Early Cretaceous atmospheric CO2 estimates based on stomatal index of Pseudofrenelopsis papillosa (Cheirolepidiaceae) from southeast China

Accepted Manuscript Early Cretaceous atmospheric CO2 estimates based on stomatal index of Pseudofrenelopsis papillosa (Cheirolepidiaceae) from southeast China Dai Jing, Sun Bainian PII:

S0195-6671(16)30315-9

DOI:

10.1016/j.cretres.2017.08.011

Reference:

YCRES 3684

To appear in:

Cretaceous Research

Received Date: 3 November 2016 Revised Date:

2 August 2017

Accepted Date: 19 August 2017

Please cite this article as: Jing, D., Bainian, S., Early Cretaceous atmospheric CO2 estimates based on stomatal index of Pseudofrenelopsis papillosa (Cheirolepidiaceae) from southeast China, Cretaceous Research (2017), doi: 10.1016/j.cretres.2017.08.011. This is a PDF file of an unedited manuscript that has been accepted for publication. As a service to our customers we are providing this early version of the manuscript. The manuscript will undergo copyediting, typesetting, and review of the resulting proof before it is published in its final form. Please note that during the production process errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain.

ACCEPTED MANUSCRIPT Early Cretaceous atmospheric CO2 estimates based on stomatal index of

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Pseudofrenelopsis papillosa (Cheirolepidiaceae) from southeast China

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Dai Jing,a, * Sun Bainianb

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a

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650091, China

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b

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730000, China

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Corresponding Author: Dai Jing

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Corresponding Author's Address: School of Earth Science and Resource Environment

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School of Earth Science and Resource Environment, Yunnan University, Kunming

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School of Earth Science and Mineral Resource, Lanzhou University, Lanzhou

Chenggong Campus, Yunnan University, Kunming, Yunnan 650091, China

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E-Mail: daijing@ ynu.edu.cn

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ACCEPTED MANUSCRIPT Abstract: Estimates of the atmospheric carbon dioxide concentration levels were

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made for three time intervals of the Early Cretaceous using the stomatal indices of an

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extinct fossil conifer, Pseudofrenelopsis papillosa (Chow et Tsao) Cao ex Zhou. The

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fossil materials were collected from the upper Hauterivian, upper Aptian, and upper

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Albian of the Lower Cretaceous in the Fujian and Jiangxi Provinces of southeast

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China. The estimated paleo-CO2 (pCO2) was 600–1300 ppmv from the late

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Hauterivian to the late Albian based on the ratio between the stomatal indices of fossil

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species P. papillosa and those of four modern nearest living equivalent (NLE) species,

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using Carboniferous and recent standardizations. The results showed a low value of

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595–957 ppmv in the late Hauterivian, and a high value of 805–1292 ppmv in the late

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Albian, which was only slightly higher than the value of 753–1210 ppmv in the late

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Aptian. Our calculated CO2 values were consistent with GECORB II, and similar to

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the previously published estimates of CO2 based on stomatal indices or carbon

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isotopes. Thus, it could be inferred that the stomatal index of P. papillosa is a potential

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indicator for estimating the pCO2 content during the geological history. Furthermore,

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the global mean land surface temperature (GMLST) was estimated based on the CO2

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data. This showed that the change ratios of GMLST increased from 2.8–4.7 °C in the

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late Hauterivian to 3.6–5.5°C in the late Albian and 3.8–5.7°C in the late Aptian. It

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appears that the temperature gradually increased from the early to late Early

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Cretaceous.

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Keywords: Pseudofrenelopsis papillosa; stomatal index; atmospheric CO2 concentration; Early Cretaceous

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1. Introduction As an important greenhouse gas, carbon dioxide (CO2) plays a central role in

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climate change and terrestrial ecosystem evolution (Royer et al., 2004; 2007; Beerling,

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2005; Kürschner et al., 2008). A clear understanding of the CO2 variations and

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relationship between CO2 and surface temperature in the geological past is critical for

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predicting the climate response to future elevated atmospheric CO2 levels (Retallack,

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2009a; Breecker et al., 2010). In recent years, multiple proxies have been used to

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estimate the paleo-CO2 levels over geological time, including geochemical and

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biogeochemical models (Berner, 1991, 1994, 2006; Tajika, 1998; Berner and

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Kothavala, 2001; Bergman et al., 2004; Franks et al., 2014), carbon isotope (δ13C)

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analyses from diagenetic minerals, paleosol carbonates, ice-core records, and marine

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phytoplankton (e.g. Cerling, 1992; Mora et al., 1996; Pagani et al., 1999, 2005; Leier

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et al., 2009; Tripati et al., 2009; van de Wal et al., 2011; Huang et al., 2012), as well as

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the boron isotope δ11B found in the chitin of pelagic foraminifera (Pearson and Palmer,

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2000; Pearson et al., 2009) and the stomatal parameters of fossil leaves (McElwain

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and Chaloner, 1996; McElwain et al., 1999; Retallack, 2001, 2002; Beerling and

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Royer, 2002).

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The Cretaceous has long been regarded as one of the best examples of

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greenhouse climates in Earth history (Skelton et al., 2003; Hu et al., 2005). The

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temperature of Earth was relatively high, the Polar Regions were free from permanent

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ice sheets, and the climate changed between arid and humid during the Cretaceous

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(Tarduno et al., 1998; Föllmi, 2012; Wang et al., 2014). The atmospheric CO2

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ACCEPTED MANUSCRIPT concentration was relatively high and reached its peak in the mid-Cretaceous, which

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was evaluated to have been 4–10 times higher than that prior to the Industrial

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Revolution (Cojan et al., 2000; Berner and Kothavala, 2001; Bice and Norris, 2002).

