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Fruits of Ceratophyllum (Ceratophyllaceae) from the late Miocene in Huaning, Southwest China and its paleoecological and paleophytogeographical significances
Journal Pre-proof Fruits of Ceratophyllum (Ceratophyllaceae) from the late Miocene in Huaning, Southwest China and its paleoecological and paleophytogeographical significances
Xiao-Qing Liang, Ping Lu, Tao Su PII:
S0034-6667(19)30261-1
DOI:
https://doi.org/10.1016/j.revpalbo.2019.104155
Reference:
PALBO 104155
To appear in:
Review of Palaeobotany and Palynology
Received date:
22 August 2019
Revised date:
20 December 2019
Accepted date:
27 December 2019
Please cite this article as: X.-Q. Liang, P. Lu and T. Su, Fruits of Ceratophyllum (Ceratophyllaceae) from the late Miocene in Huaning, Southwest China and its paleoecological and paleophytogeographical significances, Review of Palaeobotany and Palynology(2020), https://doi.org/10.1016/j.revpalbo.2019.104155
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Fruits of Ceratophyllum (Ceratophyllaceae) from the late Miocene in Huaning, Southwest
China
and
its
palaecological
and
palaeophytogeographical
significances
Xiao-Qing Liang
a, b
, Ping Lu b, *, Tao Su a, *
a CAS Key Laboratory of Tropical Forest Ecology, Xishuangbanna Tropical Botanical
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f
Garden, Chinese Academy of Sciences, Mengla 666303, China
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b School of Chemical, Biological and Environmental Sciences, Yuxi Normal
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University, Yuxi 653100, China
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Abstract
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* corresponding author. E-mail address: [email protected]; [email protected]
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Ceratophyllum L. is a genus of submerged aquatic plant with a cosmopolitan distribution. In this study, we first described fruit fossils of C. demersum collected in the Miocene (Xiaolongtang Formation) in Huaning, Yunnan, Southwest China. The materials indicated that a lake with shallow water existed in Huaning in the late Miocene. Based on fossil data, the genus may earliest appeared in the Cretaceous of North America and evolved into sect. Ceratophyllum, sect. Muricatum and sect. Submersum accompanying by the global climate change during the Cenozoic. Its distribution gradually expanded throughout the period. Plants of the genus was present in Southwest China by the late Miocene.
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Keywords: Ceratophyllum, late Miocene, palaeophytogeography, palaeoecology, Southwest China
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1 Introduction
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Ceratophyllaceae Gray is a family of submersed, herbaceous, perennial and
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hydrophilous plants. The fruits of Ceratophyllaceae are elliptical and symmetric with
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a smooth or variously papillose to tuberculate surface and prominent spines (Les,
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1993), which usually include an long or short apical stylar spine and a pair of basal spines, although these are lacking in some species. Some species may have additional
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marginal spines (often joined by a wing) or a pair of elongate facial spines (Les, 1993).
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This cosmopolitan aquatic family has one genus, Ceratophyllum L., and six species,
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which is divided into three sections, sect. Ceratophyllum L. (C. demersum, C. platyacanthum), sect. Muricatum Les (C. muricatum, C. tanaiticum), and sect. Submersum Les (C. submersum, C. echinatum) based on fruit morphological features (Les, 1989; Les, 1993).
Some fossils of Ceratophyllaceae have been described in the literature. The extinct genus Donlesia, its earliest fruit fossils from the Early Cretaceous deposits in Kansas, USA, was interpreted to have taxonomic affinities to Ceratophyllaceae (Dilcher and Wang, 2009). Many fossil fruits of Ceratophyllum also have been reported. These fossil specimens were collected from the Cretaceous (Late Campanian
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or early Maastrichtian) of southern Alberta, Canada (Serbet et al., 2008) and from the Cerro del Pueblo Formation (late Campanian [73.5 ma]), Coahuila, Northeast Mexico (Estrada-Ruiz et al., 2009). Fossil fruits of C. furcatispinum were found from the Paleocene Fort Union Formation (Herendeen et al., 1990). Fossil fruits assignable to the extant species C. muricatum and C. echinatum were recognized from the Eocene
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Green River and Claiborne formations, and the Miocene Esmerelda Formation
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(Herendeen et al., 1990). Fruits of C. zaisanicum were described from the early
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Oligocene Zaysan basin, Kazakhstan (Avakov, 1962). Many fruits of the genus were
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collected from the Oligocene – Pliocene Siberia, Russia (Dorofeev, 1963; Nikitin,
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2006), and others from the Miocene of Big Orlovka, Russia (Takhtajan, 1974), Joban, Japan (Yabe, 2008), Leipzig and Klettwitz, Germany (Mai and Wähnert, 2000),
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Shanwang, China (Wang et al., 2005) and Lower Rhenish Basin, Germany (Van der
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Burgh, 1987), the Pliocene Matanov and Krivobor'ye, Russia (Takhtajan, 1974), Żary,
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Poland (Mai and Wähnert, 2000), the Holocene Northwest Territories, Canada (Terasmae and Craig, 1958) and West Okoboji Lake, Iowa (Van Zant, 1979).
In this paper, we described fruits of Ceratophyllum demersum from the late Miocene deposit of Huaning, Yunnan, Southwest China and discussed evolution of morphology and historical distribution of the genus based on fossil data. 2 Methods and Materials
2.1 Site and stratigraphy The fossil site is located in the Xiangyang coal Mine, about 10 km north of
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Huaning County, Yunnan Province, in Southwest China (24.24° N, 102.93° E, 1648 m) (Fig. 1). The section consists of red clay on the surface, preceded by layers of siltstone, sandstone, and coal, with gray mudstone at the bottom. Based on geological studies, the section is composed of the Holocene, Pliocene and Miocene deposits, and is ascribed to the Ciying and Xiaolongtang Formations (Fig. 2) (Sun, 2010). The
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magnetostratigraphic study results indicated the Xiaolongtang Formations, Yunnan
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ranged from 10 Ma to 12.7 Ma (Li et al., 2015). In this study, collected from upper
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part of the gray mudstone of the Xiaolongtang Formation, our materials were dated to
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the late Miocene.
