sign in sign up
<<
Home , Nelumbo, Nelumbonaceae

Research 84 (2018) 134e140

Contents lists available at ScienceDirect

Cretaceous Research

journal homepage: www.elsevier.com/locate/CretRes

Short communication jiayinensis sp. nov. from the Upper Cretaceous Yong'ancun Formation in Jiayin, Heilongjiang, Northeast China

* Fei Liang a, b, Ge Sun a, b, c, , Tao Yang a, b, Shuchong Bai a, b a College of Paleontology, Shenyang Normal University, Shenyang 110034, China b Key Laboratory of of Past Life in NE Asia, Ministry of Land ＆ Resources, Shenyang 110034, China c Key Laboratory for Evolution of Past Life and Environment in NE Asia, MOEC, Jilin University, Changchun 130026, China article info abstract

Article history: Fossil of Nelumbo jiayinensis sp. nov. are described from the Yong'ancun Formation (Santonian) in Received 6 July 2017 Jiayin, Heilongjiang, Northeast China. This is the first report on fossil Nelumbo from the Upper Cretaceous Received in revised form of China. The leaves are simple with entire margins, orbicular or sub-orbicular in shape, with a peltate 18 October 2017 and symmetric lamina. The venation is actinodromous with 20e25 primary veins, the secondary and Accepted in revised form 7 November 2017 tertiary veins are poorly developed and interweave into meshes. The areoles are irregularly polygonal in Available online 8 November 2017 shape and well developed both in upper and lower surfaces. Combined with data derived from associ- ated fossil mega-, spores and , bivalves and dinosaur footprints, the aquatic angiosperm Keywords: fl Nelumbo Nelumbo existed in a uviolacustrine environment under a warm but seasonal temperate climate. © New species 2017 Elsevier Ltd. All rights reserved. Upper Cretaceous Santonian Jiayin

1. Introduction Many fossil leaves, and pollen of Nelumbo have been described from Early Cretaceous and younger deposits (Kuprianova The earliest known flowering plants from the fossil records seem and Tarasevich, 1983; Erickson, 1991; Tao, 2000; Johnson, 2002; to be aquatic and herbaceous in nature (Sun et al., 1998, 2002; Gandolfo and Cuneo, 2005; He et al., 2010; Gabrielyan et al., Dilcher et al., 2007), which prompted us to pay more attention to 2012; Li et al., 2014). Additionally, fossil Nelumbo leaves from the the significance of aquatic plants in regard to the Asuwa flora (Upper Cretaceous) have been described from , early evolutionary trends of angiosperms. Nelumbo is the sole extant which is so far the earliest record in eastern Asia (Matsuo, 1954). of the family Nelumbonaceae, and consists of two extant However, in China, most Nelumbo fossils are reported from species Gaertner and N. lutea Willdenow deposits including the Changchang Formation of Chang- (Nicolson, 1991; Ni et al., 1995). According to the previous records chang Basin, Hainan Island (Guo, 1979; He et al., 2010; Li et al., the earliest fossil Nelumbo emerged in the Albian (Early Cretaceous), 2014) and the Dalianhe Formation in Yilan of Heilongjiang Prov- yet the systematic position, the evolution and phytogeography of ince (Tao, 2000). this genus have long been intensively discussed by both botanists In this paper, we describe a new species, Nelumbo jiayinensis sp. and paleobotanists (Crabtree, 1987; Upchurch et al., 1994; Parkinson nov., preserved as remains collected from the Upper Creta- et al., 1999; Xue et al., 2012). However, as an aquatic angiosperm, ceous Yong'ancun Formation in the Jiayin area of NE China. The age fossil Nelumbo is a clearly indicator of non-marine aquatic envi- of the Yong'ancun Formation is assigned to the Santonian based on ronments, such as lakes, wetlands and slow flowing rivers, and likely the combined data mainly of megafossils and palynological as- indicates a warm climate, which is significant for understanding semblages (Sun et al., 2007, 2011; Markevich et al., 2011; Liang past environments and climates. et al., 2015a). Ostracods, bivalves, conchostracans, dinosaur foot- prints (Jiayinosauropsis johnsoni) in addition to many aquatic an- giosperms have been found in this formation (Dong et al., 2003; * Corresponding author. College of Paleontology, Shenyang Normal University, Sun et al., 2007, 2011; Markevich et al., 2011; Liang and Sun, Shenyang 110034, China. 2015b), which indicates abundance of fresh water environments. E-mail address: [email protected] (G. Sun). https://doi.org/10.1016/j.cretres.2017.11.007 0195-6671/© 2017 Elsevier Ltd. All rights reserved. F. Liang et al. / Cretaceous Research 84 (2018) 134e140 135

