Equisetum Cf. Pratense (Equisetaceae) from the Miocene of Yunnan in Southwestern China and Its Paleoecological Implications Author(S): Yu‐Ling Zhang, David K

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Equisetum cf. pratense (Equisetaceae) from the Miocene of Yunnan in Southwestern China and Its Paleoecological Implications Author(s): Yu‐Ling Zhang, David K. Ferguson, Albert G. Ablaev, Yu‐Fei Wang, Cheng‐Sen Li, and Lei Xie Source: International Journal of Plant Sciences, Vol. 168, No. 3 (March/April 2007), pp. 351- 359 Published by: The University of Chicago Press Stable URL: http://www.jstor.org/stable/10.1086/510411 . Accessed: 02/04/2015 03:52

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This content downloaded from 159.226.100.224 on Thu, 2 Apr 2015 03:52:13 AM All use subject to JSTOR Terms and Conditions Int. J. Plant Sci. 168(3):351–359. 2007. Ó 2007 by The University of Chicago. All rights reserved. 1058-5893/2007/16803-0009$15.00

EQUISETUM CF. PRATENSE (EQUISETACEAE) FROM THE MIOCENE OF YUNNAN IN SOUTHWESTERN CHINA AND ITS PALEOECOLOGICAL IMPLICATIONS

Yu-Ling Zhang,*,y David K. Ferguson,z Albert G. Ablaev,§ Yu-Fei Wang,1,* Cheng-Sen Li,* and Lei Xie*

*State Key Laboratory of Systematic and Evolutionary Botany, Institute of Botany, Chinese Academy of Sciences, 20 Nan Xin Cun, Xiangshan, Beijing 100093, People’s Republic of China; yGraduate University, Chinese Academy of Sciences, Beijing 100039, People’s Republic of China; zDepartment of Paleontology, University of Vienna, Althanstrasse 14, A-1090 Vienna, Austria; and §Paciﬁc Oceanological Institute, Russian Academy of Sciences, Vladivostok 600041, Russia

Rhizomes with tubers of Equisetum cf. pratense Ehrhart are described for the ﬁrst time from the late Miocene of Lu¨ he, Yunnan Province, southwestern China. The rhizomes consist of distinct nodes and internodes. The nodes bear one to four bunches of tubers (two to four tubers per bunch). The tubers are elliptical, rounded, ovate, or spindle shaped, and the most distal is mucronate. The occurrence of E. cf. pratense would indicate a wet habitat, and the presence of rhizomes with tubers implies that burial occurred during the late fall or winter, assuming that the fossil and its nearest living relative have similar climatic tolerances and phenology. These ﬁnds, combined with the presence of thermophilous genera Cyclobalanopsis, Castanopsis, and Liquidambar and hygrophilous elements Alnus and Taxodioxylon, indicate a warm and humid subtropical climate at Lu¨ he in the Miocene.

Keywords: China, Equisetum, Miocene, paleoecology, paleophenology, tubers.

