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Palaeogeography, Palaeoclimatology, Palaeoecology 252 (2007) 291 – 303

www.elsevier.com/locate/palaeo

Abundance anomalies of aromatic biomarkers in the


Permian–Triassic boundary section at Meishan, China — Evidence
of end-Permian terrestrial ecosystem collapse
Chunjiang Wang a,⁎, Henk Visscher b
a
Laboratory of Geochemistry and Environmental Science, Faculty of Geosciences, China University of Petroleum, Beijing 102249, China
b
Laborotary of Palaeobotany and Palynology, Faculty of Science, Utrecht University, Budapestlaan 4, 3584 CD Utrecht, The Netherlands
Accepted 30 November 2006

Abstract

Several aromatic biomarkers detected in solvent extracts and kerogen pyrolysates from samples of the Global Stratotype Section
and Point (GSSP) for the Permian–Triassic boundary at Meishan, China, show distinctive relative-abundance anomalies that may
be related to the end-Permian biotic crisis on land. Enrichment of dibenzofuran homologues across the Permian–Triassic boundary
may corroborate the concept of excessive soil erosion following loss of rooted vegetation. Enrichment of alkylphenol entities
occurs just below the main marine mass extinction horizon and prior to the characteristic end-Permian δ13C decline. The
alkylphenols were probably derived from lignin and may provide a molecular record of dieback of woody vegetation. Highly
decreased relative abundances of dibenzothiophenes could be indicative of excessive supply of Fe2+. It is suggested that Fe2+ was
land-derived and may have originated from soils. In addition to the Permian–Triassic boundary interval, biomarker abundance
anomalies also occur around the Wuchiapingian–Changhsingian boundary in the basal part of the Meishan section.
© 2007 Elsevier B.V. All rights reserved.

Keywords: Permian–Triassic boundary; Aromatic biomarkers; Biotic crisis; Soil erosion

1. Introduction Palynological studies show that terrestrial ecosystems


experienced preferential dieback of woody vegetation,
End-Permian extinctions devastated both marine and while in many parts of the world surviving herbaceous
terrestrial ecosystems (Erwin, 1993). Comparison of the lycopsids played a pioneering role in repopulating
timing of biotic crises on land and in the sea indicates that deforested terrain (Looy et al., 1999, 2001). Peat
these were coincident events (Twitchett et al., 2001). Most formation ceased to occur (Retallack et al., 1996).
of our understanding of the extinctions has been based on Evidence for terrestrial ecosystem collapse is also
the study of marine biota, but in recent years the severity provided by a proliferation of fungal remains in
of the terrestrial crisis is increasingly recognized. Permian–Triassic transition sections from various parts
of the world (Eshet et al., 1995; Visscher et al., 1996;
⁎ Corresponding author. Tel.: +86 10 89733399; fax: +86 10 Steiner et al., 2003). These remains have been interpreted
89733422. as terrestrial microfossils reflecting massive decomposi-
E-mail address: wchj333@126.com (C. Wang). tion of dead plant material. Further confirmation of the
0031-0182/$ - see front matter © 2007 Elsevier B.V. All rights reserved.
doi:10.1016/j.palaeo.2006.11.048
292 C. Wang, H. Visscher / Palaeogeography, Palaeoclimatology, Palaeoecology 252 (2007) 291–303

Fig. 1. Variation in relative abundance of dibenzofurans and dibenzothiophenes across the Meishan section. Lithological subdivision and age after
Jin et al. (2000). L, Longtan Formation; ∑OF, C0–C3-dibenzofurans; ∑SF, C0–C3-dibenzothiophenes; ∑F, C0–C3-fluorenes; Ar, total ions of various
series of aromatic compounds, including C0–C3-naphthalenes, C0–C3-biphenyls, C0–C3-phenanthrenes, C0–C3-dibenzofurans, C0–C3-
dibenzothiophenes, C0–C3-fluorenes, C0–C2-fluoranthenes and pyrenes, C0–C2-chrysenes, C0–C2-benzonaphthothiophenes, C0–C2-benzofluor-
anthenes and benzopyrenes, C26–C28 triaromatic-steranes. Individual compounds are quantified by calculating their peak area on the specific mass
chromatogram of the series of compounds.