2. Materials and methods Type locality: East hill of Yong'ancun village, Jiayin, Heilongjiang, China. The specimens of Nelumbo jiayinensis sp. nov. described here Geological horizon: Yong'ancun Formation (Santonian) were collected from the upper part of the Yong'ancun Formation Derivation of specific name: From the Jiayin Basin where the fossils (Fig. 1), Jiayin County of Heilongjiang Province. Outcrops of the collected. Yong'ancun Formation (Fig. 2) are mainly distributed along the Diagnosis. Simple leaves, orbicular or sub-orbicular with entire Heilongjiang (Amur) River near the Yong'ancun village. The Yon- margin, primary veins strong, almost straight, 20e25 in number, g'ancun Formation is mainly composed of alternating yellow- radiating from the center at acute angles, secondary veins forming brown cross-bedded sandstones, greyish-brown siltstones and meshes in the intercostal area, finer veins usually forming small mudstones, intercalated with pebbly sandstone, representing a quadrangular or pentagonal areoles. Epidermal cells of leaves basin dominated by alluvial-lacustrine (Bureau of Geology and usually polygonal and regular, while the petiole cells show an Mineral Resources of Heilongjiang Province, 1993; Sun et al., 2011, elongate and compact arrangement. 2016). The age of the Yong'ancun Formation is Santonian mainly Description. Leaves are simple, nearly orbicular or sub-orbicular in based on palynological studies (Sun et al., 2007, 2011; Markevich shape, with peltate and symmetric lamina (Fig. 3, 4, 5). Even though et al., 2011; Liang et al., 2015a). The terminology we use for the preserved fossil lamina fragments are 9e12 cm long and almost describing leaf morphology follows Ellis et al. (2009). 11 cm wide in size, the material suggests the whole orbicular leaves Six specimens of Nelumbo in total were collected from the fossil could approach 15e24 cm in diameter. The lamina surface is site (Fig. 2), which is located in the upper part of the Yong'ancun membranous in texture and the margin is entire or undulates Formation. The fossil leaves of Nelumbo are preserved as impres- slightly, but is incompletely preserved (Fig. 3A, B, C, D, E; Fig. 4; sions and compressions, and were photographed using a Nikon Fig. 5). The petiole is about 6e10 mm in diameter, situated in the digital camera (Nikon D600). Details of the leaf structures were center of the lamina (Figs. 3A, 4A, B), and the epidermal cells of the observed and photographed using 3D super depth microscopy petiole are highly elongate (Fig. 4C). In the preserved specimens, systems (Keyence VHX-600). All specimens described here are the leaf venation shows actinodromous branching, which is com- housed in the Paleontological Museum of Liaoning (PMOL) in mon in living and fossil species of Nelumbo. Primary veins or ribs Shenyang, China. are 20e25 in number, almost straight or bend slightly and radiate from the leaf center at an angle of 5e15 on the upper surface (Fig. 3A, B) while on the lower surface the primary veins are clearer 3. Systematic paleontology and more prominent (Fig. 4A; Fig. 5A). In the intercostal zones of primary veins the secondary vein branches from the primary veins Family: Nelumbonaceae  with an angle of 40e60 and interweave into meshes (Fig. 3B, C, D; Genus: Nelumbo Adanson, 1763 Fig. 5B), in these meshes, tertiary veins become feeble and form Species: Nelumbo jiayinensis Liang, Sun et Yang, sp. nov. into irregular and polygonal areoles, usually 0.5e1.0 mm in diam- eter and 3- to 5-sided (Figs. 3E and 4D, E; Fig. 5C, D, E, F, G). Holotype: specimens YX-B-300, Yong'ancun village of Jiayin County, NE China, the Yong'ancun Formation, Upper Cretaceous d Epidermal cells of the upper surface are relatively regular in size Fig. 3 and shape, which are generally polygonal and usually 20e50 mmin Paratype: specimens YX-B-301d Fig. 4 diameter; the anticlinal cell wall is generally regular and almost Material: samples YX-B-300, YX-B-301, YX-B-302, YX-B-304, YX-B- straight (Fig. 3D, E; Fig. 5G). On the lower surface, the epidermal 307a, YX-B-307b cells are more or less same as those of the upper surface in size and shape, usually regular and polygonal, the average size of cells is 40 mm long by 30 mm wide (Figs. 3E and 4D, E; Fig. 5C, D, E, G). Stomata were not observed.