Introduction (2004) suggested that E. bogotense is basal within the genus, and all other members of subgenus Equisetum and all species The genus Equisetum L. (horsetails), the sole living repre- of subgenus Hippochaete group into two major sister clades sentative of the class Sphenopsida, contains 15 species with based on the chloroplast rps4 gene and adjacent noncoding herbaceous habit. It has a nearly worldwide distribution ex- sequences. cept for Australia and New Zealand and is commonly associ- Equisetum-like remains preserved as stems, leaves, cones, ated with wet places (Hauke 1993; Kenrick and Crane 1997; rhizomes, and tubers are common in the sediments of the Nor- Page 1997). Equisetum has been considered to be the sister thern Hemisphere from the Carboniferous to the Pleistocene group to all ferns (Kenrick and Crane 1997), the sister group (Brown 1975; McIver and Basinger 1989). Equisetum bryanii to leptosporangiate ferns (Duff and Nickrent 1999), or the Gould with well-preserved stems and leaves, reported from sister group to Marattiopsida (Pryer et al. 2001). the Jurassic of southeastern Queensland, is regarded as the The genus Equisetum is divided into two subgenera: Equi- earliest member of subgenus Equisetum (Gould 1968), while setum L. and Hippochaete Milde (Hauke 1963, 1974, 1978, Equisetum clarnoi Brown, with silicified stem fragments and 1983, 1993; Page 1972; Gifford and Foster 1989; Zhang numerous small roots, found in the Eocene of Oregon, repre- 2004). Subgenus Equisetum comprises eight species that are sents the first conclusive report of subgenus Hippochaete annual, with superficial stomata, regularly branched stems, (Brown 1975). and obtuse cones. Subgenus Hippochaete consists of seven The tuberous rhizomes of Equisetum have been found species that are usually perennial, with sunken stomata, un- in North America in the Cenomanian (upper Cretaceous) branched stems, and apiculate cones (Hauke 1963, 1974, Dakota Formation of Kansas (Skog and Dilcher 1994) and 1978, 1983, 1993). Rhizomes with tubers are common to most the St. Mary River Formation and Edmonton Formation of species of subgenus Equisetum but are never found in subgenus Alberta (Bell 1949), in the Paleocene Ravenscrag Formation Hippochaete (Thome´ 1885; Campbell 1928; Mehra and Bir of Saskatchewan (McIver and Basinger 1989) and the Smoky 1959; Hauke 1963, 1974, 1978; Bir 1978; Watson and Batten Tower Locality (Christophel 1976), and in the Eocene (Lamotte 1990; Doll 2001). 1952) of Barrell’s Springs and Carbon Station of Wyoming Recent molecular studies support the treatment of two (Lesquereux 1878), as well as in the Oligocene to Miocene subgenera within the genus Equisetum in general (Marais Beaverhead Basins in southwestern Montana (Becker 1969). et al. 2003; Guillon 2004). Marais et al. (2003) identified In Europe they have been discovered in early Cretaceous two monophyletic clades corresponding to the two subgenera (Berriasian) Wealden assemblages from England and Germany (except Equisetum bogotense Kunth) based on a combined (Watson and Batten 1990) and Miocene floras of Iceland (Denk analysis of two chloroplast markers, rbcL and trnL-F.Guillon et al. 2005). In Asia they are known from the Jurassic (Bajocian to Bathonian) Utano Formation of Ochi Shimizu-mura and 1 Author for correspondence; e-mail [email protected]. Shimonoseki, Japan (Kon’no 1962); the early Cretaceous of Manuscript received April 2006; revised manuscript received September 2006. China in the Yixian Formation, Beipiao, Liaoning (Wu 1999;

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Fig. 1 Map of China indicating the Lu¨ he locality of Yunnan.

Sun et al. 2001, pp. 70–71; Zhou et al. 2003), the Muling The fossil tubers (33 specimens) and rhizomes with tubers (13 Formation of Jixi Basin, Heilongjiang (Yang 2003), Fuxin For- specimens) of Equisetum are preserved as impressions. They are mation in Liaoning (Chen et al. 1988, pp. 31–32), Huolinghe housed in the National Museum of Plant History of China, Formation, Damoguaihe Formation, and Yinmin Formation Institute of Botany, Chinese Academy of Sciences, Xiangshan, in Inner Mongolia (Deng 1995, pp. 11–14; Deng et al. 1997, Beijing. The morphology was revealed using the degagement pp. 18–20); the middle Eocene (Ablaev et al. 2003) Hunchun technique and was observed under a stereomicroscope. Formation, Jilin in China (Guo 2000); and the Miocene Lawula The herbarium sheets that we examined originated from Formation of Markam and Wulong Formation of Nanmulin PE, Institute of Botany, Chinese Academy of Sciences; For- in Tibet (Xizang) (Geng and Tao 1982; Tao and Du 1987). estry Herbarium of Beijing Forestry University; and ﬁeld col- In this article, we describe fossil specimens preserved as lections by Yu-Ling Zhang. The habitat and phenology of rhizomes with tubers from a new Miocene locality, Lu¨ he in Equisetum pratense Ehrhart in Songshan Mountain (40°309N, Yunnan, southwestern China, and assign them to Equisetum 115°489E), Beijing, were observed and recorded. cf. pratense Ehrhart. The paleoenvironments of Lu¨he, Yunnan Province, are interpreted using the combined data of sporo- morphs, fossil wood, and other macrofossils. Systematic Description

