Plant Ecology and Evolution 153(3): 361-372, doi: 10.5091/plecevo.2020.1757
Cordia subcordata (Boraginaceae), a distylous species on oceanic coral islands, is self-compatible and pollinated by a passerine bird
expand article infoXiangping Wang‡, Meihong Wen‡, Mingsong Wu‡, Dianxiang Zhang§
‡ Key Laboratory of Plant Resources Conservation and Sustainable Utilization, South China Botanical Garden, Chinese Academy of Sciences, Guangzhou 510650, Guangdong, China§ South China Botanical Garden, Guandong, China

Corresponding author: Dianxiang Zhang ( dx-zhang@scbg.ac.cn )

© Xiangping Wang, Meihong Wen, Mingsong Wu, Dianxiang Zhang.
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: Wang X, Wen M, Wu M, Zhang D (2020) Cordia subcordata (Boraginaceae), a distylous species on oceanic coral islands, is self-compatible and pollinated by a passerine bird. Plant Ecology and Evolution 153(3): 361-372. https://doi.org/10.5091/plecevo.2020.1757
Open Access
Abstract

Background and aims – Distyly is usually rare on oceanic islands, which is probably due to the difficulty for distylous plants to colonize those islands. However, Cordia subcordata was observed to be distylous with short- and long-styled morphs on the Xisha Islands in the South China Sea. To characterize the reproduction system of Cordia subcordata and to understand how this distylous species maintains itself on these islands, we studied its reproductive and pollination biology.

Methods – Seed set and pollen tube growth under manipulated intermorph, intramorph, and self-pollination were examined to investigate self-incompatibility in the species. The number of pollen grains deposited on the stigmas after a single pollinator visit were counted to investigate the pollination efficiency of different visitors.

Key results – Our study indicated that Cordia subcordata shows reciprocal herkogamy as is typical in distylous species. Pollen tubes could reach the base of the style and move into the ovules under all the manipulated pollination treatments in both morphs. Seed set resulting from four hand-pollination experiments did not show any differences between both morphs, suggesting that Cordia subcordata lacks heterostylous self-incompatibility. The most frequent flower visitors, Zosterops japonicus and Apis cerana, were observed foraging on the large volumes of nectar and pollen grains, respectively, with Zosterops japonicus being the most effective pollinator, depositing large number of pollen grains on the stigmas during their visits.

Conclusions – Our findings show that Cordia subcordata established itself and persists in the archipelago by producing fruits through a combination of self-compatibility and pollination by the most common passerine bird on the oceanic islands.

Keywords
Cordia subcordata, distyly, heterostylous self-incompatibility, oceanic island, passerine pollination

