698

Haber W.A. & Frankie G.W. 1989. A tropical hawkmoth community: Costa Rican dry forest sphingidae. Biotropica 21: 155–172. https://doi.org/10.2307/2388706

Hernández-Conrique D., Ornelas J.F., García-Franco J.G. & Vargas F. 2007. Nectar production of Calliandra longipedicellata (Fabaceae: Mimosoideae), an endemic Mexican shrub with multiple potential pollinators. Biotropica 39: 459–467. https://doi.org/10.1111/j.1744-7429.2007.00277.x

Hughes C. & Eastwood R. 2006. Island radiation on a continental scale: exceptional rates of plant diversification after uplift of the Andes. Proceedings of the National Academy of Sciences of the United States of America 103: 10334–10339. https://doi.org/10.1073/pnas.0601928103

Inouye D.W. 1980. The terminology of floral larceny. Ecology 61: 1251–1253. https://doi.org/10.2307/1936841

Johnson S.D. 2010. The pollination niche and its role in the diversiﬁcation and maintenance of the southern African ﬂora. Philosophical Transactions of the Royal Society B 365: 499–516. https://doi.org/10.1098/rstb.2009.0243

Kulbaba M. & Worley A. 2012. Selection on floral design in Polemonium brandegeei (Polemoniaceae): female and male fitness under hawkmoth pollination. Evolution 66: 1344–59. https://doi.org/10.1111/j.1558-5646.2011.01536.x

Lewis G.P., Simpson B.B. & Neff J.L. 2000. Progress in understanding the reproductive biology of the Caesalpinioideae (Leguminosae). In: Herendeen P.S. & Bruneau A. (eds) Advances in legume systematics: part 9, 65–78. Royal Botanic Gardens, Kew, Richmond.

Mackinder B. 2005. Detarieae. In: Lewis G., Schrire B., MacKinder B. & Lock M. (eds) Legumes of the world: 69–71. Royal Botanic Gardens, Kew, Richmond.

Manning J.C. & Snijman D. 2002. Hawkmoth-pollination in Crinum variabile (Amaryllidaceae) and the biogeography of sphingophily in southern African Amaryllidaceae. South African Journal of Botany 68: 212–216. https://doi.org/10.1016/S0254-6299(15)30422-1

Martén-Rodríguez S., Fenster C.B., Agnarsson I., Skog L.E. & Zimmer E.A. 2010. Evolutionary breakdown of pollination specialization in a Caribbean plant radiation. New Phytologist 188: 403–417. https://doi.org/10.1111/j.1469-8137.2010.03330.x

Martin F.W. 1959. Staining and observing pollen tubes in the style by means of fluorescence. Stain Technology 34: 125–128. https://doi.org/10.3109/10520295909114663

Nadia T.D.L., De Menezes N.L. & Machado I.C. 2013. Floral traits and reproduction of Avicennia schaueriana Moldenke (Acanthaceae): a generalist pollination system in the Lamiales. Plant Species Biology 28: 70–80. https://doi.org/10.1111/j.1442-1984.2011.00361.x

Ne’eman G., Jürgens A., Newstrom-Lloyd L., Potts S.G. & Dafni A. 2010. A framework for comparing pollinator performance: effectiveness and efficiency. Biological Reviews 85: 435– 451. https://doi.org/10.1111/j.1469-185X.2009.00108.x

Oliveira A.F., Carvalho D. & Rosado S.C.S. 2002. Taxa de cruzamento e sistema reprodutivo de uma população natural de Copaifera langsdorffii Desf. na região de Lavras (MG) por meio de isoenzimas. Brazilian Journal of Botany 25: 331–338. https:// doi.org/ https://doi.org/10.1590/S0100-84042002000300009

Ollerton J. 1996. Reconciling ecological processes with phylogenetic patterns: the apparent paradox of plant-pollinator systems. Journal of Ecology 84: 767–769. https://doi.org/10.2307/2261338

Ollerton J., Alarcón R., Waser N.M., et al. 2009. A global test of the pollination syndrome hypothesis. Annals of Botany 103: 1471–1480. https://doi.org/10.1093/aob/mcp031

Primack R.B. 1982. Ultraviolet patterns in flowers, or flowers as viewed by insects. Arnoldia 42: 139–146. https://www.jstor.org/stable/42955058

Queiroz J.A., Quirino Z. & Machado I. 2015. Floral traits driving reproductive isolation of two co-flowering taxa that share vertebrate pollinators. Annals of Botany Plants 7: plv127. https://doi.org/10.1093/aobpla/plv127

