Spirematospermum wetzleri (Heer) Chandler (Zingiberaceae) from the Miocene of Weichang, Hebei Province, North China and the phytogeographic history of the genus
Spirematospermum is a well-known extinct zingiberalean taxon, characterized by trilocular capsules containing many distinctive, spirally striate and arillate seeds. It is frequently found and studied in European Neogene carpological floras, but is scarcely represented in East Asia floras. In this work we recognize a new fossil record of Spirematospermum wetzleri (Heer) Chandler based on the capsules and seeds from the Miocene of Weichang, Hebei Province, North China. These fossils represent the first record of the species in the Miocene of China. Fossil data indicate that Spirematospermum probably originated in the Late Cretaceous of North America or Central Europe. The genus still existed in the Paleocene of North America, but became extinct after that time. However, the genus successively survived in Europe from the Eocene to Pliocene, and flourished luxuriantly during the Oligocene to Miocene. As there was Turgai Strait between Europe and Asia during the Eocene, the genus did not spread to Central Asia and West Siberia until the strait closed in the late Eocene/early Oligocene, and further expanded eastwardly to eastern Siberia, Russia, northern China and central Japan during the Miocene, but became extinct in Asia after the Miocene. The genus contracted its distribution to Europe in the Pliocene, and afterwards it became extinct in the world.
KeywordsSpirematospermum Zingiberaceae Musaceae Phytogeographic history Neogene Miocene Weichang North China
Spirematospermum Chandler (Zingiberales) is an extinct genus, established for trilocular capsules containing many distinctive seeds with spirally striate testa and aril (Chandler 1925; Friedrich and Koch 1970; Fischer et al. 2009). Spirematospermum has long been a subject of controversy regarding its systematic affinity, since Heer (1859) first described its capsules and seeds from the Miocene of Günzburg, Germany, but he identified them as Gardenia wetzleri Heer (Rubiaceae). Then, Ludwig (1860) described its capsules from the Miocene of Salzhausen and other localities, Germany as Passiflora braunii Heer & Ludwig (Passifloraceae). Menzel (1913) suggested a possible relationship with monocotyledonous plants. Chandler (1925) studied its capsules and seeds from the late Eocene of Hordle, Hants, UK, and intensively examined many extant plants, but only in the family Zingiberaceae did they find similar peculiar seed structure, so he established a new genus, Spirematospermum, to accommodate these fossils and named them as S. wetzleri (Heer) Chandler. Friedrich and Koch (1970) further pointed out that S. wetzleri is quite similar to the living species Alpinia oxymitra K.Schum. (syn. Cenolophon oxymitrum (K.Schum.) Holttum) (Zingiberaceae) based on comparative study between extant Zingiberaceous materials and 70 capsules and hundreds of seeds fossils from the Miocene of Jutland, Denmark. This opinion was strengthened by their following studies (Koch and Friedrich 1971; Friedrich and Koch 1972).
However, Manchester and Kress (1993) noticed that the unribbed fruits that taper into the basal stalk, multiple seeds per locule and the presence of a chalazal chamber in the seed suggest a close affinity to Musaceae, but Spirematospermum possesses a spirally striate testa that is found today in Zingiberaceae, not in Musaceae, thus displays combined characters of both Musaceae and Zingiberaceae. Rodríguez-de la Rosa and Cevallos-Ferriz (1994) interpreted Spirematospermum as a member of the Musaceae based on the presence of a chalazal chamber and hilar cavity in seeds. Fischer et al. (2009) made a comprehensive study of S. wetzleri based on an extraordinary mass occurrence of capsules and seeds, petioles, a putative pollen grain, associated rhizomes and Zingiberales-type leaves, and phytoliths of these organs from the middle Miocene of Ponholz, Germany. They placed Spirematospermum as sister to Musa L. + Ensete Bruce ex Horan. clade and proposed a new subfamily Parietimusoideae in the Musaceae to accommodate Spirematospermum, taking into account its capsule with parietal placentation and probable rhizomatous growth.
Smith et al. (2012, 2014) studied the seeds of over 50 extant species from all eight families of Zingiberales, plus the fossil Spirematospermum by synchrotron X-ray tomographic microscopy (SRXTM), and found that a chalazal chamber is not diagnostic of Musaceae, but also was found in Costaceae and tribe Alpiniae (Zingiberaceae), thus suggesting an affinity of Spirematospermum with subfamily Alpinioideae within Zingiberaceae again. The result was strengthened by the phytolith study of Zingiberales that both Zingiberaceae and Spirematospermum produce silica sand but Musaceae produce troughs (Chen and Smith 2013).
Spirematospermum has an exceptionally wide distribution in space and time, ranging from the Late Cretaceous of North America and Europe to the Paleogene and Neogene of Eurasia, and exists as a common element in many European Neogene carpological floras (Fischer et al. 2009; Smith et al. 2014), but it is less represented and studied in East Asia. Here we reported the capsules and seeds of Spirematospermum from the early Miocene of Weichang, Hebei Province, North China, which was preliminary identified to the genus by Yi et al. (2008). And in this article, we further identified them as S. wetzleri by comparison with all fossil species of the genus. Based on the fossil record of Spirematospermum, the biogeographic history and possible migration routes of the genus are discussed.
2 Materials and methods
The plant materials were collected directly from the lignite or separated from the muddy siltstone by washing in water on a 500 um sieve. The materials were successively treated with 10% HCl and 48% HF, and then rinsed with water and air dried. The Spirematospermum specimens with 30 capsules and 50 seeds were all deposited at the National Museum of Plant History of China, the Chinese National Herbarium, Institute of Botany, Chinese Academy of Sciences, and were allocated the inventory numbers PEPB70701–70780. The prefix PE is an international code for the Chinese National Herbarium, while the PB stands for palaeobotanical collections in the National Museum of Plant History of China.
