Seed cones of Tsuga (Pinaceae) from the upper Miocene of eastern China: Biogeographic and paleoclimatic implications
Introduction
Tsuga (Endl.) Carrière is a genus of conifer family Pinaceae, commonly called the Hemlock, which is a key component of humid mixed coniferous and broad-leaved deciduous forests in subalpine or lowland areas of North America and East Asia (Hirokawa, 1972, Burns and Honkala, 1990, Farjon, 1990, Fu et al., 1999, Havill et al., 2008, Fang et al., 2010). There are nine species within the genus (Fig. 1): T. chinensis (Franch.) E. Pritz., T. forrestii Downie and T. dumosa (D. Don) Eichler occur in China and the Himalayas, T. diversifolia (Maxim.) Mast. and T. sieboldii Carrière in Japan, T. heterophylla (Raf.) Sarg. and T. mertensiana (Bong.) Carrière in western North America, and T. canadensis (L.) Carrière and T. caroliniana Engelm. in eastern North America (Farjon, 1990). In addition, the Chinese endemic species T. longibracteata W.C. Chen has been transferred to the monospecific genus Nothotsuga Hu ex C.N. Page (Page, 1988). The hemlocks prefer shady and moist sites and are vulnerable to drought, and therefore are usually considered as a good indicator of humid environment (LePage, 2003a, Yang et al., 2009, Xing et al., 2013, Wang et al., 2015).
The earliest record of Tsuga can be traced back to the Late Cretaceous (ca. 90 Ma) from Poland (Macko, 1963), and it rapidly spread to Eurasia and North America in forms of pollens, leaves, woods, seed cones and seeds in the Cenozoic (LePage, 2003a). Although Tsuga pollen is well represented from the Upper Cretaceous to the Eocene in Europe, the macrofossils occurred in this region until to the late Oligocene (Geinitz, 1842, Mai and Walther, 1978). The earliest known seed cones of Tsuga were discovered from the middle Eocene (41.3–47.5 Ma) in the Far North of Canada (Eberle and Storer, 1999, Harrison et al., 1999, LePage, 2003a, LePage, 2003b).
Detailed description of morphological features of leaves, cones and bracts of all extant Tsuga species as well as of the fossil T. swedaea LePage was presented by LePage (2003a). Based on the distribution of Tsuga fossils, LePage, 2003a, LePage, 2003b suggested that Tsuga spread from western Europe into North America by the DeGeer Route before the Eocene/Oligocene boundary, and the exchange of Tsuga between North America and Asia occurred throughout the Cenozoic across the Beringian Corridor.
The oldest twigs of Tsuga were reported from the lower Cretaceous in North China (Tan and Zhu, 1982), which is earlier than the pollen record from the upper Cretaceous of Poland although further evidences are still needed for the identification (Wu et al., 2020). During the Paleocene, fossil pollen of Tsuga had been reported from eastern and northern China (Sun et al., 1982, Song et al., 1999). In a recent study, Wu et al. (2020) described two species of this genus based on seed cones from the late Eocene (34.6 ± 0.8 Ma) deposits in eastern Tibet and the early Oligocene (32 ± 1 Ma) deposits in central Yunnan Province. Subsequently, Tsuga fossil pollen records are widely distributed throughout in China from the lower Miocene to the Pleistocene (Sun et al., 1980, Sun et al., 1981, Xia et al., 1987, Wang and Zhang, 1990, Wang, 1999). The macrofossils, such as seed cones of T. xianfengensis Xing et Zhou (Xing et al., 2013) and fossil wood of T. nanfengensis Bondarenko, Wang et Zhou (Wang et al., 2015) from the upper Miocene in Yunnan, and fossil wood of T. cf. dumosa from the upper Pliocene in western Yunnan (Yi et al., 2005), and cones of Tsuga sp. from the upper Pliocene to the lower Pleistocene in Sichuan (Chen et al., 1986), have also been reported. In addition, Tsuga pollens, leaves, seeds, twigs, cones and scales had also been well documented in Japan since the Miocene (Hikita, 1954, Miki, 1957, Onoe, 1971, Onoe, 1989, Kamoi et al., 1988, Takahara and Takeoka, 1992, Matsumoto et al., 1995). Abundant Tsuga records from East Asia provide new view to reveal its systematic evolution and biogeographical history.
