Sci. Bull. (2015) 60(20):1768–1777 www.scibull.com DOI 10.1007/s11434-015-0870-4 www.springer.com/scp

Article Earth Sciences

Fossil of Euryale () indicate a lake or swamp environment in the late Miocene Zhaotong Basin of southwestern China

Yongjiang Huang • Xueping Ji • Tao Su • Li Wang • Chenglong Deng • Wenqi Li • Hongfen Luo • Zhekun Zhou

Received: 22 May 2015 / Accepted: 31 July 2015 / Published online: 25 August 2015 Ó Science China Press and Springer-Verlag Berlin Heidelberg 2015

Abstract Euryale (Nymphaeaceae) is a monotypic genus morphology and anatomy demonstrate that the newly distributed in eastern Asia, but fossils in its native distribu- described fossil species differs from modern and other fossil tion are sparse as compared to Europe where the genus has species of Euryale and thus verify the assignment to a new disappeared. Here, we describe a new fossil species, Euryale fossil species. As the modern Euryale is an aquatic , yunnanensis sp. nov., from the late Miocene Zhaotong Basin preferably living in swamps and lakes with shallow and in southwestern China on the basis of seed remains. Char- stable water, we hypothesize that a lake and/or swamp acteristics including an ellipsoidal to almost spherical shape, environment with shallow water was present near Shui- a smooth surface, a germination cap that covers the micro- tangba in the Zhaotong Basin, where the Shuitangba homi- pyle, the separation of the hilum and germination cap (mi- noid lived during the late Miocene. This inference is cropyle), elliptic testa surface cells with undulate margins generally consistent with paleoenvironmental data extracted and thickened cell walls collectively indicate a close affinity from avian, fish, frog, turtle and crocodile fossils, as well as with the genus Euryale in Nymphaeaceae. Comparisons of from aquatic . The fossil history suggests a compara- tively recent (Miocene) emergence of Euryale, which is roughly in agreement with the divergence time inferred from Y. Huang Á Z. Zhou (&) the molecular information. Key Laboratory for Plant Biodiversity and Biogeography of East Asia, Kunming Institute of Botany, Chinese Academy of Keywords Euryale Á Nymphaeaceae Á Aquatic Á Sciences, Kunming 650201, China e-mail: [email protected] Late Miocene Á Zhaotong Basin Á Southwestern China

X. Ji Yunnan Institute of Cultural Relics and Archaeology and 1 Introduction Research Center for Southeast Asian Archeology, Kunming 650118, China Euryale Salisb. is a monotypic genus in the water lily T. Su Á L. Wang Á Z. Zhou family Nymphaeaceae [1, 2]. It comprises Euryale ferox Key Laboratory of Tropical Forest Ecology, Xishuangbanna Salisb., which is known as foxnut or gorgon nut [3–5]. Tropical Botanical Garden, Chinese Academy of Sciences, Mengla 666303, China Euryale ferox is an aquatic plant, with floating or partially to entirely submerged [4, 5]. It lives preferably in C. Deng swamps and lakes with shallow and stable water but in a State Key Laboratory of Lithospheric Evolution, Institute of few cases occurs in somewhat deeper water environments Geology and Geophysics, Chinese Academy of Sciences, Beijing 100029, China [4]. Phytogeographically, E. ferox is native to eastern Asia, distributed from northeastern to China, and W. Li Japan, as well as the Far East of Russia [4, 5]. Zhaotong Institute of Cultural Relics, Zhaotong 657000, China Nymphaeaceae is a member of the ANITA, a well-known H. Luo basal grade in angiosperms [6]. Several genera of the family, Zhaoyang Museum, Zhaotong 657000, China both extinct and extant, have old fossil records [7–10]. Unlike 123 Sci. Bull. (2015) 60(20):1768–1777 1769 other living members in Nymphaeaceae with records from the known from Europe. Only three fossil records have been Paleogene, e.g., Nuphar [8]andNymphaea [7], Euryale, documented to date; they are E. ferox from the Pleistocene of however, seems to be a younger group. The molecular phy- Zhejiang, eastern China [22], E. akashiensis from the Plio- logenetic tree has revealed that Euryale emerged more cene of Japan [15] and an undetermined species (Euryale sp.) recently [2]. To be consistent, fossils of this genus are rela- from the Miocene of Hebei, northern China [23]. According tively young, extending only into the Miocene [11–23]. The to these accounts, the fossil distribution of Euryale shows a fossil occurrence of Euryale was discovered for the first time concentration in Eurasia (Fig. 1a). Most of its known fossils about a century ago from the Pleistocene of western Russia, are from Europe where the genus has become extinct, and Europe [11, 12]. Several other fossil occurrences were sub- they are comparatively rare in eastern Asia despite the sequently reported from the Neogene and Pleistocene of modern range of the genus there. Europe [13, 14, 16–21]. In North America, fossils possibly In this study, we describe a new fossil species of Euryale related to Euryale were represented only by the late Pale- from eastern Asia, based on seed entities from the late Miocene ocene seeds from North Dakota, USA [24]. However, the of Yunnan, southwestern China. The fossil seeds were studied Dakota seeds were thought to lack promising characters for a morphologically and anatomically, and were compared with credible placement in Euryale and were ultimately treated as the seeds of extant and other fossil species of Euryale.The an extinct genus named Susiea [24]. In eastern Asia, fossil paleoenvironmental implications of this new fossil discovery records of Euryale are relatively few as compared to those and the fossil history of this genus are discussed briefly.