4. Discussion

4.1. Comparisons

The features of the monotypic family Nelumbonaceae include a simple, orbicular lamina with an entire margin, actinodromous veins, a central petiole and the hexagonal areoles (Hickey and Wolfe, 1975; Upchurch et al., 1994). It is clear that the new spe- cies shares many such characters and so should be assigned to the family Nelumbonaceae. Obviously, the new species differs from the extant species Nelumbo nucifera and N. lutea in the number of the primary veins and the lamina size, and Hollick (1894) noticed that it was possible that Nelumbo leaf size could progressively increase over geological time. Up to now, many of fossil species of Nelumbo have been re- ported, and most of fossil specimens represent only leaf portions. Nevertheless many of the descriptions and illustrations could provide valuable information allowing comparisons with the present material (Matsuo, 1954; Gandolfo and Cuneo, 2005; He et al., 2010; Li et al., 2014). The radial vein number and the leaf margin of the present specimens are similar to those of Nelumbo Fig. 1. Location of Jiayin, China (the arrow shows the fossil site). orientalis from the Upper Cretaceous of Japan described by Matsuo 136 F. Liang et al. / Cretaceous Research 84 (2018) 134e140

Fig. 2. Fossil site of Nelumbo jiayinensis sp. nov., Yong'ancun Formation in Jiayin, China: A-Outcrop picture of upper part of the Yong'ancun Fm.; B-Stratigraphic profile of upper part of the Yong'ancun Fm., showing the fossil layer yielding N. jiayinensis.).

(1954), but the lamina size and the angles of the radial veins are (Tao, 2000), N. changchangensis X. Y. He et J. H. Jin from the larger than in Nelumbo orientalis. Compared with Nelumbo puertae Changchang Formation of Hainan (He et al., 2010; Li et al., 2014), described by Gandolfo and Cuneo (2005), which is from the Upper were all exhumed from the Eocene deposits, and are more or less Cretaceous of Chubut, Patagonia, Argentina, similar with the present specimens as regards leaf shape and finer the new specimens differ in leaf diameter, the primary vein venation, but differ in the lamina diameter, number of ribs and the number and angles between two adjacent ribs, but are similar in angle of adjacent ribs. the shape of the areoles. Additionally, many fossil species of Fossil leaves of Nelumbites Berry are more similar to L. Nelumbo leaves have been described from China, N. protospeciosa rather than Nelumbo (Berry, 1911; Knowlton, 1930). In addition, Saporta from the Changchang Formation of Qiongshan and the Exnelumbites callejasiae Estrada-Ruiz et al., from the Olmos For- Linjiang Formation of Jiangxi (Guo, 1979; Li and Chen, 2002), mation (Campanian-Maastrichtian) of Coahuila, and the Nelumbo sp. from Dalianhe Formation in Yilan of Heilongjiang McRae Formation of New Mexico of USA, is somewhat similar to the F. Liang et al. / Cretaceous Research 84 (2018) 134e140 137

Fig. 3. Nelumbo jiayinensis sp. nov., (specimen YX-B-300) A - General aspect of leaf showing an orbicular lamina. B, C - showing the detail of the secondary and tertiary veins. D, E - showing the venation meshes and polygonal areoles on the upper surface of the leaf. 138 F. Liang et al. / Cretaceous Research 84 (2018) 134e140

Fig. 4. Leaf of Nelumbo jiayinensis sp. nov., (specimen YX-B-301) A - showing the lower surface of the leaf and a centered petiole. B, C - an enlargement of A, showing details of the petiole. D, E - showing the epidermal cells of the lower surface.