The present seed cones of Tsuga were recovered from the upper Miocene Shengxian Formation in eastern Zhejiang, China. These cones are preserved with fine cone–scale complexes including bracts and seed impressions. Based on a detailed comparison with all extant and selected fossil cone species of Tsuga, these fossil cones are assigned to Tsuga cf. dumosa. It provides valuable evidence for the diversification of the Asian Tsuga lineage during the Miocene and the migration of Tsuga driven by the paleoclimate changes.
Section snippets
Materials and methods
The fossil cones described here were recovered from the Miocene Shengxian Formation at the border of Ninghai County and Tiantai County, Zhejiang Province, eastern China (121°14′E, 29°09’N; Fig. 2). The Shengxian Formation is characterized by multiple volcanic eruptions and sedimentary interlayers with plenty of plant fossils (Ding, 2011, Li et al., 2014). Based on 40Ar/39Ar dating, the basalts underlying the present fossil-bearing horizon yield an age of 10.8 ± 1.9 Ma, and the overlying basalts
Systematics
Order: Pinales Gorozh.
Family: Pinaceae Lindley
Genus: Tsuga (Endlicher) Carrière
Species: Tsuga cf. dumosa (D. Don) Eichler
Studied materials: HNT-701 (Plate I, 1; Fig. 3, A), HNT-258 (Plate I, 2), JHU-1-054 (Plate I, 3), JHU-206 (Plate I, 4), JHU-1-3075 (Plate I, 5), JHU-1-488 (Plate I, 6).
Repository: Fossil cones are deposited in the Institute of Palaeontology and Stratigraphy, Lanzhou University, Lanzhou, China.
Locality: Jiahu Village and Huangnitang Village, near the border of Ninghai County
Comparison with extant genera of Pinaceae
The present fossil cones possess helically arranged cone-scale complexes, which only occurred in the families Pinaceae and Araucariaceae (Xing et al., 2013). However, the cone scales of Araucariaceae are one-seeded lacking distinct bracts (Silba, 1986), which differ from our fossils. Frankis (1988) had put some key characters, such as cone scale shape, seed position and bract size and form, to distinguish the genera of Pinaceae. The present fossil cones differ from those of Pinus Linn. which
Biogeographical and paleoclimatic implications
Based on the fossil record, LePage, 2003a, LePage, 2003b concluded that Tsuga had spread from western Europe into North America during the late Paleocene and Eocene via the DeGeer Route and the Thulian Route, whereas the exchange between North America and Asia occurred throughout the Cenozoic across the Beringian Corridor. Due to lack of the key fossil record from East Asia, the origin and evolutionary history of Tsuga is still not very clear (Chen et al., 2018). However, the oldest Tsuga twigs
Declaration of Competing Interest
None.
Acknowledgment
We are grateful to two anonymous reviewers for their constructive suggestions and comments. This work was supported by the National Natural Science Foundation of China [grant numbers 41972010 and 31870200], the Strategic Priority Research Program (B) of the Chinese Academy of Sciences [grant number XDB26000000], the Second Tibetan Plateau Scientific Expedition and Research Program [grant number 2019QZKK0704], and the State Key Laboratory of Palaeobiology and Stratigraphy, Nanjing Institute of
References (69)
- et al.
Needles and seed cones of Pinus premassoniana sp. nov., and associated pollen cone from the upper Miocene in East China
Rev. Palaeobot. Palynol.
(2013) - et al.
A new species of Castanopsis (Fagaceae) from the upper Pliocene of West Yunnan, China and its biogeographical implications
Palaeoworld
(2014) - et al.
Tsuga seed cones from the late Paleogene of southwestern China and their biogeographical and paleoenvironmental implications
Palaeoworld
(2020) - et al.
A new Tsuga species from the upper Miocene of Yunnan, southwestern China and its palaeogeographic significance
Palaeoworld
(2013) - et al.
Two Pinus species from the upper Miocene in Zhejiang, China and their palaeobiogeographic significance
Rev. Palaeobot. Palynol.
(2015) - et al.
A preliminary study on environmental change since the last 20,000 years
The Eocene Copper Basin flora of northeastern Nevada
Univ. Calif. Publ. Geol. Sci.
(1966)The Eocene Thunder Mountain flora of central Idaho
Univ. Calif. Publ. Geol. Sci.
(1998)- et al.
Silvics of North America: 1. Conifers
- et al.