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However, the geochemical and paleobotanical data showed that a high or continuous

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CO2 greenhouse effect was not present throughout the Cretaceous, especially during

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the Early Cretaceous (Kessels et al., 2006; McArthur et al., 2007; Huang et al., 2012).

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Many climate and ecosystem records during the Early Cretaceous remain incomplete

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(Heimhofer et al., 2005), and a more detailed time series for the CO2 concentration

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would be helpful in understanding Early Cretaceous climate change and terrestrial

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ecosystem evolution.

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Pseudofrenelopsis (Cheirolepidiaceae) is a potential indicator for CO2 estimates

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during the Early Cretaceous (Haworth et al., 2005; Ren et al., 2008; Du et al., 2016),

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with estimates mainly being reported from the Lower Cretaceous of Europe, Asia, and

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North America (Reymanówna and Watson, 1976; Upchurch and Doyle, 1981; Watson

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and Fisher 1984; Watson, 1988; Cao, 1994; Zhou, 1995; Deng et al., 2005; Axsmith

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et al., 2005; Axsmith, 2006; Yang et al., 2009; Du et al., 2014). In recent years, many

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fossil conifers of Pseudofrenelopsis papillosa have been collected with well-preserved

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cuticles from the Fujian and Jiangxi Provinces of southeast China. In the present

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research, a stomatal-based method was applied to estimate the paleo-CO2 levels

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during the three time intervals of the late Hauterivian, late Aptian, and late Albian of

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the Early Cretaceous, using P. papillosa samples from the Fujian and Jiangxi

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Provinces of southeast China. Moreover, the similarity of the stomatal parameters for

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ACCEPTED MANUSCRIPT P. papillosa, P. parceramosa and analogous fossil conifers from different areas of the

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Northern and Southern Hemispheres was investigated. The results of our study

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supplement the global database of CO2 concentration.

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2. Geological settings

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Very thick volcanic rocks, and fluvial and lacustrine clastic rocks, were formed

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during the Mesozoic in southeast China by tectonic movements and magmatic activity

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(Ding et al., 1989). The Cretaceous strata are well-developed and exposed in several

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large and small basins. These basins are characterized by red rocks, in which some

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fossil remains have been reported (Li, 1997; Wu et al., 2002). The plant fossils were

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collected from the Bantou and Junkou Formations in the Fujian Province, and the

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Zhoujiadian Formation in the Jiangxi Province of southeast China (Fig.1).

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(Fig.1 inserted near here)

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Fossils were collected from the Bantou Formation near the Jishan Village (E

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117°19′，N 25°57′), at about 5 km to the southwest of the Yong’an City; from the

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Junkou Formation near the Longdong Village (E 117°43′，N 26°22′), at about 7 km to

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the west of the Shaxian Country; and from the Zhoujiadian Formation near the

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Xintian Village (E 117°10′，N 28°13′) in Luohe Town, Guixi City of Jiangxi Province.

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The Bantou Formation was deposited in a freshwater lacustrine environment

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(Sze, 1945), which is angularly unconformably underlain by the Nanyuan Formation

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and conformably overlain by the Jishan Formation (Cao et al., 1990). It mainly

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consists of grayish-green and grayish-black siltstones, tuffaceous sandstones, and

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shales, with thin interbeds of fine sandstones, sandy conglomerates, and small tuffs 5

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(Cao et al., 1990). The paleoclimate was relatively dry, being subtropical to tropical

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(Sze, 1945). Paleobotanical and palynological data support the conclusion that the

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formation is late Hauterivian in age (Zheng et al. 1986; Chen, 1991). The Junkou Formation exposed in the Shaxian Basin is unconformably underlain

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by the Baiyashan Formation and conformably overlain by the Shaxian Formation (Li

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et al., 1997). The age is late Aptian (112–116Ma) based on the paleomagnetic data and

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K-Ar isotope dating (Li, 1994). The Junkou Formation mainly consists of grayish,

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grayish-yellow, and grayish-green siltstones, along with calcareous siltstones and dark

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gray mudstones in a fluvial environment. It occasionally contains thin gypsum

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interbeds. The fossil-bearing horizon occurs in the upper part of the formation.

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The Zhoujiadian Formation is comparatively well-developed to the south of the

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Guixi City, Jiangxi Province, and is predominantly composed of fluvial and lacustrine

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clastic and muddy sediments, with a small amount of volcanic rock (Ding et al., 1989).

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It is conformably underlain by the Shixi Formation and overlain by the Nanxiong

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Formation with disconformity. Lithologically, the Zhoujiadian Formation is mainly

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composed of white-gray conglomerates, pebbly sandstones, grayish-green and

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yellowish-green sandstones, and mudstones. It contains gypsum beds (Wu, 1996; Wu

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et al., 2002). The sedimentological and paleontological data suggest that the

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Zhoujiadian Formation formed under high temperatures, and frequently experienced

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drought conditions, with low precipitation compared to the evaporation (Ding et al.,

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1989; Sun et al., 2011). The fossil remains were collected from the grayish-green

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mudstones in the middle part of the Zhoujiadian Formation. Based on the isotope

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fossil-bearing bed is late Albian in age and thought to be from 101 to 105 Ma (Zhao et

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al., 1997; Wang et al., 2002; Lu et al., 2007).

