Late Triassic ecosystem variations inferred by palynological records from Hechuan, southern Sichuan Basin, China

Abstract The Late Triassic deposits of the Sichuan Basin, southwestern China are significant for hosting abundant and diverse fossil assemblages including plants (containing spores and pollen), bivalves and insects. However, the Late Triassic palaeoecological variations are still poorly documented in this region. Here we present results from a palynological study from the Upper Triassic Xujiahe Formation in Hechuan of Chongqing, southern Sichuan Basin. The palynological analysis revealed a well-preserved terrestrial palynoflora of high diversity, comprising 184 species in 75 genera of spores and pollen. Three palynological assemblages were recognized, reflecting terrestrial successions throughout the entire interval with significant changes in the vegetation. Cycads/bennettites/ginkgophytes and conifers show an increasing trend into younger deposits, while ferns and lycopsids decrease in relative abundance. The Late Triassic vegetation underwent changes from lowland fern forest to a mixed forest with more canopy trees. We applied the Spore-pollen Morphological Group (SMG) method and Sporomorph EcoGroup (SEG) model to interpret the palaeoclimate features. The results reveal that the lower part of the Xujiahe Formation was deposited under relatively warm and humid conditions with an overall cooling and drying trend from latest Norian to Rhaetian time, accompanied by a general decrease of ferns and simultaneous increase of gymnosperms, and a decline in diversity of miospores. This study presents data on variations within the terrestrial ecosystem prior to the end-Triassic extinction event in the Sichuan Basin, and therefore provides important information for understanding the changes in the vegetation preceding the end-Triassic event.

With regards to the duration of the end-Triassic extinction, many workers argue that the extinction occurred over a prolonged interval marked by a series of discrete extinction events during Carnian-Rhaetian, rather than a single mass extinction at the end of the Rhaetian Age (Benton, 1986;Hallam, 2002;Tanner, Lucas & Chapman, 2004;Bambach, 2006;Lucas & Tanner, 2008; studies on the Late Triassic ecosystem therefore form a very important role for better understanding the environmental changes prior to the end-Triassic extinction event.
In East Asia, the end-Triassic palaeobotanical and palynological records are somewhat scarce compared with Europe and North America. Two prime localities have so far been identified in China, both with wellexposed successions spanning the Triassic-Jurassic boundary, yielding diverse mega-and micro-floral records from terrestrial ecosystems. The regions include the Junggar Basin in the northwestern part of the country (Deng et al. 2010;Sha et al. 2011Sha et al. , 2015 and the Sichuan Basin in southwestern China . In particular, the Upper Triassic strata of the Xujiahe Formation are well developed in the Sichuan Basin, and contain diverse fossil plant assemblages (Ye et al. 1986;Huang & Lu, 1992;Huang, 1995;. Recent magnetostratigraphic studies revealed that the age of the Xujiahe Formation ranges from latest Norian to Rhaetian (from 207.2 Ma to 201.3 Ma at Qilixia, Xuanhan, northeastern Sichuan Basin) (Li et al. 2017). Previous palynological studies on the Upper Triassic successions within the Sichuan Basin have contributed much to understanding the diversity and stratigraphy of the basin (Li, 1974;Cao & Huang, 1980;Liu, 1982;Bai et al. 1983;Zhang, 1984;Lu & Wang, 1987;Yuan, 1989;Huang, 1991;Shang & Li, 1992;Wang et al. 2008. Recent efforts to decipher the regional responses of terrestrial plant communities prior to the end-Triassic event have been undertaken at several localities within the Sichuan Basin (Liu, Li & Wang, 2015a, b;. However, studies on the Late Triassic terrestrial palaeoenvironment based on palynology are still poorly documented in this region, thus our understanding on the Late Triassic ecosystem in the Sichuan basin therefore needs to be enhanced. The present study documents a detailed palynological record from the Upper Triassic Xujiahe Formation of the Tanba section in the Hechuan region, southern Sichuan Basin (Fig. 1). Based on our palynological data, we aim to: (1) describe the Late Triassic vegetation in terms of abundance and diversity; and (2) decipher the Late Triassic climate variations in the studied area and place the results in a broader palaeogeographical context of the Late Triassic Period.

