Floral resource availability of Dicliptera squarrosa (Acanthaceae) and its dependence on hummingbirds for fruit formation in a forest fragment of Central Brazil
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flowering phenology

How to Cite

Matias, R., Furtado, M., Rodrigues, S. and Consolaro, H. (2019) “Floral resource availability of Dicliptera squarrosa (Acanthaceae) and its dependence on hummingbirds for fruit formation in a forest fragment of Central Brazil”, Plant Ecology and Evolution, 152(1), pp. 68-77. doi: 10.5091/plecevo.2019.1537.


Background and aims – Hummingbirds are dependent and specialized on nectar-feeding, and many plants depend upon them for pollination. However, the degree of plant-pollinator interdependence varies greatly among species; thus, information on plant mating systems and availability of resources may help to clarify the dependence of interacting organisms. The goals of this study were to (1) quantify the floral resource available during the flowering of Dicliptera squarrosa Nees for comparison with other co-flowering ornithophilous species, and to (2) determine the importance of floral visitors for the reproductive success of this plant.
Methods – Data collection was performed in a forest fragment within the urban perimeter of Catalão, Goiás, from September 2012 to August 2013. We investigated the flowering phenology, floral biology, nectar characteristics, flower visitors and mating systems of D. squarrosa. Additionally, we evaluated the amount of floral resource offered (number of flowers and energy in joules) by co-flowering ornithophilous species within an area of 6000 m2 for comparison with D. squarrosa.
Key resultsDicliptera squarrosa presents flowers adapted to pollination by hummingbirds, which act as the sole pollinator group for flowers of this species. Flowering occurs from June to September and is synchronous with five other co-flowering species. During the months between July and September, D. squarrosa is the main food source for hummingbirds in the area, offering more floral resources than all of the other five ornithophilous species together. Plants of this species are self-compatible, but they depend on hummingbirds to transfer pollen; levels of autonomous autogamy were low.
Conclusions – We suggest that D. squarrosa is an important species for maintaining hummingbirds in the forest fragment due to its high production of nectar resources. In addition, data on floral biology, flower visitors, and mating systems showed the importance of hummingbirds for reproduction of D. squarrosa, suggesting a mutualistic interaction between plant and hummingbirds.



Aguilar R., Ashworth L., Galetto L., Aizen M.A. (2006) Plant reproductive susceptibility to habitat fragmentation: review and synthesis through a meta-analysis. Ecology Letters 9: 968–980. https://doi.org/10.1111/j.1461-0248.2006.00927.x

Aizen M.A., Feinsinger P. (1994) Forest fragmentation, pollination, and plant reproduction in a Chaco dry forest, Argentina. Ecology 75: 330–351. https://doi.org/10.2307/1939538

Aizen M.A., Rovere A.E. (2010) Reproductive interactions mediated by flowering overlap in a temperate hummingbird-plant assemblage. Oikos 119: 696–706. https://doi.org/10.1111/j.1600-0706.2009.17762.x

Araújo F.P. (2010) A comunidade de plantas utilizadas e suas interações com beija-flores em uma área de Cerrado. PhD thesis, Universidade Federal de Uberlândia, Minas Gerais, Brazil.

Araújo F.P., Sazima M., Oliveira P.E. (2013) The assembly of plants used as nectar sources by hummingbirds in a Cerrado area of Central Brazil. Plant Systematics and Evolution 299: 1119–1133. https://doi.org/10.1007/s00606-013-0783-0

Barroso G.M. (1986) Sistemática de angiosperma do Brasil Vol. III. Viçosa, Imprensa Universitária da Universidade Federal de Viçosa.

Bawa K.S. (1990) Plant-pollinator interactions in tropical rain forests. Annual Review of Ecology and Systematics 21: 399–422. https://doi.org/10.1146/annurev.es.21.110190.002151

Bond W.J. (1994) Do mutualisms matter? Assessing the impact of pollinator and disperser disruption on plant extinction. Philosophical Transactions of the Royal Society of London B 344: 83–90. https://doi.org/10.1098/rstb.1994.0055

Buchmann S.L., Nabhan G.P. (1996) The Forgotten pollinators. Washington, Island Press.