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3. Materials and Methods

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3.1 Stomatal ratio method for paleo-CO2 reconstructing

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The stomatal ratio (SR) is the stomatal index of the nearest living equivalent

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(NLE) over that of the fossil plant. The NLE is defined as a living taxon that, as far as

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possible, has an ecological setting and structure that are comparable to its Paleozoic or

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Mesozoic counterparts (McElwain and Chaloner, 1995). The NLE-based SR method

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for CO2 estimates is semi-quantitative. It was developed in the 1990s based on the fact

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that the stomatal index (SI) of plants has an inverse relation to the atmospheric CO2

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concentration (Woodward 1987; Woodward and Kelly, 1995; McElwain and Chaloner,

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1995; McElwain, 1998). The SR method shows a pattern of paleo-CO2 trends through

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geological time similar to those predicted using GEOCARB geochemical models for

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the long-term carbon cycle (Berner, 1994; Royer et al., 2001). Two calibrations were

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proposed by Chaloner and McElwain (1997) and McElwain (1998) to correlate the SR

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to RCO2, where RCO2 is the ratio of the paleo-CO2 concentration over the

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pre-industrial revolution level (approximately 300 ppmv). One calibration involved

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Carboniferous standardization, which was performed using the SR of the SI of the

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conifer fossil Lebachia frondosa from the Permian over the SI of Swillingtonia

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denticulata from the Carboniferous correlated with the RCO2 of GEOCARB II

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(Berner, 1994). The results showed that one unit of SR was equal to two units of

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ACCEPTED MANUSCRIPT RCO2 (1SR=2RCO2). The other calibration involved recent standardization, based on

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the SR of the SI of the fossil Lauraceae over that of its NLE species. It showed that

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one SR unit was equivalent to one RCO2 unit (1SR=1RCO2) when presuming that the

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atmospheric CO2 concentration of the NLE species collected was 300ppmv

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(McElwain, 1998). However, the CO2 values of the NLE species collected (CO2n)

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were variable. Thus, CO2n data were needed to estimate the paleo-CO2. Therefore, it

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was concluded that pCO2=SR×CO2n. The CO2n data were based on data from an

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observation station located on Mauna Loa Mountain in Hawaii (cited from Tans P.

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NOAA/ESRL,

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http://www.esrl.noaa.gov/gmd/ccgg/trends/).

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standardizations are regarded as broad minimum and maximum estimates of

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paleo-CO2.

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3.2 Fossil materials and cuticle preparation

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CO2

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annual

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mean and

data,

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All the specimens and slides are housed in the Paleontological Laboratory of

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Lanzhou University, Lanzhou, China. The curatorial museum numbers YA, SX and

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GX represent Yong’an, Shaxian, and Guixi, respectively, where the samples were

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collected. The leafy shoots of Pseudofrenelopsis papillosa are sparsely branched, with

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fine parallel longitudinal ridges and grooves on their surfaces and small triangular

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leaves loosely arranged in a simple spiral (Fig. 2). Cuticles of P. papillosa were

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isolated using standard maceration and mounted in glycerol on glass slides. Digital

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images were taken using a camera attached to a Leica DM4000B light microscope. As

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cuticular features, stomata are irregularly and sparsely distributed on the leaf surface

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ACCEPTED MANUSCRIPT and well-defined on both adaxial and abaxial internode cuticles. Stomatal and

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non-stomatal rows are clearly arranged longitudinally on internode cuticles. The

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non-stomatal bands are composed of 2–3 rows of square or rectangular cells, and the

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stomatal bands are uniseriate, with 6–9 rows per millimeter. The stomata are sparsely

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distributed or even absent at the base of the internode, but dense and well-defined in

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the middle part. They are generally separated from each other by 1–3 ordinary

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epidermal cells. Each stoma usually has 4–6 subsidiary cells, on which papillae are

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well-developed and overhang the mouths of the stomatal pit, protruding proximally to

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form a thick Florin ring around the stomatal pit (Sun et al., 2011; Fig. 3).

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(Fig. 2 and Fig. 3 inserted near here).

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3.3 Counting approaches and statistical analysis

Counts were taken in the middle parts of internode cuticles, where the stomata

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and ordinary epidermal cells are arranged in regular longitudinal rows. Generally, two

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stomatal rows are separated by 3–6 ordinary epidermal cells. The counting was

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conducted with digital images and the software Adobe Photoshop CS3, using the

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method of Poole and Kürschner (1999). For each count, a relatively large area was

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selected prior to counting. Generally, the statistical area was approximately 0.3 mm2,

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whereas for some cuticle fragments, the area was approximately 0.15 mm2. Usually,

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each counting area covered 10–30 stomata and 250–550 ordinary epidermal cells. We

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only considered stomata and ordinary epidermal cells on the border of the area when

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their area was more than half of the total area. Overall, 16 cuticles of

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Pseudofrenelopsis papillosa were prepared. From five to seven cuticular areas were

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counted per cuticle specimen, and 2–3 different grids for each cuticle were counted.

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Thus, the statistics corresponded to the average of at least 10 times the counting

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results. An ANOVA analysis was established based on the SI sets and estimated pCO2

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values in order to test the inter-group difference in pCO2 values between the three

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time intervals of the late Hauterivian, late Aptian and late Albian. Assuming a

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CO2–temperature coupling (Royer, 2006), the globe mean land surface temperature

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(GMLST) was calculated based on the obtained stomatal data of conifers in this paper,

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and the change ratio of the mean global surface temperature has been determined,

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using the CO2 climate sensitivity formula of Kothavala et al. (1999), δT=4×lnRCO2.