Geological setting
Located at the western margin of the South China block and the eastern margin of the Tibet Plateau, the Sichuan Basin is a large terrestrial petroliferous and coal-bearing basin, covering an area of 260 000 km 2 . It is bounded to the west by the Longmenshan orogenic belt, to the east by the Xuefengshan intercontinental tectonic deformation system, to the north by the Micangshan and Dabashan uplift belts, and to the south by the Emeishan-Liangshan fault-fold belt . Palaeozoic -early Mesozoic marine strata are well developed in the adjacent mountain areas, including Precambrian, Cambrian, Ordovician, Silurian, Carboniferous, Permian and Lower-Middle Triassic deposits. The Upper Triassic is dominated by terrestrial successions, mainly distributed in the eastern and northeastern margin of the basin. The remaining part of the basin is covered by massive Jurassic and Cretaceous red beds Fig. 1).
Most importantly, the Upper Triassic strata represented by the Xujiahe Formation mainly consist of coalbearing clastic rocks deposited in an inland lacustrinefluvial-coal-swamp environment, varying over 400-650 m in thickness . The coal seams, which contain diverse plant remains (e.g. Xujiahe flora), play an important economic and scientific role in the Sichuan Basin .
The Xujiahe Formation is well exposed at the Tanba Section in the Hechuan region, southern Sichuan Basin ( Fig. 1), administratively belonging to Chongqing City. The Xujiahe Formation overlies the Middle Triassic marine Leikoupo Formation and is, in turn, conformably overlain by the terrestrial Lower Jurassic Zhenzhuchong Formation (Fig. 2). At the Tanba section, an c. 500 m outcrop of the Xujiahe Formation is well exposed. The lithology mainly comprises sandstones, siltstones, mudstones and coal beds, yielding a diverse and rich fossil assemblages of plants and bivalves. The Xujiahe Formation is subdivided into six lithological members (I-VI), numbered in ascending order. Members I, III and V are mainly dominated by mudstones and thin coal beds, representing floodplainlacustrine and coal swamp deposits, whereas members II, IV and VI mainly comprise sandstones, representing fluvial-delta deposits ; Fig. 2).

Materials and methods
Thirty-three palynological samples were collected from the Upper Triassic Xujiahe Formation (from the members I-VI) across the Tanba section in the Hechuan region. Eighteen samples were productive and yielded well-preserved and rich miospores (spores and pollen). No productive samples were however recovered from Member II (Fig. 2). All the productive samples were collected from organic-rich mudstones, siltstone and coal, therefore minimizing the taphonomic bias.
For palynological preparation, approximately 30 g of sediment was treated with HCl and HF to remove carbonates and silicate minerals, respectively.
The residue of each sample was then washed with distilled water until a neutral pH was reached. The residue was subsequently sieved through a 10 μm size mesh. Finally, the palynomorph-bearing residues were mounted on slides using glycerin jelly, and were sealed with paraffin wax. At least c. 250 sporomorphs were counted per sample. All samples were studied using an Olympus BX41 microscope. Photomicrographs were taken using a Zeiss Imager Z2 microscope and an Ax-ioCam HRc imaging system. The SMG (Spore-pollen Morphological Group) method outlined by Visscher & Van der Zwan (1981) and the SEG (Sporomorph EcoGroup) model established by Abbink (1998) and Abbink, van Konijnenburg-van Cittert & Visscher (2004) were applied in this study to reconstruct the palaeoclimatic variations. All palynological slides are stored at the Nanjing Institute of Geology and Palaeontology, Chinese Academy of Sciences, Nanjing, China.

Palynology
The miospores of the Xujiahe Formation in the Hechuan Section of Chongqing City, southern Sichuan Basin are diverse and well preserved, represented by 184 species of spores and pollen in 75 genera (see online Supplementary Table S1, available at http://journals.cambridge.org/geo). The representative miospores are illustrated in Figures 3-5. The palynoflora of the Xujiahe Formation from the Hechuan region has previously been assigned a Norian-Rhaetian age (Liu, Li & Wang, 2015b), which is supported by a recent geomagnetic study (Li et al. 2017). Here we provide a more detailed vegetation reconstruction coupled with palaeoclimatic interpretations through the studied succession. For palaeoclimatic and palaeoecological purposes, the palynological assemblages were divided based on relative abundance. Three assemblages were recognized and the percentages of selected taxa are illustrated in Figure 6. The characteristic features for each assemblage are outlined below in ascending stratigraphic order. The percentages are expressed in whole numbers.

4.b. Cycadopites reticulata -Pinuspollenites divulgatus -Dictyophyllidites harrisii -Aratrisporites fischeri (CPDA) assemblage (samples HC11-HC22)
The CPDA assemblage occurs in the upper part of Member III of the Xujiahe Formation (Fig. 6). It is characterized by the predominance of gymnosperm pollen grains (average relative abundance of 56 %) and a significantly lower portion of spores (44 %) compared to the other two assemblages.