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Figure 1
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Figure 2
2.2 Material and methods
The fossils were isolated from the sediment using the bulk acid maceration procedure described by Wellman and Axe (1999), and were observed with a light microscope. Fossil specimens were deposited in the fossil repository of the Chemistry, Biology and Environment School at Yuxi Normal University.
3 Systematics
Journal Pre-proof Family: Ceratophyllaceae Genus: Cerataphyllum L. Species: Ceratophyllum demersum L. (Plate 1)
Description The fruits are ovate, elliptical to broadly elliptical in shape (Pls 1, 2).
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They (excl. spines) are 3.9±0.3 mm in length and 2.9±0.5 mm in width. The surfaces have papillae or are smooth (Pl. 1). They have an apex with a persistent style, and a
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Plate 1continued
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Plate 1
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are 5.2±2.1 mm in length (Pl. 1).
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base with two spines (Pl. 1). The stylar spine is 5.9±2.4 mm long, while the basal ones
Comment Plants of Ceratophyllum have been ascribed into three sections according to the fruit characteristics (Les, 1989). Sect. Ceratophyllum (C. demersum and C. platyacanthum) has fruits with 3-5 long spines, sect. Submersum (C. submersum, and C. echinatum) has fruits with a spiny margin without stylar and basal spines, and sect. Muricatum (C. muricatum, and C. tanaiticum) has fruits with spiny and winged margins with stylar and basal spines (Les, 1989).
Our specimens from the late Miocene of Huaning have three spines (the stylar
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and basal spines) and have wingless margins, and are most similar to fruits from sect. Ceratophyllum (Pl. 1). Among them, one specimen with a long stylar spine (Pl. 1f) is similar to fruits of C. apiculatum, but C. apiculatum has fruits with short stylar tubercles, which are like those in C. demersum (Les, 1986). The fossil fruits differ from C. platyacanthum, which has five spines. Phenotypes of one fossil fruit with
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smooth surface and a stylar spine (Pl. 1f) also exist in modern species (C. demersum)
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(Les, 1986; Nikitin, 2006). Therefore, these fossils are assigned to C. demersum. We
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follow Herendeen et al. (1990) in assigning these Cenozoic fossils to a modern
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species, because there are no significant morphological differences.
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4 Discussion
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4.1 Ecological significance of C. demersum from Huaning, Yunnan
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Plants reflect the ecological landscape and their fossils can be used to help
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reconstruct a past environment (e.g. Euryale, Cladium) (Les, 1988b, c). Ceratophyllum is a submersed, herbaceous, perennial and hydrophilous plant (Les, 1993). Occurrence of Ceratophyllum suggested the presence of a lake and lakeside vegetation in Shanwang in the Miocene (Wang et al., 2005). The presence of C. demersum in the late Miocene of Huaning also indicates that there was a shallow lake in the region during that time.
4.2 Evolution of fruit morphology of Ceratophyllum
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Morphological variation and evolutionary trends of fruit morphology of Ceratophyllum had been studied within species based on features including shape, size, spine length, surface, and wings (Les, 1986, 1988a, b, c, 1989). Fruits of C. demersum are variable. By comparison, the spineless fruit phenotype of C. submersum may have evolved from a spiny- fruited C. demersum (Les, 1986). Basal
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and stylar spines are significantly correlated in the spiny- margined group of the genus,
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and the lateral spine lengths of most species are correlated with the basal and stylar
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spine lengths (Les, 1988a). Fruit phenotypes of C. echinatum highly resemble those of
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C. submersum, and leaf characteristics are similar between the both species which are
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ascribed into the same section (Les, 1988a). Les also noted (1988) that achene morphology typical of other species is usually observed in the fruit variations of C.
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demersum. Fruit variations (winged fruit) of C. demersum are very close to fruits of C.
Table 1
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platyacanthum (Les, 1988b).
Figure 3
Fossilized fruits of the extinct taxon, Donlesia dakotensis, with two winged lateral spines, two winged facial spines and one stylar spine were found in Early Cretaceous, and interpreted to represent Ceratophyllaceae (Dilcher and Wang, 2009). However, fruit fossils assignable to Ceratophyllum with stylar spine and two basal
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spines are first seen during the Cretaceous in southern Alberta, Canada, and Coahuila, Mexico, e.g. Ceratophyllum sp. and C. lesii, which are very similar to extant C. demersum in fruit features (Estrada-Ruiz et al., 2009; Serbet et al., 2008). Although there are no fossils of sect. Ceratophyllum found in the Palaeogene deposits, its’ fruit fossils with three spines were found in the Neogene, e.g. C. demersum from North
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America, Europe and Siberia (Dorofeev, 1963; Pals et al. 1980; Takhtajan, 1974;
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Terasmae and Craig, 1958; Van Zant, 1979).
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Spiny fruits with T-shaped spine apex and an unequally branched spine of C.
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furcatispinum from Montana, USA have a resemblance to the spiny margined species
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of the genus, which is consistent with those of C. tanaiticum (sect. Muricatum) in fruit size and spiny features (Herendeen et al., 1990).Then, many species of sect.
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Muricatum occurred since the Eocene, e.g. C. muricatum ssp. incertum, C. zaisanicum,
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Ceratophyllum cf. muricatum ssp. muricatum, respectively (Avakov, 1962; Herendeen
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et al., 1990; Wang et al., 2005). Lower and Middle Eocene C. muricatum ssp. incertum had small fruits with long lateral spines (Herendeen et al., 1990). Middle Miocene C. muricatum ssp. muricatum from Shanwang, China had fruits with a small length to width ratio (Herendeen et al., 1990; Wang et al., 2005). Fruit fossils of sect. Submersum (C. submersum) without spines appeared first in the Oligocene (Takhtajan, 1974). The species of the section (C. echinatum and C. submersum) occurred in the Neogene (Table 1) (Herendeen et al., 1990; Takhtajan, 1974; Van der Burgh, 1987). Three sections synchronouslyappeared in or before the Oligocene. Consequently, Ceratophyllum may have
gradually evolved other two sections with the
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morphological features in its fruit, such as: fruit with a spiny and winged margin and fruit without spines, respectively (Figs. 3).
