terrestrial ecosystems on north gondwana following the end-permian mass extinction
TRANSCRIPT
Gondwana Research 20 (2011) 630–637
Contents lists available at ScienceDirect
Gondwana Research
j ourna l homepage: www.e lsev ie r.com/ locate /gr
Terrestrial ecosystems on North Gondwana following the end-Permianmass extinction
Elke Hermann a,⁎, Peter A. Hochuli a, Hugo Bucher a, Thomas Brühwiler a, Michael Hautmann a,David Ware a, Ghazala Roohi b
a Institute and Museum of Palaeontology, University of Zurich, Karl Schmid-Str. 4, CH-8006 Zurich, Switzerlandb Pakistan Museum of Natural History, Garden Avenue, Islamabad 44000, Pakistan
⁎ Corresponding author. Tel.: +41 44 634 23 29; faxE-mail address: [email protected] (E. Hermann
1342-937X/$ – see front matter © 2011 International Adoi:10.1016/j.gr.2011.01.008
a b s t r a c t
a r t i c l e i n f oArticle history:Received 27 October 2010Received in revised form 21 January 2011Accepted 25 January 2011Available online 2 March 2011
Handling Editor: R.D. Nance
Keywords:Early TriassicTerrestrial ecosystemsPalynologyPakistan
The impact of the end-Permian mass extinction on terrestrial ecosystems is still highly controversial. Here,new high-resolution palynological data from biostratigraphically well-dated Upper Permian to MiddleTriassic successions of the Salt Range and Surghar Range (Pakistan) are presented. Our results reveal sevensuccessive floral phases between the Late Permian and the Middle Triassic. At the onset of the Mesozoic, theflora is characterised by high abundances of lycopods associated with pteridosperms and conifers. Thisassociation prevails up to themiddle Smithian and is followed by a prominent spore spike similar to the globalspore spike reported from the Permian–Triassic boundary. Like that of the end-Permian, the middle Smithianspore spike is associated with a negative isotope excursion and is succeeded by a major marine faunalextinction event in the late Smithian. The recurrent patterns observed at the Permian–Triassic boundary andin the middle–upper Smithian suggest a common cause such as massive ejections of volcanic gases. Theincreasing abundance of conifers still associated with common lycopods in the Spathian suggests fadingvolcanically induced environmental perturbations and stabilisation of terrestrial ecosystems ca. 2.1 My afterthe end-Permian event.
: +41 44 634 49 23.).
ssociation for Gondwana Research. Published by Elsevie
a Research. Published by Elsevier B.V. All rights reserved.
© 2011 International Association for Gondwan1. Introduction
The end-Permian mass extinction about 252 My ago was thelargest crisis in the Phanerozoic history of marine life. However, theimpact of this event on terrestrial plant communities is still debatedand views about the magnitude of the deterioration of terrestrialecosystems are strongly diverging. Interpretations range fromvirtually no effects on terrestrial plants (e. g. Knoll, 1984; McElwainand Punyasena, 2007; Xiong and Wang, 2011) to an almost completedevastation of terrestrial ecosystems (e. g. Utting et al., 2004; Visscheret al., 1996). The first hypothesis points to a long-term (25 My)gradual floristic transition across the Permian–Triassic boundaryreflected in the fossil record by a gradual change from palaeophyticfloras to mesophytic floras without evidence for a major plantbiomass decay (Knoll, 1984). Long-term floristic turnover has beendocumented in the macrofossil data from the South African KarooBasin. There, the diversity of woody vegetation is already decreasingat the transition from the middle to the Late Permian. The successionof the Upper Permian to Middle Triassic assemblages is marked byunchanged diversity and replacement of the glossopterids by otherplant groups (cycads, benettitaleans, ginkgos and other seed ferns,
Bamford, 2004). This does not preclude significant short-termchanges in ecosystems during the Palaeozoic–Mesozoic transition.Opposing scenarios rely on the so-called fungal event (Visscher et al.,1996), advocating instead the total collapse of terrestrial ecosystemsafter the end-Permian mass extinction. Some authors even attributemost of the Lower Triassic palynofloral records to reworking (Uttinget al., 2004). To assess whether or not these short-term changesaffected the functionality of the ecosystem, it is essential toincorporate abundance data and dominance structures of plantcommunities rather than relying solely on total biodiversity data(McElwain and Punyasena, 2007).
The significance of palynofloral records on the reconstruction ofterrestrial ecosystem responses to mass extinction has received majorattention over the last decade (e. g. Hochuli et al., 2010b; Looy et al.,1999, 2001; McLoughlin et al., 1997). Reviews of floral records haverevealed that faunal mass extinctions are commonly associated withinstabilities of terrestrial ecosystems (McElwain and Punyasena,2007). The onsets of these instabilities are often marked by a shortinterval during which pteridophytes dominate terrestrial plantassemblages. The fern spike at the Cretaceous–Palaeogene boundaryis assumed to represent the devastation of vegetation caused by theclimatic and atmospheric perturbations of the impact event at thisboundary (Vajda et al., 2001). High abundances of fern spores are alsoreported from the Triassic–Jurassic boundary (van de Schootbruggeet al., 2009). Pioneering studies documenting ecological perturbation
r B.V. All rights reserved.
631E. Hermann et al. / Gondwana Research 20 (2011) 630–637
around the Permian–Triassic boundary and in the Early Triassic havebeen published by Looy et al. (1999, 2001). They documented a sporepeak close to the end-Permian extinction event in sections fromJameson Land in East Greenland and suggested a great loss of plantdiversity from their data. Furthermore, they inferred that the recoveryof plant communities took 4–5 My.
The aforementioned floral changes (spore spike) observed in thepalynological records have been interpreted as responses of terrestrialecosystems to palaeoenvironmental perturbations. For the Triassic–Jurassic spore spike, Bonis et al. (2010) demonstrated that the highabundances of spores are related to climatic changes. Recent publica-tions of Hochuli et al. (2010a,b), and Lindström and McLoughlin (2007)also showed that the palynological turnover near the Permian–Triassicboundary is associated with changes in humidity. The striking recurrentpatterns of high spore abundances, large perturbations of the globalC-cycle and faunalmass extinctions suggestmajor andgeologically rapidclimatic changes affecting both marine and terrestrial biotas. Theultimate causes that triggered these global changes still need to bedetermined.
During Late Permian and Triassic times, Gondwana provided astable plate configuration of southern hemisphere continents that hadbeen established in the late Proterozoic and continued to exist untilthe Early Cretaceous (Comin-Chiaramonti et al., 2010; Meert andLieberman, 2008; Renne et al., 1992). Despite the stable configurationof landmasses, physical environmental conditions fluctuated throughtime (Veevers, 2006) and environmental changes determined theTriassic vegetation history on Gondwana (Spalletti et al., 2003).
