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

Reproductive biology of duodichogamous Koelreuteria elegans (Sapindaceae): the rare case of a female–male–female flowering sequence

Adan Alberto Avalos A D E , Elsa Clorinda Lattar A B , María Silvia Ferrucci A D and Juan Pablo Torretta C D
+ Author Affiliations
- Author Affiliations

A Instituto de Botánica del Nordeste, IBONE-UNNE-CONICET, Corrientes, Argentina.

B Cátedra de Morfología de Plantas Vasculares. Facultad de Ciencias Agrarias, FCA-UNNE, Corrientes, Argentina.

C Universidad de Buenos Aires, Facultad de Agronomía, Cátedra de Botánica General, Av. San Martín 4453, C1417DSE, Buenos Aires, Argentina.

D Consejo Nacional de Investigaciones Científicas y Técnicas, Argentina.

E Corresponding author. Email: adanalbertoavalos@gmail.com

Australian Journal of Botany 67(2) 149-158 https://doi.org/10.1071/BT18159
Submitted: 15 August 2018  Accepted: 18 March 2019   Published: 3 May 2019

Abstract

Monoecious species are common within Sapindaceae, and among them a large variation in sexual expression has been reported. In this work we evaluate the sexual expression, phenology, floral biology, and mating system in eight to sixteen individuals of the duodichogamous Koelreuteria elegans (Seem.) A.C. Sm. subsp. formosana (Hayata) F.G. Mey. Results from our study show that all individuals exhibited a pattern of flowering characterised by two cycles of pistillate flowers with an intervening one of staminate flowers. The synflorescences presented a high synchronisation between the male and female phases at the individual level. Therefore, very little functional overlap was observed between pollen receipt and pollen dispatch within individuals. Pollination was by bees, and the manual pollination experiments showed that this species is a xenogamous although self-compatible species. Nevertheless, seed set increased significantly with hand cross-pollination and open pollination experiments. Decrease of fruits and seeds set by geitonogamy could favour the establishment of duodichogamy with interfloral protogyny promoting cross-pollination. In the family this is the first report of a pattern of flowering in which there are two cycles of female with an intervening cycle of male flowers. The importance of detailed these studies for understanding mechanisms underlying duodichogamy was demonstrated, and findings will help to broaden our understanding about this rare sexual system to generalise the specific ecological factors that explain its evolutionary meaning.

Additional keywords: cross-pollination, duodichogamy, Koelreuterieae, self-compatibility.


References

Acevedo-Rodríguez P (1993) Systematics of Serjania (Sapindaceae). Part I: A revision of Serjania sect. Platycoccus. Memoirs of the New York Botanical Garden 67, 1–93.

Acevedo-Rodríguez P (2003) Melicocceae (Sapindaceae): Melicoccus and Talisia. In ‘Flora Neotropica Monograph’. pp. 1–179. (New York Botanical Garden: New York, USA)

Acevedo-Rodríguez P, van Welzen PC, Adema F, van der Ham RWJM (2011) Sapindaceae. In ‘The families and genera of vascular plants. Eudicots: Sapindales, Cucurbitales, Myrtaceae’. (Ed. K Kubitzki) pp. 357–407. (Springer-Verlag: Berlin)

Acevedo-Rodríguez P, Wurdack KJ, Ferrucci MS, Johnson G, Pedro Dias P, Coelho RG, Somner GV, Steinmann VW, Zimmer EA, Strong MT (2017) Generic relationships and classification of tribe Paullinieae (Sapindaceae) with a new concept of supertribe Paulliniodae. Systematic Botany 42, 96–114.
Generic relationships and classification of tribe Paullinieae (Sapindaceae) with a new concept of supertribe Paulliniodae.Crossref | GoogleScholarGoogle Scholar |

Aluri JSR, Subba Reddi C, Rama Das K (1998) Temporal dioecism and pollination by wasps and bees in Allophylus serratus (Roxb.) Radlk. (Sapindaceae). Plant Species Biology 13, 1–5.
Temporal dioecism and pollination by wasps and bees in Allophylus serratus (Roxb.) Radlk. (Sapindaceae).Crossref | GoogleScholarGoogle Scholar |