The trend of global climate change includes the warming phase in the Paleocene and a cooling phase after the Eocene (Zachos et al., 2001), Evolution of the genus reflects its adaptation to the global climate change (Fig. 3). In the warming Paleocene,
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the thermophilous plants of sect. Muricatum, appeared (Herendeen et al., 1990). And in the cooling Oligocene, the temperate species of sect. Submersum evolved
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(Dorofeev, 1963; Nikitin, 2006; Takhtajan, 1974).
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4.3 Palaeobiogeographical implication of Ceratophyllum
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Fossils of Ceratophyllum provide materials to help us to understand its’ historical
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distribution. Fossils were found in the late Cretaceous, Paleocene, Eocene, Miocene,
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Pliocene, and Holocene North Hemisphere (Avakov, 1962; Dorofeev, 1963;
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Estrada-Ruiz et al., 2009; Griffin, 1980; Gümbel and Mai, 2006; Herendeen et al., 1990; Kerner, 1905; Knobloch, 1977; Mai and Wähnert, 2000; Nikitin, 2006; Ohlhorst et al., 1982; Ozaki, 1991; Pals et al., 1980; Ritchie and DeVries, 1964; Serbet et al., 2008; Takhtajan, 1974; Terasmae and Craig, 1958; Unger, 1850; Van der Burgh, 1987; Wang et al., 2005; Yabe, 2008). Based on fossil data, Ceratophyllum (Ceratophyllum sp. and C. lesii) appeared first in North America during the Cretaceous Period (Estrada-Ruiz et al., 2009; Serbet et al., 2008).
The genus dispersed during the Cenozoic Period (Figs. 5, 6). C. furcatispinum of sect. Muricatum occurred in Montana in the Palaeocene (Herendeen et al., 1990),
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other species of the section (e.g. C. zaisanicum) appeared in the eastern Asia in the Oligocene and Miocene (Dorofeev, 1963; Takhtajan, 1974; Wang et al., 2005). Ceratophyllites faujas appeared in the Eocene (Unger, 1850). C. demersum existed in Europe and Asia in the Miocene (Dorofeev, 1963; Nikitin, 2006) (this study).
Trends in distributions of three sections were different during the geological ages.
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Sect. Ceratophyllum gradually adapts the global climate and becomes cosmopolitan (Fig. 6). The historical distributions of the other two sections were larger than the
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present (Fig. 5). Species of sect. Muricatum early appeared in the Paleocene Montana,
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USA (Herendeen et al., 1990), and dispersed in middle latitudinal region of America
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and Asia during the Eocene and Miocene (Dorofeev, 1963; Herendeen et al., 1990; Wang et al., 2005). But in the cooling Neogene, the sect. Muricatum reduced its
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distribution and was mainly confined to the tropical and subtropical region. Section
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Submersum possibly appeared in temperate regions in the Oligocene (Dorofeev, 1963),
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but disappeared in the high latitude so that it ranges from 30° N to 60° N of North America and Europe (Fig. 5).
Figure 4
5 Conclusion
Fruit fossils of Ceratophyllum demersum were reported in the late Miocene in
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Huaning, Yunnan. Appearance of fossils indicated that there was a lake in this location. With the global climate change during the Cenozoic, sect. Muricatum with fruit with a spiny and winged margin gradually evolved in the Paleocene which adapted the warm climate, and sect. Submersum with fruit without spines developed in the Oligocene which like temperate climate. The oldest known fossils occurred in the Cretaceous
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North America. Plants of Ceratophyllum spread in Europe in the Eocene and Asia in
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the Oligocene, then dispersed worldwide.
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Acknowledge ment This research was supported by grants from the National Natural
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Science Foundation of China [Grant Nos. 31760057 and 31860049], and the CAS
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Key Laboratory of Tropical Forest Ecology at the Xishuangbanna Tropical Bo tanical
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Table legends:
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Table 1 Fossil species of Ceratophyllum based on published literatures
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Figure legends:
Figure 1 Locality of fossil site in Huaning, Yunnan, China.
Figure 2 Stratigraphy of Xiaolongtang Formation in Huaning.
Figure 3 Geological ages of fruit fossils of three sections of Ceratophyllum based on
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fossil data. Curve indicates trend in the global climate change during the Cenozoic
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drew according to Zachos et al. (2001).
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Figure 4 Fossil sites of sect. Ceratophyllum, sect. Submersum, and sect. Muricatum in
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the geological ages. Present distributions of the sections outlined based on Herendeen
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et al. (1990). Cre, Pal, Eoc, Oli, Mio, Pli, Hol-Plei show Cretaceous, Paleocene,
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Eocene, Oligocene, Miocene, Pliocene, and Pleistocene, respectively.
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Figure 5 Historical distribution of Ceratophyllum based on fossil data. 1 and 2 arrows show migration routes during the Paleogene and Neogene, respectively. Dashed lines
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show the recent distribution.
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Plate legends:
Plate 1 Fruit fossils of Ceratophyllum demersum from Xiaolongtang formation in Huaning, Yunnan, China. c: another side of b. Arrows show papillae. Scale bar:
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a=5mm; b, c, d, e, k=1mm; f, g, h, i, j=2mm.
Journal Pre-proof Conflict of interest We declare that we do not have any commercial or associative interest that
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represents a conflict of interest in connection with the work submitted.
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Species
Site
C. lesii
Date
References
Late Cretaceous
(Estrada-Ruiz et
(73.5 Ma)
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Coahuila, Mexico
Ceratophyllum sp.
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Alberta, Cretaceous
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Montana
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Green River C. muricatum ssp.
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C. muricatum ssp.