severity of the crisis comes from worldwide occurrences confirmation of the terrestrial crisis. In shallow-marine
of abnormal morphotypes of spores and pollen, which Permian–Triassic sections in northern Italy, an unusual
may be considered to reflect increased mutagenesis abundance of oxygen-containing aromatic compounds
during a period of excessive environmental stress (such as dibenzofurans) has been discovered close to the
(Visscher et al., 2004; Foster and Afonin, 2005). Apart extinction interval. These compounds represent land-
from floral turnover, dramatic changes on land are also derived diagenetic products of polysaccharides, and may
indicated by widespread soil redeposition (Retallack, be indicative of massive soil erosion (Sephton et al.,
2005) and changing fluviatile regimes due to massive loss 2005).
of rooted plant life (Ward et al., 2000; Michaelsen, 2002; Also in the Meishan section, China, the Global
Arche and López-Gómez, 2005). Marine environmental Stratotype Section and Point (GSSP) for the Permian–
changes that have been ascribed to effects of terrestrial Triassic boundary (PTB), a variety of organic–geo-
ecosystem crisis are related to an elevated freshwater chemical features have been found. Anomalous dis-
input into shallow seas (Kozur, 1998; Korte et al., 2003). tributions of pristane (Wang et al., 2005a) and hopane
In recent years, several molecular organic geochemical (Xie et al., 2005; Wang, 2007) near the PTB reflect
studies of the biological and environmental changes dramatic changes in marine ecosystems. In order to
during the end-Permian biotic crisis have been carried out obtain further information on possible effects of
(Sephton et al., 1999, 2001; Schwab and Spangenberg, terrestrial ecological crises around the PTB, the present
2004; Sephton et al., 2005; Watson et al., 2005; Xie et al., paper focuses on the detection and interpretation of
2005; Grice et al., 2005a,b; Wang et al., 2005a,b; Wang, aromatic biomarkers through this important reference
2007). Some of the results provide organic–geochemical section.
C. Wang, H. Visscher / Palaeogeography, Palaeoclimatology, Palaeoecology 252 (2007) 291–303 293

2. Sampling and experimental 27b, 27c and 27d on the basis of fossil assemblages;
the PTB is defined at the base of Hindeodus parvus
2.1. Samples (conodont) horizon, i.e. the base of Bed 27c (Yin et al.,
2001, 2005). The illite–montmorillonite claystone of
The Permian–Triassic boundary section at Meishan Bed 25 is of volcanic origin and is regarded as the
is exposed in a series of abandoned limestone quarries principal event horizon. Bed 24e represents the last-
near Meishan in Changxing County, Zhejiang Province, appearance datum of a wide variety of Late Permian
China. The quarries are labeled A, B, C, D, E and Z from faunal species (Jin et al., 2000). Apart from the PTB, the
west to east. Quarry D serves as the GSSP of the PTB. Meishan section also includes the proposed GSSP for
For locality and lithological description of the individual the Wuchiapingian–Changhsingian boundary (WCB,
beds, see Yin et al. (1996, 2001, 2005). The section located in the basal part of Bed 4; Jin et al., 2003). This
comprises the Changxing Formation and the lower part boundary is characterized by the extinction of a
of the Yinkeng Formation (Fig. 1). Bed 27 is significant number of marine faunal elements (Jin
lithologically homogeneous but is subdivided into 27a, et al., 1995; Knoll et al., 1996; Bowring et al., 1998).

Fig. 2. Partial aromatic TIC and the integrated mass chromatogram (m/z 168 + 196 + 210 + 224) showing the relative abundance and distribution of
dibenzofurans in Bed 24 and Bed 26. OF, dibenzofuran; MOF, C1-dibenzofurans; DMOF, C2-dibenzofurans; TMOF, C3-dibenzofurans; Ph,
phenanthrene; M-Ph, methylphenanthrene.
294 C. Wang, H. Visscher / Palaeogeography, Palaeoclimatology, Palaeoecology 252 (2007) 291–303

