Abstract
This study provides a checklist of Onagraceae in the Pan-Himalayan region based on extensive specimen consultation, literature investigation, and field surveys. According to recent phylogenetic studies and taxonomic revisions, five genera of Onagraceae are recognized including a total of 56 species in the Pan-Himalayan region. The five genera are Chamaenerion, Circaea, Epilobium, Oenothera, and Ludwigia. In this checklist, we verified all the validly published names in this region and confirmed their taxonomic status. Type status of names are checked according to the International Code of Nomenclature for algae, fungi and plants (ICN). Epilobium ladakhianum is treated as a new synonym of E. williamsii and lectotypification of Chamaenerion conspersum is made, which are the taxonomic novelties in this study. In addition, we provide identification keys to all the genera and their species, descriptions of the five genera, and distribution ranges as well as taxonomic notes for the species.
References
Aiton, W. (1789) Hortus Kewensis, vol. 2. George Nicol, London, 460 pp.
Ascherson, P. & Magnus, P. (1870) Bemerkungen über die Arten der Gattung Circaea Tourn. Botanische Zeitung 47: 745–760.
APG IV (2016) An update of the Angiosperm Phylogeny Group classification for the orders and families of flowering plants: APG IV. Botanical Journal of the Linnaeus Society 181 (1): 1–20. https://doi.org/10.1111/boj.12385
Akiyama, S., Thijsse, G., Esser, H.J. & Ohba, H. (2016) Siebold and Zuccarini’s type specimens and original materials from Japan, part 8. Angiosperms. Dicotyledoneae 7. The Journal of Japanese Botany 91 (1): 19–32.
Baum, D.A., Sytsma, K.J. & Hoch, P.C. (1994) The phylogeny of Epilobium (Onagraceae) based on nuclear ribosomal DNA sequences. Systematic Botany 19: 363–388. https://doi.org/10.2307/2419763
Berry, P.E., Hahn, W.J., Sytsma, K.J., Hall, J.C. & Mast, A. (2004) Phylogenetic relationships and biogeography of Fuchsia (Onagraceae) based on noncoding nuclear and chloroplast DNA data. American Journal of Botany 91 (4): 601–614. https://doi.org/10.3732/ajb.91.4.601
Brenan, J.P.M. (1953a) Notes on African Onagraceae and Trapaceae. Kew Bulletin 8: 163–172. https://doi.org/10.2307/4117169
Brenan, J.P.M. (1953b) Flora of Tropical East Africa: Onagraceae. Crown Agents for Overseas Governments & Administrations, London, 23 pp.
Britton, N.L. & Brown, A. (1913) An Illustrated Flora of the Northern United States, Canada and the British Possessions, vol. 1. C. Scribner’s sons, New York, 680 pp.
Bizzarri, M.P. & Raven, P.H. (1972) Adumbratio Florae Aethiopicae—23. Onagraceae. Webbia 27 (2): 467–504. https://doi.org/10.1080/00837792.1973.10669983
Boufford, D.E. (1982) The systematics and evolution of Circaea (Onagraceae). Annals of the Missouri Botanical Garden 69 (4): 804–994. https://doi.org/10.2307/2398997
Boufford, D.E. (1990) The Onagraceae of Guizhou, China. Botanical Bulletin of Academia Sinica 31: 321–342.
Boufford, D.E., Crisci, J.V., Tobe, H. & Hoch, P.C. (1990) A cladistic analysis of Circaea (Onagraceae). Cladistics 6: 171–182. https://doi.org/10.1111/j.1096-0031.1990.tb00534.x
Boissier, P.E. (1888) Flora Orientalis Supplementum. A. Asher & Co. B.V, Amsterdam, 466 pp.
Cavanilles, A.J. (1796) Icones et Descriptiones Plantarum, vol. 3. Ex Regia Typographia, Matriti, 300 pp.
Chen, C.J., Hoch, P.C. & Raven, P.H. (1992) Systematics of Epilobium (Onagraceae) in China. Systematic Botany, Monographs 34: 1–209.
Chen, C.J., Hoch, P.C., Raven, P.H., Boufford, D.E. & Wagner, W.L. (2007) Onagraceae. In: Wu, Z.Y., Raven, P.H. & Hong, D.Y. (Eds.) Flora of China, vol. 13. Science Press & Missouri Botanical Garden Press, Beijing & St. Louis, pp. 400–427.