References

  • Barrett S.C.H. (2002) Evolution of sex: the evolution of plant sexual diversity. Nature Reviews Genetics 3: 274–284. https://doi.org/10.1038/nrg776
  • Barrett S.C.H., Cruzan M.B. (1994) Incompatibility in heterostylous plants. In: Williams E.G., Clarke A.E., Knox R.B. (eds) Genetic control of self-incompatibility and reproductive development in flowering plants: 189–219. Dordrecht, Springer. https://doi.org/10.1007/978-94-017-1669-7_10
  • Barrett S.C.H. (1996) The reproductive biology and genetics of island plants. Philosophical Transactions of the Royal Society of London Series B: Biological Sciences 351: 725–733. https://doi.org/10.1098/rstb.1996.0067
  • Bramow C., Hartvig I., Larsen S.B., Philipp M. (2013) How a heterostylous plant species responds to life on remote islands: a comparative study of the morphology and reproductive biology of Waltheria ovata on the coasts of Ecuador and the Galápagos Islands. Evolutionary Ecology 27: 83–100. https://doi.org/10.1007/s10682-012-9588-9
  • Canché-Collí C., Canto A. (2014) Distylous traits in Cordia dodecandra and Cordia sebestena (Boraginaceae) from the Yucatan Peninsula. Botanical Sciences 92(2): 289–297. https://doi.org/10.17129/botsci.97
  • Crawford D.J., Anderson, G.J., Bernardello G. (2011) The reproductive biology of island plants. In: Bramwell D., Caujapé-Castells J. (eds) The biology of island floras: 11–36. Cambridge, Cambridge University Press, https://doi.org/10.1017/CBO9780511844270.003
  • Cronk Q., Ojeda I. (2008) Bird-pollinated flowers in an evolutionary and molecular context. Journal of Experimental Botany 59(4): 715–727. https://doi.org/10.1093/jxb/ern009
  • de Castro C.C., Araujo A.C. (2004) Distyly and sequential pollinators of Psychotria nuda (Rubiaceae) in the Atlantic rain forest, Brazil. Plant Systematics and Evolution 244: 131–139. https://doi.org/10.1007/s00606-003-0036-8
  • Dulberger R. (1992) Floral polymorphisms and their functional significance in the heterostylous syndrome. In: Barrett S.C.H. (ed.) Evolution and function of heterostyly: 41–84. Berlin & Heidelberg, Springer. https://doi.org/10.1007/978-3-642-86656-2_3
  • Faria R.R., Ferrero V., Navarro L., Araujo A.C. (2012) Flexible mating system in distylous populations of Psychotria carthagenensis Jacq. (Rubiaceae) in Brazilian Cerrado. Plant Systematics and Evolution 298: 619–627. https://doi.org/10.1007/s00606-011-0571-7
  • Feinsinger P., Wolfe J.A., Swarm L.A. (1982) Island ecology: reduced hummingbird diversity and the pollination biology of plants, Trinidad and Tobago, West Indies. Ecology 63(2): 494–506. https://doi.org/10.2307/1938966
  • Ferrero V., Chapela I., Arroy J., Navarro L. (2011) Reciprocal style polymorphisms are not easily categorised: the case of heterostyly in Lithodora and Glandora (Boraginaceae). Plant Biology 13(s1): 7–18. https://doi.org/10.1111/j.1438-8677.2009.00307.x
  • Friday J.B., Okano D. (2006) Cordia subcordata (kou). Species Profiles for Pacific Island Agroforestry version 3.1. Available at https://raskisimani.files.wordpress.com/2013/01/cordia-kou.pdf [accessed 5 Aug. 2020].
  • Funamoto D. (2019) Plant-pollinator interactions in East Asia: A review. Journal of Pollination Ecology 25: 46–68.
  • Gibbs P.E., Taroda N. (1983) Heterostyly in the Cordia alliodora-C. trichotoma complex in Brazil. Revista Brasileira de Botânica 6(1): 1–10.
  • Gill F.B. (1971) Ecology and evolution of the sympatric Mascarene white-eyes, Zosterops borbonica and Zosterops olivacea. The Auk 88(1): 35–60. https://doi.org/10.2307/4083960