Class—Sphenophytina Material and Methods Order—Equisetales

The fossils described here were all collected from the Lu¨ he Family—Equisetaceae lignite mine (25°79–109N, 101°189–229E) of Chuxiong Yi Au- Genus—Equisetum Linnaeus 1753 tonomous Prefecture, Yunnan Province, southwestern China (fig. 1). They were embedded in a gray sandy underclay im- Subgenus—Equisetum 1887 mediately below the lower part of brown coal layer K5, Species—Equisetum cf. pratense Ehrhart 1784 Shigucun beds, Xiaolongtan Formation (BGMRYP 1996; and the 1962 geological report from Geological Team 11 of Description Yunnan Province [GTYN]). The age of the Xiaolongtan For- Rhizomes have distinct nodes (fig. 2A,2H–2J, see arrows a mation is Miocene, based on lithostratigraphic grounds in fig. 2; fig. 3) and internodes (fig. 2I, arrow b). Internodes (BGMRYP 1996). Unfortunately, we lack more precise radio- are 6–10 mm wide and at least 7 cm long, with six to eight metric dating for this. longitudinal ribs on their surface (three to four on each side;

Fig. 2 Equisetum cf. pratense. A, Specimen LH1401. B, Specimen LH1511. C, Specimen LH1603. D, Specimen LH1605. E, Specimen LH1405. F, Specimen LH1510. G, Specimen LH1508. H, Specimen LH1411. I, Specimen LH1413. J, Specimen LH1407. a ¼ node; b ¼ internode. Scale bar ¼ 1 cm.

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Fig. 3 Reconstruction of Equisetum cf. pratense. A, Specimen LH1401. B, Specimen LH1411. C, Specimen LH1407. Scale bar ¼ 1 cm.