A total of 64 samples, collected from quarries B, C then to 300 at 2 °C/min, followed by an isothermal
and D, was selected for this study (Fig. 1). Samples are period of 15 min. Pyrolysis–GC analysis was carried out
representative of each individual bed, including various using a SGE II pyroprobe coupled to a HP5890 II Plus
lithological types, so that the possible effect of lithology GC with a HP5 column (30 m × 0.32 mm × 0.25 μm),
on molecular composition could be taken into account. and with flame ionization detector (FID). The flash
pyrolysis temperature was 610 °C (10 s). Helium was
2.2. Experimental used as carrier gas. The GC was held isothermally at
30 °C for 5 min and then ramped at 5 °C/min to 300
The samples were Soxhlet extracted (with solvent where it was held for 10 min. The Py–GC–MS system
dichloromethane/methanol, 97:3), and the extracts were was equipped by a CDS pyroprobe 2000 fitted with a
separated into maltene and asphaltene fractions by CDS1500 valve interface held at 250 °C and coupled to
precipitation in heptane. The maltenes were fractionated a Finnigan Voyager GC800TOP GC–MS with a CP-
by silica–alumna column chromatography into aliphat- SIL5-CB column (30 m × 0.25 mm × 0.25 μm). Follow-
ic, aromatic and polar fractions by silica–alumna ing heating to 610 °C at a rate of 20 °C/ms the sample
column chromatography, using hexane, benzene, and was held at this temperature for 10 s in a flow of helium.
alcohol as the developers, respectively. To obtain the The GC–MS conditions, EI mode, helium was used as
kerogen, the extracted samples were subjected to cyclic carrier gas; the GC was held isothermally at 35 °C for
treatments with hydrochloric and hydrofluoric acids. In 5 min and then ramped at 3 °C/min to 300 °C where it
preparation for pyrolysis, the kerogens were extracted was held for 10 min.
with dichloromethane.
The detection and identification of the aromatic 3. Results and discussion
compounds was performed on a Finnigan SSQ710 GC–
MS using a HP-5MS (30 m × 0.25 mm × 0.25 μm) 3.1. Enrichment of dibenzofurans around the PTB
flexible quartz capillary column. EI mode, helium was
used as carrier gas. After an initial period of 1 min at Dibenzofuran (DBF) homologues in the aromatic
80 °C, the column was heated to 250 °C at 7 °C/min, and fractions of the samples have been detected from the

Fig. 3. Partial TIC and selected mass chromatograms (m/z 168+182+196+210+224) from Py–GC–MS analysis of kerogen showing the relative abundance
and distribution of dibenzofuran entities in the Bed 24e. Squares are used to indicate dibenzofuran homologues: A, dibenzofuran; B–C, C1-dibenzofurans; E–F,
C2-dibenzofurans; G–H, C3-dibenzofurans. Alkene/alkane pairs are indicated by inverted “V”. Mass spectra are shown in Fig. 4.
C. Wang, H. Visscher / Palaeogeography, Palaeoclimatology, Palaeoecology 252 (2007) 291–303 295

base of the Changxing Formation up to the lower part of uppermost Changxing Formation and the lower Yinkeng
the Yinkeng Formation (Fig. 1). Quantification of the Formation are significantly enriched in DBF entities,
DBF record was based on gas chromatography–mass with the two ratios being higher than 0.50 and 0.20,
spectrometry (GC–MS) traces of total ion current (TIC) respectively.
of the aromatic compound fraction and integrated mass DBF entities are also present in the kerogens derived
chromatograms (m/z 168 + 196 + 210 + 224) showing the from individual beds near the PTB at Meishan. Fig. 3
relative DBF abundance of dibenzofurans in the gives a partial TIC and selected mass chromatograms
individual beds of the Meishan section. Examples for (m/z 168 + 182 + 196 + 210 + 224) showing the relative
Bed 24 and Bed 26, shown in Fig. 2, indicate similar abundance and distribution of DBF entities obtained by
distribution patterns of the DBF entities, which occur Py–GC–MS analysis of kerogen from Bed 24e. Results
irrespectively of differences in sedimentary facies or of Py–GC analysis of kerogens are shown in Fig. 5.
lithology (the two beds are composed of dark grey DBF entities are abundant in the interval from Bed 22 to
micrites and dark grey shale, respectively). There are Bed 30, except Bed 27.
only small differences in demethylation and isomeriza-
tion of methyldibenzofurans (MDBFs) between differ- 3.2. Causes of the enrichment of dibenzofurans
ent beds. These are probably related to lithologic
variation because the DBF/MDBFs values in carbonates DBF and its derivatives may be common compo-
are higher than those in mudstones. nents in the aromatic fraction of extracts from terrestrial
In Fig. 1 we use the ∑OF/∑(OF + SF + F) and (OF + sediments, which are rich in plant organic matter (e.g.
MOF)/tAr ratios to show the variation in relative Fan et al., 1990; Radke et al., 2000). However, the
abundance of DBF entities. Values of both ratios vary Meishan strata represent typical marine sediments
in a rather regular way: higher values in Beds 1–6, deposited in slope to shallow-water basin facies under
followed by lower values in Beds 7–19, and then predominant anoxic/dysoxic conditions (Wignall and
increased values in Beds 20–32. Highest levels occur in Hallam, 1993; Yin and Tong, 1998; Wignall and
Beds 23–26. It is obvious that the sediments from the Twitchett, 2002; Grice et al., 2005a; Wang et al., 2005a).

