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

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

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Article

Earth Sciences

Fossil seeds of Euryale (Nymphaeaceae) 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 distributed in eastern Asia, but fossils in its native distribution are sparse as compared to Europe where the genus has disappeared. Here, we describe a new fossil species, Euryale yunnanensis sp. nov., from the late Miocene Zhaotong Basin in southwestern China on the basis of seed remains. Characteristics including an ellipsoidal to almost spherical shape, a smooth surface, a germination cap that covers the micropyle, the separation of the hilum and germination cap (micropyle), elliptic testa surface cells with undulate margins and thickened cell walls collectively indicate a close affinity with the genus Euryale in Nymphaeaceae. Comparisons of

Y. Huang  Z. Zhou (&) Key Laboratory for Plant Biodiversity and Biogeography of East Asia, Kunming Institute of Botany, Chinese Academy of Sciences, Kunming 650201, China e-mail: [email protected] X. Ji Yunnan Institute of Cultural Relics and Archaeology and Research Center for Southeast Asian Archeology, Kunming 650118, China T. Su  L. Wang  Z. Zhou Key Laboratory of Tropical Forest Ecology, Xishuangbanna Tropical Botanical Garden, Chinese Academy of Sciences, Mengla 666303, China C. Deng State Key Laboratory of Lithospheric Evolution, Institute of Geology and Geophysics, Chinese Academy of Sciences, Beijing 100029, China W. Li Zhaotong Institute of Cultural Relics, Zhaotong 657000, China H. Luo Zhaoyang Museum, Zhaotong 657000, China

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seed morphology and anatomy demonstrate that the newly described fossil species differs from modern and other fossil species of Euryale and thus verify the assignment to a new fossil species. As the modern Euryale is an aquatic plant, preferably living in swamps and lakes with shallow and stable water, we hypothesize that a lake and/or swamp environment with shallow water was present near Shuitangba in the Zhaotong Basin, where the Shuitangba hominoid lived during the late Miocene. This inference is generally consistent with paleoenvironmental data extracted from avian, fish, frog, turtle and crocodile fossils, as well as from aquatic pollen. The fossil history suggests a comparatively recent (Miocene) emergence of Euryale, which is roughly in agreement with the divergence time inferred from the molecular information. Keywords Euryale  Nymphaeaceae  Aquatic  Late Miocene  Zhaotong Basin  Southwestern China

1 Introduction Euryale Salisb. is a monotypic genus in the water lily family Nymphaeaceae [1, 2]. It comprises Euryale ferox Salisb., which is known as foxnut or gorgon nut [3–5]. Euryale ferox is an aquatic plant, with floating or partially to entirely submerged leaves [4, 5]. It lives preferably in swamps and lakes with shallow and stable water but in a few cases occurs in somewhat deeper water environments [4]. Phytogeographically, E. ferox is native to eastern Asia, distributed from northeastern India to China, Korea and Japan, as well as the Far East of Russia [4, 5]. Nymphaeaceae is a member of the ANITA, a well-known basal grade in angiosperms [6]. Several genera of the family, both extinct and extant, have old fossil records [7–10]. Unlike

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other living members in Nymphaeaceae with records from the Paleogene, e.g., Nuphar [8] and Nymphaea [7], Euryale, however, seems to be a younger group. The molecular phylogenetic tree has revealed that Euryale emerged more recently [2]. To be consistent, fossils of this genus are relatively young, extending only into the Miocene [11–23]. The fossil occurrence of Euryale was discovered for the first time about a century ago from the Pleistocene of western Russia, Europe [11, 12]. Several other fossil occurrences were subsequently reported from the Neogene and Pleistocene of Europe [13, 14, 16–21]. In North America, fossils possibly related to Euryale were represented only by the late Paleocene seeds from North Dakota, USA [24]. However, the Dakota seeds were thought to lack promising characters for a credible placement in Euryale and were ultimately treated as an extinct genus named Susiea [24]. In eastern Asia, fossil records of Euryale are relatively few as compared to those