fig. 2I, arrow b). Each rhizome node bears one to four and bunches of two to four tubers attached to the nodes of the bunches of tubers (fig. 2A,2J; fig. 3). Each bunch comprises rhizomes, are found only in the genus Equisetum. two to four tubers (fig. 2A–2H,2J; fig. 3). Of the 46 speci- Tubers are common in all species of the subgenus Equise- mens with tubers, 55% had two tubers per bunch (figs. 2A, tum (E. arvense L., E. diffusum Don, E. palustre L., E. 3A), 33% had three (fig. 2F), and 12% had four (fig. 2G, pratense Ehrhart, E. sylvaticum L., E. telmateia Ehrhart), ex- 2H; fig. 3B). The tubers are elliptical (figs. 2H,3B), ovate cept E. bogotense Kunth and E. fluviatile L. (Thome´ 1885; (fig. 2D), nearly round (fig. 2F), or spindle shaped (fig. 2E); Campbell 1928; Mehra and Bir 1959; Bir 1978; Hauke most (61%) are elliptical, while ovate, subrounded, and spin- 1978; Doll 2001). On the other hand, tubers are never found dly ones account for 21%, 11%, and 7%, respectively. The in the subgenus Hippochaete (seven species: E. giganteum L., shape of the tubers in a bunch varies from ovate to nearly E. hyemale L., E. laevigatum Brown, E. myriochaetum Desf., round (fig. 2A–2H,2J; fig. 3). The apices of the tubers at the E. ramosissimum Desf., E. scirpoides Miche, E. variegatum tip of the bunch are mucronate (fig. 2A,2C,2D,2H; fig. 3A, Schleich) (Hauke 1963, 1978; Watson and Batten 1990). 3B). The average size of the tubers is 12.8 mm (6–21 mm) Two or more tubers per bunch are recorded only in E. long and 8.0 mm (5–12 mm) wide; the length to width ratio pratense (fig. 4; fig. 6B,6C; Thome´ 1885; ), while only a sin- is 1 to 2.7. Some ridges are found on the surface of the tubers gle tuber per bunch is found in the other five tuberous species (fig. 2A,2B; fig. 3A). of subgenus Equisetum (table 1). Bir (1978) indicated that the tubers of E. palustre and E. sylvaticum are similar to those Specimens Examined of E. arvense and E. telmateia, so we assume they also have a single tuber. National Museum of Plant History of China, Institute of The unique morphological features of fossil rhizomes with Botany, Chinese Academy of Sciences: LH1401 (figs. 2A, two to four tubers per bunch are the same as those of 3A), LH1402–LH1404, LH1405 (fig. 2E), LH1406, LH1407 E. pratense (figs. 2–4; table 1). Some ridges occurred on the (figs. 2J,3C), LH1408–LH1410, LH1411 (figs. 2H,3B), surface of the fossil tubers; this might be caused by shrink- LH1412, LH1413 (fig. 2I), LH1404, LH1501–LH1507, age during fossilization. Based on the similarity of the fossil LH1508 (fig. 2G), LH1509, LH1510 (fig. 2F), LH1511 specimens to E. pratense, we assigned these specimens to (fig. 2B), LH1512–LH1515, LH1601, LH1602, LH1603 E. cf. pratense. (fig. 2C), LH1604, LH1605 (fig. 2D), LH1606–LH1617. Comparison with Equisetum-Like Fossils Discussion Fourteen Equisetum-like fossil species were recorded as having rhizomes with tubers. Five of them bear rhizomes Comparison with Extant Species of Equisetum with bunches of tubers (table 2): E. haydenii Lesquereux The fossil specimens were preserved as rhizomes with tu- from the Eocene of Wyoming (Lesquereux 1878; Lamotte bers. Such rhizomes, with distinct nodes and ribbed internodes 1952); E. perlaevigatum Cockerell from late Cretaceous

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assemblages of St. Mary River and Edmonton Formations, western Alberta (Bell 1949); E.cf.arcticum Heer from Oligo- cene to Miocene floras of Montana (Becker 1969); E. hunchunense Guo (Guo 2000) from middle Eocene floras of Hunchun, Jilin, northeastern China (Ablaev et al. 2003); and Equisetites longevaginatus Wu (Sun et al. 2001, pp. 70–71) from early Cretaceous Yixian Formation, Beipiao, Liaoning Province, northeastern China (Zhou et al. 2003). Others have rhizomes with only a single tuber per bunch. Equisetum cf. pratense from Lu¨ he differs from E. haydenii in having inflated articulations of rhizome and unbranched tubers (figs. 2, 3), while E. haydenii has constricted articulations and two tubers ‘‘being attached to the inflated end of a single one’’ (fig. 5C; Lesquereux 1878, pp. 67–69, pl. VI). Equisetum cf. pratense differs from E. cf. arcticum Heer (Becker 1969) and E. hunchunense (Guo 2000) in having single or acervate tubers (fig. 2A,2H,2J), while the latter two have whorled tubers on the rhizome (fig. 5A,5B). Although E. perlaevigatum (Bell 1949) and Equisetites longevaginatus Wu (Sun et al. 2001, pp. 70–71) are described as having chains of tubers, the illustrations Bell (1949) and Sun et al. (2001) provide show only a single tuber (table 2). Those Miocene Equisetum sp. with bunches of tubers recorded from Lawula Formation of Markam and Wulong Formation of Nanmulin in Tibet (fig. 5D; Tao and Du 1987) and Ice- land (fig. 5E; Denk et al. 2005) may also be treated as E. cf. pratense based on their morphological features.