Ashman T-L, Knight TM, Steets JA, Amarasekare P, Burd M, Campbell DR, Dudash MR, Johnston MO, Mazer SJ, Mitchell RJ, Morgan MT, Wilson WG (2004) Pollen limitation of plant reproduction: ecological and evolutionary causes and consequences. Ecology 85, 2408–2421.
Pollen limitation of plant reproduction: ecological and evolutionary causes and consequences.Crossref | GoogleScholarGoogle Scholar |

Avalos AA, Lattar EC, Galati BG, Ferrucci MS (2017) Nectary structure and ultrastructure in two floral morphs of Koelreuteria elegans subsp. formosana (Sapindaceae). Flora 226, 29–37.
Nectary structure and ultrastructure in two floral morphs of Koelreuteria elegans subsp. formosana (Sapindaceae).Crossref | GoogleScholarGoogle Scholar |

Bassani M, Pacini E, Franchi GG (1994) Humidity stress responses in pollen of anemophilous and entomophilous species. Grana 33, 146–150.
Humidity stress responses in pollen of anemophilous and entomophilous species.Crossref | GoogleScholarGoogle Scholar |

Bawa KS (1977) The reproductive biology of Cupania guatemalensis Radlk. (Sapindaceae). Evolution 31, 52–63.
The reproductive biology of Cupania guatemalensis Radlk. (Sapindaceae).Crossref | GoogleScholarGoogle Scholar | 28567724PubMed |

Bennett AW (1870) Observations on protandry and protogyny in British plants. Le Journal de Botanique 8, 315–321.

Bertin RI (1993) Incidence of monoecy and dichogamy in relation to self-fertilization in angiosperms. American Journal of Botany 80, 557–560.
Incidence of monoecy and dichogamy in relation to self-fertilization in angiosperms.Crossref | GoogleScholarGoogle Scholar | 30139145PubMed |

Bertin RI, Newman CM (1993) Dichogamy in angiosperms. Botanical Review 59, 112–152.
Dichogamy in angiosperms.Crossref | GoogleScholarGoogle Scholar |

Bierzychudek P (1981) Pollinator limitation of plant reproductive effort. American Naturalist 117, 838–840.
Pollinator limitation of plant reproductive effort.Crossref | GoogleScholarGoogle Scholar |

Cane JH (1987) Estimation of bee size using intertegular span (Apoidea). Journal of the Kansas Entomological Society 60, 145–147.

Centibas A, Unal M (2014) An overview of dichogamy in angiosperms. Research in Plant Biology 4, 9–27.

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

Darwin C (1876) ‘The effects of cross and self-fertilisation in the vegetable kingdom.’ (John Murray: London)

de Jong  PC 1976 Flowering and sex expression in Acer L.: a biosystematic study.Mededelingen Landbouwhogeschool Wageningen 72 1201

de Jong TJ, Waser NM, Klinkhamer PGL (1993) Geitonogamy: the neglected side of selfing. Trends in Ecology & Evolution 8, 321–325.
Geitonogamy: the neglected side of selfing.Crossref | GoogleScholarGoogle Scholar |

de Lima HA, Somner GV, Giulietti AM (2016) Duodichogamy and sex lability in Sapindaceae: the case of Paullinia weinmanniifolia. Plant Systematics and Evolution 302, 109–120.
Duodichogamy and sex lability in Sapindaceae: the case of Paullinia weinmanniifolia.Crossref | GoogleScholarGoogle Scholar |

Delpino F (1874) Ulteriori osservazioni e considerazioni sulla dicogamia nel regno vegetale. Appendice. Dimorfismo nel noce (Juglans regia) e pleiontismo nelle piante. Atti della Sociedade Italiana di Scienze Naturali 17, 402–407.

Endress PK, Lorence DH (2004) Heterodichogamy of a novel type in Hernandia (Hernandiaceae) and its structural basis. International Journal of Plant Sciences 165, 753–763.
Heterodichogamy of a novel type in Hernandia (Hernandiaceae) and its structural basis.Crossref | GoogleScholarGoogle Scholar |

Escobar JR, Correa MPF, Aguilera FJP (1984) Estruturas florais, floração e técnicas para a polinização controlada do guaranazeiro. Pesquisa Agropecuária Brasileira 19, 615–622.