Here we present the composite palynological record from Nammal,Chhidru, Chitta-Landu, and Narmia in the Salt Range and Surghar Rangein Pakistan (Fig. 1), spanning the latest Permian to early Middle Triassic
Landu
North-WesProvince
71°00’
71°00’
33°00’
32°30’
N00Chitta-Landu
Fig. 1. Location of the studied sites. a) Early Triassic palaeogeographic position of the Salt Ra(2000), b) location of the Salt Range and Surghar Range in Pakistan, and c) location of Nam
time interval. The palynological assemblages record floral turnovers,which reflect profound changes in the composition of the terrestrialplant community on the northern margin of Gondwana borderingtropical Tethys. The detailed ammonoid age control of the studiedsections allows precise dating of the floral events (Brühwiler et al., inpress, 2010). Our data provide detailed insights into terrestrialecosystem turnovers associated with the environmental changesduring the Palaeozoic–Mesozoic transition.
2. Methods
Samples were preferentially taken from the fine-grained silici-clastic intervals of the sections at Nammal, Chhidru, Chitta-Landu andNarmia. Siltstones and, in a few cases, limestone and fine-grainedsandstone were sampled. The samples were crushed and weighed (5–25 g) and subsequently treated with hydrochloric and hydrofluoricacid according to standard palynological preparation techniques. Ashort oxidation with nitric acid was performed before the residueswere sieved over an 11 μm mesh screen. From strew mounts aminimum of 300 spores and pollen per sample were counted. In a fewsamples with high amorphous organic matter contents, low spor-omorph concentration or poor preservation, the intended 300sporomorph counts could not be reached.
3. The palynological record and its significance
The excellently preserved organic walled microfossils from theNammal, Chhidru, Chitta-Landu and Narmia gorges in the Salt Rangeand Surghar Range allowed a detailed succession of palynologicalassemblages to be established for the first time. The assemblages
1
Narmia
Nammal
t Frontier
Mianwali
71°30’ 72°00’
71°30’ 72°00’
33°00’
Indu
s
Islamabad
Afghanistan
Pakistan
India
ISLAMABAD
64
24
32
72
0 50 km
SurgharRange
armia
Kamar Mashani
Chhidru3Salt Range
Punjab
Daud Khel
c
a
bArabian Sea
32°30’
nge and the Surghar Range in Pakistan after Smith et al. (1994) and Golonka and Fordmal, Chhidru, Chitta-Landu, and Narmia gorges.
632 E. Hermann et al. / Gondwana Research 20 (2011) 630–637
range from the uppermost Permian Chhidru Formation to the LowerTriassic Mianwali Formation and the lower part of the Middle TriassicTredian Formation, and represent several distinct changes of theterrestrial ecosystem on the northernmargin of Gondwana within thecorresponding time interval. Changes in the depositional environ-ment and climatic conditions have been determined using sedimen-tological evidence, palynofacies and spore–pollen ratios (Hermannet al., submitted for publication).
In the quantitatively analysed palynological data seven floralphases have been distinguished. These are illustrated in Fig. 2 andreferred to as numbers (1 to 7) in parentheses in the text. Permianassemblages (1) are characterised by high abundances of striate andnon striate bisaccate pollen. These assemblages are substituted byspore rich assemblages of uppermost Permian age (2), in whichtypical Lower Triassic sporomorph taxa (e.g. Lunatisporites pellucidus)co-occur with lingering Permian forms (e. g. Weylandites spp.).Dienerian and lower Smithian assemblages (3) are characterised byabundant cavate trilete spores (lycopods) with common fern sporesand striate bisaccate pollen. This spore dominance culminates in anacme of Densoisporites spp. in the middle Smithian (4). The upperSmithian assemblages (5) are dominated by striate bisaccate pollen.These are replaced in the Spathian (6) by assemblages characterisedby non-striate bisaccate pollen combined with Densoisporites spp.,Aratrisporites spp., and ornamented spores. At the onset of the MiddleTriassic (Anisian) (7) the dominance of non-striate bisaccate pollenincreaseswhereas cavate trilete spores and striate bisaccate pollen arereduced and occur only in low numbers.
For the reconstruction of Lower Triassic plant communities thesepalynological data have to be translated into a parent plant record.Present-day surface pollen assemblages are known to representsurrounding plant communities (e. g. Lézine et al., 2009). According tonumerous studies, specific pollen spectra can be used for thereconstruction of past ecosystems. However, some limitations areindicated concerning quantitative reconstruction of plant communi-ties inferred from pollen spectra (Fletcher and Thomas, 2007;McGlone and Moar, 1997; Stutz and Prieto, 2003). Palaeopalynologi-cal assemblages recovered from sedimentary basins are known toreflect the flora of the hinterland from which the spores and pollenhave been transported into the basin (Muller, 1959; Traverse, 2007).For Holocene and Pleistocene palynological records analysed usingmodern analogue techniques, reconstructions of past vegetationproduced convincing results (e. g. Delcourt and Delcourt, 1985;Pross et al., 2009). However, taphonomic effects have to be kept inmind. Owing to the various morphologies of sporomorph taxa, theyare subject to different buoyancy and transportation modes. Spor-omorphs with higher buoyancy, e. g. bisaccate pollen, can betransported over longer distances, and are therefore generally moreabundant in more distal settings (e. g. highstand system tracts; Tyson,1995 and references therein).
Nevertheless, given the low taxa density and generally poor timeresolution of plant macrofossil data, palynological records offer amore complete record of past vegetation with greater taxonomicrichness and with high temporal resolution. For the Lower Triassicsuccession from Pakistan it can be shown that the floral changes areindependent of sea-level changes as reflected in the sedimentary andpalynofacies patterns (Hermann et al., 2011).
For the Lower Triassic palynological record, the botanical affinitiesof sporomorphs are mainly provided by in-situ occurrences ofsporomorph taxa. These affinities are crucial for ecological recon-
Fig. 2. Late Permian to Middle Triassic vegetation history on North Gondwana, represented i(1978), and ongoing work of Bucher, H. and Ware, D.: Prh=Prohungarites beds; Tr=TNya=Nyalamites angustecostatus beds; Psc=Pseudoceltites multiplicatus beds; Nam=Nammbeds; Fl. n.=Flemingites nanus beds; Xed=Xenodiscoides perplicatus beds; F. bh.=Flemingiteevolutionary trends of the North Indian Margin (NIM) after Brühwiler et al. (2010). Carbonconodont species Hindeodus parvus (Pakistani–Japanese Research Group, 1985).
structions. In the present study, spore–pollen representing majorcomponents of the Early Triassic vegetation of Gondwana have beenassigned to major plant groups, essentially based on the compilationof Balme (1995) (Table 1). However, in some cases these assignmentsare not straightforward. Alisporites spp., for example, has beenassigned to Corystospermae by de Jersey and Hamilton (1967). Incontrast, this pollen type has been recovered from in-situ occurrencesin the male conifer coneWillsiostrobus (Grauvogel-Stamm, 1978); thelatter affinity is favoured herein.