Development of the vegetation
Based on the botanical affinity of the dispersed spore and pollen genera recovered from the studied succes-sions within the Hechuan region of the Sichuan Basin (Table 1), a picture of a diverse Late Triassic ecosystem emerges. Although the vegetation is chiefly dominated by ferns and conifers, other plant groups are present in lower relative abundance. These include mosses, horsetails and lycopsids which vary considerably in relative abundance through the studied succession (Fig. 7). The overall evolution of the Late Triassic vegetation in the Hechuan region is suggested to have undergone changes from lowland fern forest to a mixed forest with more canopy trees. The earliest Late Triassic DCKA ecosystem (represented in Member I and the base of Member III) was dominated by ferns, mainly Dipteridaceae/Matoniaceae together with a variety of other fern families including Cyatheaceae/Dicksoniaceae, Osmundaceae and Marattiaceae. These ferns, together with typical Triassic lycopsids and rare mosses, comprised the ground cover vegetation during the earliest part of Late Triassic time. The midstorey was represented by gymnosperms related to cycads/bennettites/ginkgophytes. Canopy trees were relatively scarce, represented by Pinaceae, Araucariaceae and Podocarpaceae, and the pollen may have been transported in from elevated areas into the lowlands. Seed ferns existed, but made up a very limited portion of this ecosystem.
The CPDA ecosystem was characterized by dominance in gymnosperms, mainly represented by cycads/bennettites/ginkgophytes making up the midstorey bush vegetation together with seed ferns. Canopy vegetation was represented by relatives of Pinaceae. The ferns are much less prominent in the CPDA assemblage compared to the older DCKA assemblage (Fig. 7b), and these were mainly represented by Dipteridaceae/Matoniaceae. Lycopsids are not as abundant compared with the DCKA assemblage. A new element, the family Cheirolepidiaceae (Classopollis), a group that was common during Jurassic and Early Cretaceous time around the world (Alvin, 1982;Vajda, 2001;Vajda & Wigforss-Lange, 2006;Jansson et al. 2008), interestingly appears in this assemblage.
In assemblage CMCQ, represented within the upper part of the Xujiahe Formation (Member V and VI), cycads/bennettites/ginkgophytes and conifers characterize the flora. It is interesting to note that Cyatheaceae/Dicksoniaceae show a sharp increase in abundance (average 10 %). Other fern families include Dipteridaceae/Matoniaceae, Osmundaceae, Marattiaceae and Pteridaceae. The mid-storey vegetation was dominated by monosulcate pollen producers, cycads/bennettites/ginkgophytes (Fig. 7c). Conifers including Cheirolepidiaceae, Araucariaceae, Pinaceae, Podocarpaceae and Taxodiaceae were prominent (average 24 %), making up the canopy. It is notable that Cheirolepidiaceae shows a remarkable increase in relative abundance and becomes common during this period (average 6 %). Seed ferns show an increasing trend (8 %). Lycopsids are less frequent, and mosses and horsetails are rare.

Palaeoclimatic interpretations
As a complement to the vegetation reconstruction based on the abundance data of pollen and spores related to their affinities, we have carried out palaeoclimatic interpretations by applying the Sporepollen Morphological Group (SMG) method (Visscher & Van der Zwan, 1981) and the Sporomorph EcoGroup model (SEG) (Abbink, 1998;Abbink, van Konijnenburg-van Cittert & Visscher, 2004).
Twelve Spore-pollen Morphological Groups (SMGs) A-L were identified in this study (Fig. 8), reflecting different ecological adaptations, including hygrophytic (water-loving, groups A-D), xerophytic (dry-loving, groups H-L) and intermediate elements (groups E-G). We have applied the ratio of hygrophytic elements to xerophytic elements (hygrophytic/xerophytic) as an index of humidity variation. The results (Fig. 8) show that the hygrophytic/xerophytic ratio is high in the lowermost part of the Xujiahe Formation, particularly at the base of Member III (Fig. 8, line A), indicating a humid pulse of short duration and expressed in one sample within the Xujiahe Formation. This is in agreement with the results based on the vegetation composition in Assemblage DCKA. The hygrophytic/xerophytic ratio is markedly low for the rest of the succession (with the exception for sample HC16; Fig. 8, line B), suggesting a drying trend upwards, interrupted by a short humid pulse.
Using the Sporomorph EcoGroup model (SEG) (Abbink, 1998;Abbink, van Konijnenburg-van Cittert & Visscher, 2004), we classified the palynomorphs into three SEG groups, including: (1) Lowland SEG; (2) Upland SEG; and (3) River SEG (Table 1, Fig. 9). Elements attributed to the Lowland SEG show a marked dominance in the Xujiahe Formation, with a maximum of 81 % and a minimum of 46 %; the River SEG and Upland SEG are less abundant. The total for the Lowland SEG and River SEG is a minimum of 69 % (Fig. 9). This implies that the studied area during Late Triassic time was represented by a general lake-marsh environment set in a lowland ecosystem. However, variations in the ecosystem and the climate during Late Triassic time are reflected in the palynological assemblages of this study, revealing that the ecosystem was not constant throughout this period as previously suggested (Huang & Lu, 1992;Wang et al. 2008. As indicated by the hygrophytic elements (groups A-D; Fig. 8), the highest abundance of the Lowland SEG is found in the lowermost sample of Member III (Fig. 9, line A), corresponding to the highest values of the Lowland/Upland ratio and Lowland wet/dry ratio, the lowest value of the Upland SEG and a relatively high warm/cool ratio, suggesting a relatively warm and humid interval. The Lowland wet/dry ratio is only high in the lowermost two samples, and shows a striking upwards decreasing trend, suggesting a general drying trend. The Lowland SEG and the Lowland/Upland ratio show two smaller peaks at samples HC16 of Member III (Fig. 9, line B) and HC24 of Member IV (Fig. 9), indicating two short intervals of humid climate conditions. The Lowland warm/cool ratio shows an overall decreasing upwards trend in the Xujiahe Formation, but has a striking peak at sample HC25 of Member IV (Fig. 9, line C), indicating an overall cooling trend during the Late Triassic period interrupted by a short warmer climate interval.
Previous palynological and palaeobotanical studies from the Sichuan Basin have shown that the Late Triassic palaeoclimate was generally one of humid and warm tropics-subtropics (Huang & Lu, 1992;Wang et al. 2008. However, with our more detailed, high-resolution palynological study, a different picture emerges. Our data reveal a highly variable Late Triassic ecosystem represented by a warm and humid climate during the earliest Late Triassic period (Mem-ber I and base of Member III), followed by a cooler and drier interval interrupted by two wetter and one warmer episodes.

