Register      Login
Australian Journal of Botany Australian Journal of Botany Society
Southern hemisphere botanical ecosystems
RESEARCH ARTICLE

Generalised pollination system of Erythrina dominguezii (Fabaceae : Papilionoideae) involving hummingbirds, passerines and bees

Ángela V. Etcheverry A C , Dulce Figueroa-Castro B , Trinidad Figueroa-Fleming A , María M. Alemán A , Víctor D. Juárez A , Diego López-Spahr A , Carolina N. Yáñez A and Carlos A. Gómez A
+ Author Affiliations
- Author Affiliations

A Facultad de Ciencias Naturales, Universidad Nacional de Salta, Bolivia 5150, 4400 Salta, Argentina.

B Present address: Escuela de Biología, Benemérita Universidad Autónoma de Puebla; Blvd. Valsequillo y Av. San Claudio, Edif. 112A, Ciudad Universitaria, Col. Jardines de San Manuel, C.P. 72570, Puebla, México.

C Corresponding author. Email: avetcheverry@yahoo.com.ar

Australian Journal of Botany 60(6) 484-494 https://doi.org/10.1071/BT11325
Submitted: 30 December 2011  Accepted: 12 June 2012   Published: 11 September 2012

Abstract

Plants in the genus Erythrina are pollinated by birds, such that passerine pollination is the plesiomorphic state, whereas hummingbird pollination is the derived character. Phylogenetic studies suggest that Erythrina dominguezii belongs to a basal clade characterised as pollinated by both passerines and hummingbirds. Here, we characterise the pollination system of E. dominguezii. Floral morphology, nectar traits, breeding system, visitation rates and pollen deposition by its floral visitors were studied. Floral morphology of E. dominguezii showed traits associated with both passerine and hummingbird pollination. Nectar sugar concentration showed an intermediate value but closer to the hummingbird type; however, it was rich in hexose, which is typical of the passerine type. Approximately 5% of the flowers set fruits under free pollination. Almost 80% of recorded flowers were visited by birds, with the rest visited by hymenopterans (bumblebees and honeybees). Among avian pollinators, five species of hummingbirds and three passerine species were identified as pollinators. The hummingbird Chlorostilbon lucidus was the most efficient visitor in terms of pollen deposition and was second in frequency of visits. The passerine Icterus cayanensis was second in efficiency at depositing pollen and was the most frequent pollinator. Our results show that E. dominguezii has a generalised pollination system. In addition, we report a new case of closed flowers and secondary nectar presentation. This is the first study that compares effectiveness among different pollinators in Erythrina.


References

Baker HG, Baker I (1975) Studies of nectar constitution in pollinator-plant coevolution. In ‘Coevolution of animals and plants’. (Eds LE Gilbert, PH Raven) pp. 100–140. (University of Texas Press: Austin, TX)

Baker I, Baker HG (1982) Some chemical constituents of floral nectars of Erythrina in relation to pollinators and systematics. Allertonia 3, 25–37.

Baker HG, Baker I (1983) Floral nectar sugar constituents in relation to pollinator type. In ‘Handbook of experimental pollination biology’. (Eds CE Jones, RJ Little) pp. 117–141. (Scientific and Academic Editions: New York)

Baker HG, Baker I (1990) The predictive value of nectar chemistry to the recognition of pollination types. Israel Journal of Botany 39, 157–166.

Basso-Alves JP, Agostini K, de Pádua Teixeira S (2011) Pollen and stigma morphology of some Phaseoleae species (Leguminosae) with different pollinators. Plant Biology 13, 602–610.
Pollen and stigma morphology of some Phaseoleae species (Leguminosae) with different pollinators.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC3MngtFyltA%3D%3D&md5=21167eb4b84a1d354dca51c07439ad9eCAS |

Bianchi AR, Yáñez CE (1992) ‘Las precipitaciones del Noroeste Argentino.’ (Instituto Nacional de Tecnología Agropecuaria: Salta, Argentina)

Botes C, Johnson SD, Cowling RM (2009) The birds and the bees: using selective exclusion to identify effective pollinators of African tree aloes. International Journal of Plant Sciences 170, 151–156.
The birds and the bees: using selective exclusion to identify effective pollinators of African tree aloes.Crossref | GoogleScholarGoogle Scholar |