4. Discussion
4.1. Ecological changes
Seven distinct floral associations (floral phases 1 to 7) representingterrestrial ecosystem turnovers are reflected in the Upper Permian–Lower Triassic palynological record from Pakistan.
Phase (1). The palynological assemblages are dominated bynon-striate and striate bisaccate pollen and indicate the prolifer-ation of conifers and pteridosperms during the late Permian on thenorthern margin of Gondwana. In contemporaneous coal-bearingsequences of Australia, the last occurrences of glossopterid mega-fossil plant remains are documented (Foster, 1982). Ferns, lycopodsand equisetopids are minor component of the uppermost Permianvegetation.
Phase (2). Immediately before the end-Permian mass extinction,which coincides with the formational boundary between the ChhidruFormation and the Mianwali Formation (Schindewolf, 1954), thecomposition of the Gondwanan flora changes significantly. Theincreased abundance of cavate trilete spore (Kraeuselisporites spp.)in the uppermost Permian assemblages reflects the establishment of alycopod-dominated vegetation prior to the faunal mass extinction.Since many of the typical Permian taxa (e. g. Weylandites spp.,Lueckisporites spp.) are still present, floral diversity increases with thefloral turnover from phase (1) to phase (2) (Fig. 2).
Phase (3). The Dienerian plant communities on North Gondwanaare characterised by the dominance of lycopods as reflected in the lowdiversity assemblages of cavate trilete spores such as Densoisporitesspp. and Lundbladispora spp. (Fig. 2). The predominance of lycopodscontinues into the lower Smithian. However, ornamented sporediversity increases and reflects the prominent role of ferns within thisinterval. Pollen of the Ephedripites and Cycadopites groups and striateand non-striate bisaccate pollen document a mixed vegetation ofconifers, pteridosperms, Gnetales and cycads.
Phase (4). A rapid and conspicuous floral change is documented inthe middle Smithian. The palynological assemblages up to the lowerboundary of the Wasatchites distractum beds represent a spore spike.They are dominated by Densoisporites spp., intermittently reachingpercentages higher than 90% of the total sporomorph count, thussuggesting monotonous stands of the lycopsid order Pleuromeiales(Abbink, 1998).
Phase (5). In the upper Smithian, above theWasatchites distractumbeds, the monotonous lycopod assemblages are replaced by apteridosperm dominated vegetation reflected in the high abundancesof striate bisaccate pollen (Lunatisporites spp.). The diversity in theupper Smithian plant communities is still low but increases rapidly inthe lowermost Spathian (Fig. 2).
Phase (6). The Spathian plant communities have a transitionalcharacter between the lycopod-dominated Griesbachian to Smithian
n seven floral phases. Ammonoid biostratigraphy after Brühwiler et al. (in press), Guexirolites beds; Gly=Glyptophiceras sinatum beds; Was=Wasatchites distractum beds;alites pilatoides beds; Bry=Brayardites compressus beds; Fl. f.=Flemingites flemingianuss bhargavai beds; Prbl.=Prionolobus rotundatus beds; Gyr=Gyronites beds. Ammonoidisotopes after Hermann et al. (2011). The asterisk indicates the first appearance of the
633E. Hermann et al. / Gondwana Research 20 (2011) 630–637
vegetation and the Middle Triassic conifer-dominated vegeta-tion. Lycopods mainly represented by Densoisporites spp. andAratrisporites spp. are still a prominent component of the vegeta-
110
105
100
95
85
75
80
70
65
90
155
150
145
140
135
125
120
130
Spa
thia
n
Niv
eaux
Inte
rméd
iaire
sTo
pmos
t Lim
esto
neLa
nda
Mem
ber
Uppe
r Cer
atite
Lim
esto
neKa
thwaiLCL
Cera
tite
Mar
lsCe
ratit
e Sa
ndst
one
Biva
lve
Beds
Gr.
Dien
eria
nS
mith
ian
55
60
45
50
35
40
25
30
15
20
0
5
10
160
Perm
ian
Chhid
ru F
m.
C
125
N
Chi
tta-L
andu
Nam
mal
early
Sm
ithia
n
mid
dle
Sm
ithia
n la
teS
mith
Tr
GlyWas
NyaPscNamBry
Fl. f.
Fl. n.
Xed
F. bh.Prlb
Gyr
115Prh
Ani
sian
Mia
nwal
i For
mat
ion
Tred
ian
Form
atio
n
-34 -32 -28
-8 -4 0 4
C13carb
C13org
PU 200PU 198PU 197PU 196PU 195PU 194PU 193PU 192LA 82LA 81LA 80LA 79LA 78LA 77LA 76LA 75
LA 74
LA 70
LA 66
LA 66-2PU
PU 117
PU 114
LA 57
LA 55
LA 52
LA 50
PU 111
PU 109
PU 106
PU 104-3
PU 104-2
PU 104
PU 102
PU 101
PU 99PU 98PU 96
NR 11NR 10CH 94CH 93
NA 76NA 75NA 74NA 73NA 70NA 68
NA 65
NA 64NA 63
NA 62
NA 61NA 60NA 59NA 57NA 56NA 55NA 53NA 52NA 51NA 49NA 213NA 212NA 211NA 210NA 208NA 207NA 206NA 205NA 204NA 307NA 304NA 301NA 203NA 208AIONA 202NA 201AIONA 201NA 200
PU 93
% D
enso
ispor
ites
Gro
up
% L
undb
ladi
spor
a G
roup
% K
raeu
selis
porit
es G
roup
% A
ratri
spor
ites
Gro
up
% U
vaes
porit
es G
roup
% C
avat
e Tr
ilete
spo
res
LYCOPODS
< 10% 10% - 30% 30% - 50%
% B
RYO
PH
YT
ES
1
4
Lith
olog
y
Car
bon
Isot
opes
Am
mon
oid
bios
trat
igra
phy
[m]
Lith
ostr
atig
raph
y
Age
*
Sam
ples
gymnosperms
gym
no
sper
mp
rolif
erat
ion
gymnosperrecoverysporespike
lyco
pod
dom
inat
ed v
eget
atio
n
onset spore domina
a
-24
tion, but conifers begin to proliferate. The diversity of ornamentedspores indicates that ferns also played a prominent role in theseecosystems.
% C
alam
ospo
ra G
roup
% O
ther
spo
res
% T
aeni
ate
Bisa
ccat
es
incl.
Fal
cispo
rites
spp
.
% B
isacc
ate
undi
ffere
ntia
ted
% E
phed
ripite
s G
roup
%
non-
taen
iate
Bisa
ccat
e Po
llen
% C
ycad
opite
s G
roup
FER
NS
50% - 70% > 70%
Palynomorph Diversity
40
(number of taxa)
Diversity patterns of Smithian ammonoids of the NIM
(Brühwiler et al., 2010)
PTE
RID
O-
SP
ER
MS
CO
NIF
ER
S
Lithology
sandstone
siltstone
limestone
sandy limestone
oolithic limestone
coquinoid limestone
dolomite
N
C
Narmia
Chhidru
[number of genera]
[ratios]
0% 100%
0 4 12 20
turnover [%]
generic richness [n]
7
EQ
UIS
ET.