Paleoenvironments The palynological assemblage from the Miocene of Lu¨ he (angiosperms ca. 90%, gymnosperms 9%, and pteridophyta 1%) indicates an evergreen and deciduous broad-leaved for- Fig. 4 Tuberous rhizomes of Equisetum pratense (modiﬁed from est with subtropical elements (Cyclobalanopsis, Castanopsis, Thome´ 1885). Scale bar ¼ 1 cm. Davidia, Palmae) in the lower zone and warm temperate elements (Alnus, Betula, Carpinus, Quercus) in the upper zone

Fig. 5 Equisetum fossils with a chain of tubers. A, E. cf. arcticum. B, E. hunchunense.C,E. haydenii.D,Equisetum sp. from Markam, Tibet. E, Equisetum sp. from Iceland. Scale bar ¼ 1 cm.

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Fig. 6 Equisetum pratense in Songshan Mountain, Beijing. A, Habitat, June 26, 2005. B, Rhizomes with tubers (arrow), collected October 15, 2005. C, Enlargement of B (area indicated by arrow), showing two tubers in series. Scale bar ¼ 1 cm.

(Xu et al. 2000; Xu 2002). The Miocene climate in Lu¨ he is The depositional environment in the Lu¨ he lignite mine is delimited as subtropical based on the nature of the lower- lacustrine (BGMRYP 1996 and the 1962 report from the most vegetational zone. Alnus, as an indictor of a humid GTYN). Equisetum cf. pratense, together with other hy- habitat, yielded nearly half of the pollen grains (Xu et al. grophilous plants, indicates a generally humid climate and 2000). Besides, Taxodioxylon (Yi et al. 2003) and Sequoia environment in this region rather than locally wet habitats (Ma et al. 2000, 2005) found at the same locality denote a (e.g., streambanks) within an arid region. warm and humid environment. Equisetum pratense is mainly distributed in countries Paleophenology such as the United States, Canada, Ireland, Britain, Germany, Tubers of Equisetum formed from the lateral buds on the Belgium, France, Switzerland, Austria, Italy, Czech Republic rhizomes are asexual reproductive organs that appear in late and Slovakia, Hungary, Iceland, Norway, Sweden, Finland, fall or winter when its aerial stems die down (Watson and Russia, China, Korea, and Japan (ﬁg. 7; Tutin and Valentine Batten 1990; Sakamaki and Ino 2004). The accumulation of 1964; Hauke 1993; Page 1997; Thompson 1997). In China, starch in the rhizomes enables the tubers to form. Rhizomes it can be found in provinces such as Heilongjiang, Jilin, Inner with low starch concentrations cannot form tubers, so a large Mongolia, Hebei, Shanxi, Xinjiang, Shandong, at an altitude mass of tubers means that the individuals had a surplus of of 500–2800 m (Zhang 2004). The habitat of E. pratense is stored energy with which to produce new shoots (Sakamaki semishade or sun in moist woods or meadows (ﬁg. 6A;Hauke and Ino 2004). If the fossil and its nearest living relative have 1993). If the climatic tolerances documented here for extant similar climatic tolerances and phenology, the presence of E. pratense are extrapolated to E. cf. pratense, it should indi- rhizomes with tubers of E. cf. pratense would imply that fos- cate very wet surroundings in Lu¨ he during the Miocene. silization happened during the late fall or winter.

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Table 1 Morphological Comparisons between Fossil Equisetum from Lu¨he and Extant Tuberous Equisetum Species Tuberous Equisetum species Fossil Equisetum from Lu¨ he E. arvense E. diffusum E. palustre E. pratense E. sylvaticum E. telmateia Tubers: Arrangement Single to acervate Single to acervate Single Single Single to acervate Acervate Acervate Number of tubers per bunch 2–4 1 1 1 (?) 2–3 1 (?) 1 Shape Elliptical, ovate, Elliptical, round Elliptical Elliptical, round Round, ovate This content downloadedfrom 159.226.100.224 onThu,2Apr 201503:52:13AM round, spindle ...... Length (cm) .6–2.1 1.3–1.4 1.1–1.2 ... .5–1.4 ... .9–1.3 Width (mm) 5–12 11–13 8–9 ... 5–9 ... 8–10 Rhizome: Internode length (cm) 7.5 3.2, 10–12 ? ... 1.9–5.8 ... 3.5 Internode width (mm) 5–10 3–5 3 ... 3–5 ... 8 All usesubject toJSTORTerms andConditions Articulations Inflated Inflated Inflated ... Inflated ... Inflated Age Miocene Extant Extant Extant Extant Extant Extant Reference This article Hauke 1978; Doll 2001 Mehra and Bir 1959; Bir 1978 Thome´ 1885 Bir 1978 Campbell 1928; Bir 1978 Hauke 1978