Fig. 1 Modern distribution ranges and fossil records of Euryale (a), and the geographical location of the Shuitangba fossil site (b, c)

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2 Materials and methods resulting specimens were cleaned using an ultrasonic cleaner (KO-50M) at a frequency of 50 kHz for 30 s to 2.1 Fossil site, geological setting and geochronology remove clay particles adhering to the seed surface. Air- dried, the seeds were observed under a binocular micro- The Zhaotong Basin is located in northeastern Yunnan scope (Zeiss Stereo REO Discovery V20), and digital Province, southwestern China (Fig. 1b, c). It is one of the images were taken using a Zeiss camera (AxioCam HRc) fault-related basins of the late Neogene at the southeastern anchored on the Zeiss binocular microscope. The seed margin of the Qinghai-Tibetan Plateau [25, 26]. The basin surface, germination cap and seed coat transection were is filled with late Miocene to Pliocene lacustrine or studied using a scanning electron microscope (SEM; Zeiss swampy clays, silts, peaty clays and lignites [27, 28]. The EVOLS10). Modern seeds of Euryale, viz. E. ferox, were fossil site known as Shuitangba, from which our fossil examined following the same procedures as for the fossil seeds were unearthed, lies in an open-pit lignite mine seeds except that an observation with the SEM was not located at Shuitangba village in the basin (27°1904400N, performed. The studied fossil specimens are deposited 103°4401500E; Fig. 1c). An outcrop section at the mine primarily at the Herbarium of Kunming Institute of Botany, is *16 m thick, composed of seven sedimentary layers Chinese Academy of Sciences, and partly at the Zhaoyang [29]. The upper part of the black peaty clay layer is Museum. bracketed by the middle and lower lignite layers (Table 1). This part has produced the famous Shuitangba hominoid (Lufengpithecus cf. lufengensis) and large amounts of other 3 Results mammal fossils such as beaver (Sinocastor sp.), hamster (Kowalskia sp.) and flying squirrel (Pliopetaurista sp.) 3.1 Systematics [27, 30], as well as avian remains [28]. The coexistence of the mammalian species points to the East Asian Baodean Family: Nymphaeaceae Salisb., 1805. Stage/Age with a time span of 7.2–5.3 Ma [27]. Moreover, Genus: Euryale Salisb., 1805. the black peaty clay layer was considered to be located Species: Euryale yunnanensis Y. Huang & Z. Zhou sp. near the C3An.1r–C3An.1n transition [27, 30], which was nov. estimated to be *6.2 Ma based on the Astronomically Etymology: The specific Latin epithet yunnanensis is Tuned Neogene Time Scale of Hilgen et al. [31]. There- chosen in reference to Yunnan Province where the fossil fore, the fossiliferous peaty clay layer can be unambigu- site is located. ously assigned to the late Miocene evidenced by both Holotype: STB 028 (Fig. 2a) here designated. biostratigraphic and magnetostratigraphic data. Paratypes: STB 029–STB 048. Materials: More than 500 seeds that are anatomically 2.2 Fossil materials and examinations preserved but largely compressed. Type locality: Shuitangba village in the Zhaotong Basin Recent field work has shown that the black peaty clay layer of northeastern Yunnan Province, southwestern China. at the Shuitangba fossil site also bears plant fossils, of Age: Late Miocene. which seed remains are the most abundant. More than 500 Repository: About 400 fossil specimens are kept at the anatomically preserved seeds of Euryale were collected Herbarium of Kunming Institute of Botany, Chinese from this layer successively during 2013–2015. The