Finer MS, Morgan MT (2003) Effects of natural rates of geitonogamy on fruit set in Asclepias speciosa (Apocynaceae): evidence favoring the plant’s dilemma. American Journal of Botany 90, 1746–1750.
Effects of natural rates of geitonogamy on fruit set in Asclepias speciosa (Apocynaceae): evidence favoring the plant’s dilemma.Crossref | GoogleScholarGoogle Scholar | 21653351PubMed |

Galen C, Gregory T, Galloway LF (1989) Costs of self-pollination in a self-incompatible plant, Polemonium viscosum. American Journal of Botany 76, 1675–1680.
Costs of self-pollination in a self-incompatible plant, Polemonium viscosum.Crossref | GoogleScholarGoogle Scholar |

Gleeson SK (1982) Heterodichogamy in walnuts: inheritance and stable ratios. Evolution 36, 892–902.
Heterodichogamy in walnuts: inheritance and stable ratios.Crossref | GoogleScholarGoogle Scholar | 28567826PubMed |

González VV, Solís SM, Ferrucci MS (2014) Anatomía reproductiva en flores estaminadas y pistiladas de Allophylus edulis (Sapindaceae). Boletín de la Sociedad Argentina de Botánica 49, 207–216.

González VV, Solís SM, Ferrucci MS (2017) Embryological studies of Magonia pubescens (Dodonaeaeae, Sapindaceae): development of male and female gametophytes in both floral morphs and its phylogenetic implications. Australian Systematic Botany 30, 279–289.
Embryological studies of Magonia pubescens (Dodonaeaeae, Sapindaceae): development of male and female gametophytes in both floral morphs and its phylogenetic implications.Crossref | GoogleScholarGoogle Scholar |

Harder LD, Barrett SCH (1995) Mating cost of large floral displays in hermaphrodite plants. Nature 373, 512–515.
Mating cost of large floral displays in hermaphrodite plants.Crossref | GoogleScholarGoogle Scholar |

Harder LD, Wilson WG (1998) A clarification of pollen discounting and its joint effects with inbreeding depression on mating system evolution. American Naturalist 152, 684–695.
A clarification of pollen discounting and its joint effects with inbreeding depression on mating system evolution.Crossref | GoogleScholarGoogle Scholar | 18811343PubMed |

Holsinger KE, Thomson JD (1994) Pollen discounting in Erythronium grandiflorum: mass-action estimates from pollen transfer dynamics. American Naturalist 144, 799–812.
Pollen discounting in Erythronium grandiflorum: mass-action estimates from pollen transfer dynamics.Crossref | GoogleScholarGoogle Scholar |

Ishida K, Yoshimaru H, Itô H (2003) Effects of geitonogamy on the seed set of Magnolia obovata Thunb. (Magnoliaceae). International Journal of Plant Sciences 164, 729–735.
Effects of geitonogamy on the seed set of Magnolia obovata Thunb. (Magnoliaceae).Crossref | GoogleScholarGoogle Scholar |

Jaynes RA (1975) Chestnuts. In ‘Advances in fruit breeding’. (Eds J Janick, JN Moore) pp. 490–503. (Purdue University Press: West Lafayette, IN, USA)

Kay QON (1987) The comparative ecology of flowering. New Phytologist 106, 265–281.
The comparative ecology of flowering.Crossref | GoogleScholarGoogle Scholar |

Klinkhamer GL, de Jong TJ (1993) Attractiveness to pollinators: a plant’s dilemma. Oikos 66, 180–184.
Attractiveness to pollinators: a plant’s dilemma.Crossref | GoogleScholarGoogle Scholar |

Knight TM, Steets JA, Vamosi JC, Mazer SJ, Burd M, Campbell DR, Dudash MR, Johnston MO, Mitchell RJ, Ashman T-L (2005) Pollen limitation of plant reproduction: pattern and process. Annual Review of Ecology Evolution and Systematics 36, 467–497.
Pollen limitation of plant reproduction: pattern and process.Crossref | GoogleScholarGoogle Scholar |