Discussion
Our palynological study indicates an overall cooling and drying trend during latest Norian-Rhaetian time, accompanied by a general decrease in ferns (mainly represented by trilete spores), an increase in gymnosperms (represented by bisaccate and monocolpate pollen), and a decline in diversity of both pollen and spores (Fig. 10). Similar results have been reported from coeval deposits in Xuanhan, northeastern Sichuan Basin, indicating a cooling and drying climate during the development of the uppermost part of the Xujiahe Formation . The above outlined climate change is consistent with macrofloral studies of the Xujiahe Formation, which also implied a palaeoclimatic trend from humid to arid conditions (Huang & Lu, 1992). Palynological records from northwestern and central Europe, Western Australia and northeastern Greenland revealed a cooling during latest Triassic time (Hubbard & Boulter 1997 and the trend from humid to arid has also been noted from the Newark Basin  where it has been linked to the northwards drift of the North American continent. Palynological data from Austria and the United Kingdom indicated a warming trend from the Triassic to the Jurassic periods, interrupted by a cooler period (Bonis & Kürschner, 2012). Further, a bentho-planktonic study from the Austrian Alps suggested that cooling episodes might have occurred during latest Triassic time (Clémence et al. 2010). The above results may suggest a global cooling event during latest Triassic time. Tucker & Benton (1982) proposed climate-induced (increasing aridity) floral changes as a factor in Late Triassic tetrapod extinction. The present palynological record seems more consistent with a gradual ecosystem degradation extended over the Norian-Rhaetian interval. The cooling and drying climate from latest Norian to Rhaetian time may have caused a gradual ecosystem breakdown during latest Triassic time, and later triggered the end-Triassic biotic crisis.

Conclusions
Our detailed palynological investigation of Upper Triassic terrestrial deposits within the Sichuan Basin has revealed a well-preserved and diverse palynoflora.
(1) Our study reveals an ecosystem in change where a fern-dominated vegetation was replaced by conifers and cycadoids, supplemented by relative high portions of Classopollis in the uppermost Triassic strata. Palynological diversity patterns show a decreasing trend upsection.
(2) Three palynological assemblages were distinguished by variations in the abundance of major plant groups, reflecting remarkable changes in the terrestrial vegetation throughout the entire interval. Cycads/bennettites/ginkgophytes and conifers show an increasing trend into younger deposits, while ferns and lycopsids decrease in relative abundance.
(3) By applying the SMG method and SEG model analysis, we show that the early stage of the Late Triassic period was characterized by a relatively warm and humid climate which was followed by a cooler and drier interval. This demonstrates that the climate was not static, but rather variable.
(4) Our results reveal vegetation changes within the Sichuan Basin during the Late Triassic Period, adding to knowledge on biotic changes immediately prior to the end-Triassic event. . This is a contribution to the IGCP project 632, sponsored by Unesco/IUGS. We also thank Evelyn Kustatscher and an anonymous reviewer for their constructive comments which led to the improvement of the manuscript.

Supplementary material
To view supplementary material for this article, please visit https://doi.org/10.1017/S0016756817000735.