Table 1 Lithological facies of the late Miocene Shuitangba section after Chang et al. [29] Bed number Lithology Depth interval (m)

Overlying strata: cultivated soil 1 Gray or yellowish-gray clays 0–2.7 2 Gray clayey silts 2.7–5.4 3 Gravels 5.4–5.9 4 Clayey silts containing a large number of fossil shellfish 5.9–6.4 5 Middle lignite layer 6.4–7.6 6 Black peaty clay containing animal and plant fossils 7.6–12.3 7 Lower lignite layer 12.3–16 Underlying strata: lignite

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Fig. 2 General view of Euryale yunnanensis sp. nov. seeds. a STB 028. b STB 029. c STB 030. d STB 031. e STB 032. f STB 033. g STB 034. h STB 035. i STB 036. j STB 037. k STB 038. l STB 039. Scale bar 2mm

Academy of Sciences; more than 100 fossil specimens circular in outline; seed coat relatively thin; and the pal- are housed at the Zhaoyang Museum. isade structure in the outer layer of the seed coat only weakly developed. 3.2 Specific diagnosis 3.3 Description Seeds elliptic or ellipsoidal in shape, and relatively small as compared to the previously reported fossil seeds; raphe Seeds are mostly compressed, elliptic in outline (for those ridge near the hilum area not prominent; germination cap compressed) and ellipsoidal in shape (for those uncompressed)

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(Fig. 2). They are 5–8 mm long and 4–6 mm broad, with a the hilum area but thinner in the ventral part. The outer layer of length and breadth ratio of 1.1–1.4 (100 measurements). The the seed coat has a weakly developed palisade structure, while dorsal (basal) part is roundly inflated, and the ventral (apical) the rest contains numerous small, irregular cavities as revealed part is slightly narrowed (Fig. 2). The seed surface is smooth from its transection (Fig. 4g, h). (Fig. 2), and cells on the seed surface are elliptic and arranged in a reticulate pattern. The raphe ridge near the hilum area is not prominent (Fig. 3). The hilar scar is circular to elliptic in outline 4 Discussion and a little raised (Fig. 3). The germination cap that covers the micropyle is circular and measures 0.7–0.9 mm in diameter 4.1 Comparisons and taxonomic treatment (Figs. 3a–c, e, 4b, d). The hilum and germination cap (or micropyle) are positioned separately (Fig. 3).Locatedinthe The family Nymphaeaceae is generally accepted to be center of the cap is a small protuberance (Figs. 3a–c, e, 4b, d). divided into six genera, namely Barclaya, Euryale, Cells on the cap surface are elliptic and arranged in a reticulate Nuphar, Nymphaea, Ondinea and [1, 2, 32]. pattern (Fig. 4e). The interior face of the seed coat bears no Although this intrafamilial classification has been debated notable sculpture, and no surface cell can be observed (Fig. 4f). particularly based on molecular phylogenetic data [33–37], The seed coat is 0.2–0.4 mm thick (Fig. 4g); it is thicker near it correlates well with seed morphology [7, 8].