Chowdhery, H.J. & Singh, S. (1988) Epilobium semiamplexicaule Chowdhery et S. Singh—a new species of Epilobium L. (Onagraceae) from Himachal Pradesh, India. Indian Journal of Forestry 11 (1): 80.
Clarke, C.B. (1879) LXII Onagraceae. In: Hooker, J.D. & Clarke, C.B. (Eds.) The Flora of British India, vol. 2. L. Reeve, London, pp. 582–590.
Conti, E., Fischbach, A. & Sytsma, K.J. (1993) Tribal relationships in Onagraceae: implications from rbcL sequence data. Annals of the Missouri Botanical Garden 80: 672–685. https://doi.org/10.2307/2399853
Cuong, V.V. & Vidal, J.E. (1973) Onagraceae. In: Aubréville, A. & Leroy, J.-F. (Eds.) Flore du Cambodeg du Laos et du Viêt-nam. Museìum National d’Histoire Naturelle, Paris, pp. 17–39.
Decaisne, J. (1844) Planae rariores, quas in India orientali collegit Victor Jacquemont. In: Jacquemont, V. (Ed.) Voyage dans l’Inde, vol. 4. Firmin Didot freÌres, Paris, pp. 57.
Diels, L. (1912) New and imperfectly known species. Notes from the Royal Botanic Garden, Edinburgh 5: 161–308.
Dietrich, W. (1977) The South American species of Oenothera sect. Oenothera (Raimannia, Renneria; Onagraceae). Annals of the Missouri Botanical Garden 64: 425–626. https://doi.org/10.2307/2395257
Dietrich, W., Wagner, W.L. & Raven, P.H. (1997) Systematics of Oenothera section Oenothera subsection Oenothera (Onagraceae). Systematic Botany Monographs 50: 1–234.
Don, D. (1825) Prodromus Florae Nepalensis. J. Gale, London, 256 pp.
Don, G. (1832) A General History of the Dichlamydeous Plants, vol. 2. J.G. & F. Rivington, London, 875 pp.
Editorial Committee of Flora of Pan-Himalaya (2017) General Guideline of the Flora of Pan-Himalaya. Available from: http://www.flph.org/news/30 (accessed: 5 April 2022).
Exell, A.W. (1957) Ludwigia hyssopifolia (G.Don) Exell. Garcia de Orta 5: 471.
Ford, V.S. & Gottlieb, L.D. (2007) Tribal relationships within Onagraceae inferred from PgiC sequences. Systematic Botany 32: 348–356. https://doi.org/10.1600/036364407781179725
Franchet, A. & Savatier, L. (1878) Enumeratio Plantarum, vol. 2. F. Savy, Paris, 789 pp.
Garilleti, R. (1993) Herbarium cavanillesianum. S.L. Cyanus, Madrid, 249 pp.
Gates, R.R. (1911) Mutation in Oenothera. The American Naturalist 45 (538): 577–606.
Handel-Mazzetti, H. (1933) Symbolae Sinicae, vol. 7. J. Springer, Vienna, 730 pp.
Hara, H. (1953) Ludwigia versus Jussiaea. The Journal of Japanese Botany 28 (10): 289–294.
Haussknecht, C. (1884) Monographie der Gattung Epilobium. G. Fisher, Jena, 318 pp.
Haussknecht, C. (1879) Epilobia nova. Österreichische Botanische Zeitschrift 29: 51–59.
Hitchcock, A.S. & Green, M.L. (1929) Standard-species of Linnaean genera of Phanerogamae (1753-54). In: International Botanical Congress, Cambridge (England), 1930: Nomenclature. Proposals by British botanists, Wyman & Sons, Ltd., Fetter Lane, London, 111–199 pp.
Hoch, P.C. (1999) Onagraceae. In: Iwatsuki, K., Boufford, D.E. & Ohba, H. (Eds.) Flora of Japan, vol. 2c. Kodansha Ltd., Tokyo, pp. 224–246.