present material in leaf shape and tertiary venation, but differs in 4.2. Paleoenvironment the number of primary veins, lamina diameter and leaf margin (Estrada-Ruiz et al., 2011). It is worth mentioning that the leaves of As above-mentioned, the genus Nelumbo has two extant species Nelumbites cf. extenuinervis Upchurch et al. from the Taipinglin- Nelumbo nucifera Gaertner and N. lutea Willdenow, widespread in chang Formation and the upper layer of the Yong'ancun Formation the subtropics and temperate zone of Asia, Australia and North in Jiayin (Quan and Sun, 2008) are similar to the present specimens America. It is important to note that these two extant species in leaf margin and venation, but we could not make a detailed usually live in quite water or slow flowing streams like ponds, lakes comparison due to incomplete preservation of the leaf remains. and along river margins. Obviously, the aquatic angiosperm F. Liang et al. / Cretaceous Research 84 (2018) 134e140 139

Fig. 5. Incomplete leaves of Nelumbo jiayinensis sp. nov. (A, C, D, E, specimen YX-B-302; B, F, G, specimen YX-B-304) A - the lower surface of the leaf. B, F - showing the entire leaf margin (F is an enlargement of part of B). C - details of the primary veins (the enlargement of part A). D, E - showing details of the lower surface of the leaf cuticle. G - the enlargement of part of E, showing the polygonal areoles. 140 F. Liang et al. / Cretaceous Research 84 (2018) 134e140