Knuth P (1906) ‘Handbook of flower pollination. Vol. 1.’ (Clarendon Press: Oxford, UK)

Knuth P (1909) ‘Handbook of flower pollination. Vol. 3.’ (Clarendon Press: Oxford, UK)

Lansac AR, Sullivan CY, Johnson BE, Lee KW (1994) Viability and germination of the pollen of sorghum (Sorghum bicolor (L.) Moench). Annals of Botany 74, 27–33.
Viability and germination of the pollen of sorghum (Sorghum bicolor (L.) Moench).Crossref | GoogleScholarGoogle Scholar | 19700459PubMed |

Lee H, Kang H, Park WG (2018) A rare duodichogamous flowering system in monoecious Toona sinensis (Meliaceae). Journal of Ecology and Environment 42, 7
A rare duodichogamous flowering system in monoecious Toona sinensis (Meliaceae).Crossref | GoogleScholarGoogle Scholar |

Li Y, Luo S, Zhang D (2014) Fly pollination and duodichogamy in Bridelia stipularis and Cleistanthus sumatranus (Phyllanthaceae). Plant Species Biology 29, E85–E92.
Fly pollination and duodichogamy in Bridelia stipularis and Cleistanthus sumatranus (Phyllanthaceae).Crossref | GoogleScholarGoogle Scholar |

Lloyd DG (1992) Self- and cross-fertilization in plants. I. The selection of self-fertilization. International Journal of Plant Sciences 153, 370–380.
Self- and cross-fertilization in plants. I. The selection of self-fertilization.Crossref | GoogleScholarGoogle Scholar |

Lloyd DG, Webb CJ (1986) The avoidance of interference between the presentation of pollen and stigmas in angiosperms. I. Dichogamy. New Zealand Journal of Botany 24, 135–162.
The avoidance of interference between the presentation of pollen and stigmas in angiosperms. I. Dichogamy.Crossref | GoogleScholarGoogle Scholar |

Luo SX, Zhang DX, Renner SS (2007) Duodichogamy and androdioecy in the Chinese Phyllanthaceae Bridelia tomentosa. American Journal of Botany 94, 260–265.
Duodichogamy and androdioecy in the Chinese Phyllanthaceae Bridelia tomentosa.Crossref | GoogleScholarGoogle Scholar |

Moreira Filho A, Ribeiro OC, Ferreira MA, Martins GA (1975) Polinização e polinizadores de guaraná Inf. Téc. ACAR-AM 3, 4–7.

Muller H (1883) ‘The fertilization of flowers.’ (MacMillan: London)

Opler PA, Bawa KS (1978) Sex ratios in tropical forest trees. Evolution 32, 812–821.
Sex ratios in tropical forest trees.Crossref | GoogleScholarGoogle Scholar | 28567933PubMed |

Pacini E, Franchi GG, Lisci M, Nepi M (1997) Pollen viability related to type of pollination in six angiosperm species. Annals of Botany 80, 83–87.
Pollen viability related to type of pollination in six angiosperm species.Crossref | GoogleScholarGoogle Scholar |

Paula NMC (1989) Aspectos da biología reprodutiva de Paullinia rugosa Benth. ex Radlk. (Sapindaceae). Dissertation, Instituto Nacional de Pesquisa da Amazônia (INPA) e Fundação Universidade do Amazonas.

Pellmyr O (1987) Multiple sex expressions in Cimicifuga simplex: dichogamy destabilizes hermaphroditism. Biological Journal of the Linnean Society. Linnean Society of London 31, 161–174.
Multiple sex expressions in Cimicifuga simplex: dichogamy destabilizes hermaphroditism.Crossref | GoogleScholarGoogle Scholar |

R Core Team (2011) ‘R: A language and environment for statistical computing.’ (R Foundation for Statistical Computing: Vienna, Austria) Available at: http://www.r-project.org (accessed 31 January 2011)

Radford AE, Dickison WC, Massey JR, Bell CR (1974) ‘Vascular plant systematics.’ (Harper & Row Publishers: New York)