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4. Results and discussion

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4.1 Stomatal index

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The SI of Pseudofrenelopsis papillosa from the upper Hauterivian Bantou

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Formation had a range of 5.4–6.1, with an average of 5.8. The SI from the upper

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Aptian Junkou Formation was 4.2–4.9, with an average of 4.6. The SI from the upper

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Albian Zhoujiadian Formation had a range of 3.9–4.6, with an average of 4.3. In

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general, the SI values of Pseudofrenelopsis papillosa showed a significant decline

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from the upper Hauterivian to the upper Albian, which suggest that the SI was

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influenced by environmental conditions. Specifically, the fossil beds were deposited

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in fluvial and lacustrine environments, experiencing a relative drought paleoclimate

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with no stressful conditions. It was assumed that the main forcing on the stomatal

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frequency of P. papillosa was the paleoatmospheric CO2 content, although several

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environmental factors might have acted on its physiology (Royer, 2001; Passalia,

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2009). Haworth et al. (2005) analyzed the stomatal indices of Pseudofrenelopsis

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parceramosa (Fontaine) Watson from the lower Hauterivian to upper Albian of the

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Potomac Group of the eastern USA and Wealden Group of southern England. The SI

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values of P. parceramosa were 6.0 from the upper Hauterivian, 5.4 from the upper

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Aptian and 5.3 from the upper Albian. Obviously, the mean SI values of P.

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parceramosa found by Haworth et al. (2005) were similar to those of the present

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specimens from the same age. Passalia (2009) analyzed the SI of another extinct

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conifer genus Brachyphyllum from the middle Aptian to the upper Albian of

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Patagonia, Argentina. Brachyphyllum leaves are morphologically similar to those of

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Pseudofrenelopsis, both have scale-like adpressed, spirally arranged leaves. The SI

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values of Patagonia were 5.7 from the middle Aptian and 5.2 from the upper Albian.

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Passalia (2009) suggested that Brachyphyllum leaves had SI values similar to those of

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P. parceramosa of the same age, as reported by Haworth et al. (2005). They were also

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similar to those of P. papillosa in our study. The similarity in the SI values between

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the genera Brachyphyllum and Pseudofrenelopsis was also noted by Du et al. (2016)

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based on conifer samples from the upper Aptian to lower Albian of Jiuquan, northwest

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China. Their results showed that the SI values were 5.4–5.7 for Brachyphyllum, and

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5.9 for Pseudofrenelopsis from the upper Aptian, which were slightly higher but not

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very different from those of our study of the same time. Although the fossil conifers

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represent several species and come from different parts of the world, their SI values

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ACCEPTED MANUSCRIPT show considerable similarity. This observation supports the concept of McElwain and

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Chaloner (1996) that the different fossil species with similar morphological,

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ecological, and physiological traits display similarity in SI values. Assuming that the

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main forcing on the SI values of these fossil species was the pCO2 content, the

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similarities found in the SI values of fossils from the Northern and Southern

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Hemispheres for the same time intervals support the use of the SI as a proxy of CO2.

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4.2 Estimation of Early Cretaceous CO2 concentration

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The shoots of Pseudofrenelopsis papillosa morphologically and ecologically

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resemble those of the living cupressacean conifers Callitris, Calocedrus, and

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Tetraclinis (Watson, 1977; Alvin et al., 1981; Haworth et al., 2005). All of these

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species have small leaves and thick cuticles that are very suitable for a drought

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environment (Waston, 1977). Similarities also exist between P. parceramosa and the

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halophytic angiosperm Salicornia (Upchurch and Doyle, 1981), but the paleoecology

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is likely to have been different. Athrotaxis cupressoides was regarded as one of the

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NLE species of Pseudofrenelopsis and Brachyphyllum by Passalia (2009) and Du et

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al., (2016), based on the similarity of its morphological, environmental and ecological

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traits. However, a study of the sensitivity of the SI response to atmospheric CO2

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variation among some living conifers showed that Tetraclinis articulata, Callitris

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columnaris, Callitris rhomboidea, and Athrotaxis cupressoides displayed significant

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decreases in their SI values with an increase in the CO2 concentration (Haworth et al.,

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2010). Therefore, these four sensitive species are considered to be the NLE species of

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the fossil P. papillosa studied here. A generalized NLE stomatal index was produced

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concentration data for the collected years are cited from Haworth et al. (2010). As a

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result, the mean SI of the NLE species is 9.2±1.2, and the corresponding average CO2

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concentration is 373.6 ppmv (Table 1).

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(Table 1 inserted near here)

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Based on the SI data of Pseudofrenelopsis papillosa and its NLE species, the

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estimated CO2 values had ranges of 905–1022 ppmv in the late Hauterivian,

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1127–1314 in the late Aptian, and 1200–1415 ppmv in the late Albian when corrected

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with the Carboniferous standardization; and they were 563–636 ppmv in the late

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Hauterivian, 701–818 ppmv in the late Aptian, and 747–881 ppmv in the late Albian

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when corrected with the recent standardization (Table 2). Taking the minimum and

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maximum limits of the CO2 values defined by the Carboniferous and recent

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standardization, the average data indicate pCO2 ranges of 595–957 ppmv for the late

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Hauterivian, 753–1210 ppmv for late Aptian, and 805–1292 ppmv for late Albian

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(Table 3). A minimum P-value of 4.25×10-6 was obtained using an ANOVA analysis

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of the three sets of pCO2 values in the three time intervals (Table 4), assuming CO2

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values from the same time interval represent one set of data. This indicates that the

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three sets of pCO2 values are statistically significantly different. Therefore, the

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average pCO2 values of the three data sets are statistically different between the late

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Hauterivian, Aptian and Albian. Consequently, we concluded that the paleo-CO2

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concentration increased in the middle–late Early Cretaceous (late Hauterivian–late

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Albian) interval based on the negative correlation between SI and pCO2.