Plant fossils from Mula Formation in Litang County and their significance in palaeogeography and palaeoclimate
Is the East Asian flora ancient or not?
Natl. Sci. Rev.
Reconstruction of paleovegetation and paleoclimate of the late Miocene flora in Tiantai, Zhejiang, China
The Gymnosperm Database
Northernmost record of brontotheres, Axel Heiberg Island, Canada–Implications for age of the Buchanan Lake Formation and brontothere paleobiology
J. Paleontol.
Atlas of Woody Plants in China: Distribution and Climate
Pinaceae: Drawings and Descriptions of the Genera Abies, Cedrus, Pseudolarix, Keteleeria, Nothotsuga, Tsuga, Cathaya, Pseudotsuga, Larix, and Picea
A Handbook of the World’s Conifers
Generic inter-relationships in Pinaceae
Notes R. Bot. Garden Edinb.
Pinaceae
A monograph of the British Eocene flora
Über Versteinerungen von Altenburg und Ronneburg
Mitteilungen Akademie der Osterlande
Correlation of Cenozoic sequences of the Canadian Arctic region and Greenland; Implications for the tectonic history of northern North America
Bull. Can. Petrol. Geol.
Phylogeny and biogeography of Tsuga (Pinaceae) inferred from nuclear ribosomal ITS and chloroplast DNA sequence data
Syst. Bot.
Geologic time and ecological environment of the Shengxian Formation flora from eastern Zhejiang and volcanic activity influence
A study on the floral remains around Osaka Bay in Japan since the Pliocene
Rep. Board Educ., Osaka Prefecture
Atlas of the Japanese Flora: An Introduction to Plant Sociology of East Asia
The Aniai flora of Akita Prefecture, and the Aniai-type floras in Honshu, Japan
J. Mining Coll., Akita Univ. Ser. A, Mining Geol.
Plant fossil assemblage of the last glacial age in the northern part of Niigata Prefecture, central Japan
Quat. Res. (Tokyo)
Conifers of the Mastixioideae-flora from Wiesa near Kamenz (Saxony, Miocene) with special consideration of leaves
Palaeontographica
A new species of Tsuga (Pinaceae) from the middle Eocene of Axel Heiberg Island, Canada, and an assessment of the evolution and bio-geographical history of the genus
Bot. J. Linn. Soc.
The evolution, biogeography, and paleoecology of the Pinaceae based on fossil and extant representatives. Pinaceae based on fossil and extant representatives. Proceedings of the Fourth International Conifer Conference
Acta Hortic.
Hemisphere-scale differences in conifer evolutionary dynamics
Proc. Natl. Acad. Sci. USA
Stratum characteristics of the Neogene Shengxian Formation in Zhejiang Province and its related fossil studies
J. Lanzhou Univ. (Nat. Sci.)
Two new Castanopsis (Fagaceae) species based on cupule and foliage from the upper Miocene of eastern Zhejiang, China
Plant Syst. Evol.
Cited by (5)
Influence of climate factors on the global dynamic distribution of Tsuga (Pinaceae)
2024, Ecological IndicatorsA novel seed cone of Pinus from the Miocene of coastal Southeast China indicates kinship with Southeast Asian pines
2023, Plant DiversityCitation Excerpt :As mentioned above, four fossil species excluding our specimens were previously described from varying fossil sites of the equivalent strata based on morphological distinctions, that is, Pinus premassoniana from Jiahu in Tiantai (Ding et al., 2013), P. speciosa from Lüjia in Ninghai (Li and Guo, 1982) and P. preyunnanensis from Huangnitang in Ninghai and P. prekesiya from Daluxia in Ninghai (Xu et al., 2015b). Additionally, there are several coniferous taxa documented from the equivalent strata in eastern Zhejiang, e.g., deciduous Pseudolarix Gordon (Bai and Li, 2017), and evergreen Nothotsuga Hu ex C.N. Page (Ding et al., 2021a), Tsuga Carrière (Ding et al., 2021b), Calocedrus Kurz (Zhang et al., 2015) and Cunninghamia R. Brown (Du et al., 2012). These diverse, coeval fossil records indicate that eastern Zhejiang was one of the hot spots for coniferophyte diversity during the late Miocene.
Enhanced precipitation has driven the evolution of subtropical evergreen broad-leaved forests in eastern China since the early Miocene: Evidence from ring-cupped oaks
2023, Journal of Systematics and Evolution