Fig. 3 Apical view of Euryale yunnanensis sp. nov. seeds. a–c, e Hilum (arrowed) and germination cap that are positioned separately. a STB 028. b STB 040. c STB 041. e STB 043. d, f Hilum and micropyle (arrowed) that are positioned separately, with the cap being shed. d STB 042. f. STB 044. Scale bar 0.5 mm

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Fig. 4 Seeds of Euryale yunnanensis sp. nov. viewed by the SEM. a–c STB 045. a General view. b Side view of the germination cap. c Surface details of the seed coat, showing elliptic cells (arrowed) with undulate margins and thickened cell walls arranged in a reticulate pattern. d, e STB 046. d Apical view of the germination cap. e Surface details of the cap, showing elliptic cells (arrowed) with undulate margins and thickened cell walls arranged in a reticulate pattern. f STB 047. Interior surface of the seed coat. g, h STB 048. g Transection of the seed coat. h Magnified view of the testa transection, showing small, irregular cavities (arrowed)

Cabombaceae is a sister family with Nymphaeaceae in the Nymphaea, Ondinea and Barclaya are much smaller, order , consisting of two genera, namely measuring only 1–3 mm in length and 1–2 mm in breadth, Brasenia and Cabomba [2, 38–41]. while those of Euryale, Victoria and Nuphar are larger, up The seed morphology and anatomy of extant genera in to 12 mm long and 10 mm wide. Testa surface cells of the Nymphaeales have been surveyed in several studies Euryale and Nuphar are elliptic to circular in shape and [7, 42–44]. The position of the hilum in relation to the smooth at the margin, whereas those of Victoria, Nym- germination cap and micropyle and the shape of testa phaea, Ondinea and Barclaya are elongate in outline and surface cells were thought to be the most important char- undulate at the margin. Among the six genera in Nym- acteristics in distinguishing the genera of Cabombaceae phaeaceae, only Euryale and Nuphar have a prominent and Nymphaeaceae [8]. Based on selected seed characters, raphe ridge. Therefore, seeds of Euryale and Nuphar are Collinson [7] and Chen et al. [8] made a summary of seed the most similar in morphology and anatomy, but these two morphological and anatomical distinctions among genera genera can be distinguished chiefly by the position of the in these two families. As shown in (Fig. 5), seeds of hilum and germination cap. The hilum in Euryale is situ- Cabombaceae (Brasenia and Cabomba) have the hilum and ated outside of the cap, but it is located inside the cap in micropyle sharing the same opening situated on the center Nuphar [42, 44]. They can also be separated by the wall of the germination cap and thus can be distinguished from character of testa cells: testa cell walls of Euryale are those of Nymphaeaceae. In Nymphaeaceae, seeds of

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Fig. 5 Diagnostic seed characters among extant genera in relation to current understandings of phylogenetic relationships within Cabombaceae and Nymphaeaceae. The cladogram is after Chen et al. [8] based on combined data set of non-molecular, rbcL, matK and 18S rDNA data [1], and diagrams are modified from Collinson [7] obviously thickened, whereas this thickening is not pro- of E. yunnanensis (5–8 mm 9 4–6 mm). In addition, seeds nounced in Nuphar. of E. ferox have a larger germination cap, thicker seed coat The Shuitangba fossil seeds are characterized by an and a more developed palisade structure in the outer layer of ellipsoidal to almost spherical shape, a smooth surface, the the seed coat (Fig. 6). Seeds of four other fossil species (E. separation of the hilum and germination cap, elliptic testa akashiensis, E. nodulosa, E. lissa and E. sukaczevii) are also surface cells with undulate margins and thickened cell larger than seeds of E. yunnanensis. Moreover, the surface of walls. These characteristics collectively indicate a close E. akashiensis seeds is gnarled and that of E. nodulosa seeds resemblance to Euryale. Although the raphe ridge in the is irregularly ridged, different from the smooth surface of E. fossils is only weakly visible, which is not the case in the yunnanensis seeds. The remaining two fossil species (E. modern species of this genus, affinities with the remaining europaea and E. tenuicostata) generate seeds with a similar seven genera can be eliminated even more convincingly. size to the Shuitangba fossil seeds. The difference lies in that Moreover, the Shuitangba seeds are compressed along the seeds of E. europaea have a larger germination cap raphe ridge area. This compression may have caused the (2.1 mm 9 1.3 mm) than our fossils (0.7–0.9 mm in diam- raphe ridge to be less visible. eter) and seeds of E. tenuicostata are spherical to ovate, Euryale contains only one extant species (E. ferox) living whereas those of E. yunnanensis are elliptic or ellipsoidal. in eastern Asia [4, 5], but it was shown to be more diverse in All these morphological and anatomical distinctions support the geological past, e.g., the Neogene and Pleistocene the designation to a new fossil species for the Shuitangba [11, 13, 15, 18, 20, 21]. Up to 10 fossil species of this genus seeds. have been documented in the literature [11, 13, 15, 18]. We herein compare the Shuitangba fossil seeds that are desig- 4.2 Paleoenvironmental implications nated to E. yunnanensis with both extant and selected species of other fossils of Euryale (Table 2). Modern seeds of E. As aforementioned, the Shuitangba fossil site in the ferox (10–12 mm 9 7–10 mm) are much larger than seeds Zhaotong Basin has produced a large number of avian