GN
ETO
P.
CY
CA
DO
P.
2
3
5
6
mix
ed p
teri
do
phy
te-
gym
no
sper
m v
eget
atio
n
m
nce168
50%
Table 1Botanical affinities of relevant sporomorph taxa.After Balme, 1995; Grauvogel-Stamm, 1978.
Plant phylum/class Plant order Sporomorph genera
Pteridophytes Bryophyta Maculatasporites spp., alete spores SporesLycopodiopsida Selaginellales, Pleuromeiales,
Lydopodiales, IsoetalesAratrisporites spp., Densoisporites spp., Endosporites spp.,Kraeuselisporites spp., Lundbladispora spp., Lycopodiacidites spp.,Uvaesporites spp.,
Equisetopsida Calamospora spp.Pteridopsida (ferns) Apiculatisporis spp., Apiculatisporites spp., Camptotriletes spp.,
Concavisporites spp., Converrucosisporites spp., Convolutispora spp.,Cyclogranisporites spp., Grandispora spp., Granulatisporites spp.,Laevigatosporites spp., Leiotriletes spp., Leschikisporis spp.,Lophotriletes spp., Osmundacidites spp., Polycingulatisporites spp.,Polypodiisporites spp.Raistrickia spp., Triquitrites spp.,Verrucosisporites spp.,
Spores with uncertainbotanical affinity
Annulispora spp., Jerseyiaspora spp., Limatulasporites spp.,Naumovaspora spp., Playfordiaspora spp., Punctatisporites spp.,Retusotriletes spp., Triplexisporites spp., and undifferentiated spores
Gymnosperms Lyginopteridopsida(Pteridospermae)
Falcisporites spp., Lunatisporites spp., Protohaploxypinus spp.,Striatoabieites spp., Striatopodocarpites spp., Striomonosaccites spp.,Vitreisporites spp., Weylandites spp., and undifferentiated striatebisaccate pollen
Pollen
Coniferopsida Alisporites spp., Brachisaccus spp., Chordasporites spp., Cordaitina spp.,Jugasporites spp., Klausipollenites spp., Limitisporites spp.,Lueckisporites spp,. Platysaccus spp., Sulcatisporites spp., andundifferentiated non-striate bisaccate pollen
Coniferopsida andpteridospermae
Undeterminable bisaccate pollen, due to their preservation ororientation in the slide.
Gnetopsida Ephedripites spp.Cycadopsida Cycadopites spp., Pretricopipollenites spp.
634 E. Hermann et al. / Gondwana Research 20 (2011) 630–637
Phase (7). Gymnosperm forests with conifers, Gentopsida, Cyca-dopsida, and pteridosperms associated with ferns and lycopods wereestablished in the Anisian. This interval records the highest palyno-floral diversity of the studied succession.
The profound changes in the vegetation of North Gondwana in theSmithian are paralleled by synchronous changes in the ammonoidfaunas of the North Indian Margin (southern Tethys). In the lowerSmithian (floral phase 3), the generic richness of ammonoids(number of ammonoid genera that have been directly observed in abiostratigraphic unit or inferred from their presence below and abovethe considered biostratigraphic unit) increases steadily and showsmoderate to high turnover rates (Brühwiler et al., 2010). During thetime of themiddle Smithian spore spike, ammonoid turnover rates arehighest, and the peak values of generic richness of ammonoid faunasare reached. It is striking that the top of the Smithian spore spike (4)coincides with a major extinction event in the marine realm reflectedin high extinction rates in the ammonoid faunas of the Wasatchitesdistractum beds (Fig. 2).
4.2. Environmental context of ecosystem changes
One of the most widely discussed causes of the end-Permian massextinction advocates rapid climatic changes induced by the massiverelease of greenhouse gases by volcanic activity. The synchronicity of theextinction event with the Siberian Traps supports this hypothesis (e. g.Wignall, 2001). An additional source of CO2 comes from the C-richsedimentsheatedby the intrudingmagma inSiberia,whichwas releasedby pipe structures that have been dated at 252±0.4 My (ID–TIMS,Svensen et al., 2009). Additionally, Permian volcanism in Gondwana isdocumented in the Argentinean Choiyoi igneous province. Here, the lastmajor volcanic pulsewith extensive rhyolitic ignimbrites andpyroclasitcflows has been dated as 251.9±2.7 My (SHRIMP U–Pb zircon, Rocha-Campos et al., 2011). The climate forcing potential of ignimbriteeruptions by enhancing primary productivity through iron fertilisationhas been suggested by Cather et al. (2009). Enhanced primaryproduction and burial of organic carbon leads to a CO2 drawdown andimplies a global cooling (Cather et al., 2009). This contrasts with the
warmingeffect caused by the large CO2 amounts induced by theSiberianTrap volcanism. The CO2 release from the Siberian Traps through pipestructures, as described by Svensen et al. (2009), appears to be arelatively fast process, probably outpacing the CO2 drawdown byenhanced primary productivity. Therefore, the impact of the felsicvolcanism in Argentina on global climate remains open for discussion.Nevertheless, the ejection of large amounts of volcanic ash might implyan additional source of environmental perturbations near the Permian–Triassic transition.
Carbon isotope records in Lower Triassic sedimentary sequences aremarked by recurrent excursions of high magnitude. These excursionshave been interpreted to reflect the recurrent CO2 pulses linked withthe protracted Siberian Trap volcanism (Ovtcharova et al., 2006; Payneand Kump, 2007). Such pulses might be responsible for additionalextinction events that followed the main crisis at the Permian–Triassictransition, and for the constant turnover during the recovery of marineecosystems (Brayard et al., 2006, Hautmann et al. 2011).
The palynological records recovered from the sections of the SaltRange and Surghar Range reflects a series of changes in the NorthGondwanan terrestrial ecosystems in the aftermath of the end-Permianmass extinction. Strikingly, major changes in the marine biota (ammo-noids) are closely related to these ecosystem changes on land. In manyPermian–Triassic sections from different palaeogeographic regions, theonset of lycopod-dominated plant communities reflected in a spore spikehas been observed in association with the end-Permian mass extinction(Greenland, Looy et al., 2001; Stemmerik et al., 2001; Norway, Hochuliet al., 2010a; Australia, Foster, 1982). This end-Permian spore spike occurswithin the global negative carbon isotope excursion thatmarks Permian–Triassic boundaries (Payne and Kump, 2007). In the North Gondwananrecords of Pakistan, floral phases (1) and (2) have both been recoveredfrom the uppermost Chhidru Formation, but from different localities. Thediscontinuities of the sampled succession prevent the firm identificationof the end-Permian spore spike. However, the studied palynologicalassemblages show a distinct increase of spores in the uppermost ChhidruFormation from floral phase (1) to floral phase (2).