Formation,
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incertum
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(Herendeen
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Formation, incertum
(Herendeen
Palaeocene
pr
C. furcatispinum
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2008)
f
Canada
et
(Herendeen M. Eocene
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al., 1990)
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Wheeler County,
Ceratophyllum sp.
(Manchester, Eocene
Oregon
2000)
Zaysan basin, C. zaisanicum
(Avakov, 1962) Lower Oligocene
Kazakhstan
(Dorofeev, 1963; C. submersum
Siberia, Russia
Oligocene-Pliocene Nikitin, 2006)
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(Dorofeev, 1963; C. tenuicarpum
Siberia, Russia
Oligocene-Miocene
Nikitin,
2006;
Takhtajan, 1974)
Ceratophyllum sp.
Siberia, Russia
Oligocene-Pliocene
Konur-Kura,
(Takhtajan,
C. zaisanicum
Oligocene
Esmeralda
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Middle Miocene
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Formation, Nevada
Sinj, Croatia
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C. sinjanum
(Takhtajan, 1974)
this study
(Herendeen
et
Upper Miocene
al
C. echinatum
e-
Huaning, China
1974)
Oligocene
pr
Tomsk, Russia
Pr
C. demersum
f
Kazakhstan
C. submersum
(Nikitin, 2006)
al., 1990)
(Kerner,
Knobloch, 1977)
Ampflwang,
C. dubium
1905;
Middle Miocene
(Knobloch, Upper Miocene
Austria
1977)
C. cf. muricatum
(Wang Shanwang, China
et
al.,
middle Miocene
subsp. muricatum
2005)
(Dorofeev, 1963; C. demersum
Siberia, Russia
Miocene-Pliocene Nikitin, 2006)
Journal Pre-proof
(Takhtajan, C. pannonicum
Lgovsky, Russia
Miocene 1974)
Big Orlovka,
(Takhtajan,
C. miocenicum
Miocene Russia
1974)
Mammoth Mt.,
(Takhtajan,
C. submersum
Miocene
oo
f
Russia
Isakovka,
(Takhtajan,
Miocene
pr
C. demersum
1974)
Mammoth Mt.,
al
Russia
Joban, Japan
rn
Ceratophyllum sp.
Early Miocene
Klettwitz,
Jo u
C. pannonicum
(Takhtajan,
Ukraine
1974)
(Yabe, 2008)
(Mai
and
Middle Miocene
Germany
C. pannonicum
1974)
Miocene
Pr
C. spinulosum
e-
Kazakhstan
Wähnert, 2000)
(Mai
and
Upper Miocene Wähnert, 2000)
(Mai C. lusaticum
Leipzig, Germany
and
Miocene Walther, 1978)
Lettengraben, Cerataphyllum sp.
(Gümbel Miocene
Germany
Mai, 2006)
and
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Lower Rhenish
(Van der Burgh,
C. demersum
Upper Miocene Basin, Germany
1987)
Lower Rhenish
(Van der Burgh,
C. submersum
Upper Miocene Basin, Germany
Takasaki, Japan
Upper Miocene
f
C. miodemersum
1987)
oo
Krivobor'ye, C. protanaiticuin
pr
e-
Uryv, Russia
rn
Matanov, Russia
Jo u
C. demersum
C. cf. demersum
Żary, Poland
1974)
(Takhtajan,
Pliocene
Pr
Matanov, Russia
1974)
(Takhtajan,
Pliocene
al
C. demersum
(Takhtajan,
Pliocene Russia
C. submersum
(Ozaki, 1991)
1974)
(Takhtajan, Pliocene 1974)
(Mai
and
Pliocene Wähnert, 2000)
(Mai C. pannonicum
Żary, Poland
and
Pliocene Wähnert, 2000)
(Mai C. submersum
Żary, Poland
and
Pliocene Wähnert, 2000)
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(Mai C. pannonicum
Bulgaria
Pliocene
and
Wähnert,
2000;
Palamarev, 1982)
C. submersum
Norway
Pleistocen/Holocene
Coteau des
(Watts
C. demersum
f oo
West Okoboji
Bright, 1968)
(Van Zant, 1979)
Pleistocen/Holocene
pr
C. demersum
Missouri Cateau,
(Ritchie
and
Pleistocen/Holocene
al
Canada
Pr
C. demersum
e-
Lake, Iowa
Hoogkarspel,
DeVries, 1964)
(Pals
et
al.,
rn
Pleistocen/Holocene 1980)
Jo u
Netherlands
C. demersum
and
Pleistocen/Holocene Prairies, Dakota
C. demersum
(Griffin, 1980)
(Ohlhorst et al.,
Huleh Lake, Jordan Pleistocen/Holocene 1982)
Atchison County, C. demersum
(Gruger, 1973) Pleistocen/Holocene
Kansas
Northwest C. demersum
(Terasmae Holocene
Territories, Canada
Craig, 1958)
and
Jo u
rn
al
Pr
e-
pr
oo
f
Journal Pre-proof
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1. Fruits of Ceratophyllum demersum were first collected in Huaning, Southwest China.
2. A shallow lake influenced landscape existed in Huaning in the Miocene. 3. Sect. Muricatum and sect. Submersum evolved in the Paleogene.