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(Tables 2, 3 and 4 inserted near here) 4.3 Comparison of this estimate to previous CO2 reconstructions Estimates of the Early Cretaceous atmospheric pCO2 have previously been

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published using either stomata or stable isotope analysis. Haworth et al. (2005)

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reported pCO2 variations during the Hauterivian to Albian based on stomatal indices

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of Pseudofrenelopsis parceramosa from the UK and USA. They used the ratio of the

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stomatal indices of fossil cuticles and those from four modern NLEs. Their results

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showed

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Hauterivian–Albian interval, a low of 560–960 ppmv in the early Barremian, and a

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high of 620–1200 ppmv in the Albian. Our CO2 calculations for the three periods of

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the late Hauterivian, late Aptian and late Albian, are also comparable to those inferred

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by Haworth et al. (2005), which were 567–1085 ppmv (late Hauterivian), 701–1178

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ppmv (late Aptian), and 717–1196 ppmv (late Albian). Aucour et al. (2008) inferred a

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result of 553–921 ppmv for the pCO2 value of the late Albian based on the fossil

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conifer Frenelopsis alata from coastal and saline influenced environment. This

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different result is probably because of the difference in the habitat of the fossils.

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Another suite of CO2 estimates for the Early Cretaceous was given by Passalia (2009)

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based on a stomatal frequency analysis of the fossil conifers Brachyphyllum,

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Nothopehuen, and Tomaxellia from the Lower Cretaceous of Patagonia, Argentina.

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These were 589–1020 ppmv in the middle Aptian and 740–1232 ppmv in the late

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Albian–early Cenomanian. Their results are consistent with those of the present study,

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and indicate that the atmospheric CO2 content may have become slightly higher in the

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low

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pCO2

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ACCEPTED MANUSCRIPT late Albian–early Cenomanian (Passalia, 2009). Based on fossil conifers Du et al.,

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(2016) gave 575–1060 ppmv for a CO2 estimate from the upper Lower Cretaceous of

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Jiuquan Basin, which is similar to the value range of 573–954 ppmv reconstructed by

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Ren et al. (2008), and is also consistent with that of the present paper. These pCO2

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estimates based on the stomatal data of conifer fossils are generally distributed in a

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consistent range with a slight fluctuation (Table 5; Fig. 4). It is inferred that

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morphologically close species occupying analogous habits display similar stomatal

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values and therefore demonstrate a highly sensitive SI response to pCO2.

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(Table 5 inserted near here)

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Sun et al. (2007) showed that the atmospheric CO2 concentration continuously

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increased over the Early Cretaceous, ranging from 1530 ppmv in the early Berriasian

309

to 1920 ppmv in the late Berriasian based on stomatal indices of Ginkgo coriacea

310

from Huolinhe Basin, Inner Mongolia, northwestern China. Their results essentially

311

agreed with those of GEOCARB III (Berner and Kothavala, 2001) and Tajika (1998).

312

However, Haworth et al. (2005) argued that GEOCARB II may still be a more

313

accurate reconstruction of the atmospheric CO2 concentration for the middle and late

314

Mesozoic compared to GEOCARB III. Their review was also supported by paleo-CO2

315

data estimated using stomata (Aucour et al., 2008; Passalia, 2009; Quan et al., 2009;

316

Wan et al., 2011) and carbon isotope methods (Robinson et al., 2002; Fletcher et al.,

317

2005, 2008; Huang et al., 2012). It appears that this may also be the case for the

318

present study. Huang et al. (2012) inferred that the pCO2 values were lower than those

319

that have been estimated by geochemical models based on pedogenic carbonate data

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ACCEPTED MANUSCRIPT from the Sichuan and Liaoning Provinces. Their CO2 estimates were 360ppmv in the

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early–middle Berriasian, 241ppmv in the early Valanginian, and 530 ppmv in the late

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Barremian on average. A relatively higher pCO2 value of 2037 ppmv in the late

323

Barremian was, however, suggested based on paleosol carbonate data from Tibet

324

(Leier et al., 2009). Meanwhile, Retallack (2009a) reported that the pCO2 increased

325

rapidly from the Barremian to the Aptian based on the SI of Ginkgo. These different

326

estimates definitively indicate that the pCO2 fluctuated even over very short time

327

intervals in the Early Cretaceous, and did not completely match the changing curve

328

indicated by geochemical models. Our calculations of CO2 values also confirmed that

329

the Cretaceous was only partially a high and continuous CO2 greenhouse episode

330

(Kessels et al., 2006; McArthur et al., 2007; Quan et al., 2009; Wang et al., 2014).

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Several proxies and biogeochemical models predict mean CO2 values that fall

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mostly within the range of 400–1800 ppmv in the late Hauterivian, late Aptian and

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late Albian. Proxies of stomatal indices (Haworth et al., 2005) and geochemical

334

models (Tajika, 1998; Hansen and Wallman, 2003; Bergman et al., 2004) suggest that,

335

as in this study, the mean CO2 value is lower in the late Hauterivian. In contrast, the

336

CO2 content is similar in both the late Aptian and late Albian, although it might show

337

slightly higher values in the late Albian (Fletcher et al., 2005, 2008; Berner, 2006,

338

2008). In the three intervals of the Early Cretaceous, the lowest pCO2 values are

339

suggested by stomatal indices that apply the recent standardization in this paper and in

340

the previous studies by Haworth et al. (2005) and Passalia (2009). These data are

341

consistent with those estimated from the paleosol carbon isotope by Rothman (2002).