The end-Permian spore spike has been interpreted as the signalfor pioneering plant assemblages following the destruction and
635E. Hermann et al. / Gondwana Research 20 (2011) 630–637
extinction of woody gymnosperms in Europe (Looy et al., 1999,2001). Global compilations demonstrate that the reduction of floraldiversity is a regional phenomenon and strongly biassed by lownumbers of fossiliferous localities with the Permian–Triassictransition (Rees, 2002). In other areas, diversity increases (Hochuliet al., 2010a and references therein). Owing to the plant-specificphysiological advantage to sprout from various parts (e. g. seeds,spores, and roots) after physical destruction or dormancy, plants arenot subject to the same destructive effects as marine and terrestrialfaunas. The competition for their basic requirements such as water,CO2 and light is crucial for the determination of plant diversitypatterns. Thus, climate changes have a great effect on floraldiversity. A loss of diversity might be induced when the migrationof plants cannot keep pace with climate change (Knoll, 1984). TheEarly Triassic carbon isotope perturbations are marked by an initialnegative shift at the Permian–Triassic boundary signalling enhancedgreenhouse gas releases and global warming (Wignall, 2001).Therefore, diverging from the interpretations of Looy et al. (2001),the end-Permian spore spike can be interpreted as consequence of aclimate change to more humid conditions at the Permian–Triassictransition (Hochuli et al., 2010a). For the fern spike near theTriassic–Jurassic boundary, van de Schootbrugge et al. (2009)suggested, in addition to increased humidity, the release of volcanicSO2 affecting plants by generating acid rain. In contrast to seedplants, the physiological dispositions of pteridophytes growingunder water-saturated conditions enable these plants to cope withelevated levels of atmospheric volcanic pollutants (Page, 2002; vande Schootbrugge et al., 2009).
Another floral phenomenon of the Permian–Triassic boundary isthe common occurrence of unseparated spore tetrads and anormalpollen grains, reflecting the prevailing environmental stress duringthe Permian–Triassic transition (Looy et al., 2001, Foster and Afonin,2005). One of these environmental stress factors could be increasedUV-B radiation induced by the depletion or destruction of the ozonelayer. Increased UV-B radiation is thought to cause genetic changes sothat spore tetrads of mutant pteridophytes loose the ability toseparate and probably reduce the efficiency of reproduction (Beerling,2007, Visscher et al., 2004). Probable causes for the ozone layerdestruction are volcanically induced releases of H2S and halocarbons(Kump et al., 2005, Svensen et al., 2009, Visscher et al., 2004). Anotherfactor that might have led to increased penetration of mutageniccosmic rays is a lowering of the geomagnetic field intensity, whichtogether with the ozone layer protects the biosphere from harmfulcosmic radiation. Low geomagnetic field intensity might be caused byan unstable magnetic dipole. The Illawarra Reversal in the lateGuadalupian marks the onset of a period with an unstable magneticdipole and probably intermittently low geomagnetic field intensity(Isozaki, 2009; Svensmark, 2007).
The flora reacted to the abrupt climate change near the Permian–Triassic boundary by entering into a “stress mode”, i.e. a time intervalcharacterised by ecosystem instability caused by environmental stressand reflected in fast floral adaptations. The onset of these ecosysteminstabilities is reflected in a spore spike (Greenland, Looy et al., 2001;Stemmerik et al., 2001; Norway, Hochuli et al., 2010a; Australia,Foster, 1982) and, to a lesser degree, in floral phase (2) of the presentstudy. The synchronicity of the spore spike documented in northernhemisphere records with those observed in the southern hemisphereis still a matter of ongoing research. The global significance of thisevent is reflected in the fundamental floral changes in all sectionsstraddling this time interval. However, even in the tropical succes-sions of South China, microfloral and macrofloral records of thePermian–Triassic transition are marked by increased abundances ofTriassic lycopods associated with surviving Permian floral elements(Peng et al., 2005).
The aftermath of the end-Permian extinction is characterised byrecurrent environmental perturbations (Hochuli et al., 2010b;
Galfetti et al., 2007b). The ecosystem instabilities began with theinitial end-Permian floral turnover (and faunal extinction) andcontinued into the Lower Triassic from the Griesbachian up to thelowermost Spathian. U–Pb radio-isotopic age calibration of the high-resolution Early Triassic succession of ammonoid faunas suggests aduration of about 2.1 Ma for this time interval (Galfetti et al., 2007a;Ovtcharova et al., 2006). The changing climatic conditions caused aseries of floral adaptations reflected in our floral phases (2) to (5).After the end-Permian spore spike, the vegetation of the Dienerianand especially of the early Smithian on the northern margin ofGondwana experienced a slight relief from the initial perturbation.Floral diversity increased and gymnosperms were common, butpteridophytes were still the predominent component of the flora ofphase (3). European palynological records of the same time intervalare similarly dominated by lycopods (Kürschner and Herngreen,2010; Vigran et al., 1998; Looy et al., 1999) with highest diversitiesin mid-latitudinal records (Hochuli et al., 2010a). Global ammonoiddiversity patterns of this time interval do not match the resolutionof the North Gondwana data but they show moderate increases indiversity in the Dienerian and a first major peak during theSmithian (Brayard et al., 2006, 2009). Conodonts, which passed thePermian–Triassic boundary without a significant reduction indiversity, experienced a major radiation in the Dienerian andearly Smithian time intervals (Orchard, 2007).
The second major ecological perturbation following the end-Permian spore spike is documented in the middle to upper Smithian.In the middle Smithian, a negative carbon isotope excursion isassociated with a spore spike (4) and immediately followed by theproliferation of gymnosperms (5). Similar patterns have beenobserved from the Permian–Triassic boundary in Norway (Hochuliet al., 2010a). These high-resolution records document a spore spikecoinciding with the onset of a major carbon cycle perturbation andfollowed by a rebound of gymnosperms (Hochuli et al., 2010a).Another similarity to the end-Permian spore spike is the associationwith a major and global extinction event. The late Smithian extinctionevent affected essentially the clades that had recovered rather quicklyafter the end-Permian extinction such as ammonoids and conodonts(Brayard et al., 2006; Orchard, 2007).
The environmental perturbations and the associated ecosystemupheavals finally weakened during the Spathian. The changes in thefloral communities slowed back down to a “normal mode”. Increasedgymnosperm abundances are not only reflected in the palynologicalassemblage of the transitional phase (6) of the Spathian of NorthGondwana, but also in Australia (increased abundance of Falcisporitesspp. e. g. Price, 1997) and central Europe (increased abundance ofVoltziaceaesporites heteromorphus e.g. Kürschner and Herngreen,2010; Orłowska-Zwolińska, 1984). The “normal mode” in the terres-trial ecosystems is paralleled in the marine biosphere by a protracteddiversification of ammonoids (Brayard et al., 2006, 2009), conodonts(Orchard, 2007) and benthic faunas (Hautmann et al., 2008).