Renner SS (2001) Heterodichogamy, how common is it? Trends in Ecology & Evolution 16, 595–597.
Heterodichogamy, how common is it?Crossref | GoogleScholarGoogle Scholar |

Renner SS (2014) The relative and absolute frequencies of angiosperm sexual systems: dioecy, monoecy, gynodioecy, and an updated online database. American Journal of Botany 101, 1588–1596.
The relative and absolute frequencies of angiosperm sexual systems: dioecy, monoecy, gynodioecy, and an updated online database.Crossref | GoogleScholarGoogle Scholar | 25326608PubMed |

Robbertse PJ, Du Toit ES, Cloete MO (2011) Gender expression and inflorescence structure of Pappea capensis Eckl. and Zeyh. (Sapindaceae). South African Journal of Botany 77, 425–429.
Gender expression and inflorescence structure of Pappea capensis Eckl. and Zeyh. (Sapindaceae).Crossref | GoogleScholarGoogle Scholar |

Schlessman MA (1982) Expression of andromonoecy and pollination of Tuberous lomatiums (Umbelliferae). Systematic Botany 7, 134–149.
Expression of andromonoecy and pollination of Tuberous lomatiums (Umbelliferae).Crossref | GoogleScholarGoogle Scholar |

Solís SM, Galati B, Ferrucci MS (2010) Microsporogenesis and microgametogenesis of Cardiospermum grandiflorum and Urvillea chacoensis (Sapindaceae, Paullinieae). Australian Journal of Botany 58, 597–604.
Microsporogenesis and microgametogenesis of Cardiospermum grandiflorum and Urvillea chacoensis (Sapindaceae, Paullinieae).Crossref | GoogleScholarGoogle Scholar |

Stout AB (1928) Dichogamy in flowering plants. Bulletin of the Torrey Botanical Club 55, 141–153.
Dichogamy in flowering plants.Crossref | GoogleScholarGoogle Scholar |

Subba Reddi C, Reddi EUB, Reddi NS, Reddi PS (1983) Reproductive ecology of Sapindus emarginatus Vahl (Sapindaceae). Proceedings of the Indian National Science Academy 49B, 57–72.

van der Ham RWJM (1990) Nephelieae pollen (Sapindaceae): form, function, and evolution. Leiden Botanical Series 13, 1–255.

van Welzen PC (1989) ‘Guioa Cav. (Sapindaceae): taxonomy, phylogeny, and historical biogeography.’ (Leiden Botanical Series Press: Leiden, The Netherlands)

Waser NM, Price MV (1991) Reproductive costs of self-pollination in Ipomopsis aggregata (Polemoniaceae): are ovules usurped? American Journal of Botany 78, 1036–1043.
Reproductive costs of self-pollination in Ipomopsis aggregata (Polemoniaceae): are ovules usurped?Crossref | GoogleScholarGoogle Scholar |

Webb CJ, Lloyd DG (1986) The avoidance of interference between the presentation of pollen and stigmas in angiosperms. II. Herkogamy. New Zealand Journal of Botany 24, 163–178.
The avoidance of interference between the presentation of pollen and stigmas in angiosperms. II. Herkogamy.Crossref | GoogleScholarGoogle Scholar |

Wyatt R (1980) The reproductive biology of Asclepias tuberosa: I. Flower number, arrangement, and fruit set. New Phytologist 85, 119–131.
The reproductive biology of Asclepias tuberosa: I. Flower number, arrangement, and fruit set.Crossref | GoogleScholarGoogle Scholar |

Zapata TR, Arroyo MTK (1978) Plant reproductive ecology of a secondary deciduous tropical forest in Venezuela. Biotropica 10, 221–230.
Plant reproductive ecology of a secondary deciduous tropical forest in Venezuela.Crossref | GoogleScholarGoogle Scholar |

Zini ML, Galati GB, Solís SM, Ferrucci MS (2012) Anther structure and pollen development in Melicoccus lepidopetalus (Sapindaceae): an evolutionary approach to dioecyin the family. Flora 207, 712–720.
Anther structure and pollen development in Melicoccus lepidopetalus (Sapindaceae): an evolutionary approach to dioecyin the family.Crossref | GoogleScholarGoogle Scholar |