The palaeolatitudes and palaeolongitudes of the fossil localities were converted from the present day coordinates using PointTracker v4c software (Scotese 2001). Sites were plotted on six palaeomaps (Scotese 1997; Smith et al. 2004; LePage et al. 2005) of Lambert Equal-Area Azimuthal (North Pole) projections using ArcView GIS 3.2 software, covering the following time intervals: Late Cretaceous (~ 80 Ma), Paleocene (~ 60 Ma), Eocene (~ 50 Ma), Oligocene (~ 30 Ma), Miocene (~ 20 Ma) and Pliocene (~ 5 Ma).
Genus: Spirematospermum Chandler 1925
4.1 Comparisons with fossil species of Spirematospermum
4.2 The phytogeographic history of Spirematospermum
During the Paleocene, Spirematospermum is only reported from the late Paleocene of Beicegel Creek locality, McKenzie County, North Dakota, USA (Benedict et al. 2007; Fig. 5b). There are no younger occurrences of Spirematospermum from North America (Fig. 5c–f). Spirematospermum is known from the Eocene of UK and Germany (Chandler 1925; Collinson 1983; Mai and Walther 1985; Fig. 5c), and flourished luxuriantly during the Oligocene and Miocene in Europe (Koch and Friedrich 1971; Friis 1988; Fischer et al. 2009; Fig. 5d, e). Spirematospermum probably expanded its distribution eastward into Asia during the Oligocene after the closure of the Turgai Straits in the late Eocene/early Oligocene (Tiffney 1985; Scotese 1997; Sanmartín et al. 2001; Smith et al. 2004), and was further spread eastward into eastern Siberia, Russia, northern China and central Japan during the early Miocene (Nikitin 2007; Yi et al. 2008; Tsukagoshi and Matsuhashi 2012; Figs. 5d, e and 6). Spirematospermum disappeared from Asia and became less abundant in Europe during the Pliocene (Fig. 5f), and finally became extinct after Pliocene. This extinction can be related to climate deterioration during the Pliocene, as today the relatives of Spirematospermum are exclusively tropical and subtropical plants. Its southward migration to cope with the Pliocene/Pleistocene cooling was hampered by the East−West orientation of the Alps, the Mediterranean Sea and the Himalaya (Fischer et al. 2009).
As Spirematospermum wetzleri from Weichang represents the first record of the genus from China, the other two East Asian occurrences of the genus should be mentioned. Of special interest is the occurrence from the early Miocene of Omoloi River basin, Russia (Nikitin 2007), which represents the northernmost occurrence (ca. 71.3°N of the palaeolatitude) of the genus for its phytogeographic history. The other occurrence is from the Lower Miocene Nakamura Formation in Kani City, central Japan, representing the first and sole record of the genus in Japan (Tsukagoshi and Matsuhashi 2012).
4.3 The accompanying flora with Spirematospermum at Gaoshanjian
The Miocene Gaoshanjian flora is well represented by the fossils of mosses, ferns, conifers and angiosperms (Li et al. 2009; Liang et al. 2010, 2013; Guo et al. 2013). Mosses consist of three species: Leptodictyum riparium (Hedw.) Warnst., Drepanocladus subtrichophyllus Caiqing Guo & al, Amblystegium varium (Hedw.) Lindb., all belonging to the family Amblystegiaceae and suggesting a wet habitat (Guo et al. 2013). Three species of angiosperms, viz., Comptonia naumannii (Nathorst) Huzioka, C. tymensis Dorofeev, Weigela weichangensis Ya Li & C.S.Li were discovered from this locality (Liang et al. 2010, 2013). The palynological data of the Gaoshanjian section suggest that the palaeovegetation was a mixed forest of conifers (e.g., Pinus, Picea, Tsuga) and broad-leaved trees (e.g., Betula, Alnus), with some subtropical elements (e.g., Carya), and the palaeoclimate was warm temperate to subtropical (Li et al. 2009).
The putative leaves of Spirematospermum (e.g., Zingiberoideophyllum, Musophyllum) have not been found at this locality. But some aquatic plants such as Nuphar sp. and Potamogeton sp. as well as the wetland plant Epipremnites sp. (under study) were found together with Spirematospermum wetzleri, which supports that S. wetzleri was an important wetland plant with waterside or swamp habitat (Friis 1988; Fischer et al. 2009).
We reported an important fossil record of Spirematospermum from the early Miocene of North China. We made a detailed description of the well preserved fruits and seeds, which were assigned to S. wetzleri by comparing with related fossil species of the genus. Based on the occurrences of Spirematospermum fossils, we show the biogeographical distribution of the genus for the first time on a series of palaeogeographic maps of the Northern Hemisphere, and illustrate the probable spreading routes and directions. The accompanying flora from the Miocene of North China suggests that S. wetzleri lives in a waterside or swamp habitat of a warm temperate to subtropical climate.
We are grateful to the editor and two reviewers for their valuable comments and suggestions for improving the manuscript. This work was supported by the Natural Science Foundation of China (Grants No. 41502017 and No. 41072022), and the Strategic Priority Research Program of the Chinese Academy of Sciences (Grant No. XDPB05).
CSL designed the study. YL, TMY and CSL collected the materials. YL and TMY carried out the experiment and wrote the manuscript. YZL and CSL helped modify the manuscript. All authors read and approved the final manuscript.
The authors declare that they have no competing interests.
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