Bullock S.H. (1985) Breeding systems in the flora of a tropical deciduous forest in Mexico. Biotropica 17: 287–301. https://doi.org/10.2307/2388591

Buzato S., Sazima M., Sazima I. (2000) Hummingbird-pollinated floras at three Atlantic forest sites. Biotropica 32: 824–841. https://doi.org/10.1646/0006-3606(2000)032[0824:HPFATA]2.0.CO;2

Castellanos M.C., Wilson P., Thomson J.D. (2002) Dynamic nectar replenishment in flowers of Penstemon (Scrophulariaceae). American Journal of Botany 89: 111–118. https://doi.org/10.3732/ajb.89.1.111

Castellanos M.C., Wilson P., Thomson J.D. (2004) ‘Anti-bee’ and ‘pro-bird’ changes during the evolution of hummingbird pollination in Penstemon flowers. Journal of Evolutionary Biology 17: 876–885. https://doi.org/10.1111/j.1420-9101.2004.00729.x

Cronk Q., Ojeda I. (2008) Bird-pollinated flowers in an evolutionary and molecular context. Journal of Experimental Botany 59: 715–727. https://doi.org/10.1093/jxb/ern009

Endress P.K. (1994) Diversity and evolutionary biology of tropical flowers. Cambridge, Cambridge University Press.

Faegri K., Van der Pijl L. (1979) The principles of pollination biology. Oxford, Pergamon Press.

Feinsinger F. (1976) Organization of a tropical guild of nectarivorous birds. Ecological Monographs 46: 257–291. https://doi.org/10.2307/1942255

Ferreira C., Maruyama P.K., Oliveira P.E. (2016) Convergence beyond flower morphology? Reproductive biology of hummingbird pollinated plants in the Brazilian Cerrado. Plant Biology 18: 316–324. https://doi.org/10.1111/plb.12395

Fournier L.A. (1974) Um método cuantitativo para la medición de características fenológicas em árboles. Turrialba 24: 422–423.

Galetto L., Bernardello G. (2005) Practical pollination biology. In: Dafni A., Kevan P.G. Husband B.C. (eds) Rewards in flowers: nectar: 261–313. Oxford, Enviroquest Ltd.

Ghazoul J. (2006) Floral diversity and the facilitation of pollination. Journal of Ecology 94: 295–304. https://doi.org/10.1111/j.1365-2745.2006.01098.x

Gottsberger G., Silberbauer-Gottsberger I. (2006) Life in the Cerrado: a South American tropical seasonal ecosystem,. Vol. 1. Origin, structure, dynamics and plant use. Ulm, Reta Verlag.

Grantsau R. (1989) Os beija-flores do Brasil. Rio de Janeiro, Expressão e Cultura.

Hegland S.J., Totland Ø. (2005) Relationships between species’ floral traits and pollinator visitation in a temperate grassland. Oecologia 145: 586–594. https://doi.org/10.1007/s00442-005-0165-6

Johnson S.D., Steiner K.E. (2000) Generalization versus specialization in plant pollination systems. Trends in Ecology & Evolution 15: 140–143. https://doi.org/10.1016/S0169-5347(99)01811-X

Justino D.G., Maruyama P.K., Oliveira P.E. (2012) Floral resource availability and hummingbird territorial behaviour on a Neotropical savanna shrub. Journal of Ornithology 153: 189–197. https://doi.org/10.1007/s10336-011-0726-x

Kolb A. (2005) Reduced reproductive success and offspring survival in fragmented populations of the forest herb Phyteuma spicatum. Journal of Ecology 93: 1226–1237. https://doi.org/10.1111/j.1365-2745.2005.01049.x

Köppen W. (1948) Climatologia: un estudo de lós climas de La Tierra. México, Fondo de Cultura Económica.

Lázaro A., Totland Ø. (2010) Population dependence in the interactions with neighbors for pollination: a field experiment with Taraxacum officinale. American Journal of Botany 97: 760–769. https://doi.org/10.3732/ajb.0900263

McDade L.A., Weeks J.A. (2004a) Nectar in hummingbird-pollinated neotropical plants I: Patterns of production and variability in 12 species. Biotropica 36: 196–215. https://doi.org/10.1111/j.1744-7429.2004.tb00312.x

McDade L.A., Weeks J.A. (2004b) Nectar in hummingbird-pollinated neotropical plants II: Interactions with flower visitors. Biotropica 36: 216–220. https://doi.org/10.1111/j.1744-7429.2004.tb00313.x

Machado A.O., Oliveira P.E. (2015) Diversidade beta de plantas que oferecem néctar como recurso floral aos beija-flores em cerrados do Brasil Central. Rodriguésia 66: 1–19. https://doi.org/10.1590/2175-7860201566101

Martín-González A.M., Dalsgaard B., Nogués-Bravo D., et al. (2015) The macroecology of phylogenetically structured hummingbird-plant networks. Global Ecology and Biogeography 24: 1212–1224. https://doi.org/10.1111/geb.12355