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Table 2 Comparisons of seed morphology and anatomy between Euryale yunnanensis sp. nov. and the modern E. forex plus other fossil species of Euryale Species Type Shape Size Surface Size of germination Testa References (length 9 width mm) cap (mm) thickness (mm)

E. yunnanensis sp. nov. Fossil Ellipsoidal, 5–8 9 4–6 Smooth 0.7–0.9 in diameter 0.2–0.4 This study compressed E. ferox Extant Ovate 10–12 9 7–10 Smooth 1.1–1.3 in diameter 0.5–0.9 This study E. akashiensis Fossil Ovate 7–9 9 6–8 Gnarled Unknown Unknown [15] E. europaea Fossil Ovate About 5.6 9 4.5 Smooth About 2.1 9 1.3 Unknown [11] E. nodulosa Fossil Spherical, About 8 9 8 Irregularly Unknown Unknown [13] compressed ridged E. lissa Fossil Obovate About 7 9 6 Smooth Unknown Unknown [13] E. sukaczevii Fossil Spherical to ovate 7–12 9 6–9 Smooth Unknown Unknown [18] E. tenuicostata Fossil Spherical to ovate 4–8 9 3–7 Smooth Unknown Unknown [18]

Fig. 6 Extant seeds of Euryale ferox. a Apical view, showing the hilum and germination cap that are positioned separately. b Magnified view of the germination cap, showing elliptic cells arranged in a reticulate pattern. c Testa surface, showing elliptic cells arranged in a reticulate pattern. d Transection of the testa, showing a palisade structure in the outer layer and small, irregular cavities in the other part of the transection fossils. Most of the identified avian species were deter- crocodile, beaver and otter-like mustelid remains indicates mined to be waders, including Ardeidae, Charadriidae, a depositional environment at the margin of standing water Cioniidea, Gruidae, Scolopacidae and Threskiornithidae, [30]. This interpretation is further strengthened by the and natatores such as Anatidae, Gaviidae, Pelecanidae, presence of aquatic pollen in the hominoid-bearing layer Phalacrocoracidae and Podicipedidae [28]. This implies a [29]. As Euryale is an aquatic plant that lives in swamps swamp and/or lake environment with shallow water near and lakes with shallow and stable water, the fossil occur- Shuitangba in the Zhaotong Basin during the late Miocene rence of Euryale may imply a swamp and/or lake envi- [28]. In addition, the abundance of fish, frog, turtle, ronment with areas of shallow and stable water in the

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Table 3 Known fossil records of Euryale and their ages and localities Species Age Region Fossil type References

E. ferox Late Pleistocene Zhejiang, eastern China Seed [22] E. akashiensis Early Pleistocene Japan Seed [15] Euryale sp. Pleistocene Poland Seed [21] E. ferox Pleistocene Germany Seed [20] E. cf. limburgensis Pleistocene Germany Seed [14] E. europaea Pleistocene Kaluga, eastern Russia Seed [11, 19] E. carpatica Pliocene Poland Seed [16] E. nodulosa Pliocene Dutch-Prussian Border Seed [13] E. lissa Pliocene Dutch-Prussian Border Seed [13] E. yunnanensis sp. nov. Late Miocene Yunnan, southwestern China Seed This study Euryale sp. Miocene Germany [47] Euryale sp. Miocene Hebei, northern China Seed [23] E. sukaczevii Miocene Tomsk, southwestern Russia Seed [18] E. tenuicostata Miocene Tomsk, southwestern Russia Seed [18] E. cf. europaea Miocene Poland Seed [17]