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known from Europe. Only three fossil records have been documented to date; they are E. ferox from the Pleistocene of Zhejiang, eastern China [22], E. akashiensis from the Pliocene of Japan [15] and an undetermined species (Euryale sp.) from the Miocene of Hebei, northern China [23]. According to these accounts, the fossil distribution of Euryale shows a concentration in Eurasia (Fig. 1a). Most of its known fossils are from Europe where the genus has become extinct, and they are comparatively rare in eastern Asia despite the modern range of the genus there. In this study, we describe a new fossil species of Euryale from eastern Asia, based on seed entities from the late Miocene of Yunnan, southwestern China. The fossil seeds were studied morphologically and anatomically, and were compared with the seeds of extant and other fossil species of Euryale. The paleoenvironmental implications of this new fossil discovery 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 2.1 Fossil site, geological setting and geochronology The Zhaotong Basin is located in northeastern Yunnan Province, southwestern China (Fig. 1b, c). It is one of the fault-related basins of the late Neogene at the southeastern margin of the Qinghai-Tibetan Plateau [25, 26]. The basin is filled with late Miocene to Pliocene lacustrine or swampy clays, silts, peaty clays and lignites [27, 28]. The fossil site known as Shuitangba, from which our fossil seeds were unearthed, lies in an open-pit lignite mine located at Shuitangba village in the basin (27°190 4400 N, 103°440 1500 E; Fig. 1c). An outcrop section at the mine is *16 m thick, composed of seven sedimentary layers [29]. The upper part of the black peaty clay layer is 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 mammal fossils such as beaver (Sinocastor sp.), hamster (Kowalskia sp.) and flying squirrel (Pliopetaurista sp.) [27, 30], as well as avian remains [28]. The coexistence of the mammalian species points to the East Asian Baodean Stage/Age with a time span of 7.2–5.3 Ma [27]. Moreover, the black peaty clay layer was considered to be located near the C3An.1r–C3An.1n transition [27, 30], which was estimated to be *6.2 Ma based on the Astronomically Tuned Neogene Time Scale of Hilgen et al. [31]. Therefore, the fossiliferous peaty clay layer can be unambiguously assigned to the late Miocene evidenced by both biostratigraphic and magnetostratigraphic data. 2.2 Fossil materials and examinations Recent field work has shown that the black peaty clay layer at the Shuitangba fossil site also bears plant fossils, of which seed remains are the most abundant. More than 500 anatomically preserved seeds of Euryale were collected from this layer successively during 2013–2015. The

resulting specimens were cleaned using an ultrasonic cleaner (KO-50M) at a frequency of 50 kHz for 30 s to remove clay particles adhering to the seed surface. Airdried, the seeds were observed under a binocular microscope (Zeiss Stereo REO Discovery V20), and digital images were taken using a Zeiss camera (AxioCam HRc) anchored on the Zeiss binocular microscope. The seed surface, germination cap and seed coat transection were studied using a scanning electron microscope (SEM; Zeiss EVOLS10). Modern seeds of Euryale, viz. E. ferox, were examined following the same procedures as for the fossil seeds except that an observation with the SEM was not performed. The studied fossil specimens are deposited primarily at the Herbarium of Kunming Institute of Botany, Chinese Academy of Sciences, and partly at the Zhaoyang Museum.

3 Results 3.1 Systematics Family: Nymphaeaceae Salisb., 1805. Genus: Euryale Salisb., 1805. Species: Euryale yunnanensis Y. Huang & Z. Zhou sp. nov. Etymology: The specific Latin epithet yunnanensis is chosen in reference to Yunnan Province where the fossil site is located. Holotype: STB 028 (Fig. 2a) here designated. Paratypes: STB 029–STB 048. Materials: More than 500 seeds that are anatomically preserved but largely compressed. Type locality: Shuitangba village in the Zhaotong Basin of northeastern Yunnan Province, southwestern China. Age: Late Miocene. Repository: About 400 fossil specimens are kept at the Herbarium of Kunming Institute of Botany, Chinese

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 3

Gray clayey silts Gravels

2.7–5.4 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 2 mm

Academy of Sciences; more than 100 fossil specimens are housed at the Zhaoyang Museum.

circular in outline; seed coat relatively thin; and the palisade 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 ridge near the hilum area not prominent; germination cap

Seeds are mostly compressed, elliptic in outline (for those 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 length and breadth ratio of 1.1–1.4 (100 measurements). The dorsal (basal) part is roundly inflated, and the ventral (apical) part is slightly narrowed (Fig. 2). The seed surface is smooth (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 and a little raised (Fig. 3). The germination cap that covers the micropyle is circular and measures 0.7–0.9 mm in diameter (Figs. 3a–c, e, 4b, d). The hilum and germination cap (or micropyle) are positioned separately (Fig. 3). Located in the center of the cap is a small protuberance (Figs. 3a–c, e, 4b, d). Cells on the cap surface are elliptic and arranged in a reticulate pattern (Fig. 4e). The interior face of the seed coat bears no notable sculpture, and no surface cell can be observed (Fig. 4f). The seed coat is 0.2–0.4 mm thick (Fig. 4g); it is thicker near

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the hilum area but thinner in the ventral part. The outer layer of the seed coat has a weakly developed palisade structure, while the rest contains numerous small, irregular cavities as revealed from its transection (Fig. 4g, h).

