Cordia subcordata (Boraginaceae), a distylous species on oceanic coral islands, is self-compatible and pollinated by a passerine bird
PDF

Supplementary Files

Supplementary file 1

Keywords

Cordia subcordata
distyly
heterostylous self-incompatibility
oceanic island
passerine pollination

How to Cite

Wang, X., Wen, M., Wu, M. and 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), pp. 361-372. doi: 10.5091/plecevo.2020.1757.

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.

https://doi.org/10.5091/plecevo.2020.1757
PDF

References

Baker H.G. (1967) Support for Baker’s law-as a rule. Evolution 21(4): 853–856. https://doi.org/10.2307/2406780

Baker A.M., Thompson J.D., Barrett S.C. (2000) Evolution and maintenance of stigma-height dimorphism in Narcissus. II. Fitness comparisons between style morphs. Heredity 84: 514–524. https://doi.org/10.1046/j.1365-2540.2000.00686.x

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

Cruden R.W. (2009) Pollen grain size, stigma depth, and style length: the relationships revisited. Plant Systematics and Evolution 278: 223–238. https://doi.org/10.1007/s00606-008-0142-8

Darwin C. (1877) The different forms of flowers on plants of the same species. London, John Murray. https://doi.org/10.5962/bhl.title.608

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

de Stapf M.N.S., dos Santos Silva T.R. (2013) Four new species of genus Cordia (Cordiaceae, Boraginales) from Brazil. Brittonia 65: 191–199. https://doi.org/10.1007/s12228-012-9268-7

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.

Ganders F.R. (1979) The biology of heterostyly. New Zealand Journal of Botany 17(4): 607–635. https://doi.org/10.1080/0028825X.1979.10432574

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.

Gu L., Luo Z., Zhang D., Renner S.S. (2010) Passerine pollination of Rhodoleia championii (Hamamelidaceae) in subtropical China. Biotropica 42(3): 336–341. https://doi.org/10.1111/j.1744-7429.2009.00585.x

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. (1987) Breeding systems of selected Galapagos Islands angiosperms. American Journal of Botany 74(11): 1694–1705. https://doi.org/10.1002/j.1537-2197.1987.tb08770.x

McMullen C.K. (1993) Flowering-visiting insects of the Galápagos Islands. The Pan-Pacific Entomologist 69: 95–106.

McMullen C.K. (2012) Pollination of the heterostylous Galápagos native, Cordia lutea (Boraginaceae). Plant Systematics and Evolution 298: 569–579. https://doi.org/10.1007/s00606-011-0567-3

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

Naiki A. (2012) Heterostyly and the possibility of its breakdown by polyploidization. Plant Species Biology 27(1): 3–29. https://doi.org/10.1111/j.1442-1984.2011.00363.x

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.

Olesen J.M., Dupont Y.L., Ehlers B.K., Valido A., Hansen D.M. (2003) Heterostyly in the Canarian endemic Jasminum odoratissimum (Oleaceae). Nordic Journal of Botany 23(5): 537–539. https://doi.org/10.1111/j.1756-1051.2003.tb00431.x

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

Pannell J.R. (2015) Evolution of the mating system in colonizing plants. Molecular Ecology 24(9): 2018–2037. https://doi.org/10.1111/mec.13087

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

Philipp M., Böcher J., Siegismund H.R., Nielsen R.L. (2006) Structure of a plant-pollinator network on a pahoehoe lava desert of the Galápagos Islands. Ecography 29(4): 531–540. https://doi.org/10.1111/j.0906-7590.2006.04546.x

Ren Z., Zhao Y., Liang H., Tao Z., Tang H., Zhang H., Wang H. (2018) Pollination ecology in China from 1977 to 2017. Plant Diversity 40(4): 172–180. https://doi.org/10.1016/j.pld.2018.07.007

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

Safford R.J., Jones C.G. (1998) Strategies for land-bird conservation on Mauritius. Conservation Biology 12(1): 169–176. https://doi.org/10.1111/j.1523-1739.1998.96177.x

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

Tong Y., Jian S., Chen Q., Li Y., Xing F. (2013) Vascular plant diversity of the Paracel Islands, China. Biodiversity Science 21(3): 364–374. https://doi.org/10.3724/SP.J.1003.2013.11222

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

Valido A., Dupont Y.L., Olesen J.M. (2004) Bird-flower interactions in the Macaronesian islands. Journal of Biogeography 31(12): 1945–1953. https://doi.org/10.1111/j.1365-2699.2004.01116.x

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

Watanabe K., Sugawara T. (2015) Is heterostyly rare on oceanic islands? AoB Plants 7: plv087. https://doi.org/10.1093/aobpla/plv087

Wu X., Li A., Zhang D. (2010) Cryptic self‐incompatibility and distyly in Hedyotis acutangula Champ. (Rubiaceae). Plant Biology 12(3): 484–494. https://doi.org/10.1111/j.1438-8677.2009.00242.x

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

Creative Commons License

This work is licensed under a Creative Commons Attribution 4.0 International License.