Hoch, P.C. & Gandhi, K. (2020) Nomenclatural changes in Onagraceae. PhytoKeys 145: 57–62. https://doi.org/10.3897/phytokeys.145.51139
Hoggard, G.D., Kores, P.J., Molvray, M. & Hoggard, R.K. (2004) The phylogeny of Gaura (Onagraceae) based on ITS, ETS, and trnL‐F sequence data. American Journal of Botany 91: 139–148. https://doi.org/10.3732/ajb.91.1.139
Holub, J. (1972) Taxonomic and nomenclatural remarks on Chamaenerion auct. Folia Geobotanica & Phytotaxonomica 7: 81–90. https://doi.org/10.1007/BF02856384
Hooker, W. (1805) The Paradisus Londinensis, vol. 1. William Hooker, London, 300 pp.
Hung, K.H., Schaal, B.A., Hsu, T.W., Chiang, Y.C., Peng, C.I. & Chiang, T.Y. (2009) Phylogenetic relationships of diploid and polyploid species in Ludwigia sect. Isnardia (Onagraceae) based on chloroplast and nuclear DNAs. Taxon 58: 1216–1226. https://doi.org/10.1002/tax.584013
Jacquin, N.J. (1760) Enumeratio Systematica Plantarumquas. Theodorum Haak, Leiden, 41 pp.
Jonsell, B. & Jarvis, C.E. (2002) Lectotypification of Linnaean names for Flora Nordica (Brassicaceae–Apiaceae). Nordic Journal of Botany 22 (1): 67–86. https://doi.org/10.1111/j.1756-1051.2002.tb01625.x
Jussieu, A.L. (1789) Genera Plantarum. Theophilum Barrois, Parisiis, 498 pp.
Kitamura, S. (1955) Flowering Plants and Ferns. In: Kihara, H. (Ed.) Scientific Results of the Japanese Expeditions to Nepal Himalaya. Kyoto University, Kyoto, pp. 73–283.
Kitamura, S. (1960) Flora of Afghanistan. Kyoto University, Kyoto, 486 pp.
Kitamura, S. (1966) Results of the Kyoto University Scientific Expedition to the Karakoram and Hindukush, vol. 8. Kyoto University, Kyoto, 460 pp.
Léveillé, H. (1907) Revision du Genre Epilobium. Bulletin de l’Herbier Boissier 2 (7): 587–590.
Léveillé, H. (1908) Decades plantarum novarum XI. XII. Repertorium Specierum Novarum Regni Vegetabilis 6: 110–114. https://doi.org/10.1002/fedr.19080060321
Léveillé, H. (1909) Decades plantarum novarum XXIV/XXV. Repertorium Specierum Novarum Regni Vegetabilis 7: 337–340. https://doi.org/10.1002/fedr.19120102402
Léveillé, H. (1910a) Decades plantarum novarum XXIX/XXX. Repertorium Specierum Novarum Regni Vegetabilis 8: 138–141. https://doi.org/10.1002/fedr.19100080706
Léveillé, H. (1910b) Decades plantarum novarum XLVI. Repertorium Specierum Novarum Regni Vegetabilis 9: 19–21. https://doi.org/10.1002/fedr.19100090103
Léveillé, H. (1913) Decades plantarum novarum CXIX–CXXIV. Repertorium Specierum Novarum Regni Vegetabilis 12: 281–288. https://doi.org/10.1002/fedr.19130121707
Levin, R.A., Wagner, W.L., Hoch, P.C., Nepokroeff, M., Pires, J.C., Zimmer, E.A. & Sytsma, K.J. (2003) Family‐level relationships of Onagraceae based on chloroplast rbcL and ndhF data. American Journal of Botany 90 (1): 107–115. https://doi.org/10.3732/ajb.90.1.107
Link, H.F. (1821) Enumeratio Plantarum Horti Regii Botanici Berolinensis Altera, pars 1. G. Reimer, Berlin, 458 pp.
Linnaeus, C. (1753) Species Plantarum. Laurentii Salvii, Stockholm, 1200 pp.
Linnaeus, C. (1767) Mantissa Plantarum, ed. 1. Laurentii Salvii, Stockholm, 142 pp.