Jo u
rn
al
Pr
e-
pr
oo
f
4. Ceratophyllum gradually dispersed worldwide during the Cenozoic.
Figure 1
Figure 2
Figure 3
Figure 4
Figure 5
Xiao-Qing Liang, Ping Lu, Tao Su PII:
S0034-6667(19)30261-1
DOI:
https://doi.org/10.1016/j.revpalbo.2019.104155
Reference:
PALBO 104155
To appear in:
Review of Palaeobotany and Palynology
Received date:
22 August 2019
Revised date:
20 December 2019
Accepted date:
27 December 2019
Please cite this article as: X.-Q. Liang, P. Lu and T. Su, Fruits of Ceratophyllum (Ceratophyllaceae) from the late Miocene in Huaning, Southwest China and its paleoecological and paleophytogeographical significances, Review of Palaeobotany and Palynology(2020), https://doi.org/10.1016/j.revpalbo.2019.104155
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Fruits of Ceratophyllum (Ceratophyllaceae) from the late Miocene in Huaning, Southwest
China
and
its
palaecological
and
palaeophytogeographical
significances
Xiao-Qing Liang
a, b
, Ping Lu b, *, Tao Su a, *
a CAS Key Laboratory of Tropical Forest Ecology, Xishuangbanna Tropical Botanical
oo
f
Garden, Chinese Academy of Sciences, Mengla 666303, China
pr
b School of Chemical, Biological and Environmental Sciences, Yuxi Normal
e-
University, Yuxi 653100, China
rn
Abstract
al
Pr
* corresponding author. E-mail address: [email protected]; [email protected]
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Ceratophyllum L. is a genus of submerged aquatic plant with a cosmopolitan distribution. In this study, we first described fruit fossils of C. demersum collected in the Miocene (Xiaolongtang Formation) in Huaning, Yunnan, Southwest China. The materials indicated that a lake with shallow water existed in Huaning in the late Miocene. Based on fossil data, the genus may earliest appeared in the Cretaceous of North America and evolved into sect. Ceratophyllum, sect. Muricatum and sect. Submersum accompanying by the global climate change during the Cenozoic. Its distribution gradually expanded throughout the period. Plants of the genus was present in Southwest China by the late Miocene.
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Keywords: Ceratophyllum, late Miocene, palaeophytogeography, palaeoecology, Southwest China
f
1 Introduction
oo
Ceratophyllaceae Gray is a family of submersed, herbaceous, perennial and
pr
hydrophilous plants. The fruits of Ceratophyllaceae are elliptical and symmetric with
e-
a smooth or variously papillose to tuberculate surface and prominent spines (Les,
Pr
1993), which usually include an long or short apical stylar spine and a pair of basal spines, although these are lacking in some species. Some species may have additional
al
marginal spines (often joined by a wing) or a pair of elongate facial spines (Les, 1993).
rn
This cosmopolitan aquatic family has one genus, Ceratophyllum L., and six species,
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which is divided into three sections, sect. Ceratophyllum L. (C. demersum, C. platyacanthum), sect. Muricatum Les (C. muricatum, C. tanaiticum), and sect. Submersum Les (C. submersum, C. echinatum) based on fruit morphological features (Les, 1989; Les, 1993).
Some fossils of Ceratophyllaceae have been described in the literature. The extinct genus Donlesia, its earliest fruit fossils from the Early Cretaceous deposits in Kansas, USA, was interpreted to have taxonomic affinities to Ceratophyllaceae (Dilcher and Wang, 2009). Many fossil fruits of Ceratophyllum also have been reported. These fossil specimens were collected from the Cretaceous (Late Campanian
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or early Maastrichtian) of southern Alberta, Canada (Serbet et al., 2008) and from the Cerro del Pueblo Formation (late Campanian [73.5 ma]), Coahuila, Northeast Mexico (Estrada-Ruiz et al., 2009). Fossil fruits of C. furcatispinum were found from the Paleocene Fort Union Formation (Herendeen et al., 1990). Fossil fruits assignable to the extant species C. muricatum and C. echinatum were recognized from the Eocene
f
Green River and Claiborne formations, and the Miocene Esmerelda Formation
oo
(Herendeen et al., 1990). Fruits of C. zaisanicum were described from the early
pr
Oligocene Zaysan basin, Kazakhstan (Avakov, 1962). Many fruits of the genus were
e-
collected from the Oligocene – Pliocene Siberia, Russia (Dorofeev, 1963; Nikitin,
Pr
2006), and others from the Miocene of Big Orlovka, Russia (Takhtajan, 1974), Joban, Japan (Yabe, 2008), Leipzig and Klettwitz, Germany (Mai and Wähnert, 2000),
al
Shanwang, China (Wang et al., 2005) and Lower Rhenish Basin, Germany (Van der
rn
Burgh, 1987), the Pliocene Matanov and Krivobor'ye, Russia (Takhtajan, 1974), Żary,
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Poland (Mai and Wähnert, 2000), the Holocene Northwest Territories, Canada (Terasmae and Craig, 1958) and West Okoboji Lake, Iowa (Van Zant, 1979).
In this paper, we described fruits of Ceratophyllum demersum from the late Miocene deposit of Huaning, Yunnan, Southwest China and discussed evolution of morphology and historical distribution of the genus based on fossil data. 2 Methods and Materials
2.1 Site and stratigraphy The fossil site is located in the Xiangyang coal Mine, about 10 km north of
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Huaning County, Yunnan Province, in Southwest China (24.24° N, 102.93° E, 1648 m) (Fig. 1). The section consists of red clay on the surface, preceded by layers of siltstone, sandstone, and coal, with gray mudstone at the bottom. Based on geological studies, the section is composed of the Holocene, Pliocene and Miocene deposits, and is ascribed to the Ciying and Xiaolongtang Formations (Fig. 2) (Sun, 2010). The
f
magnetostratigraphic study results indicated the Xiaolongtang Formations, Yunnan
oo
ranged from 10 Ma to 12.7 Ma (Li et al., 2015). In this study, collected from upper
pr
part of the gray mudstone of the Xiaolongtang Formation, our materials were dated to
Pr
e-
the late Miocene.
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Figure 1
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Figure 2
2.2 Material and methods
The fossils were isolated from the sediment using the bulk acid maceration procedure described by Wellman and Axe (1999), and were observed with a light microscope. Fossil specimens were deposited in the fossil repository of the Chemistry, Biology and Environment School at Yuxi Normal University.
3 Systematics
Journal Pre-proof Family: Ceratophyllaceae Genus: Cerataphyllum L. Species: Ceratophyllum demersum L. (Plate 1)
Description The fruits are ovate, elliptical to broadly elliptical in shape (Pls 1, 2).
