Evidence for atmospheric pollution across the Permian-Triassic
transition
Peter A. Hochuli1, Elke Schneebeli-Hermann1, Gunn Mangerud2, and Hugo Bucher1
1
Institute and Museum of Palaeontology, University of Zurich, Karl Schmid-Strasse 4, CH-8006 Zurich, Switzerland
2
Department of Earth Science, University of Bergen, Postboks 7803, N-5020 Bergen, Norway
ABSTRACT
Evidence for a cause-and-effect relationship between the emplace-
ment of the Siberian Traps large igneous province and the Perm-
ian-Triassic marine mass extinction has been growing over the past
decades. However, how the Siberian Traps volcanism affected the
terrestrial vegetation is still a matter of controversy. Here, we demon-
strate that a substantial part of plants’ life cycle, namely their repro-
ductive organs, was adversely affected by environmental conditions.
Effects include malformed spores and pollen grains, unseparated
tetrads, and darkened walls of spores and pollen (sporoderm) from
Permian-Triassic sediments from the Finnmark Platform offshore
Norway. The co-occurrence of these morphological changes with the
main carbon isotope excursion and the marine mass extinction may
suggest that they were caused by atmospheric pollution linked to
Siberian Traps emissions.
INTRODUCTION
The Permian-Triassic boundary (PTB) is known for the most impor-
tant mass extinction in Earth history, causing the extinction of 52% of all
marine invertebrate families (Raup and Sepkoski, 1982). Due to the frag-
mentary terrestrial fossil records, comparatively little is still known about
the impact of the environmental upheavals on terrestrial biota. Ideas range
from total devastation of plant life (Utting et al., 2004) to transient floral
changes where all major plant groups survived (Hochuli et al., 2010). Due
to the high preservation potential of sporomorphs, palynological studies
provide the best approach to decipher changes in vegetation.
Shallow stratigraphic cores from the Finnmark Platform (cores 7128/12-
U-1 and 7129/10-U-1; see Fig. DR1 in the GSA Data Repository1), offshore
northern Norway, containing well-preserved palynomorphs have been
used to reconstruct the most detailed vegetation succession across this
interval covered by the Tempelfjorden Group and the Havert Formation
(Bugge et al., 1995; Mangerud, 1994; Hochuli et al., 2010). The succes-
sion shows prominent changes in relative abundance of plant groups. The
palynoflora of the uppermost Tempelfjorden Group and the basal Havert
Formation is marked by gymnosperm pollen dominance followed by pte-
ridophyte dominance (Hochuli et al., 2010) (Fig. 1). The duration of the
pteridophyte-dominated interval has been estimated to be ~10 k.y., which
was followed by a renewed prevalence of gymnosperms. It is known as
the “spore spike” and has been called the palynological PTB (Stemmerik
et al., 2001). A similar event has been recorded at the Triassic-Jurassic
boundary (TJB) (e.g., van de Schootbrugge et al., 2009).
Processes leading to these floral turnovers are still unclear. The assem-
blages of the Permian-Triassic “spore spike” are marked by common
occurrences of spore tetrads. These have been interpreted as mutated forms
caused by ozone layer depletion and increased ultraviolet B (UV‑B) radia-
tion, preventing immature spore tetrads from separating during maturation
GSA Data Repository item 2017388, photographic documentation of spore-
1  and obvious modifications of sporomorph color (Fig. 1). The assessment
pollen teratomorphism, is available online at http://www.geosociety.org​/datarepository​
/2017/ or on request from editing@geosociety.org.
GEOLOGY, December 2017; v. 45; no. 12; p. 1123–1126  |  Data Repository item 2017388  | https://doi.org/10.1130/G39496.1 |  Published online 27 October 2017
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(Visscher et al., 2004). The prime reason for this would be the volcanic
activity of the Siberian Traps by release of organohalogens (Beerling et
al., 2007).
Other effects of the PTB event on sporomorphs have been recorded by
Foster and Afonin (2005), who found significantly increased numbers of
abnormal gymnosperm pollen across the PTB in Russia and China and
suggested that these could be expected in other coeval sections.
Abnormal pollen grains are known not only from the fossil record.
Extant spores and pollen show natural morphological variations (e.g.,
Wilson, 1965). However, higher percentages (>3%) of morphological
abnormalities such as dwarfism and gigantism as well as abnormal forms
of sporomorph walls are known to indicate environmental hazards. Other
known teratological features in modern and fossil assemblages comprise
asymmetry, changes in aperture numbers and development, and underde-
veloped or distorted sacci of saccate pollen grains (e.g., Dzyuba, 2006;
Dzyuba and Tarasevitch, 2002; Foster and Afonin, 2005). The occurrence
of increased frequency of spore tetrads is also a possible indication of
harmful environmental stress. However, the number of spore tetrads in
palynological samples is also influenced by taphonomic features, as well
as sorting effects in relation to depositional environments (e.g., Tyson,
1995). Some species also have a natural tendency for spores to remain
together, meaning that the number of tetrads might not per se represent a
reliable indicator of environmental damage (e.g., Hochuli et al., 2016). In
the studied material, normal tetrads are commonly associated with mal-
formed specimens (e.g., unequal spore size, welded tetrads, or reduced
number of spores). Almost equal numbers of teratological tetrads and
normal ones have been observed throughout the succession. Thus, in the
present context, we consider most of the tetrads to reflect reactions of the
pteridophytes to damaging environmental conditions. Another striking
feature is the presence of numerous dark-colored sporomorphs, first men-
tioned and associated with reworking (Mangerud, 1994). For the present
study, we quantify the numbers of abnormal and darkened sporomorphs
including tetrads in relation to normal forms.
In order to find indications for the processes leading to the floral
changes during and after the mass extinction, we document herein terato-
morphic features of sporomorphs in the Finnmark Platform sections. We
suggest that the teratological forms and especially the darkened sporo-
morphs reflect direct contact of the plants with damaging agents, and relate
these to severe and prolonged environmental disturbances affecting the
protective walls of the plant gametes during this time interval.
METHODS AND MATERIALS
We evaluated the preservation and the morphology of sporomorphs
in a time interval of ~100 k.y. across the Permian-Triassic transition
(Hochuli et al., 2010). We then assessed at least 250 sporomorphs for
the 25 samples, recording the quantitative distribution of normal and
teratomorphic grains, as well as normal and malformed spore tetrads
of detailed morphological features of single sporomorphs requires well-
preserved organic matter. Shapes of palynomorphs remain ductile and
1123
 Cumulative percent of
Core depth [m] spore and pollen forms sample depth [m]
62.5 < 10% 10%–30% 30%–50% > 50%
0 % 20 40 60 80 100
65.64