Liu, S.H., Hoch, P.C., Diazgranados, M., Raven, P.H. & Barber, J.C. (2017) Multi-locus phylogeny of Ludwigia (Onagraceae): Insights on infra-generic relationships and the current classification of the genus. Taxon 66: 1112–1127. https://doi.org/10.12705/665.7
Luo, Y.K., He, J., Lyu, R.D., Xiao, J.M., Li, W.H., Yao, M., Pei, L.Y., Cheng, J. & Xie, L. (2021) Comparative analysis of complete chloroplast genomes of 13 species in Epilobium, Circaea, and Chamaenerion and insights into phylogenetic relationships of Onagraceae. Frontiers in Genetics 12: 730495. https://doi.org/10.3389/fgene.2021.730495
Martinov, I.I. (1820) Tekhno-Botanîcheskiǐ Slovar. Imperial Russian Academy, Sanktpeterburgh, 682 pp.
Maximowicz, C.J. (1859) Primitiae Florae Amurensis. Buchdruckerei der kaiserlichen Akademie der Wissenschaften, St. Petersburg, 504 pp.
Micheli, M. (1875) Onagraceae. In: Martius, C.F.P. & Eichler, A.G. (Eds.) Flora Brasiliensis, vol. 13, pars 2. R. Oldenbourg, Munich & Leipzig, pp. 145–182.
Miller, P. (1754) The Gardeners Dictionary, 4th ed., vol. 3. Printed for the author and sold by J. Rivington London, London, 588 pp.
Miquel, F.A.W. (1856) Flora van Nederlandsch Indie, vol. 1, no. 1. C. G. van der Post, Amsterdam, 1116 pp.
Moldenke, H.N. (1973) Notes on new and noteworthy plants LXIV. Phytologia 27: 289.
Mosquin, T. (1966) A new taxonomy for Epilobium angustifolium L. (Onagraceae). Brittonia 18 (1): 169. https://doi.org/10.2307/2805200
Nakai, T. (1919) Notulae ad plantas Japoniae et Coreae XIX. The Botanical Magazine 33: 9.
Pampanini, R. (1910) Plante Vascolari Dell’ Hu-Peh. Nuovo Giornale Botanico Italiano, Nuova Serie 17: 223–736.
Paul, T.K. (1997) Epilobium ladakhianum T.K. Paul a new species from India. The Botanical Survey of India 39 (1–4): 197. http://dx.doi.org/10.20324/nelumbo%2Fv39%2F1997%2F74319
Paul, T.K. (1998) A conspectus of the family Onagraceae in India. Nelumbo 40 (1–4): 1–22. http://dx.doi.org/10.20324/nelumbo%2Fv40%2F1998%2F74271
Pfeiffer, L. (1873) Nomenclator botanicus, vol. 1, pars 1. Sumptibus Theodori Fischeri, Cassellis, 808 pp.
Plumier, C. (1758) Plantarum Americanarum Fasciculus Septimus. Peterum, S., Gerard, P. & Theodor, H., Amsterdam, 193 pp.
Rafinesque, C.S. (1818) A review of Pursh’s flora of North America. American Monthly Magazine and Critical Review 2: 265–269.
Raven, P.H. (1962a) The genus Epilobium in the Himalayan region. Bulletin of the British Museum (Natural History), Botany 2: 327–382.
Raven, P.H. (1962b) New Combinations in Ludwigia. Kew Bulletin 15 (3): 476. https://doi.org/10.2307/4115634
Raven, P.H. (1963) The Old World species of Ludwigia (including Jussiaea), with a synopsis of the genus (Onagraceae). Reinwardtia 6: 327–427. https://doi.org/10.14203/reinwardtia.v6i4.224
Raven, P.H. (1964) Onagraceae In: Rechinger, K.H. (Ed.) Flora Iranica, vol. 7. Akademische Druck- u. Verlagsanstalt, Graz, pp. 1–19.
Raven, P.H. (1988) Onagraceae as a model of plant evolution. In: Gottlieb, L.D. & Jain, S.K. (Eds.) Plant Evolutionary Biology. Chapman & Hall, London, pp. 85–107.
Raven, P.H. (2007) Ludwigia. In: Jarvis, C. (Ed.) Order Out of Chaos: Linnean Plant Names and Their Types. Linnean Society of London in association with the Natural History Museum, London, pp. 605–606.
Robinson, C.B. (1908) Alabastra Philippinensia, Ⅱ. The Philippine Journal of Science 3: 175–218.