Looy et al. (1999) proposed a delayed recovery of conifer forests inEurope of 4 to 5 million years, spanning more or less the entire EarlyTriassic. Our results demonstrate that the resurgences of prominentgymnosperm vegetation had already started in the early Spathianwith a transitional flora (6) composed of lycopods and conifers.Similar recovery patterns have been observed in the same timeinterval of mid-latitude successions in Norway (Hochuli and Vigran,2010) and central Europe (Kürschner and Herngreen, 2010;Orłowska-Zwolińska, 1984). The Anisian palynological assemblagesof North Gondwana reflect widespread conifer forests with a diversefern understory and rare lycopods. Similar to our result, gymnospermpollen dominate the Anisian assemblages of central Europe, showingan even higher diversity (e. g. Orłowska-Zwolińska, 1984). In contrastto this, sites from mid-latitudes of the northern hemisphere showremarkable abundances of lycopods associated with highly diversifiedgymnosperm pollen (Hochuli and Vigran, 2010).
636 E. Hermann et al. / Gondwana Research 20 (2011) 630–637
Our observations, combinedwith the radio-isotopic age calibrationof the Early Triassic stages, allow for a reassessment of the “delayedfloral recovery”. The ecosystem perturbation as reflected in thedominance of stress-resistant lycopods encompasses the Griesbachianup to the earliest Spathian, corresponding to a time interval of ca.2.1 My. The ecosystem perturbations waned during the Spathian, atime interval of ca. 2.4 My (Galfetti et al., 2007a, Ovtcharova et al.,2006), and diverse gymnosperm-rich plant communities wereestablished. We interpret the observed changes in the floral recordof the Lower Triassic as a signal of floral adaptation to changingenvironments, whereas the loss of plant diversity at a highertaxonomic level remained a minor phenomenon. Or in a nutshell, ifthe environmental conditions had become more favourable earlier,gymnosperms could have proliferated at any time during the EarlyTriassic.
5. Conclusions
The Upper Permian–Middle Triassic palynological record and theinferred floral changes on the northern margin of Gondwana show arecurrent pattern of spore peaks associated with negative excursionsin the carbon isotope record and closely linked to extinction events inmarine ecosystems.
The proliferation of pteridophytes during the Early Triassic, fromthe uppermost Permian to the Smithian (and to minor extent to theSpathian), is linked to climatic changes probably triggered byvolcanism. The data suggests that the major plant groups survivedthe end-Permian extinction event, but may have been temporallyabsent from the palynological record depending on changes inrelative abundances driven by changing climatic/atmospheric condi-tions. We propose that the observed floral changes reflect theadaptation of the vegetation to profound and recurrent environmen-tal changes in the Early Triassic and are not necessarily a signal of aglobal floral diversity decrease or disastrous extinction event. Over atime period of about 2.1 My, the vegetation on North Gondwana wasforced into a mode of fast adaptations to abiotic environmentalchanges (“stress-mode” corresponding to ecological instability)reflected in fast changes in the dominance structure within theterrestrial flora. In the Spathian and Anisian these conditions werereplaced by a “normal mode” and the development of stableecosystems.
Acknowledgements
We acknowledge financial support from the Swiss NationalScience Foundation project 200020-127716/1 (to H. Bucher). ArnaudBrayard and Stefan Piasecki are gratefully acknowledged for theirhelpful reviews that improved the manuscript.
References
Abbink, O.A., 1998. Palynological Investigation in the Jurassic of the North Sea Region.Ph.D. Thesis, Laboratory of Palaeobotany and Palynology, Utrecht, 192 pp.
Balme, B.E., 1995. Fossil in situ spores and pollen grains: an annotated catalogue.Review of Palaeobotany and Palynology 87, 81–323.
Bamford, M.K., 2004. Diversity of the woody vegetation of Gondwanan Southern Africa.Gondwana Research 7, 153–164.
Beerling, D.J., 2007. The Emerald Planet — How Plants Changed Earth's History. OxfordUniversity Press, Oxford. 288 pp.
Bonis, N.R., Ruhl, M., Kürschner, W., 2010. Milankovitch-scale palynological turnoveracross the Triassic–Jurassic transition at St. Audries Bay, SW UK. Journal of theGeological Society 167, 877–880.
Brayard, A., Bucher, H., Escarguel, G., Fluteau, F., Bourquin, S., Galfetti, T., 2006. The EarlyTriassic ammonoid recovery: paleoclimatic significance of diversity gradients.Palaeogeography, Palaeoclimatology, Palaeoecology 239, 374–395.
Brayard, A., Escarguel, G., Bucher, H., Monnet, C., Brühwiler, T., Goudemand, N., Galfetti,T., Guex, J., 2009. Good genes and good luck: ammonoid diversity and the end-Permian mass extinction. Science 325, 1118–1121.
Brühwiler, T., Bucher, H., Brayard, A., Goudemand, N., 2010. High-resolutionbiochronology and diversity dynamics of the Early Triassic ammonoid recovery:
the Smithian faunas of the Northern Indian Margin. Palaeogeography, Palaeocli-matology, Palaeoecology, doi:10.1016/j.palaeo.2010.09.001.
Brühwiler, T., Bucher, H., Ware, D., Hermann, E., Hochuli, P.A., Roohi, G., ur-Rehman, K.,and Yaseen, A., (in press), Smithian (Early Triassic) ammonoids from the SaltRange, Pakistan. Special Papers in Palaeontology.
Cather, S.M., Dunbar, N.W., McDowell, F.W., McIntosh, W.C., Scholle, P.A., 2009. Climateforcing by iron fertilization from repeated ignimbrite eruptions: the icehouse-silicic large igneous province (SLIP) hypothesis. Geosphere 5, 315–324.
Comin-Chiaramonti, P., Riccomini, C., Slejko, F., De Min, A., Ruberti, E., Gomes, C.B.,2010. Cordierite-bearing lavas from Juguarão, southern Brazil: petrologicalevidence for crustal melts during early rifting of Gondwana. Gondwana Research18, 514–527.
de Jersey, N.J., Hamilton, M., 1967. Triassic Spores and Pollen Grains from theMoolayember Formation. Geological Survey of Queensland, Brisbane. PublicationNo 336, 26 pp.
Delcourt, H.R., Delcourt, P.A., 1985. Comparison of taxon calibrations, modern analoguetechniques, and forest-stand simulation models for the quantitative reconstructionof past vegetation. Earth Surface Processes and Landforms 10, 293–304.
Fletcher, M.S., Thomas, I., 2007. Modern pollen-vegetation relationships in westernTasmania, Australia. Review of Palaeobotany and Palynology 146, 146–168.
Foster, C.B., 1982. Spore–pollen assemblages of the Bowen Basin, Queensland(Australia): their relationship to the Permian/Triassic boundary. Review ofPalaeobotany and Palynology 36, 165–183.