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1999; Lee, 1999) and also suggested in GEOCARB III (Berner and Kothavala, 2001).

344

However, Breecker et al. (2010) revised the CO2 content during the Paleozoic and

345

Mesozoic based on the carbon isotope composition of paleosol. They argued that the

346

previously reported CO2 values were significantly overestimated because the

347

previously assumed soil CO2 concentrations during carbonate formation were too high.

348

The CO2 values predicted by Carboniferous standardization based on the stomatal

349

indices of conifers are between these extreme values (Haworth et al. 2005; Passalia,

350

2009; this paper). These values are close to the data predicted by Tajika’s (1998)

351

geochemistry model and the GEOCARBSULF model (Berner, 2006, 2008).

352

Considering the different proxies for estimating pCO2, applications of paleosol as a

353

paleobarometer may be influenced by the organic matter of soils (Bowen and Beerling,

354

2004) or just because of different founding assumptions concerning the soil-respired

355

CO2 concentration applied in the formula (Leier et al., 2009; Retallack, 2009b).

356

GEOCARB III overestimates the influence of continental weathering against the CO2

357

concentration, whereas GEOCARBSULF makes a more precise analysis of the CO2

358

concentration in the late Mesozoic (Haworth et al., 2005). This view has also been

359

supported in the present study, and implies that Carboniferous standardization is better

360

than recent standardization for stomatal indices applied for estimating the Mesozoic

361

atmospheric CO2 concentration.

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(Fig. 4 inserted near here) 4.4 Global mean land surface temperature (GMLST)

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ACCEPTED MANUSCRIPT The variation of the global mean land surface temperature (GMLST) depends on

365

the sensitivity of the climate system to changes in greenhouse gas concentrations

366

(Hegerl et al., 2006), and CO2 is related to the long-term global land surface

367

temperature (Wan et al., 2011). When the pCO2 values estimated in this study from

368

the fossil conifer P. papillosa are used in the transfer function of Kothavala et al.

369

(1999) (see section 2. Materials and methods), the change ratio of the GMLST (δT)

370

increases by ~2.8–4.7 °C in the late Hauterivian, ~3.6–5.5 °C in the late Aptian, and

371

~3.8–5.7

372

Hauterivian to the late Albian. Although this is only an approximation, the results are

373

consistent with the view that the global climate cooled by the Valanginian, with the

374

coolest temperatures in the early Hauterivian, and the subsequent warming peaked

375

during the mid-Cretaceous (Huber et al., 2002; Kessels et al., 2006; Keller, 2008).

376

5. Conclusions

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°C in the late Albian. Therefore, the GMLST values increase from the late

Stomatal indices of the extinct conifer Pseudofrenelopsis papillosa from

378

southeast China were applied to estimate the atmospheric CO2 content in the late

379

Hauterivian, late Aptian, and late Albian. The SI values obtained are similar to those

380

of analogous species with similar ecological, evolutionary, and physiological traits, of

381

the same age. These observations support the concept that morphologically close

382

species occupying similar habitats show similar SI values (McElwain and Chaloner,

383

1995, 1996). The atmospheric CO2 levels estimated from P. papillosa were thus

384

different statistically for the three time intervals, with values of 595–957 ppmv in the

385

late Hauterivian, 753–1210 ppmv in the late Aptian, and 805–1292 ppmv in the late

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387

including methods using stomatal indices, stable isotope analysis, and biogeochemical

388

models. Specifically, the CO2 values predicted by the Carboniferous standardization

389

of fossil conifers, in the time intervals considered here, matched extremely well those

390

of geochemistry model (Tajika, 1998), and GEOCARBSULF model (Berner, 2006,

391

2008). Although the fossils used for CO2 estimates were different and were from a

392

wide range of areas in the Northern and Southern Hemispheres, the data also showed

393

similarity in the predicted CO2 values. Our results suggest that the SI of

394

Pseudofrenelopsis papillosa was a good proxy for CO2 in the geological time. The

395

temperatures estimated from the CO2, derived from P. papillosa in this study, showed

396

an increasing tendency in GMLST from the late Hauterivian to the late Albian. This is

397

consistent with the view by Huber et al. (2002) and Keller (2008) that the global

398

climate was extremely warm during the mid-Cretaceous.

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Acknowledgments: We are deeply grateful to Dr. Ding Suting from the School of

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Geological Science and Mineral Resources, Lanzhou University for the fossil

401

collection, and to Dr. Dong Chong from the Nanjing Institute of Geology and

402

Palaeontology, Chinese Academy of Science, for providing assistance with the

403

experimental analysis. We also thank Dr. Feng Zhuo from the Yunnan Key Laboratory

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of Paleobiology, Yunnan University for the comments and discussion. This research

405

was supported by the National Natural Science Foundation of China (no.41302013),

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Flagship Program for young teachers of Yunnan University (no. XT412003),

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Innovation team for paleobiology of Yunnan Province (no. C6155803), and the

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Special Fund for Earth Science of Yunnan University (no. 2013ck001).

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669

cheirolepidiaceous conifers in China. Review of Palaeobotany and Palynology

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Table and Figure captions

672

Table 1 Stomatal data, locations, and collection dates of NLE species Annotation: The original data from Haworth et al. (2010). Annual CO2 values are

674

based on data from the observation station located on Mauna Loa Mountain in Hawaii

675

(http://www.esrl.noaa.gov/gmd/ccgg/trends/). “SD” means stomatal density and is

676

defined as the number of stomata per mm2, “SI” means stomatal index and is the ratio

677

of the number of stomata over the number of stomata plus the number of ordinary

678

epidermal cells per unit area, expressed as a percentage.