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f
They (excl. spines) are 3.9±0.3 mm in length and 2.9±0.5 mm in width. The surfaces have papillae or are smooth (Pl. 1). They have an apex with a persistent style, and a
e-
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Plate 1continued
rn
Plate 1
al
Pr
are 5.2±2.1 mm in length (Pl. 1).
pr
base with two spines (Pl. 1). The stylar spine is 5.9±2.4 mm long, while the basal ones
Comment Plants of Ceratophyllum have been ascribed into three sections according to the fruit characteristics (Les, 1989). Sect. Ceratophyllum (C. demersum and C. platyacanthum) has fruits with 3-5 long spines, sect. Submersum (C. submersum, and C. echinatum) has fruits with a spiny margin without stylar and basal spines, and sect. Muricatum (C. muricatum, and C. tanaiticum) has fruits with spiny and winged margins with stylar and basal spines (Les, 1989).
Our specimens from the late Miocene of Huaning have three spines (the stylar
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and basal spines) and have wingless margins, and are most similar to fruits from sect. Ceratophyllum (Pl. 1). Among them, one specimen with a long stylar spine (Pl. 1f) is similar to fruits of C. apiculatum, but C. apiculatum has fruits with short stylar tubercles, which are like those in C. demersum (Les, 1986). The fossil fruits differ from C. platyacanthum, which has five spines. Phenotypes of one fossil fruit with
f
smooth surface and a stylar spine (Pl. 1f) also exist in modern species (C. demersum)
oo
(Les, 1986; Nikitin, 2006). Therefore, these fossils are assigned to C. demersum. We
pr
follow Herendeen et al. (1990) in assigning these Cenozoic fossils to a modern
e-
species, because there are no significant morphological differences.
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4 Discussion
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4.1 Ecological significance of C. demersum from Huaning, Yunnan
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Plants reflect the ecological landscape and their fossils can be used to help
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reconstruct a past environment (e.g. Euryale, Cladium) (Les, 1988b, c). Ceratophyllum is a submersed, herbaceous, perennial and hydrophilous plant (Les, 1993). Occurrence of Ceratophyllum suggested the presence of a lake and lakeside vegetation in Shanwang in the Miocene (Wang et al., 2005). The presence of C. demersum in the late Miocene of Huaning also indicates that there was a shallow lake in the region during that time.
4.2 Evolution of fruit morphology of Ceratophyllum
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Morphological variation and evolutionary trends of fruit morphology of Ceratophyllum had been studied within species based on features including shape, size, spine length, surface, and wings (Les, 1986, 1988a, b, c, 1989). Fruits of C. demersum are variable. By comparison, the spineless fruit phenotype of C. submersum may have evolved from a spiny- fruited C. demersum (Les, 1986). Basal
f
and stylar spines are significantly correlated in the spiny- margined group of the genus,
oo
and the lateral spine lengths of most species are correlated with the basal and stylar
pr
spine lengths (Les, 1988a). Fruit phenotypes of C. echinatum highly resemble those of
e-
C. submersum, and leaf characteristics are similar between the both species which are
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ascribed into the same section (Les, 1988a). Les also noted (1988) that achene morphology typical of other species is usually observed in the fruit variations of C.
al
demersum. Fruit variations (winged fruit) of C. demersum are very close to fruits of C.
Table 1
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rn
platyacanthum (Les, 1988b).
Figure 3
Fossilized fruits of the extinct taxon, Donlesia dakotensis, with two winged lateral spines, two winged facial spines and one stylar spine were found in Early Cretaceous, and interpreted to represent Ceratophyllaceae (Dilcher and Wang, 2009). However, fruit fossils assignable to Ceratophyllum with stylar spine and two basal
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spines are first seen during the Cretaceous in southern Alberta, Canada, and Coahuila, Mexico, e.g. Ceratophyllum sp. and C. lesii, which are very similar to extant C. demersum in fruit features (Estrada-Ruiz et al., 2009; Serbet et al., 2008). Although there are no fossils of sect. Ceratophyllum found in the Palaeogene deposits, its’ fruit fossils with three spines were found in the Neogene, e.g. C. demersum from North
f
America, Europe and Siberia (Dorofeev, 1963; Pals et al. 1980; Takhtajan, 1974;
oo
Terasmae and Craig, 1958; Van Zant, 1979).
pr
Spiny fruits with T-shaped spine apex and an unequally branched spine of C.
e-
furcatispinum from Montana, USA have a resemblance to the spiny margined species
Pr
of the genus, which is consistent with those of C. tanaiticum (sect. Muricatum) in fruit size and spiny features (Herendeen et al., 1990).Then, many species of sect.
al
Muricatum occurred since the Eocene, e.g. C. muricatum ssp. incertum, C. zaisanicum,
rn
Ceratophyllum cf. muricatum ssp. muricatum, respectively (Avakov, 1962; Herendeen
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et al., 1990; Wang et al., 2005). Lower and Middle Eocene C. muricatum ssp. incertum had small fruits with long lateral spines (Herendeen et al., 1990). Middle Miocene C. muricatum ssp. muricatum from Shanwang, China had fruits with a small length to width ratio (Herendeen et al., 1990; Wang et al., 2005). Fruit fossils of sect. Submersum (C. submersum) without spines appeared first in the Oligocene (Takhtajan, 1974). The species of the section (C. echinatum and C. submersum) occurred in the Neogene (Table 1) (Herendeen et al., 1990; Takhtajan, 1974; Van der Burgh, 1987). Three sections synchronouslyappeared in or before the Oligocene. Consequently, Ceratophyllum may have
gradually evolved other two sections with the
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morphological features in its fruit, such as: fruit with a spiny and winged margin and fruit without spines, respectively (Figs. 3).