Queiroz J.A., Quirino Z.G.M., Lopes A.V. & Machado I.C. 2016. Vertebrate mixed pollination system in Encholirium spectabile: a bromeliad pollinated by bats, opossum and hummingbirds in a tropical dry forest. Journal of Arid Environments 125: 21–30. https://doi.org/10.1016/j.jaridenv.2015.09.015

Ramirez N. & Arroyo M.K. 1990. Estructura Poblacional de Copaifera pubiflora Benth. (Leguminosae; Caesalpinioideae) en los Altos Llanos Centrales de Venezuela. Biotropica 22: 124. https://doi.org/10.2307/2388404

Rech A.R., Kayna A., Oliveira P.E. & Machado I.C. 2014. Biologia da polinização. First edition. Editora Projeto Cultural, Brasíl.

Riffell J.A., Alarcón R. & Abrell L. 2008. Floral trait associations in hawkmoth-specialized and mixed pollination systems. Communicative & Integrative Biology 1: 6–8. https://doi.org/10.4161/cib.1.1.6350

Rocha P.L.B., Queiroz L.P. & Pirani J.R. 2004. Plant species and habitat structure in a sand dune field in the Brazilian Caatinga: a homogeneous habitat harbouring an endemic biota. Brazilian Journal of Botany 27: 739–755. https://doi.org/10.1590/S0100-84042004000400013

Rodarte A.T.A., da Silva F.O. & Viana B.F. 2008. A flora melitófila de uma área de dunas com vegetação de caatinga, Estado da Bahia, Nordeste do Brasil. Acta Botanica Brasilica 22: 301–312. https://doi.org/10.1590/S0102-33062008000200001

Rosas-Guerrero V., Aguilar R., Martén-Rodríguez S., et al. 2014. A quantitative review of pollination syndromes: do floral traits predict effective pollinators? Ecology Letters 17: 388–400. https://doi.org/10.1111/ele.12224

Sapir Y. & Armbruster W.S. 2010. Pollinator-mediated selection and floral evolution: from pollination ecology to macroevolution. New Phytologist 188: 303–306. https://doi.org/10.1111/j.1469-8137.2010.03467.x

Sazima M., Sazima I. & Buzato S. 1994. Nectar by day and night Siphocampylus sulfureus (Lobeliaceae) pollinated by hummingbirds and bats. Plant Systematics and Evolution 191: 237–246. https://doi.org/10.1007/BF00984668

Schemske D.W. & Horvitz C.C. 1984. Variation among floral visitors in pollination ability: a precondition for mutualism specialization. Science 225: 519–521. https://doi.org/10.1126/science.225.4661.519

Schiestl F.P. & Johnson S.D. 2013. Pollinator-mediated evolution of ﬂoral signals. Trends in Ecology & Evolution 28: 307–315. https://doi.org/10.1016/j.tree.2013.01.019

Schluter D. 2009. Evidence for ecological speciation and its alternative. Science 323: 737–741. https://doi.org/10.1126/science.1160006

Scogin R.Y., Young D.A. & Jones C.E. 1977. Anthochlor pigments and pollination biology. II. The ultraviolet patterns of Coreopsis gigantea (Asteraceae). Bulletin of the Torrey Botanical Club 104(2): 155–159. https://doi.org/10.2307/2484361

Sexton J.P., Hangartner S.B. & Hoffmann A.A. 2013. Genetic isolation by environment or distance: which pattern of gene flow is most common? Evolution 68: 1–15. https://doi.org/10.1111/evo.12258

Stebbins G.L. 1970. Adaptive radiation of reproductive characters in angiosperms, I: pollination mechanisms. Annual Review of Ecology and Systematics 1: 307–326. https://doi.org/10.1146/annurev.es.01.110170.001515

Valente L.M., Manning J.C., Goldblatt P. & Vargas P. 2012. Did pollination shifts drive diversiﬁcation in Southern African Gladiolus? Evaluating the model of pollinator-driven speciation. The American Naturalist 180: 83–98. https://doi.org/10.1086/666003

van der Niet T. & Johnson S.D. 2012. Phylogenetic evidence for pollinator-driven diversification of angiosperms. Trends in Ecology & Evolution 27: 353–361. https://doi.org/10.1016/j.tree.2012.02.002

Waser N.M., Chittka L., Price M.V., Williams N.M. & Ollerton J. 1996. Generalization in pollination systems, and why it matters. Ecology 77: 1043–1060. https://doi.org/10.2307/2265575