4 Discussion 4.1 Comparisons and taxonomic treatment The family Nymphaeaceae is generally accepted to be divided into six genera, namely Barclaya, Euryale, Nuphar, Nymphaea, Ondinea and Victoria [1, 2, 32]. Although this intrafamilial classification has been debated particularly based on molecular phylogenetic data [33–37], 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 order Nymphaeales, consisting of two genera, namely Brasenia and Cabomba [2, 38–41]. The seed morphology and anatomy of extant genera in the Nymphaeales have been surveyed in several studies [7, 42–44]. The position of the hilum in relation to the germination cap and micropyle and the shape of testa surface cells were thought to be the most important characteristics in distinguishing the genera of Cabombaceae and Nymphaeaceae [8]. Based on selected seed characters, Collinson [7] and Chen et al. [8] made a summary of seed morphological and anatomical distinctions among genera in these two families. As shown in (Fig. 5), seeds of Cabombaceae (Brasenia and Cabomba) have the hilum and micropyle sharing the same opening situated on the center of the germination cap and thus can be distinguished from those of Nymphaeaceae. In Nymphaeaceae, seeds of

Nymphaea, Ondinea and Barclaya are much smaller, measuring only 1–3 mm in length and 1–2 mm in breadth, while those of Euryale, Victoria and Nuphar are larger, up to 12 mm long and 10 mm wide. Testa surface cells of Euryale and Nuphar are elliptic to circular in shape and smooth at the margin, whereas those of Victoria, Nymphaea, Ondinea and Barclaya are elongate in outline and undulate at the margin. Among the six genera in Nymphaeaceae, only Euryale and Nuphar have a prominent raphe ridge. Therefore, seeds of Euryale and Nuphar are the most similar in morphology and anatomy, but these two genera can be distinguished chiefly by the position of the hilum and germination cap. The hilum in Euryale is situated outside of the cap, but it is located inside the cap in Nuphar [42, 44]. They can also be separated by the wall character of testa cells: testa cell walls of Euryale are

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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 pronounced in Nuphar. The Shuitangba fossil seeds are characterized by an ellipsoidal to almost spherical shape, a smooth surface, the separation of the hilum and germination cap, elliptic testa surface cells with undulate margins and thickened cell walls. These characteristics collectively indicate a close resemblance to Euryale. Although the raphe ridge in the fossils is only weakly visible, which is not the case in the modern species of this genus, affinities with the remaining seven genera can be eliminated even more convincingly. Moreover, the Shuitangba seeds are compressed along the raphe ridge area. This compression may have caused the raphe ridge to be less visible. Euryale contains only one extant species (E. ferox) living in eastern Asia [4, 5], but it was shown to be more diverse in the geological past, e.g., the Neogene and Pleistocene [11, 13, 15, 18, 20, 21]. Up to 10 fossil species of this genus have been documented in the literature [11, 13, 15, 18]. We herein compare the Shuitangba fossil seeds that are designated to E. yunnanensis with both extant and selected species of other fossils of Euryale (Table 2). Modern seeds of E. ferox (10–12 mm 9 7–10 mm) are much larger than seeds

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of E. yunnanensis (5–8 mm 9 4–6 mm). In addition, seeds of E. ferox have a larger germination cap, thicker seed coat and a more developed palisade structure in the outer layer of the seed coat (Fig. 6). Seeds of four other fossil species (E. akashiensis, E. nodulosa, E. lissa and E. sukaczevii) are also larger than seeds of E. yunnanensis. Moreover, the surface of E. akashiensis seeds is gnarled and that of E. nodulosa seeds is irregularly ridged, different from the smooth surface of E. yunnanensis seeds. The remaining two fossil species (E. europaea and E. tenuicostata) generate seeds with a similar size to the Shuitangba fossil seeds. The difference lies in that seeds of E. europaea have a larger germination cap (2.1 mm 9 1.3 mm) than our fossils (0.7–0.9 mm in diameter) and seeds of E. tenuicostata are spherical to ovate, whereas those of E. yunnanensis are elliptic or ellipsoidal. All these morphological and anatomical distinctions support the designation to a new fossil species for the Shuitangba seeds. 4.2 Paleoenvironmental implications As aforementioned, the Shuitangba fossil site in the 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 (length 9 width mm)