  • Grossenbacher D.L., Brandvain Y., Auld J.R., Burd M., Cheptou P.O., Conner J.K., Grant A.G., Hovick S.M., Pannell J.R., Pauw A., Petanidou T., Randle A.M., de Casas R.R., Vamosi J., Winn A., Igic B., Busch J.W., Kalisz S., Goldberg E.E. (2017) Self-compatibility is over-represented on islands. New Phytologist 215(1): 469–478. https://doi.org/10.1111/nph.14534
  • Gu L., Zhang D. (2009) A review on ornithophily in the Chinese flora. Journal of Tropical and Subtropical Botany 17: 194–204.
  • Hansen D.M., Olesen J.M., Jones C.G. (2002) Trees, birds and bees in Mauritius: exploitative competition between introduced honey bees and endemic nectarivorous birds? Journal of Biogeography 29(5–6): 721–734. https://doi.org/10.1046/j.1365-2699.2002.00720.x
  • Hervías-Parejo S., Traveset A. (2018) Pollination effectiveness of opportunistic Galápagos birds compared to that of insects: From fruit set to seedling emergence. American journal of Botany 105(7): 1142–1153. https://doi.org/10.1002/ajb2.1122
  • Hodgins K.A., Barrett S.C. (2008) Geographic variation in floral morphology and style-morph ratios in a sexually polymorphic daffodil. American Journal of Botany 95(2): 185–195. https://doi.org/10.3732/ajb.95.2.185
  • Kálmán K., Medvegy A., Pénzes Z. S., Mihalik E. (2007) Morph-specific variation of floral traits associated with reciprocal herkogamy in natural populations of Primula vulgaris and Primula veris. Plant Systematics and Evolution 268: 15–27. https://doi.org/10.1007/s00606-007-0575-5
  • Kearns C.A., Inouye D.W. (1993) Techniques for pollination biologists. University press of Colorado.
  • Kho Y.O., Baer J. (1968) Observing pollen tubes by means of fluorescence. Euphytica 17: 298–302.
  • Klein D.E., Freitas L., Da Cunha M. (2009) Self-incompatibility in a distylous species of Rubiaceae: is there a single incompatibility response of the morphs? Sexual Plant Reproduction 22: 121–131. https://doi.org/10.1007/s00497-009-0097-0
  • Kondo Y., Nishide M., Watanabe K., Sugawara T. (2007) Floral dimorphism in Psychotria boninensis Nakai (Rubiaceae) endemic to the Bonin (Ogasawara) Islands. Journal of Japanese Botany 82(5): 251–258.
  • Lammers T.G., Weller S.G., Sakai A.K. (1987) Japanese white-eye, an introduced passerine, visits the flowers of Clermontia arborescens, an endemic Hawaiian lobelioid. Pacific Science 41(1–4): 74–78.
  • Lewis D. (1975) Heteromorphic incompatibility system under disruptive selection. Proceedings of the Royal Society of London. Series B. Biological Sciences 188: 247–256. https://doi.org/10.1098/rspb.1975.0017
  • Machado I.C., Loiola M.I. (2000) Fly pollination and pollinator sharing in two synchronopatric species: Cordia multispicata (Boraginaceae) and Borreria alata (Rubiaceae). Brazilian Journal of Botany 23(3): 305–311. https://doi.org/10.1590/S0100-84042000000300006
  • Martínez-Adriano C.A., Jurado E., Flores J., González-Rodríguez H., Cuéllar-Rodríguez G. (2016) Flower, fruit phenology and flower traits in Cordia boissieri (Boraginaceae) from northeastern Mexico. PeerJ 4: e2033. https://doi.org/10.7717/peerj.2033
  • McMullen C.K. (1993) Flowering-visiting insects of the Galápagos Islands. The Pan-Pacific Entomologist 69: 95–106.
  • Meeus S., Jacquemyn H., Honnay O., Pailler T. (2011) Self-incompatibility and pollen limitation in the rare tristylous endemic Hugonia serrata on La Réunion Island. Plant Systematics and Evolution 292: 143–151. https://doi.org/10.1007/s00606-010-0400-4
  • Micheneau C., Fournel J., Pailler T. (2006) Bird pollination in an angraecoid orchid on Reunion Island (Mascarene Archipelago, Indian Ocean). Annals of Botany 97(6): 965–974. https://doi.org/10.1093/aob/mcl056
  • Nicolson S.W. (2002) Pollination by passerine birds: why are the nectars so dilute? Comparative Biochemistry and Physiology Part B: Biochemistry and Molecular Biology 131(4): 645–652. https://doi.org/10.1016/S1096-4959(02)00014-3