Rose, J.N. (1905) Studies of Mexican and Central American plants—No. 4. Contributions from the United States National Herbarium 8: 330.
Roxburgh, W. (1832) Flora Indica, or Descriptions of Indian plants, vol. 1. Mission Press, Serampore, 741 pp.
Royle, J.F. (1839) Illustrations of the Botany and Other Branches of the Natural History of the Himalayan Mountains, vol. 1. Wm. H. Allen, London, 472 pp.
Ruthe, J.F. (1827) Flora der Mark Brandenburg, vol. 1. C. G. Lüderitz, Berlin, 491 pp.
Sabara, H.A., Kron, P. & Husband, B.C. (2013) Cytotype coexistence leads to triploid hybrid production in a diploid–tetraploid contact zone of Chamerion angustifolium (Onagraceae). American Journal of Botany 100: 962–970. https://doi.org/10.3732/ajb.1200583
Schreber, J.C.D. (1771) Spicilegium Florae Lipsicae. Dykiano, Lipsiae, 180 pp.
Scopoli, G.A. (1772) Flora Carniolica, ed. 2, tom. 1. Ioannis Pauli Krauss, Vienna, 448 pp.
Sennikov, A.N. (2011) Chamerion or Chamaenerion (Onagraceae)? The old story in new words. Taxon 60: 1485–1488. https://doi.org/10.1002/tax.605028
Séguier, J.F. (1754) Plantae Veronense, vol. 3. Typographia A. Andreonii, Verona, 316 pp.
Skvortsov, A.K. (1977) On several east Asian species of the genus Circaea (Onagraceae). Byulleten’ Glavnogo Botanicheskogo Sada 103: 35–39.
Siebold, P.F. & Zuccarini, J.G. (1845) Florae Japonicae familiae naturales. Abhandlungen der Mathematisch-Physikalischen Classe der Königlich Bayerischen Akademie der Wissenschaften 4 (2): 111–204.
Sweet, R. (1830) Sweet’s Hortus Britannicus, ed. 2. J. Ridgway, London, 623 pp.
Tacik, T. (1959) Chamaenerion. In: Władysław, S. (Ed.) Flora Polska, tom. 8. Polskiej Akademii Umiejętności, Kraków, pp. 209–257.
Tanaka, N., Katsuyama, T. & Ohnishi, W. (2016) Plant type specimens from Kanagawa, Japan, taxonomically described by A. R. Franchet and P. A. L. Savatier: Dicots. Bulletin of the Kanagawa Prefectrural Museum, Natural Science 45: 41–68.
Thiers, B. (2022) Index Herbariorum: A Global Directory of Public Herbaria and Associated Staff. New York Botanical Garden’s Virtual Herbarium. The New York Botanical Garden. Available from: http://sweetgum.nybg.org/ih/ (accessed: 12 October 2022)
Turland, N.J., Wiersema, J.H., Barrie, F.R., Greuter, W., Hawksworth, D.L., Herendeen, P.S., Knapp, S., Kusber, W.-H., Li, D.-Z., Marhold, K., May, T.W., McNeill, J., Monro, A.M., Prado, J., Price, M.J. & Smith, G.F. (2018) International Code of Nomenclature for Algae, Fungi, and Plants (Shenzhen Code) adopted by the Nineteenth International Botanical Congress Shenzhen, China, July 2017. Regnum Vegetabile 159. Glashütten: Koeltz Botanical Books. https://doi.org/10.12705/Code.2018
Ventenat, É.P. (1799) Tableau du Règne Végétal, tom. 3. J. Drisonnier, Paris, 590 pp.
Wallich, N. (1832) Numerical List of Dried Specimens of Plants in the Museum of the Honl. East India Company. London, 306 pp.
Wagner, W.L., Hoch, P.C. & Raven, P.H. (2007) Revised classification of the Onagraceae. Systematic Botany, Monographs 83: 1–240.
Xie, L., Wagner, W.L., Ree, R.H., Berry, P.E. & Wen, J. (2009) Molecular phylogeny, divergence time estimates, and historical biogeography of Circaea (Onagraceae) in the Northern Hemisphere. Molecular Phylogenetics and Evolution 53: 995–1009. https://doi.org/10.1016/j.ympev.2009.09.009