Nelumbo jiayinensis sp. nov. has similar features with both two Gabrielyan, I., Bruch, A., Alimohammadian, H., Sabouri, J., Scharrer, S., 2012. A New extent species, like the orbicular leaves, entire margins and a strong Finding of Nelumbo protospeciosa Sap. From the Upper of Tabriz, NW Iran, and Its Palaeoecological Consequence. In: NECLIME Symposium Abstract. centered petiole, which could indicate that it also lived in slowly Gandolfo, M.A., Cuneo, R.N., 2005. Fossil Nelumbonaceae from the La Colonia For- flowing streams, river margins, lakes or swamps. In terms of sedi- mation (Campanian-Maastrichtian, Upper Cretaceous), Chubut, Patagonia, e ments, the Yong'ancun Formation, from which our specimens were Argentina. Review of Palaeobotany and Palynology 133, 169 178. Guo, S.X., 1979. Late Cretaceous and Early Tertiary Floras from the Southern collected, was interpreted to have been deposited in an alluvial- Guangdong and Guangxi with Their Stratigraphic Significance. Institute of lacustrine environment (Bureau of Geology and Mineral Vertebrate Paleontology and Paleoanthropology, Nanjing Institute of Geology Resources of Heilongjiang Province, 1993; Sun et al., 2011, 2014, and Palaeontology, Academia Sinica. In: Mesozoic and Cenozoic red beds of South China. Science Press, Beijing, pp. 223e231 pls. 1e3 (in Chinese). 2016). In terms of associated fossil plants, palynological assem- He, X., Shen, R., Jin, J., 2010. A new species of Nelumbo from South China and its blages in the lower part of Yong'ancun Formation are dominated by palaeoecological implications. Review of Palaeobotany and Palynology 162, fern spores and gymnosperm pollen with only a minor angiosper- 159e167. Hickey, L.J., Wolfe, J.A., 1975. The bases of angiosperm phylogeny: vegetative mous component. Combined with megafossil elements, morphology. Annals of the Missouri Botanical Garden 62, 538e589. including Asplenium dicksonianum Heer, Cladophlebis sp., Meta- Hollick, A., 1894. A new fossil Nelumbo from the Laramie Group at Florence, Colo. sequoia disticha (Heer) Miki, Sequoia sp., Taxodium sp., Cupressino- Bulletin of the Torrey Botanical Club 21, 307e310. fl cladus sp., Ginkgo adiantoides (Ung.) Heer, Cupressinocladus Johnson, K.R., 2002. Mega ora of the Hell Creek and lower Fort Union Formations in the western Dakotas: vegetational response to climate change, the Cretaceous- sveshnikovae Ablajev, Parataxodium sp., Trochodendroides arctica Tertiary boundary event, and rapid marine transgression. Geological Society of (Heer) Berry, Platanus sp., Quereuxia angulata (Newb.) Krysht., America Special Paper 361, 329e391. fl Dalembia jiayinensis Sun et Golovneva, Cobbania corrugata (Lesq.) Knowlton, F.H., 1930. The ora of the Denver and associated formations of Colorado. U. S. Geological Survy Professional Paper 155, 1e142. Stockey et al., Nyssidium arcticum etc., this suggests that in the Kuprianova, L.A., Tarasevich, V.F., 1983. Pollen morphology of recent and fossil Jiayin area during the Santonian mixed coniferous and deciduous species of the genus Nelumbo(Nelumbonaceae). Botanicheskii Zhurnal 68, e broad leaved angiosperm forests (Sun et al., 2007, 2011, 2014, 2016; 137 146 (in Russian with an English summary). Li, Y., Smith, T., Svetlana, P., Yang, J., Jin, J.H., Li, C.S., 2014. Paleobiogeography of the Markevich et al., 2011; Liang et al., 2015a; Liang and Sun, 2015b) plant (Nelumbonaceae: Nelumbo) and its bearing on the paleoclimatic existed around a fluviolacustrine environment under a warm changes. Palaeogeography, Palaeoclimatology, Palaeoecology 399, 284e293. temperate seasonal climate. Li, H.M., Chen, Q.S., 2002. Palibinia from the Eocene of Jiangxi, Chinadwith remarks on the climate mechanism of northern hemisphere in . Acta Palae- ontologica Sinica 41 (1), 119e129 in Chinese with English abstract. Liang, F., Zhang, S.Q., Markevich, V., Bugdaeva, E., Sun, G., 2015a. New data on 5. Conclusions palynology of lower part of Yongancun Formation (Upper Cretaceous) in Jiayin of Heilongjiang, Zeya-Bureya Basin, China. Pacific Geology 34 (3), 1e9. The new species Nelumbo jiayinensis sp. nov. from the upper Liang, F., Sun, G., 2015b. A new discovery of aquatic angiosperm Cobbania (Lesq.) Stockey et al. from Upper Cretaceous Yong'ancun Formation in Jiayin of Hei- Yong'ancun Formation (Santonian) broadens the geographical and longjiang, China. Global Geology (In Chinese Edition) 34 (1), 1e6. stratigraphic ranges of the genus Nelumbo. The new species is the Markevich, V., Bugdaeva, E., Ashraf, A.R., Sun, G., 2011. Boundary of Cretaceous and earliest known in age, and the most northern in occurrence for this Paleogene continental deposits in Zeya-Bureya Basin, Amur (Heilongjiang) e genus in China in paleophytogeography. River region. Global Geology 14 (3), 144 159. Matsuo, H., 1954. Discovery of Nelumbo from theAsuwa flora (Upper Cretaceous) in Fukui prefecture in the inner side of central Japan. In: Transactions and Pro- ceedings of the Palaeontological Society of Japan, New Series. 