Bruneau A (1997) Evolution and homology of bird pollination syndromes in Erythrina (Leguminosae). American Journal of Botany 84, 54–71.
Evolution and homology of bird pollination syndromes in Erythrina (Leguminosae).Crossref | GoogleScholarGoogle Scholar |

Cabrera AL (1976) ‘Regiones fitogeográficas argentinas.’ (ACME: Buenos Aires)

Costa RACV, Morais ABB (2008) Fenologia e visitantes florais de Erythrina crista-galli L. (Leguminosae: Faboideae) em Santa Maria, Rio Grande do Sul, Brasil. Biotemas 21, 51–56.

Cruden RW (1977) Pollen−ovule ratios: a conservative indicator of breeding systems in flowering plants. Evolution 31, 32–46.
Pollen−ovule ratios: a conservative indicator of breeding systems in flowering plants.Crossref | GoogleScholarGoogle Scholar |

Curti RN, Ortega-Baes P (2011) Relationship between floral traits and floral visitors in two coexisting Tecoma species (Bignoniaceae). Plant Systematics and Evolution 293, 207–211.
Relationship between floral traits and floral visitors in two coexisting Tecoma species (Bignoniaceae).Crossref | GoogleScholarGoogle Scholar |

Dafni A (1992) ‘Pollination ecology: a practical approach.’ (Oxford University Press: Oxford, UK)

Doyle JJ, Doyle JL (1993) Chloroplast DNA phylogeny of the papilionoid legume tribe Phaseoleae. Systematic Botany 18, 309–327.
Chloroplast DNA phylogeny of the papilionoid legume tribe Phaseoleae.Crossref | GoogleScholarGoogle Scholar |

Etcheverry AV (2001) Role of staminal growth in delayed self-pollination of Crotalaria stipularia (Fabaceae: Papilionoideae). Beiträge zur Biologie der Pflanzen 72, 215–228.

Etcheverry AV, Alemán CET (2005) Reproductive biology of Erythrina falcata. Biotropica 37, 54–63.
Reproductive biology of Erythrina falcata.Crossref | GoogleScholarGoogle Scholar |

Etcheverry AV, Pérez de Bianchi SM, Martín Montiel de López D (2001) Reproductive biology in the amphicarpic legume Macroptilium panduratum (Fabaceae, Papilionoideae). Beiträge zur Biologie der Pflanzen 72, 181–197.

Etcheverry AV, Protomastro JJ, Westerkamp C (2003) Delayed autonomous self-pollination in the colonizer Crotalaria micans (Fabaceae: Papilionoideae): structural and functional aspects. Plant Systematics and Evolution 239, 15–28.
Delayed autonomous self-pollination in the colonizer Crotalaria micans (Fabaceae: Papilionoideae): structural and functional aspects.Crossref | GoogleScholarGoogle Scholar |

Etcheverry AV, Alemán MM, Figueroa Fleming T (2008) Flower morphology, pollination biology and mating system of the complex flower of Vigna caracalla (Fabaceae: Papilionoideae). Annals of Botany 102, 305–316.
Flower morphology, pollination biology and mating system of the complex flower of Vigna caracalla (Fabaceae: Papilionoideae).Crossref | GoogleScholarGoogle Scholar |

Faegri K, van der Pijl L (1979) ‘The principles of pollination ecology.’ (Pergamon Press: Oxford, UK)

Feinsinger P, Linhart YB, Swarm LA, Wolfe JA (1979) Aspects of the pollination biology of three Erythrina species on Trinidad and Tobago. Annals of the Missouri Botanical Garden 66, 451–471.
Aspects of the pollination biology of three Erythrina species on Trinidad and Tobago.Crossref | GoogleScholarGoogle Scholar |

Fumero-Cabán JJ, Meléndez-Ackerman EJ (2007) Relative pollination effectiveness of floral visitors of Pitcairnia angustifolia (Bromeliaceae). American Journal of Botany 94, 419–424.
Relative pollination effectiveness of floral visitors of Pitcairnia angustifolia (Bromeliaceae).Crossref | GoogleScholarGoogle Scholar |