Foster, C.B., Afonin, S.A., 2005. Abnormal pollen grains: an outcome of deterioratingatmospheric conditions around the Permian–Triassic boundary. Journal of theGeological Society, London 162, 653–659.
Galfetti, T., Bucher, H., Ovtcharova, M., Schaltegger, U., Brayard, A., Brühwiler, T.,Goudemand, N., Weissert, H., Hochuli, P.A., Cordey, F., Goudun, K., 2007a. Timing ofthe Early Triassic carbon cycle perturbations inferred from new U–Pb ages andammonoid biochronozones. Earth and Planetary Science Letters 258, 593–604.
Galfetti, T., Hochuli, P.A., Brayard, A., Bucher, H., Weissert, H., Vigran, J.O., 2007b.Smithian/Spathian boundary event: evidence for global climatic change in thewake of the end-Permian biotic crisis. Geology 35, 291–294.
Golonka, J., Ford, D., 2000. Pangean (Late Carboniferous–Middle Jurassic) paleoenvir-onment and lithofacies. Palaeogeography, Palaeoclimatology, Palaeoecology 161,1–34.
Grauvogel-Stamm, L., 1978. La flore du grès a Voltzia (Buntsandstein supérieur) desVosges du Nord (France), morphologie, anatomie, interprétations phylogénique etpaléogéographique, Université Louis Pasteur de Strasbourg - Institute de Géologie,Strasbourg, 225 pp.
Pakistani–Japanese Research Group, 1985. Permian and Triassic systems in the SaltRange and Surghar Range, Pakistan. In: Nakazawa, K., Dickins, J.M. (Eds.), TheTethys: Her Paleogeography and Paleobiogeography from Paleozoic to Mesozoic.Tokai University Press, Tokyo, pp. 221–312.
Guex, J., 1978. Le Trias intérieur des Salt Ranges (Pakistan): problèmes biochronolo-giques. Eclogae geologicae Helvetiae 71, 105–141.
Hautmann, M., Bucher, H., Nützel, A., Brühwiler, T., Goudemand, N., Brayard, A.,2008. Recovery of benthos versus nekton after the end-Permian mass extinctionevent — a preliminary comparison. GSA Joint Annual Meeting, Houston,paper no. 285-14.
Hautmann, M., Bucher, H., Brühwiler, T., Goudemand, N., Kaim, A., Nützel, A., 2011. Andunusually divers mollusc fauna from the earliest Triassic of South China and itsimplication for benthic recovery after the end-Permian biotic crises. Geobios 44,71–85, doi:10.1016/j.geobios.2010.07.004.
Hermann, E., Hochuli, P.A., Méhay, S., Bucher, H., Brühwiler, T., Hautmann, M., Ware, D.,Roohi, G., ur-Rehman, K., Yaseen, A., 2011. Organicmatter and palaeoenvironmentalsignals during the Early Triassic biotic recovery: the Salt Range and Surghar Rangerecords. Sedimentary Geology 234, 19–41, doi:10.1016/j.sedgeo.2010.11.003.
Hermann, E., Hochuli, P.A., Bucher, H., Brühwiler, T., Hautmann, M., Ware, D., Weissert,H., Roohi, G., Yaseen, A., ur-Rehman, K., submitted for publication. Climaticoscillations at the onset of the Mesozoic inferred from palynological records fromthe North Indian Margin. Journal of the Geological Society London.
Hochuli, P.A., Vigran, J.O., 2010. Climate variations in the Boreal Triassic— inferred frompalynological records from the Barents Sea. Palaeogeography, Palaeoclimatology,Palaeoecology 290, 20–42.
Hochuli, P.A., Hermann, E., Vigran, J.O., Bucher, H., Weissert, H., 2010a. Rapid demiseand recovery of plant ecosystems across the end-Permian extinction-event. Globaland Planetary Change 74 (3–4), 144–155.
Hochuli, P.A., Vigran, J.O., Hermann, E., Bucher, H., 2010b. Multiple climatic changesaround the Permian Triassic boundary event revealed by an expanded palynolog-ical record from Mid Norway. GSA Bulletin 122, 884–896.
Isozaki, Y., 2009. Illawarra reversal: the fingerprint of a superplume that triggeredPangean breakup and the end-Guadalupian (Permian) mass extinction. GondwanaResearch 15, 421–432.
Knoll, A.H., 1984. Patterns of extinction in the fossil record of vascular plants. In:Nitecki, M.H. (Ed.), Extinctions. The University of Chicago Press, Chicago, pp. 21–68.
Kump, L.R., Pavlov, A., Arthur, M.A., 2005. Massive release of hydrogen sulfide to thesurface ocean and atmosphere during intervals of oceanic anoxia. Geology 33,397–400.
Kürschner, W.M., Herngreen, G.F.W., 2010. Triassic palynology of central andnorthwestern Europe: a review of palynoflora diversity patterns and biostrati-graphic subdivisions. Geological Society London, Special Publications 334,263–283.
Lézine, A.M., Watrin, J., Vincens, A., Hély, C., 2009. Are modern pollen datarepresentative of west African vegetation? Review of Palaeobotany and Palynology156, 265–276.
637E. Hermann et al. / Gondwana Research 20 (2011) 630–637
Lindström, S., McLoughlin, S., 2007. Synchronous palynofloristic extinction andrecovery after the end-Permian event in the Prince Charles Mountains, Antarctica:implications for palynofloristic turnover across Gondwana. Review of Palaeobotanyand Palynology 145, 89–122.
Looy, C.V., Brugman, W.A., Dilcher, D.L., Visscher, H., 1999. The Delayed Resurgence ofEquatorial Forests after the Permian–Triassic Ecologic Crisis. Proceedings of theNational Academy of Sciences of the United States of America 96, 13,857–13,862.
Looy, C.V., Twitchett, R.J., Dilcher, D.L., Van Konijnenburg-Van Cittert, J.H.A., Visscher, H.,2001. Life in the End-Permian Dead Zone. Proceedings of the National Academy ofSciences 98, 7879–7883.
McElwain, J.C., Punyasena, S.W., 2007. Mass extinction events and the plant fossilrecord. Trends in Ecology and Evolution 22, 548–557.
McGlone, M.S., Moar, N.T., 1997. Pollen–vegetation relationship on the subantarcticAuckland Islands, New Zealand. Review of Palaeobotany and Palynology 96,317–338.
McLoughlin, S., Lindström, S., Drinnan, A.N., 1997. Gondwanan floristic and sedimen-tological trends during the Permian–Triassic transition: new evidence from theAmery Group, northern Prince Charles Mountains, East Antarctica. AntarcticScience 9, 281–298.
Meert, J.G., Lieberman, B.S., 2008. The Neoproterozoic assembly of Gondwana andits relationship to the Ediacaran–Cambrian radiation. Gondwana Research 14,5–21.