Zhaotong Basin during the late Miocene. It is worth represents an old record for this genus. This appears to agree mentioning that more than 500 fossil seeds of Euryale have with the phylogenetic estimate that Euryale diversified pre- been obtained so far and more specimens are being sumably in the middle to late Miocene (13.44–7.78 Ma), recovered. Despite the high seed production of Euryale or later than the other genera in Nymphaeaceae and its sister any possible taphonomic bias, the large number of fossil family Cabombaceae [2]. specimens may indicate that Euryale was likely a dominant component in the Zhaotong Basin at that time. This new Acknowledgments This work was supported by the National Nat- fossil finding, coupled with previous multidisciplinary ural Science Foundation of China (31300187, 31300188), the Natural Science Foundation of Yunnan Province (2010CC010), Zhaotong investigations by paleontology [28, 30] and palynology Institute of Cultural Relics, Cultural Bureau of Zhaoyang District [29], suggests that the Shuitangba hominoid may have Government and an Excavation Annual Foundation of 2015 from the lived in the vicinity of a lake and/or swamp. Institute of Vertebrate Paleontology and Paleoanthropology, Chinese Academy of Sciences. Fossil collection was assisted by doctoral students of the Palaeoecology Research Group from Kunming Insti- 4.3 Fossil history and implications tute of Botany, Chinese Academy of Sciences, and members from Yunnan Institute of Cultural Relics and Archaeology, Zhaotong Being an ANITA family of angiosperms [6], Nymphaeaceae Institute of Cultural Relics, and Zhaoyang Museum; extant seeds of was considered to have risen very early [45]. Some extinct Euryale ferox were provided by the Herbarium of Institute of Botany and prepared by Dr. Xiao-Guo Xiang from Institute of Botany, Chi- groups embedded in this family can be dated back into the nese Academy of Sciences; seed observations with the Zeiss binocular Cretaceous, e.g., Microvictoria [10] and Monetianthus [9]. microscope and SEM were performed in the Central Lab of Several extant genera in Nymphaeaceae also have fossil Xishuangbanna Tropical Botanical Garden, Chinese Academy of records yielding an old geological age. For example, the Sciences. oldest fossil related to the modern Nuphar was recorded from the Paleocene of North Dakota, USA [8, 46], and the oldest References record for the modern Nymphaea was found from the late Eocene to early Oligocene of England [7]. This suggests an 1. Les DH, Schneider EL, Padgett DJ et al (1999) Phylogeny, early emergence for these extant genera, consistent with their classification and floral evolution of water lilies (Nymphaeaceae; divergence times derived from molecular phylogenetic Nymphaeales): a synthesis of non-molecular, rbcL, matK, and analyses [2, 45]. Fossils of Euryale, however, are compara- 18S rDNA data. Syst Bot 24:28–46 2. Yoo MJ, Bell CD, Soltis PS et al (2005) Divergence times and tively young (Table 3). The oldest known records of Euryale historical biogeography of Nymphaeales. Syst Bot 30:693–704 are dated to be only of Miocene, represented by seed remains 3. Jha V, Kargupta AN, Dutta RN et al (1991) Utilization and from the Miocene of Poland [17], southwestern Russia [18] conservation of Euryale ferox Sablisbery in Mithila (North and northern China [23], and a leaf occurrence from the Bihar), India. Aquat Bot 39:295–314 4. Fu D, Wiersema JH, Padgett D (2001) Nymphaeaceae. In: Wu Miocene of Germany [47]. Euryale yunnanensis from the ZY, Raven PH (eds) Flora of China, vol 6. Science Press, Beijing; late Miocene (7.2–5.3 Ma) [27] of southwestern China also Missouri Botanical Garden Press, St. Louis, pp 115–118

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