Galetto L, Bernardello G, Isele IC, Vesprini J, Speroni G, Berduc A (2000) Reproductive biology of Erythrina crista-galli (Fabaceae). Annals of the Missouri Botanical Garden 87, 127–145.
Reproductive biology of Erythrina crista-galli (Fabaceae).Crossref | GoogleScholarGoogle Scholar |

Gallardo R, Dominguez E, Munoz JM (1993) The heterochronic origin of the cleistogamous flower in Astragalus cymbicarpos (Fabaceae). American Journal of Botany 80, 814–823.
The heterochronic origin of the cleistogamous flower in Astragalus cymbicarpos (Fabaceae).Crossref | GoogleScholarGoogle Scholar |

Genise J, Palacios RA, Hoc PS, Carrizo R, Moffat L, Mom MP, Agulló MA, Picca P, Torregrosa S (1990) Observaciones sobre la biología floral de Prosopis (Leguminosae, Mimosoideae). II: Fases florales y visitantes en el distrito chaqueño serrano. Darwiniana 32, 27–39.

Gómez JM (2004) Generalización en las interacciones entre plantas y polinizadores. Revista Chilena de Historia Natural (Valparaiso, Chile) 75, 105–116.

Gómez JM, Zamora R (1999) Generalization vs. specialization in the pollination system of Hormathophylla spinosa (Cruciferae). Ecology 80, 796–805.

Harder LD, Barrett SCH (1996) Pollen dispersal and mating patterns in animal pollinated plants. In ‘Floral biology: studies on floral evolution in animal-pollinated plants’. (Eds DG Lloyd, SCH Barrett) pp. 140–190. (Chapman and Hall: New York)

Hemsley AJ, Ferguson IK (1985) Pollen morphology of the genus Erythrina (Leguminosae: Papilionoideae) in relation to floral structure and pollinators. Annals of the Missouri Botanical Garden 72, 570–590.
Pollen morphology of the genus Erythrina (Leguminosae: Papilionoideae) in relation to floral structure and pollinators.Crossref | GoogleScholarGoogle Scholar |

Herrera CM (1996) Floral traits and plant adaptation to insect pollinators: a devil’s advocate approach. In ‘Floral biology: studies on floral evolution in animal-pollinated plants’. (Eds DG Lloyd, SCH Barrett) pp. 65–87. (Chapman and Hall: New York)

Herrera J (1987) Flower and fruit biology in Southern Spanish Mediterranean shrublands. Annals of the Missouri Botanical Garden 74, 69–78.
Flower and fruit biology in Southern Spanish Mediterranean shrublands.Crossref | GoogleScholarGoogle Scholar |

Herrera J (1988) Datos sobre biología floral en la flora de Andalucía Oriental. Lagascalia 15, 607–614.

Herrera J (1989) Aminoácidos en el néctar de plantas del sur de España. Anales del Jardin Botanico de Madrid 45, 475–482.

Heslop-Harrison Y, Shivanna KR (1977) The receptive surface of the angiosperm stigma. Annals of Botany 41, 1233–1258.

InfoStat (2009) ‘InfoStat version 2009.’ (Grupo InfoStat, FCA, Universidad Nacional de Córdoba, Argentina)

Ivey CT, Martinez P, Wyatt R (2003) Variation in pollinator effectiveness in swamp milkweed, Asclepia incarnata (Apocynaceae). American Journal of Botany 90, 214–225.
Variation in pollinator effectiveness in swamp milkweed, Asclepia incarnata (Apocynaceae).Crossref | GoogleScholarGoogle Scholar |

Jackson S, Nicolson SW, van Wyk BE (1998) Apparent absorption efficiencies of nectar sugars in the Cape sugarbird, with a comparison of methods. Physiological Zoology 71, 106–115.
Apparent absorption efficiencies of nectar sugars in the Cape sugarbird, with a comparison of methods.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXpt1yrtQ%3D%3D&md5=cefcd51319b9fcb46e85eb458c9b6932CAS |

Johnson SD, Nicolson SW (2008) Evolutionary associations between nectar properties and specificity in bird pollination systems. Biology Letters 4, 49–52.
Evolutionary associations between nectar properties and specificity in bird pollination systems.Crossref | GoogleScholarGoogle Scholar |

Kearns CA, Inouye DW (1993) ‘Techniques for pollination biologists.’ (University Press of Colorado: Niwot, CO)

Krukoff BA, Barneby RC (1974) Conspectus of species of the genus Erythrina. Lloydia 37, 332–459.