The trend of global climate change includes the warming phase in the Paleocene and a cooling phase after the Eocene (Zachos et al., 2001), Evolution of the genus reflects its adaptation to the global climate change (Fig. 3). In the warming Paleocene,
oo
f
the thermophilous plants of sect. Muricatum, appeared (Herendeen et al., 1990). And in the cooling Oligocene, the temperate species of sect. Submersum evolved
pr
(Dorofeev, 1963; Nikitin, 2006; Takhtajan, 1974).
e-
4.3 Palaeobiogeographical implication of Ceratophyllum
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Fossils of Ceratophyllum provide materials to help us to understand its’ historical
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distribution. Fossils were found in the late Cretaceous, Paleocene, Eocene, Miocene,
rn
Pliocene, and Holocene North Hemisphere (Avakov, 1962; Dorofeev, 1963;
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Estrada-Ruiz et al., 2009; Griffin, 1980; Gümbel and Mai, 2006; Herendeen et al., 1990; Kerner, 1905; Knobloch, 1977; Mai and Wähnert, 2000; Nikitin, 2006; Ohlhorst et al., 1982; Ozaki, 1991; Pals et al., 1980; Ritchie and DeVries, 1964; Serbet et al., 2008; Takhtajan, 1974; Terasmae and Craig, 1958; Unger, 1850; Van der Burgh, 1987; Wang et al., 2005; Yabe, 2008). Based on fossil data, Ceratophyllum (Ceratophyllum sp. and C. lesii) appeared first in North America during the Cretaceous Period (Estrada-Ruiz et al., 2009; Serbet et al., 2008).
The genus dispersed during the Cenozoic Period (Figs. 5, 6). C. furcatispinum of sect. Muricatum occurred in Montana in the Palaeocene (Herendeen et al., 1990),
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other species of the section (e.g. C. zaisanicum) appeared in the eastern Asia in the Oligocene and Miocene (Dorofeev, 1963; Takhtajan, 1974; Wang et al., 2005). Ceratophyllites faujas appeared in the Eocene (Unger, 1850). C. demersum existed in Europe and Asia in the Miocene (Dorofeev, 1963; Nikitin, 2006) (this study).
Trends in distributions of three sections were different during the geological ages.
oo
f
Sect. Ceratophyllum gradually adapts the global climate and becomes cosmopolitan (Fig. 6). The historical distributions of the other two sections were larger than the
pr
present (Fig. 5). Species of sect. Muricatum early appeared in the Paleocene Montana,
e-
USA (Herendeen et al., 1990), and dispersed in middle latitudinal region of America
Pr
and Asia during the Eocene and Miocene (Dorofeev, 1963; Herendeen et al., 1990; Wang et al., 2005). But in the cooling Neogene, the sect. Muricatum reduced its
al
distribution and was mainly confined to the tropical and subtropical region. Section
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Submersum possibly appeared in temperate regions in the Oligocene (Dorofeev, 1963),
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but disappeared in the high latitude so that it ranges from 30° N to 60° N of North America and Europe (Fig. 5).
Figure 4
5 Conclusion
Fruit fossils of Ceratophyllum demersum were reported in the late Miocene in
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Huaning, Yunnan. Appearance of fossils indicated that there was a lake in this location. With the global climate change during the Cenozoic, sect. Muricatum with fruit with a spiny and winged margin gradually evolved in the Paleocene which adapted the warm climate, and sect. Submersum with fruit without spines developed in the Oligocene which like temperate climate. The oldest known fossils occurred in the Cretaceous
f
North America. Plants of Ceratophyllum spread in Europe in the Eocene and Asia in
pr
oo
the Oligocene, then dispersed worldwide.
e-
Acknowledge ment This research was supported by grants from the National Natural
Pr
Science Foundation of China [Grant Nos. 31760057 and 31860049], and the CAS
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Key Laboratory of Tropical Forest Ecology at the Xishuangbanna Tropical Bo tanical
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Van Zant, K., 1979. Late glacial and postglacial pollen and plant macrofossils from Lake West Okoboji, northeastern Iowa. Quaternary Reserch 12, 358-380.
Wang, Y.-F., Ferguson, D.K., Li, C.-S., 2005. Ceratophyllum (Ceratophyllaceae) from the Miocene of Eastern China and its paleoecological significance. Systematic Botany 30, 705-711.
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Watts, W.A., Bright, R.C., 1968. Pollen, seed, and mollusk analysis of a sediment core from Pickerel Lake, northeastern South Dakota. The Geological Society of America Bulletin 79, 855-876.
Wellman, C.H., Axe, L., 1999. Extracting Plant Mesofossils and Megafossils by Bulk Acid Maceration, in: Jones, T.P., Rowe, N.P. (Eds.), Fossil plants and spores: modern
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techniques. London: Geological Society of London, 11–14.
Yabe, A., 2008. Early Miocene terrestrial climate inferred from plant megafossil
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Geological Survey of Japan 59, 397-413.
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assemblages of the Joban and Soma areas, Northeast Honshu, Japan. Bulletin of the
Zachos, J., Pagani, M., Sloan, L., Thomas, E., Billups, K., 2001. Trends, Rhythms,
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and Aberrations in Global Climate 65 Ma to Present. Science 292, 686-693.
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Table legends:
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Table 1 Fossil species of Ceratophyllum based on published literatures
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Figure legends:
Figure 1 Locality of fossil site in Huaning, Yunnan, China.
Figure 2 Stratigraphy of Xiaolongtang Formation in Huaning.
Figure 3 Geological ages of fruit fossils of three sections of Ceratophyllum based on
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fossil data. Curve indicates trend in the global climate change during the Cenozoic
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drew according to Zachos et al. (2001).
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Figure 4 Fossil sites of sect. Ceratophyllum, sect. Submersum, and sect. Muricatum in
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the geological ages. Present distributions of the sections outlined based on Herendeen
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et al. (1990). Cre, Pal, Eoc, Oli, Mio, Pli, Hol-Plei show Cretaceous, Paleocene,
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Eocene, Oligocene, Miocene, Pliocene, and Pleistocene, respectively.
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Figure 5 Historical distribution of Ceratophyllum based on fossil data. 1 and 2 arrows show migration routes during the Paleogene and Neogene, respectively. Dashed lines
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show the recent distribution.