Fig. 4. Mass spectra corresponding to the retention times of compounds A to G in Fig. 3. The exact positions of the methyl substituents are unknown.
296 C. Wang, H. Visscher / Palaeogeography, Palaeoclimatology, Palaeoecology 252 (2007) 291–303

In marine PTB sections in northern Italy, abundant considered to be predominantly marine (Wang et al.,
DBF entities were found in solvent extracts and kerogen 2005a). In palynomorph assemblages, terrestrial com-
pyrolysates from organic-rich marls at the top of the ponents are rare (Li et al., 2004). Dominance of marine
shallow-marine Bellerophon Formation, just below the organic matter may be supported by molecular
Tesero horizon (Sephton et al., 1999, 2001, 2005; and compound-specific carbon-isotopic studies of n-
Watson et al., 2005). Microscopic sedimentary organic alkanes, isoprenoid HCs, aryl isoprenoids and 2-
matter in these marls was essentially land-derived. The methylhopanes (Wang et al., 2005a; Grice et al.,
furan-containing compounds are interpreted as the 2005a; Xie et al., 2005).
remains of dehydrated polysaccharides originating In theory, DBFs might be partly derived from marine
from eroded soils of terrestrial ecosystems (Sephton organisms including algae, fungi and bacteria. How-
et al., 2005). ever, there are no records that these organisms actually
At Meishan, overall organic matter composition is produce precursor compounds for furan structures.
different from that in northern Italy. Because of its Interestingly, the enrichment of DBF moieties at
amorphous character and the rarity of distinctive land Meishan does not correlate with other biomarker indices,
plant debris, microscopic sedimentary organic matter of such as the pristane/phytane ratio (Wang et al., 2005a),
the Changxing Formation and the Yinkeng Formation is and the hopane/sterane and moretane/hopane ratios

Fig. 5. a: Py–GCs of the kerogens from Beds 26–30 in the lowermost Yinkeng Formation. B, benzene; T, toluene; b: Py–GCs of the kerogens from Beds
23–24e at the top of the Changxing Formation; c: Py–GCs of the kerogens from selected beds in the middle part of the Changxing Formation. X, xylene;
P, phenol; MP, C1-phenol; DMP, C2-phenol; DMN, C2-naphethalene; OF, dibenzofuran; MOF, C1-dibenzofurans; DMOF, C2-dibenzofurans; TMOF,
C3-dibenzofurans. Compounds marked with filled squares could not be identified.
C. Wang, H. Visscher / Palaeogeography, Palaeoclimatology, Palaeoecology 252 (2007) 291–303 297

Fig. 5 (continued ).