  • Olesen J.M., Valido A. (2003) Bird pollination in Madeira island. Ardeola 50(1): 65–67.
  • Opler P.A., Baker H.G., Frankie G.W. (1975) Reproductive biology of some Costa Rican Cordia species (Boraginaceae). Biotropica 7(4): 234–247. https://doi.org/10.2307/2989736
  • Pailler T., Thompson J.D. (1997) Distyly and variation in heteromorphic incompatibility in Gaertnera vaginata (Rubiaceae) endemic to La Réunion Island. American Journal of Botany 84(3): 315–327. https://doi.org/10.2307/2446005
  • Pailler T., Humeau L., Thompson J.D. (1998) Distyly and heteromorphic incompatibility in oceanic island species of Erythroxylum (Erythroxylaceae). Plant Systematics and Evolution 213: 187–198. https://doi.org/10.1007/BF00985199
  • Philipp M., Hansen L.B., Adsersen H., Siegismund H.R. (2004) Reproductive ecology of the endemic Lecocarpus pinnatifidus (Asteraceae) in an isolated population in the Galápagos Islands. Botanical Journal of the Linnean Society 146(2): 171–180. https://doi.org/10.1111/j.1095-8339.2004.00323.x
  • Richards J.H., Koptur S. (1993) Floral variation and distyly in Guettarda scabra (Rubiaceae). American Journal of Botany 80(1): 31–40. https://doi.org/10.2307/2445117
  • Sanchez J.M., Ferrero V., Navarro L. (2008) A new approach to the quantification of degree of reciprocity in distylous (sensu lato) plant populations. Annals of Botany 102(3): 463–472. https://doi.org/10.1093/aob/mcn111
  • Stebbins G.L. (1957) Self-fertilization and population variability in the higher plants. The American Naturalist 91(861): 337–354. https://doi.org/10.1086/281999
  • Sugawara T., Yumoto T., Tsuneki S., Watanabe K. (2014) Incompatibility and reproductive output in distylous Psychotria boninensis (Rubiaceae), endemic to the Bonin (Ogasawara) Islands, Japan. Journal of Japanese Botany 89: 22–26.
  • Taisma M.A., Wolfang Varela C. (2005) Sistema de compatibilidad en la especie distílica Cordia curassavica (Jacq.) R&S (Boraginaceae). Interciencia 30(7): 431–435.
  • Taylor B., Hayes D.E. (1980) The tectonic evolution of the South China Basin. In: Hayes D.E. (ed.) The tectonic and geologic evolution of Southeast Asian seas and islands, vol. 23: 89–104. https://doi.org/10.1029/GM023p0089
  • Valido A., Dupont Y.L., Hansen D.M. (2002) Native birds and insects, and introduced honey bees visiting Echium wildpretii (Boraginaceae) in the Canary Islands. Acta Oecologica 23(6): 413–419. https://doi.org/10.1016/S1146-609X(02)01167-0
  • Valois-Cuesta H., Soriano P.J., Ornelas J.F. (2011) Dimorphisms and self-incompatibility in the distylous species Palicourea demissa (Rubiaceae): possible implications for its reproductive output. Journal of Plant Research 124: 137–146. https://doi.org/10.1007/s10265-010-0359-9
  • Wang X., Yu W., Sun S., Huang S. (2016) Pollen size strongly correlates with stigma depth among Pedicularis species. Journal of Integrative Plant Biology 58(10): 818–821. https://doi.org/10.1111/jipb.12477
  • Watanabe K., Kato H., Kuraya E., Sugawara T. (2018) Pollination and reproduction of Psychotria homalosperma, an endangered distylous tree endemic to the oceanic Bonin (Ogasawara) Islands, Japan. Plant Species Biology 33(1): 16–27. https://doi.org/10.1111/1442-1984.12183
  • Watanabe K., Kato H., Sugawara T. (2014) Distyly and incompatibility in Psychotria homalosperma (Rubiaceae), an endemic plant of the oceanic Bonin (Ogasawara) Islands. Flora 209(11): 641–648. https://doi.org/10.1016/j.flora.2014.09.006
  • Xu Y., Luo Z., Gao S., Zhang D. (2018) Pollination niche availability facilitates colonization of Guettarda speciosa with heteromorphic self-incompatibility on oceanic islands. Scientific Reports 8: 13765. https://doi.org/10.1038/s41598-018-32143-5