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Plate legends:
Plate 1 Fruit fossils of Ceratophyllum demersum from Xiaolongtang formation in Huaning, Yunnan, China. c: another side of b. Arrows show papillae. Scale bar:
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a=5mm; b, c, d, e, k=1mm; f, g, h, i, j=2mm.
Journal Pre-proof Conflict of interest We declare that we do not have any commercial or associative interest that
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represents a conflict of interest in connection with the work submitted.
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Species
Site
C. lesii
Date
References
Late Cretaceous
(Estrada-Ruiz et
(73.5 Ma)
al., 2009)
Coahuila, Mexico
Ceratophyllum sp.
southern
Alberta, Cretaceous
(Serbet
oo
Montana
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Green River C. muricatum ssp.
L. and M. Eocene
al
Wyoming
Claiborne
rn
C. muricatum ssp.
Formation,
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incertum
et
al., 1990)
(Herendeen
et
al., 1990)
Pr
Formation, incertum
(Herendeen
Palaeocene
pr
C. furcatispinum
al.,
2008)
f
Canada
et
(Herendeen M. Eocene
et
al., 1990)
Tennessee
Wheeler County,
Ceratophyllum sp.
(Manchester, Eocene
Oregon
2000)
Zaysan basin, C. zaisanicum
(Avakov, 1962) Lower Oligocene
Kazakhstan
(Dorofeev, 1963; C. submersum
Siberia, Russia
Oligocene-Pliocene Nikitin, 2006)
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(Dorofeev, 1963; C. tenuicarpum
Siberia, Russia
Oligocene-Miocene
Nikitin,
2006;
Takhtajan, 1974)
Ceratophyllum sp.
Siberia, Russia
Oligocene-Pliocene
Konur-Kura,
(Takhtajan,
C. zaisanicum
Oligocene
Esmeralda
oo
Middle Miocene
rn
Formation, Nevada
Sinj, Croatia
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C. sinjanum
(Takhtajan, 1974)
this study
(Herendeen
et
Upper Miocene
al
C. echinatum
e-
Huaning, China
1974)
Oligocene
pr
Tomsk, Russia
Pr
C. demersum
f
Kazakhstan
C. submersum
(Nikitin, 2006)
al., 1990)
(Kerner,
Knobloch, 1977)
Ampflwang,
C. dubium
1905;
Middle Miocene
(Knobloch, Upper Miocene
Austria
1977)
C. cf. muricatum
(Wang Shanwang, China
et
al.,
middle Miocene
subsp. muricatum
2005)
(Dorofeev, 1963; C. demersum
Siberia, Russia
Miocene-Pliocene Nikitin, 2006)
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(Takhtajan, C. pannonicum
Lgovsky, Russia
Miocene 1974)
Big Orlovka,
(Takhtajan,
C. miocenicum
Miocene Russia
1974)
Mammoth Mt.,
(Takhtajan,
C. submersum
Miocene
oo
f
Russia
Isakovka,
(Takhtajan,
Miocene
pr
C. demersum
1974)
Mammoth Mt.,
al
Russia
Joban, Japan
rn
Ceratophyllum sp.
Early Miocene
Klettwitz,
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C. pannonicum
(Takhtajan,
Ukraine
1974)
(Yabe, 2008)
(Mai
and
Middle Miocene
Germany
C. pannonicum
1974)
Miocene
Pr
C. spinulosum
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Kazakhstan
Wähnert, 2000)
(Mai
and
Upper Miocene Wähnert, 2000)
(Mai C. lusaticum
Leipzig, Germany
and
Miocene Walther, 1978)
Lettengraben, Cerataphyllum sp.
(Gümbel Miocene
Germany
Mai, 2006)
and
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Lower Rhenish
(Van der Burgh,
C. demersum
Upper Miocene Basin, Germany
1987)
Lower Rhenish
(Van der Burgh,
C. submersum
Upper Miocene Basin, Germany
Takasaki, Japan
Upper Miocene
f
C. miodemersum
1987)
oo
Krivobor'ye, C. protanaiticuin
pr
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Uryv, Russia
rn
Matanov, Russia
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C. demersum
C. cf. demersum
Żary, Poland
1974)
(Takhtajan,
Pliocene
Pr
Matanov, Russia
1974)
(Takhtajan,
Pliocene
al
C. demersum
(Takhtajan,
Pliocene Russia
C. submersum
(Ozaki, 1991)
1974)
(Takhtajan, Pliocene 1974)
(Mai
and
Pliocene Wähnert, 2000)
(Mai C. pannonicum
Żary, Poland
and
Pliocene Wähnert, 2000)
(Mai C. submersum
Żary, Poland
and
Pliocene Wähnert, 2000)
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(Mai C. pannonicum
Bulgaria
Pliocene
and
Wähnert,
2000;
Palamarev, 1982)
C. submersum
Norway
Pleistocen/Holocene
Coteau des
(Watts
C. demersum
f oo
West Okoboji
Bright, 1968)
(Van Zant, 1979)
Pleistocen/Holocene
pr
C. demersum
Missouri Cateau,
(Ritchie
and
Pleistocen/Holocene
al
Canada
Pr
C. demersum
e-
Lake, Iowa
Hoogkarspel,
DeVries, 1964)
(Pals
et
al.,
rn
Pleistocen/Holocene 1980)
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Netherlands
C. demersum
and
Pleistocen/Holocene Prairies, Dakota
C. demersum
(Griffin, 1980)
(Ohlhorst et al.,
Huleh Lake, Jordan Pleistocen/Holocene 1982)
Atchison County, C. demersum
(Gruger, 1973) Pleistocen/Holocene
Kansas
Northwest C. demersum
(Terasmae Holocene
Territories, Canada
Craig, 1958)
and
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Pr
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f
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1. Fruits of Ceratophyllum demersum were first collected in Huaning, Southwest China.
2. A shallow lake influenced landscape existed in Huaning in the Miocene. 3. Sect. Muricatum and sect. Submersum evolved in the Paleogene.
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4. Ceratophyllum gradually dispersed worldwide during the Cenozoic.
Figure 1
Figure 2
Figure 3
Figure 4
Figure 5