(Wang, 2007) around the PTB. This lack of correlation enrichment in Beds 23–26 at Meishan may point to
substantiates the concept that the DBFs were not derived massive soil erosion following end-Permian destruction
from marine biota. of land vegetation.
Consequently, in view of the fact that elevated DBF Soil-derived end-Permian DBF enrichment provides
concentrations are indicative of terrestrial organic independent evidence of terrestrial ecosystem collapse
matter, accumulations around the PTB in the Meishan that may have been caused by atmospheric acidification
marine sediments are likely to be the result of excessive and enhanced UV-B radiation resulting from strato-
input of land-derived degradation products of poly- spheric ozone depletion induced by the Siberian Trap
saccharides. Because of the scarcity of particulate land- volcanism (Campbell et al., 1992; Wignall, 2001;
derived organic matter in the deeper-marine Meishan Visscher et al., 2004; Sephton et al., 2005). In contrast
sediments, influx of submicroscopic DBFs should have to the Italian sections, DBF occurrences at Meishan are
been directly from terrestrial sources. In terrestrial not restricted to the PTB interval. Occurrences of DBFs
ecosystems, polysaccharides, particularly cellulose of throughout the Changxing Formation may therefore
vascular plants, form the bulk of organic matter added to corroborate the concept of a prolonged period of
soils. Furan structures can be produced through ecosystem destabilization preceding ecosystem col-
microbially mediated dehydration of soil polysacchar- lapse. Particularly the WCB interval in the lowermost
ides (Huang et al., 1998). Therefore, similar to the part of the section may be characterized by increased
situation in northern Italy (Sephton et al., 2005), DBF input of soil organic matter.
298 C. Wang, H. Visscher / Palaeogeography, Palaeoclimatology, Palaeoecology 252 (2007) 291–303

Fig. 5 (continued ).

3.3. Lowered abundance of dibenzothiophenes around tions as evidenced by low Pr/Ph values and low
the PTB and WCB abundance of DBFs, are enriched in DBT entities. In
marked contrast, the relative abundance of DBTs is
The relative abundance of S- and O-heterocyclic lowered in Beds 1–6 and Beds 23–32, (SF + MSF)/tAr
families in sedimentary organic matter notably varies values being basically lower than 0.1. These low values
with depositional environment. Alkyldibenzothio- would suggest that these beds were formed under
phenes (DBTs or SF) are particularly abundant in oxygenated and freshwater depositional conditions.
marine organic-rich deposits where they dominate over Such an interpretation conflicts with the well-estab-
alkylfluorenes (F) and alkyldibenzofurans (DBF or OF) lished anoxic depositional conditions around the PTB
(Radke et al., 2000). The latter seem to prevail in (Wignall and Hallam, 1993; Yin and Tong, 1998;
organic-rich freshwater deposits and coal measures (Fan Wignall and Twitchett, 2002; Grice et al., 2005a; Wang
et al., 1990; Radke et al., 2000). The relative abundances et al., 2005a), and around the WCB (Wang, 2007).
of the three series of compounds are usually used as Thus, the formation of DBT entities in the Meishan
proxies for depositional conditions such as redox status. section needs a re-evaluation.
In Fig. 1, the relative abundance of DBT entities Organic sulfur-containing compounds such as DBTs
shows an opposite trend to that of DBF entities. The are predominantly formed by the reaction of reduced
Beds 7–19, characterized by the absence of terrestrial inorganic sulfur species with functionalized organic
organic matter and deposited under reducing condi- molecules during deposition and early diagenesis
C. Wang, H. Visscher / Palaeogeography, Palaeoclimatology, Palaeoecology 252 (2007) 291–303 299