Muller, J., 1959. Palynology of recent Orinoco delta and shelf sediments: reports of theOrinoco Shelf Expedition. Micropaleontology 5, 1–32.
Orchard, M.J., 2007. Conodont diversity and evolution through the latest Permian andEarly Triassic upheavals. Palaeogeography, Palaeoclimatology, Palaeoecology 252,93–117.
Orłowska-Zwolińska, T., 1984. Palynostratigraphy of the Buntsandstein in sections ofwestern Poland. Palaeontologia Polonica 29, 161–194.
Ovtcharova, M., Bucher, H., Schaltegger, U., Galfetti, T., Brayard, A., Guex, J., 2006. NewEarly to Middle Triassic U–Pb ages from South China: calibration with ammonoidbiochronozones and implications for the timing of the Triassic biotic recovery.Earth and Planetary Science Letters 243, 463–475.
Page, C.N., 2002. Ecological strategies in fern evolution: a neopteridological overview.Review of Palaeobotany and Palynology 119, 1–33.
Payne, J.L., Kump, L.R., 2007. Evidence for recurrent Early Triassic massive volcanismfrom quantitative interpretation of carbon isotope fluctuations. Earth and PlanetaryScience Letters 256, 264–277.
Peng, Y., Zhang, S., Yu, T., Yang, F., Gao, Y., Shi, G.R., 2005. High-resolution terrestrialPermian–Triassic eventostratigraphic boundary in western Guizhou and easternYunnan, southwestern China. Palaeogeography, Palaeoclimatology, Palaeoecology215, 285–295.
Price, P.L., 1997. Permian to Jurassic palynostratigraphic nomenclature. In: Green, P.M.(Ed.), The Surat and Bowen Basins, South-east Queensland Brisbane. QueenslandDepartment of Mines and Energy, Brisbane, pp. 137–178.
Pross, J., Kotthoff, U., Müller, U.C., Peyron, O., Dormoy, I., Schmiedl, G., Kalaitzidis, S.,Smith, A.M., 2009. Massiv perturbation in terrestrial ecosystems of the EasternMediterranean region associated with the 8.2 kyr B.P. climatic event. Geology 37,887–890.
Rees, P., 2002. Land–plant diversity and the end-Permian mass extinction. Geology 30,827–830.
Renne, P.R., Ernesto, M., Pacca, I.G., Coe, R.S., Glen, J.M.G., Prévot, M., Perrin, M., 1992.The age of Paraná flood volcanism, rifting of Gondwanaland, and the Jurassic–Cretaceous boundary. Science 258, 975–979.
Rocha-Campos, A.C., Basei, M.A., Nutman, A.P., Kleiman, L.E., Varela, R., Llambias, E.,Canile, F.M., da Rosa, O.d.C.R., 2011. 30 million years of Permian volcanismrecorded in the Choiyoi igneous province (W Argentina) and their source foryounger ash fall deposits in the Paraná Basin: SHRIMP U–Pb zircon geochronologyevidence. Gondwana Research 19, 509–523, doi:10.1016/j.palaeo.2010.09.001.
Schindewolf, O.H., 1954. Über die Faunenwende vom Paläozoikum zum Mesozoikum.Zeitschrift der Deutschen Geologischen Gesellschaft 105, 154–183.
Smith, A.G., Smith, D.G., Funnell, B.M., 1994. Atlas of Mesozoic and Cenozoic Coastlines.Cambridge University Press, Cambridge.
Spalletti, L.A., Artabe, A.E., Morel, E.M., 2003. Geological factors and evolution ofsouthwestern Gondwana Triassic plants. Gondwana Research 6, 119–134.
Stemmerik, L., Bendix-Almgreen, S.E., Piasecki, S., 2001. The Permian–Triassic boundaryin central East Greenland: past and present views. Bulletin of the Geological Societyof Denmark 48, 159–167.
Stutz, S., Prieto, A.R., 2003. Modern pollen and vegetation relationships in Mar Chiquitacoastal lagoon area, southeastern Pampa grasslands, Argentina. Review ofPalaeobotany and Palynology 126, 183–195.
Svensen, H., Planke, S., Polozov, A.G., Schmidbauer, N., Corfu, F., Podladchikov, Y.,Jamtveit, B., 2009. Siberian gas venting and the end-Permian environmental crisis.Earth and Planetary Science Letters 277, 490–500.
Svensmark, H., 2007. Cosmoclimatology: a new theory emerges. Astronomy andGeophysics 48, 1.18–1.24.
Traverse, A., 2007. Paleopalynology. Springer Verlag, Dordrecht. 813 pp.Tyson, R.V., 1995. Sedimentary Organic Matter — Organic Facies and Palynofacies.
Chapman & Hall, London. 615 pp.Utting, J., Spina, A., Jansonius, J., McGregor, D.C., Marschall, J.E.A., 2004. Reworked
miospores in the upper Paleozoic and Lower Triassic of the Northern circum-polararea and selected localities. Palynology 28, 75–119.
Vajda, V., Raine, J.I., Hollis, C.J., 2001. Indication of global deforestation at theCretaceous–Tertiary boundary by New Zealand fern spike. Science 294, 1700–1702.
van de Schootbrugge, B., Quan, T.M., Lindström, S., Püttmann, W., Heunisch, C., Pross, J.,Fiebig, J., Petschick, R., Röhling, H.-G., Richoz, S., Rosenthal, Y., Falkowski, P.G., 2009.Floral changes across the Triassic/Jurassic boundary linked to flood basaltvolcanism. Nature Geoscience 2, 589–594.
Veevers, J.J., 2006. Updated Gondwana (Permian–Cretaceous) earth history of Australia.Gondwana Research 9, 231–260.
Vigran, J.O., Mangerud, G., Mørk, A., Bugge, T., Weitschat, W., 1998. Biostratigraphy andsequence stratigraphy of the Lower and Middle Triassic deposits from the SvalisDome, Central Barents Sea, Norway. Palynology 22, 89–141.
Visscher, H., Brinkhuis, H., Dilcher, D.L., Elsik, W.C., Eshet, Y., Looy, C.V., Rampino, M.R.,Traverse, A., 1996. The terminal Paleozoic fungal event: evidence of terrestrialecosystem destabilization and collapse. Proceedings of the National Academy ofSciences 93, 2155–2158.
Visscher, H., Looy, C.V., Collinson, M.E., Brinkhuis, H., van Konijenburg-van Cittert, J.H.A.,Kürschner, W.M., Sephton, M.A., 2004. Environmental Mutagenesis during the End-Permian Ecologial Crisis. Proceedings of the National Academy of Sciences of theUnited States of America 101, 12,952–12,956.
Wignall, P.B., 2001. Large igneous provinces and mass extinctions. Earth-ScienceReviews 53, 1–33.
Xiong, C.H., Wang, Q., 2011. Permian–Triassic land-plant diversity in South China: wasthere a mass extinction at the Permian/Triassic boundary? Paleobiology 37,157–167.