Surface

Size of germination cap (mm)

Testa thickness (mm)

References

E. yunnanensis sp. nov.

Fossil

Ellipsoidal, compressed

5–8 9 4–6

Smooth

0.7–0.9 in diameter

0.2–0.4

This study

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, compressed

About 8 9 8

Irregularly ridged

Unknown

Unknown

[13]

E. lissa E. sukaczevii

Fossil Fossil

Obovate Spherical to ovate

About 7 9 6 7–12 9 6–9

Smooth Smooth

Unknown Unknown

Unknown Unknown

[13] [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 determined to be waders, including Ardeidae, Charadriidae, Cioniidea, Gruidae, Scolopacidae and Threskiornithidae, and natatores such as Anatidae, Gaviidae, Pelecanidae, Phalacrocoracidae and Podicipedidae [28]. This implies a swamp and/or lake environment with shallow water near Shuitangba in the Zhaotong Basin during the late Miocene [28]. In addition, the abundance of fish, frog, turtle,

crocodile, beaver and otter-like mustelid remains indicates a depositional environment at the margin of standing water [30]. This interpretation is further strengthened by the presence of aquatic pollen in the hominoid-bearing layer [29]. As Euryale is an aquatic plant that lives in swamps and lakes with shallow and stable water, the fossil occurrence of Euryale may imply a swamp and/or lake environment 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. Euryale sp.

Miocene Miocene

Germany Hebei, northern China

Leaf Seed

[47] [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 mentioning that more than 500 fossil seeds of Euryale have been obtained so far and more specimens are being recovered. Despite the high seed production of Euryale or any possible taphonomic bias, the large number of fossil specimens may indicate that Euryale was likely a dominant component in the Zhaotong Basin at that time. This new fossil finding, coupled with previous multidisciplinary investigations by paleontology [28, 30] and palynology [29], suggests that the Shuitangba hominoid may have lived in the vicinity of a lake and/or swamp. 4.3 Fossil history and implications Being an ANITA family of angiosperms [6], Nymphaeaceae was considered to have risen very early [45]. Some extinct groups embedded in this family can be dated back into the Cretaceous, e.g., Microvictoria [10] and Monetianthus [9]. Several extant genera in Nymphaeaceae also have fossil records yielding an old geological age. For example, the oldest fossil related to the modern Nuphar was recorded from the Paleocene of North Dakota, USA [8, 46], and the oldest record for the modern Nymphaea was found from the late Eocene to early Oligocene of England [7]. This suggests an early emergence for these extant genera, consistent with their divergence times derived from molecular phylogenetic analyses [2, 45]. Fossils of Euryale, however, are comparatively young (Table 3). The oldest known records of Euryale are dated to be only of Miocene, represented by seed remains from the Miocene of Poland [17], southwestern Russia [18] and northern China [23], and a leaf occurrence from the Miocene of Germany [47]. Euryale yunnanensis from the late Miocene (7.2–5.3 Ma) [27] of southwestern China also

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represents an old record for this genus. This appears to agree with the phylogenetic estimate that Euryale diversified presumably in the middle to late Miocene (13.44–7.78 Ma), later than the other genera in Nymphaeaceae and its sister family Cabombaceae [2]. Acknowledgments This work was supported by the National Natural Science Foundation of China (31300187, 31300188), the Natural Science Foundation of Yunnan Province (2010CC010), Zhaotong Institute of Cultural Relics, Cultural Bureau of Zhaoyang District Government and an Excavation Annual Foundation of 2015 from the Institute of Vertebrate Paleontology and Paleoanthropology, Chinese Academy of Sciences. Fossil collection was assisted by doctoral students of the Palaeoecology Research Group from Kunming Institute of Botany, Chinese Academy of Sciences, and members from Yunnan Institute of Cultural Relics and Archaeology, Zhaotong Institute of Cultural Relics, and Zhaoyang Museum; extant seeds of Euryale ferox were provided by the Herbarium of Institute of Botany and prepared by Dr. Xiao-Guo Xiang from Institute of Botany, Chinese Academy of Sciences; seed observations with the Zeiss binocular microscope and SEM were performed in the Central Lab of Xishuangbanna Tropical Botanical Garden, Chinese Academy of Sciences.

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