(Hughes, 1984; Sinninghe Damsté and De Leeuw, containing soil dust is transported from land through the
1990). A critical factor controlling the formation of atmosphere to the oceans (Jickells et al., 2005).
DBTs should be the input of Fe2+ relative to that of S2−.
In carbonate depositional environments, the supply of 3.4. Enrichment of alkylphenols preceding the marine
S2− is generally excessive over Fe2+ owing to extensive mass extinction level
development of sulphate-reducing bacteria, which
enable organic molecules with functional groups In the Meishan section, also the aromatic group of
(mainly double bonds) to combine with S2− to form alkylphenols shows variation in relative abundances.
organic S-containing compounds, including DBTs. Fig. 5a, b, and c shows the variation in relative abun-
Conversely, in situations of excessive Fe2+ supply, S2− dance and in distribution of alkylphenol entities in
will prefer to react with Fe2+ to form FeS2 while selected beds from the middle part of the Changxing
formation of DBTs is inhibited. It is likely, therefore, Fm. to the lower part of the Yinkeng Fm. Notably the
that increased Fe2+ input has played an important role in interval of Bed 23 to Bed 24e is enriched in alkylphenol
lowering DBT concentrations in the PTB and WCB entities (Fig. 5b). Fig. 6 gives the partial TICs and
intervals of the Meishan section. Soils were a plausible selected mass chromatograms (m/z 94 + 108 + 122 + 136)
source of Fe2+. Loss of rooted vegetation may have based on Py–GC–MS analysis of kerogen samples from
resulted in excessive Fe2+ transport by river action to two key beds below and above the mass extinction level
marine depositional environments. Alternatively, there (the base of Bed 25). It is clear that the distribution of
may have been a role for the iron cycle, in which iron- alkylphenol entities in Bed 24e and Bed 26 are very

Fig. 6. Partial TICs and selected mass chromatograms (m/z 94 + 108 + 122 + 136) from Py–GC–MS analysis of kerogens. It is clear that the
alkylphenols are much more abundant (as main peaks) in Bed 24e than in Bed 26. A, phenol (P); B–C, C1-phenols (MP); E–G, C2-phenols (DMP);
H–J, C3-phenols (TMP). Mass spectra are shown in Fig. 7.
300 C. Wang, H. Visscher / Palaeogeography, Palaeoclimatology, Palaeoecology 252 (2007) 291–303

Fig. 7. Mass spectra corresponding to the retention times of compounds A to J in Fig. 6. A, phenol; B, 2-me-phenol; C, 4- + 3-me-phenol. The exact
positions of the methyl substituents in C2- and C3-phenols are unknown.

similar. However, the relative abundances of alkylphe- here considered to be indicative of a significant input of
nols, as compared with n-alkanes, are different. TIC lignin-derived organic material to the marine environ-
traces indicate that alkylphenols are much more ment. As evidenced by a predominantly amorphous
abundant in Bed 24e than in Bed 26. nature, the remains of woody plants must have been
The alkylphenol-rich interval is also characterized by heavily biodegraded. Only a small amount could be
the onset of other important geochemical changes, such identified as a typical lignin-derived maceral (vitrinite)
as the onset of DBF enrichment (Fig. 1), the hopane (Wang et al., 2005a).
distribution anomaly (Wang, 2007), and the onset of the In theory, there may be many other potential
characteristic end-Permian negative shift in δ13Ccarb (Li, precursors of alkylphenols, including marine algae
1999; Jin et al., 2000; Cao et al., 2002; Wang et al., (Van Heemst et al., 1999). However, since alkylphenol
2005b). Accordingly, the geochemical significance of enrichment is restricted to Beds 23–24, a predominant
the enrichment of alkylphenol entities in Beds 23–24 marine origin would be difficult to explain.
needs further explanation. Enrichment of alkylphenols occurs just before the
Phenols are the main units in the chemical structure main marine mass extinction event recognized at the
of suberine (Kolattukudy, 1980). Alkylphenols, along base of Bed 25 (Jin et al., 2000). Considering a
with methoxy-substituted alkylphenols and alkylated terrestrial origin of the alkylphenols, their enrichment in
catechols, are typical pyrolysis products of lignins and marine sediments may record the onset of ecological
altered lignins (Saiz-Jimenez and De Leeuw, 1986; Saiz- crisis on land characterized by collapse of woody
Jimenez et al., 1987; Nip et al., 1987; Hatcher and vegetation. The duration of this molecular record could
Clifford, 1997). They are also major components of the be in the order of several hundred thousands years, but
pyrolysates of coals (Khorasania and Michelsen, 1991). is considerably shorter than the record of DBF
Because the distribution of alkylphenol entities in Beds enrichment, which can be traced up to Bed 30
23–24 is basically similar to that in coals, enrichment is (Fig. 1). Interestingly, the enrichment interval of the
C. Wang, H. Visscher / Palaeogeography, Palaeoclimatology, Palaeoecology 252 (2007) 291–303 301

alkylphenol entities basically precedes the onset of the References


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