Table 2 Morphological Comparisons between Equisetum cf. pratense and Tuberous Equisetum-Like Fossils Equisetites E. cf. pratense E. haydenii E. perlaevigatum E. cf. arcticum E. hunchunense E. sp. E. sp. longevaginatus Tubers: Arrangement Single to acervate Opposite Opposite Whorled Whorled Acervate ? Single or opposite Number of tubers per bunch 2–4 2 2 2–3 2–3 2–5 3 2–3 Shape Elliptical, ovate, Ovate Cylindrical Elongate, ovate, Elliptical, ovate Elliptical, round Elliptical Elliptical, round round, spindle round Length (cm) .6–2.1 1.3–2.1 3 1.5–2.5 1–2 1.5–2 1–1.2 .5–.8 Width (mm) 5–12 10–15 13 5–7 4–9 7–20 6–8 3–5 Rhizome: Internode length (cm) 7.5 ? 10 14 8 10 ? .4–.5 Internode width (mm) 5–10 20 30 7 5–8 7 ? 3–4 Articulations Inflated Constricted Constricted Inflated Inflated Inflated ? Inflated Locality Xiaolongtan Barrell’s Springs, St. Mary River Beaverhead Basins, Hunchun Formation, Lawula Formation, Iceland Yixian Formation, Formation, Lu¨ he, Carbon Station, Formation, Montana, USA Jilin, China Nanmulin, Beipiao, Liaoning, Yunnan, China Wyoming, USA Alberta, Canada Markam, Tibet China Age Miocene Eocene Late Cretaceous Oligocene to Miocene Eocene Miocene Miocene Cretaceous Reference This article Lesquereux 1878; Bell 1949 Becker 1969 Guo 2000; Ablaev Tao and Du Denk et al. Sun et al. 2001; Lamotte 1952 et al. 2003 1987 2005 Zhou et al. 2003 358 INTERNATIONAL JOURNAL OF PLANT SCIENCES

Fig. 7 Distribution of Equisetum pratense (circles) and fossils of E. cf. pratense (trefoils) in the world. The data of E. pratense come from the Flora of North America North of Mexico (Hauke 1993), Flora europaea (Tutin and Valentine 1964), New Flora of the British Isles (Thompson 1997), The Ferns of Britain and Ireland (Page 1997), Flora reipublicae popularis sinicae (Zhang 2004), Herbaceous Flora of Northeast China (IFSS 1958), Flora of Beijing (Yin 1992), Flora hebeiensis (CRFH 1986), Flora shanxiensis (CRFS 1992), Flora xinjiangensis (CRFX 1993), and Flora shandongensis (Chen 1990).

Acknowledgments stitut fu¨ rZu¨ chtungsforschung, Cologne, for his pictures and literature; Dr. Xian-Chun Zhang at PE, Institute of Botany, We thank Professor John McNeill, Rapporteur-Ge´ne´ral of Chinese Academy of Sciences, Beijing, and Dr. Jan J. Wo´jcicki, the Nomenclature Section of the International Botanical Con- Institute of Botany, Polish Academy of Sciences, Krako´ w, for gress, Director Emeritus of the Royal Ontario Museum, and providing related references; and Yin-Bao Sun for preparing Honorary Associate of the Royal Botanic Garden, Edinburgh, the illustrations. This research was supported by the projects and Professor Gerry Moore, Brooklyn Botanic Garden, New of the Natural Science Foundation of China (30470117, York, for their kind guidance on the citation of subgenus 30530050) and the National Basic Research Program of Equisetum. We thank Dr. Kurt Stu¨ ber from Max Planck In- China (2004CB720205).

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