679

Table 2 Stomatal data of Pseudofrenelopsis papillosa and estimated pCO2 values

M AN U

SC

RI PT

673

Annotation: “Bt” means Bantou Formation, “Jk” means Junkou Formation, “Zjd”

681

means Zhoujiadian Formation; “Ha.” is an abbreviation for Hauterivian, “Ap.” is an

682

abbreviation for Aptian, “Al.” is an abbreviation for Albian; “ED” means epidermal

683

cell density; “SD” is stomatal density; “SI” is stomatal index; “SR” is stomatal ratio,

684

which is the ratio of the mean stomatal index of the nearest living equivalent over that

685

of each fossil species; “RCO2” is the ratio of the paleo-CO2 concentration over the

686

pre-industrial revolution value; “pCO2” is the estimated CO2 level based on the

687

stomatal-ratio method. The data for every specimen are averaged from 4 to 7 cuticular

688

fragments.

689

Table 3 Stomatal data of Pseudofrenelopsis papillosa from the Lower Cretaceous of

690

southeast China and estimated pCO2 values

AC C

EP

TE D

680

691

Annotation: “n” means the number of specimens counted; “N” means the total

692

counts, including 4–7 cuticular fragments for each specimen; “S” is the area of the

33

ACCEPTED MANUSCRIPT field view.

694

Table 4 ANOVA table of pCO2 values in three time intervals investigated, including

695

late Hauterivian, late Aptian and late Albian

696

Table 5 Estimated CO2 values in three time intervals of Early Cretaceous

697

based on stomatal indices of fossil conifers

698

Fig. 1 Geographical positions of fossil sites

699

Fig. 2 Fossil specimens of Pseudofrenelopsis papillosa from the Lower Cretaceous of

700

Southeast China. 1–8, Fossil specimens from the upper Albian Zhoujiadian Formation

701

(Sun et al., 2011; this study), specimen no. GX18-1, GX18-4, GX18-5, GX18-9,

702

GX18-13, GX18-17, GX18-25, and GX18-28; 9–12, specimens from the upper

703

Aptian Junkou Formation, specimen no. SX9-3, SX9-5, SX9-6, and SX9-8; 13–17,

704

specimens from the upper Hauterivian Bantou Formation, specimen no. YA5-2,

705

YA5-4, YA5-5, YA5-6, and YA5-7. Scale bars=1cm.

706

Fig.3 Cuticular structures of Pseudofrenelopsis papillosa under the stereomicroscope

707

and SEM. 1–4, 13, Specimens from the upper Hauterivian Bantou Formation; 5–8, 14,

708

specimens from the upper Aptian Junkou Formation; 9–12, 15–16, specimens from

709

the upper Albian of Zhoujiadian Formation (Sun et al., 2011; this study). Scale

710

bars=100µm.

711

Fig. 4 Estimates of Early Cretaceous pCO2 from this paper and previously published

712

data based on geochemical and paleobotanical proxies

AC C

EP

TE D

M AN U

SC

RI PT

693

34

ACCEPTED MANUSCRIPT Table 1 Stomatal data, locations and collection dates of NLE species

Species

Location

Annual CO2

date

SD

SI/%

（ppmv） Morocco

2007

383.0

204.4±18.3

12.0±0.9

Tetraclinis articulata

Ireland

2007

383.0

222.2±39.5

11.9±1.4

Tetraclinis articulata

RBG Kew

2003

375.6

192.4±38.2

10.7±1.0

Callitris rhomboidea

UCD, Ireland

2008

383.0

82.4±19.2

8.0±0.9

Callitris rhomboidea

South Australia

2004

378.0

81.5±14.5

7.5±1.3

Callitris rhomboidea

Tasmania

1997

363.8

148.9±28.3

10.7±1.4

Callitris rhomboidea

Australia

1997

363.8

97.0±11.2

9.2±1.2

Callitris columnaris

NSW, Australia

1997

363.8

70.7±24.5

6.7±1.2

Callitris columnaris

NSW, Australia

1997

363.8

122.2±24.2

6.6±1.2

Athrotaxis cupressoides

UCD, Dublin

2007

383.0

114.2±32.6

8.7±1.7

Athrotaxis cupressoides

Lancaster, UK

2002

373.1

129.6±30.9

10.1±1.5

Athrotaxis cupressoides

Tasmania

2000

369.4

117.8±15.9

8.7±1.2

131.9

9.2

SC

M AN U

Average value

RI PT

Tetraclinis articulata

373.6

Annotation: The original data from Haworth et al. (2010). Annual CO2 values are based on data

from

the

observation

station

located

on

Mauna

Loa

Mountain

in

Hawaii

TE D

(http://www.esrl.noaa.gov/gmd/ccgg/trends/). “SD” means stomatal density and is defined as the number of stomata per mm2, “SI” means stomatal index and is the ratio of the number of stomata over the number of stomata plus the number of ordinary epidermal cells per unit area, expressed as

AC C

EP

a percentage.

ACCEPTED MANUSCRIPT

Table 2 Stomatal data of Pseudofrenelopsis papillosa and estimated pCO2 values

Jk

SD

SI(%)

SR

Carboniferous

Recent

standardization

standardization

YA5-2

370.5±36.5

23.3±3.3

5.9±0.4

1.56±0.1

936±77.8

582±48.5

YA5-3

503.4±46.1

29.6±4.3

5.5±0.5

1.67±0.2

1003±101.4

625±63.1

Late

YA5-4

473.2±27.8

28.8±2.9

5.7±0.2

1.61±0.1

968±37.8

603±23.6

Ha.