Larson BMH, Barrett SCH (1999) The ecology of pollen limitation in buzz-pollinated Rhexia virginica (Melastomataceae). Journal of Ecology 87, 371–381.
The ecology of pollen limitation in buzz-pollinated Rhexia virginica (Melastomataceae).Crossref | GoogleScholarGoogle Scholar |

Legname PR (1982) Árboles indígenas del Noroeste Argentino. Opera Lilloana 14, 1–136.

Lloyd DG, Schoen DJ (1992) Self- and cross-fertilization in plants. I. Functional dimensions. International Journal of Plant Sciences 153, 358–369.
Self- and cross-fertilization in plants. I. Functional dimensions.Crossref | GoogleScholarGoogle Scholar |

Lotz CN, Nicolson SW (1996) Sugar preferences of a nectarivorous passerine bird, the Lesser Double-Collared Sunbird (Nectarinia chalybea). Functional Ecology 10, 360–365.
Sugar preferences of a nectarivorous passerine bird, the Lesser Double-Collared Sunbird (Nectarinia chalybea).Crossref | GoogleScholarGoogle Scholar |

Mayfield MM, Waser NM, Price MV (2001) Exploring the ‘most effective pollinator principle’ with complex flowers: bumblebees and Ipomopsis aggregata. Annals of Botany 88, 591–596.
Exploring the ‘most effective pollinator principle’ with complex flowers: bumblebees and Ipomopsis aggregata.Crossref | GoogleScholarGoogle Scholar |

Morton ES (1979) Effective pollination of Erythrina fusca by the orchard oriole (I. spurius): coevolved behavioral manipulation? Annals of the Missouri Botanical Garden 66, 482–489.
Effective pollination of Erythrina fusca by the orchard oriole (I. spurius): coevolved behavioral manipulation?Crossref | GoogleScholarGoogle Scholar |

Munsell Color Charts (1977) ‘Charts for plant tissues.’ (Macbeth Division of Killmorgen Instruments Corporation: New York)

Narosky T, Yzurieta D (2003) ‘Aves de Argentina y Uruguay: guía para la identificación.’ (L.O.L.A. editores: Buenos Aires)

Neill DA (1987) Trapliners in the trees: hummingbird pollination of Erythrina sect. Erythrina (Leguminosae: Papilionoideae). Annals of the Missouri Botanical Garden 74, 27–41.
Trapliners in the trees: hummingbird pollination of Erythrina sect. Erythrina (Leguminosae: Papilionoideae).Crossref | GoogleScholarGoogle Scholar |

Neill DA (1988) Experimental studies on species relationships in Erythrina (Leguminosae: Papilionoideae). Annals of the Missouri Botanical Garden 75, 886–969.
Experimental studies on species relationships in Erythrina (Leguminosae: Papilionoideae).Crossref | GoogleScholarGoogle Scholar |

Ollerton J, Killick A, Lamborn E, Watts S, Whiston M (2007) Multiple meanings and modes: on the many ways to a generalist flower. Taxon 56, 717–728.
Multiple meanings and modes: on the many ways to a generalist flower.Crossref | GoogleScholarGoogle Scholar |

Ollerton J, Alarcón R, Waser NM, Price MV, Watts S, Cranmer L, Hingston A, Peter CI, Rotenberry J (2009) A global test of the pollination syndrome hypothesis. Annals of Botany 103, 1471–1480.
A global test of the pollination syndrome hypothesis.Crossref | GoogleScholarGoogle Scholar |

Pacini E, Nepi M, Vesprini JL (2003) Nectar biodiversity: a short review. Plant Systematics and Evolution 238, 7–21.

Ragusa-Netto J (2002) Exploitation of Erytrina dominguezii Hassl. (Fabaceae) nectar by perching birds in a dry forest in western Brazil. Brazilian Journal of Biology 62, 877–883.
Exploitation of Erytrina dominguezii Hassl. (Fabaceae) nectar by perching birds in a dry forest in western Brazil.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD3s7ksVaqsA%3D%3D&md5=38130a7e56206ff1e1d728c6e96c642aCAS |

Rangaiah K, Solomon Raju AJ, Rao SP (2004) Passerine bird-pollination in the Indian coral tree, Erythrina variegata var. orientalis (Fabaceae). Current Science 87, 736–739.