14, pp. 155e158. Acknowledgments Ni, X.M., Zhou, Y.J., Yu, B., Zhao, J.R., 1995. On the geographical distribution of the Nymphaelaes. Journal Wuhan Botany Research 13 (2), 137e146. e The authors thank to the financial supports of the Projects of Nicolson, D.H., 1991. Proposals (1002 1003) to reject two 1788 Thomas Walter names of American waterlilies (). Taxon 40 (3), 509e516. China No.2015FY310100 and No. DD20160120-04, and the NSFC Parkinson, C.L., Adams, K.L., Palmer, J.D., 1999. Multigene analyses identify the three No.41602015. Thanks are extended to Chinese colleagues W.H Wu, earliest lineages of extant flowering plants. Current Biology 9, 1485e1488. F. Chen, Y.G. Yang, and P. Yu for their help in the field work in Jiayin. Quan, C., Sun, G., 2008. Late Cretaceous Aquatic Angiosperms from Jiayin, Hei- longjiang, Northeast China. Acta Geologica Sinica-English Edition 82, 1133e1140. Moreover, we are sincerely grateful to anonymous reviewers for Sun, G., Dilcher, D.L., Zheng, S., Zhou, Z., 1998. In search of the first flower: a their helpful comments during review of the manuscript. Special angiosperm, Archaefructus, from northeast China. Science 282, 1692e1695. thanks to Prof. B.A. Spicer (UK) to the help in linguistic revision. Sun, G., Ji, Q., Dilcher, D.L., Zheng, S., Nixon, K.C., Wang, X., 2002. Archaefructaceae, a new basal angiosperm family. Science 296, 899e904. Sun, G., Akhmetiev, M.A., Golovneva, L., Bugdaeva, E., Quan, C., Kodrul, T., Nishida, H., Sun, Y., Sun, C., Johnson, K., Dilcher, D., 2007. Late Cretaceous Plants References from Jiayin along Heilongjiang River, Northeast China. CFS Courier For- schungsinstitut Senckenberg 258, 75e83. Berry, E.W., 1911. Systematic paleontology, Lower Cretaceous: fossil plants. In: Sun, G., Akhmetiev, M., Markevich, V., Ashraf, A.R., Bugdaeva, E., Godefroit, P., Clark, W.B. (Ed.), Lower Cretaceous. Maryland Geological Survey, Baltimore, Bolotsky, Yu, Dong, Z.M., Golovneva, L., Yang, H.X., Sun, C.L., Sun, Y.W., Quan, C., pp. 214e508. Kodrul, T., Kezina, T., Johnson, K., Nishida, H., Dilcher, D.L., Harding, I., Chen, Y.J., Bureau of Geology and Mineral Resources of Heilongjiang Province, 1993. Regional 2011. Late Cretaceous biota and Cretaceous-Paleogene (K-Pg) boundary in Jiayin Geology of Heilongjiang Province. Geol. Publ. House, Beijing (in Chinese with of Heilongjiang, China. Global Geology 14 (3), 115e143. English abstract). Sun, G., Dong, Z.M., Akhmetiev, M., Markevich, V., Ashraf, A.R., Godefroit, P., Crabtree, D.R., 1987. Angiosperms of the Northern Rocky Mountains: Albian to Dilcher, D.L., Sun, C.L., Sun, Y.W., Quan, C., Golovneva, L., Bugdaeva, E., Campanian (Cretaceous) megafossil floras. Annals of the Missouri Botanical Bolotsky, Yu, Suzuki, S., Kodrul, T., Nishida, H., Kezina, T., Harding, I., Yang, H.X., Garden 74, 707e747. Ge, W.C., Chen, Y.J., Yang, T., 2014. Late Cretaceous-Paleocene Biota and the K-Pg Dilcher, D.L., Sun, G., Ji, Q., Li, H., 2007. An early infructescence Hyrcantha decussata Boundary from Jiayin of Heilongjiang, China with Discussion on the Extinction (comb. nov.) from the Yixian Formation in northeastern China. Proceedings of of Dinosaurs. Shanghai Sci. Techn. Educ. Publishing House, Shanghai. the National Academy of Sciences 104, 9370e9374. Sun, G., Golovneva, L., Alekseev, P., Liang, F., Yang, T., 2016. New species Dalembia Dong, Z.M., Zhou, Z.L., Wu, Y., 2003. Note on a hadrosaur footprint from Hei- jiayinensis (Magnoliopsida) from the Upper Cretaceous Yong'ancun Formation, longjiang River area of China. Vertebrata Pal Asiatica 41 (4), 324e326. Heilongjiang, northern China. Cretaceous Research 67, 8e15. Ellis, B., Daly, D.C., Hickey, L.J., Mitchell, J.V., Johnson, K.R., Wilf, P., Wing, S.L., 2009. Tao, J.R., 2000. The Evolution of the Late CretaceouseCenozoic Floras in China. Manual of Leaf Architecture. Cornell University Press, New York. Science Press, Beijing. Erickson, B.R., 1991. Flora and fauna of the Wannagan Creek Quarry: Late Paleocene Upchurch, G.R., Crane, P.R., Drinnan, A.N., 1994. The megaflora from the Quantico of . Scientific Publications of the Science Museum of Minnesota 7, locality (Upper Albian), Lower Cretaceous Potomac Group of Virginia. Virginia 1e19. Museum of Natural History Memoir 4, 1e57. Estrada-Ruiz, E., Upchurch, G.R., Wolfe, J.A., Cevallos-Ferriz, S.R.S., 2011. Compara- Xue, J.-H., Dong, W.-P., Cheng, T., Zhou, S.-L., 2012. Nelumbonaceae: Systematic tive Morphology of Fossil and Extant Leaves of Nelumbonaceae, Including a position and species diversification revealed by the complete chloroplast New Genus from the Late Cretaceous of Western North America. Systematic genome. Journal of Systematics and Evolution 50, 477e487. Botany 36, 337e351.