Maruyama P.K., Oliveira G.M., Ferreira C., Dalsgaard B., Oliveira P.E. (2013) Pollination syndromes ignored: importance of non-ornithophilous flowers to Neotropical savanna hummingbirds. Naturwissenschaften 100: 1061–1068. https://doi.org/10.1007/s00114-013-1111-9

Maruyama P.K., Vizentin-Bugoni J., Oliveira G.M., Oliveira P.E., Dalsgaard B. (2014) Morphological and spatio-temporal mismatches shape a Neotropical savanna plant-hummingbird network. Biotropica 46: 740–747. https://doi.org/10.1111/btp.12170

Matias R., Consolaro H. (2014) Pollination biology of Geissomeria pubescens Nees (Acanthaceae) in a forest remnant in central Brazil. Botany 92: 215–222. https://doi.org/10.1139/cjb-2013-0211

Matias R., Consolaro H. (2015) Polinização e sistema reprodutivo de Acanthaceae Juss. no Brasil: uma revisão. Bioscience Journal 31: 890–907. https://doi.org/10.14393/BJ-v31n3a2015-23979

Matias R., Maruyama P.K., Consolaro H. (2016) A non-hermit hummingbird as main pollinator for ornithophilous plants in two isolated forest fragments of the Cerrados. Plant Systematics and Evolution 302: 1217–1226. https://doi.org/10.1007/s00606-016-1327-1

Medrano M., Herrera C.M., 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

Mendonça L.B., Anjos L. (2006) Feeding behavior of hummingbirds and perching birds on Erythrina speciosa Andrews (Fabaceae) flowers in an urban area, Londrina, Paraná, Brazil. Revista Brasileira de Zoologia 23: 42–49. https://doi.org/10.1590/S0101-81752006000100002

Piovano M., Galetto L., Bernardello L. (1995) Floral morphology, nectar features and breeding system in Ruellia brevifolia (Acanthaceae). Revista Brasileira de Biologia 55: 409–418.

Profice S.R., Kameyama C., Côrtes A.L.A., Braz D.M., Indriunas A., Vilar T., Pessoa C., Ezcurra C., Wasshausen D. (2015) Dicliptera squarrosa (Acanthaceae) in Lista de Espécies da Flora do Brasil. Jardim Botânico do Rio de Janeiro [online]. Available from http://floradobrasil.jbrj.gov.br/jabot/floradobrasil/FB4122 [accessed 6 Aug. 2018].

R Development Core Team (2013) R: a language and environment for statistical computing. Vienna, R Foundation for Statistical Computing.

Radford A.E., Dickinson W.C., Massey J.R., Bell C.R. (1974) Vascular plant systematics. New York, Harper & Row Publishers.

Ribeiro J.F., Walter. B.M.T. (2008) Cerrado: ecologia e Flora. In: Sano S.M., Almeida S.P. (eds) As principais fitofisionomias do Bioma Cerrado: 151–212. Planaltina, Embrapa Cerrados.

Smith-Ramírez C., Martinez P., Nuñez M., González C., Armesto J.J. (2005) Diversity, flower visitation frequency and generalism of pollinators in temperate rain forests of Chiloé Island, Chile. Botanical Journal of the Linnean Society 147: 399–416. https://doi.org/10.1111/j.1095-8339.2005.00388.x

Stacciarini J.H.R. (1991) Interação sociedade natureza – Luta ecológica – Um caso Catalano: mata do setor universitário. Boletim Goiano de Geografia 11: 90–103.

Stiles F.G., Wolf L.L. (1970) Hummingbird territoriality at a tropical flowering tree. The Auk 87: 467–491. https://doi.org/10.2307/4083791

Tripp E.A., Manos P.S. (2008) Is floral specialization an evolutionary dead-end? Pollination system transitions in Ruellia (Acanthaceae). Evolution: International Journal of Organic Evolution 62: 1712–1737. https://doi.org/10.1111/j.1558-5646.2008.00398.x

Vieira D.L.M., Coutinho A.G., da Rocha G.P.E. (2013) Resprouting ability of dry forest tree species after disturbance does not relate to propagation possibility by stem and root cuttings. Restoration Ecology 21: 305–311. https://doi.org/10.1111/j.1526-100X.2012.00935.x

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. https://doi.org/10.1080/0028825X.1986.10409726

Wolowski M., Saad C.F., Ashman T., Freitas L. (2013) Predominance of self-compatibility in hummingbird-pollinated plants in the Neotropics. Naturwissenschaften 100: 69–79. https://doi.org/10.1007/s00114-012-0995-0

Zapata T.R., Arroyo M.T.K. (1978) Plant reproductive ecology of a secondary deciduous tropical forest in Venezuela. Biotropica 10: 221–230. https://doi.org/10.2307/2387907

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