YA5-5

436.7±32.0

28.5±1.3

6.1±0.2

1.51±0.1

905±38.9

563±24.2

YA5-6

335.4±18.3

21.8±1.1

6.1±0.4

1.51±0.2

905±69.7

563±43.4

YA5-7

414.4±51.2

23.6±3.4

5.4±0.3

1.70±0.1

1022±59.3

636±36.9

SX9-3

537.3±25.7

27.5±0.8

4.9±0.2

1.88±0.1

1127±63.1

701±39.3

Late

SX9-5

589.2±19.2

28.8±1.2

4.6±0.2

2.00±0.1

1200±438.3

747±28.8

Ap.

SX9-6

598.1±21.5

26.7±1.3

4.2±0.3

2.19±0.1

1314±78.1

818±48.6

SX9-8

597.3±18.7

28.9±1.4

4.6±0.1

2.00±0.1

1200±31.2

747±19.5

GX18-1

445.4±31.1

19.2±1.4

4.1±0.3

2.24±0.2

1346±99.7

838±62.1

GX18-4

484.7±21.7

21.5±0.8

4.2±0.2

2.19±0.1

1314±65.4

818±40.7

Late

GX18-5

535.8±32.6

21.8±0.6

3.9±0.2

2.36±0.1

1415±83.1

881±51.8

Al.

GX18-17

486.6±32.5

23.6±2.0

4.6±0.1

2.00±0.1

1200±61.9

747±33.7

GX18-25

518.8±23.8

24.6±0.9

4.5±0.2

2.04±0.1

1227±40.0

763±24.9

GX18-28

476.2±25.9

22.1±2.0

4.4±0.3

2.09±0.2

1254±79.3

781±45.6

TE D

Zjd

ED

No.

RI PT

Bt

Age

SC

levels

pCO2(ppmv)

Specimen

M AN U

Fossil

Annotation: “Bt” means Bantou Formation, “Jk” means Junkou Formation, “Zjd” means

EP

Zhoujiadian Formation; “Ha.” is an abbreviation for Hauterivian, “Ap.” is an abbreviation for Aptian, “Al.” is an abbreviation for Albian; “ED” means epidermal cell density; “SD” is stomatal

AC C

density; “SI” is stomatal index; “SR” is stomatal ratio, which is the ratio of the mean stomatal index of the nearest living equivalent over that of each fossil species; “RCO2” is the ratio of the ancient atmospheric CO2 concentration over the pre-industrial revolution value; “pCO2” is the estimated CO2 level based on the stomatal-ratio method. The data for every specimen are averaged from 4 to 7 cuticular fragments.

ACCEPTED MANUSCRIPT Table 3 Stomatal data of Pseudofrenelopsis papillosa from the Lower Cretaceous of southeast China and estimated pCO2 values Age

P.

Late Ha.

papillosa

(132±2Ma)

P.

Late Ap.

papillosa

(113±3Ma)

P.

Late Al.

papillosa

(112±2Ma)

n

N

S/mm2

SD

SI/%

SR

Carboniferous

Recent

standardization

standardization

RCO2

pCO2

RCO2

pCO2

957±121

2.0±0.2

595±75

6

60

0.15-0.3

66.4±10.1

5.8±0.5

1.6±0.1

3.2±0.5

4

58

0.1-0.2

71.2±1.7

4.6±0.3

2.0±0.2

4.0±0.3

1210±88

2.5±0.1

753±55

6

67

0.1-0.3

64.2±9.5

4.3±0.4

2.1±0.1

4.2±0.4

1292±120

2.6±0.2

805±75

RI PT

Species

SC

Annotation: “n” means the number of specimens counted; “N” means the total counts,

AC C

EP

TE D

M AN U

including 4–7 cuticular fragments for each specimen; “S” is the area of the field view.

ACCEPTED MANUSCRIPT Table 4 ANOVA table of pCO2 values in three time intervals investigated, including late Hauterivian, late Aptian and late Albian

SS

df

MS

F

P-value

F crit

Groups

361139.5

2

180569.7

37.08844

4.25×10-6

3.80556525

Error

63292.13

13

4868.626

Total

424431.6

15

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EP

TE D

M AN U

SC

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Source

ACCEPTED MANUSCRIPT Table 5 Estimated CO2 values in three time intervals of Early Cretaceous based on stomatal indices of fossil conifers pCO2/ppmv

Pseudofrenelopsis papillosa Pseudofrenelopsis

Reference

Late Hauterivian

Late Aptian

Late Albian

(~129-133Ma)

(~112-118Ma)

(~99-106Ma)

595-957

753-1210

805-1292

567-1085

710-1178

717-1196

parceramosa

573-954

Pseudofrenelopsis

575-959

Brachyphyllum

599-1060

Haworth et al. (2005) Ren et al. (2008) Du et al. (2016)

740-1232

Passalia (2009)

SC

Brachyphyllum

this paper

RI PT

Methods

553-921

AC C

EP

TE D

M AN U

Frenelopsis alata

Aucour et al. (2008)

AC C

EP

TE D

M AN U

SC

RI PT

ACCEPTED MANUSCRIPT

AC C

EP

TE D

M AN U

SC

RI PT

ACCEPTED MANUSCRIPT

AC C

EP

TE D

M AN U

SC

RI PT

ACCEPTED MANUSCRIPT

AC C

EP

TE D

M AN U

SC

RI PT

ACCEPTED MANUSCRIPT