Raven PH (1974) Erythrina (Fabaceae): achievements and opportunities. Lloydia 37, 321–331.

Rocca MA, Sazima M (2010) Beyond hummingbird-flowers: the other side of ornitophily in the Neotropics. Oecologia Australis 14, 67–99.
Beyond hummingbird-flowers: the other side of ornitophily in the Neotropics.Crossref | GoogleScholarGoogle Scholar |

Sazima I, Sazima C, Sazima M (2009) A catch-all leguminous tree: Erythrina velutina visited and pollinated by vertebrates at an oceanic island. Australian Journal of Botany 57, 26–30.
A catch-all leguminous tree: Erythrina velutina visited and pollinated by vertebrates at an oceanic island.Crossref | GoogleScholarGoogle Scholar |

Schmid S, Schmid VS, Zillikens A, Harter-Marques B, Steiner J (2011) Bimodal pollination system of the bromeliad Aechmea nudicaulis involving hummingbirds and bees. Plant Biology 13, 41–50.
Bimodal pollination system of the bromeliad Aechmea nudicaulis involving hummingbirds and bees.Crossref | GoogleScholarGoogle Scholar |

Schondube JE, Martínez del Rio C (2003) Concentration dependent sugar preferences in nectar-feeding birds: mechanisms and consequences. Functional Ecology 17, 445–453.
Concentration dependent sugar preferences in nectar-feeding birds: mechanisms and consequences.Crossref | GoogleScholarGoogle Scholar |

Sokal RR, Rohlf FJ (1995) ‘Biometry.’ (Freeman: New York)

Stone JL (1996) Components of pollination effectiveness in Psychotria suerrensis, a tropical distylous shrub. Oecologia 107, 504–512.
Components of pollination effectiveness in Psychotria suerrensis, a tropical distylous shrub.Crossref | GoogleScholarGoogle Scholar |

Thomson JD, Goodell K (2001) Pollen removal and deposition by honeybee and bumblebee visitors to apple and almond flowers. Journal of Applied Ecology 38, 1032–1044.
Pollen removal and deposition by honeybee and bumblebee visitors to apple and almond flowers.Crossref | GoogleScholarGoogle Scholar |

Thomson JD, Wilson P, Valenzuela M, Malzone M (2000) Pollen presentation and pollination syndromes with special reference to Penstemon. Plant Species Biology 15, 11–29.
Pollen presentation and pollination syndromes with special reference to Penstemon.Crossref | GoogleScholarGoogle Scholar |

Toledo VM, Hernández HM (1979) Erythrina oliviae: a new case of oriole pollination in Mexico. Annals of the Missouri Botanical Garden 66, 503–511.
Erythrina oliviae: a new case of oriole pollination in Mexico.Crossref | GoogleScholarGoogle Scholar |

Tucker S (1987) Pseudoracemes in papilionoid legumes: their nature, development, and variation. Botanical Journal of the Linnean Society 95, 181–206.
Pseudoracemes in papilionoid legumes: their nature, development, and variation.Crossref | GoogleScholarGoogle Scholar |

Waser NM, Chittka L, Price MV, Williams NM, Ollerton J (1996) Generalization of pollination systems, and why it matters. Ecology 77, 1043–1060.
Generalization of pollination systems, and why it matters.Crossref | GoogleScholarGoogle Scholar |

Wilson P, Thomson JD (1991) Heterogeneity among floral visitors leads to discordance between removal and deposition of pollen. Ecology 72, 1503–1507.
Heterogeneity among floral visitors leads to discordance between removal and deposition of pollen.Crossref | GoogleScholarGoogle Scholar |

Wilson P, Castellanos MC, Wolfe AD, Thomson JD (2006) Shifts between bee and bird pollination in Penstemon. In ‘Plant−pollinator interactions: from specialization to generalization’. (Eds NM Waser, J Ollerton) pp. 47–68. (University of Chicago Press: Chicago)