Coal fly ash Hg anomalies

67.86
70 69.3
73.39

Marine extinction
H
80 79.85
81.87

Recovery of gymnosperms
84.74
85.95

events
87.7
90 90.96
e G
94.88

100 100.04
Early Triassic

Terrestrial event
Havert Fm.

105.69

Spore spike
108.79
spore spike

55.4 d
110 110.06
60 112.76 63.48
114.37 115.9 E
116 c
65.68 64.51 D
b
palynological PTB

120 119.09 116.47 C

70 B
Tempelfjorden Gp.
Late Permian

gymnosperms
130

Demise of
80
a
140 141.09 A
90
undeformed

Bisaccate undifferentiated (%)

excl Lueckisporites spp.(%)
93.3

Lueckisporites group (%)

A B

Uvaesporites group (%)

Palynological phases

Ephedripites group (%)

undetermined

Cavate trilete spores (%)

150

Other trilete spores(%)

Cordaites group (%)

tetrads

bisaccate Pollen (%)

Vittatina group(%)
13
δ C org [‰]

Taeniate bisaccates
Spore tetrads (%)
deformed

Bryophytes (%)
-30 -26 -22 tetrads

Non-taeniate
160.2 deformed
7128/12-U-1 darkened
7129/10-U-1 20 μm

Figure 1. Occurrence and abundance of teratomorphic spores and pollen grains across Permian-Triassic boundary (PTB) in Norway. Black
numbers on depth scale and black carbon isotope curve refer to core 7128/12-U-1; gray color is used for core 7129/10-U-1. Pale horizontal
bar indicates an interval of uncertainty regarding occurrences of teratomorph sporomorphs. Bulk organic carbon isotope (δ13Corg) data and
floral phases are after Hochuli et al. (2010). Chronostratigraphy is after Mangerud (1994). Lowercase letters indicate marine extinction events
as documented in relation to the carbon isotope curve in: a—East Greenland, Jameson Land (Twitchett et al., 2001); b—Iran (Heydari et al.,
2008); c and d—East Greenland, Jameson Land (Stemmerik et al., 2001); e—Meishan, China (Jin, et al., 2000), Gartnerkofel, Austria (Holser
et al., 1989), and Buchanan Lake, Canada (Grasby and Beauchamp, 2008). Pulses of coal fly ash–induced Hg anomalies are after Sanei et al.
(2012). Palynological boundary is after Stemmerik et al. (2001). excl—excluding. A: Photograph of Uvaesporites imperialis. Left specimen is
deformed; right specimen is normal. B: Photograph of bisaccate pollen grain with reduced and malformed saccus.

deformable after deposition and are commonly modified by a number Sporomorphs with darker colors regularly occur in most of the studied
of processes, including extraction. Additionally, corrosion can hamper samples. Their colors vary from dark brown to black. Opaque black spo-
precise evaluation of the palynomorph morphology, as can their orienta- roderm is observed in the case of thick-walled spores, showing a distinct
tion in palynological strew mounts. In many cases, such modifications difference from the yellow and translucent conditions of the majority
might be difficult to differentiate from abnormal forms. Therefore, we of palynomorphs. The distinctly darker sporomorphs are recorded as
classified unclear or indeterminate morphologies—folded or in unfavor- “darkened” (see the Data Repository); slight changes in color were not
able position on the slide—as “indeterminate.” Their number depends included in the counts.
essentially on the preservation of the sporomorphs in the samples. The
majority of sporomorph grains belong to this category for most studied RESULTS
samples. Only specimens with distinctive abnormal features were con- Figure 1 shows the quantitative distribution of teratomorphic and dark-
sidered as teratomorphic. The observed teratological features in spores ened sporomorphs, and deformed and normal spore tetrads, together with
include modified trilete marks or distinctly abnormal modifications of undeformed and “indeterminate” sporomorphs. The two last-mentioned
the sporoderm (see Figs. DR1–DR4). The more complex morphology of categories are dominant in all assemblages. The relative abundances of
pollen grains, especially the clearly lateral symmetrical bisaccate grains the two might be influenced by the preservation in the respective samples.
with two equally shaped sacci and laterally symmetrical central body, However, distinct minima in the number of undeformed sporomorphs can
allows differentiating numerous morphological modifications, including be noticed around the onset of the “spore spike” during palynofloral phase
modified number, size, and shape of sacs, shape of the central body (e.g., D and basal phase E as well as in the middle part of phase G. Coinciding
asymmetry or modified thickness of exines), or surface features. The changes in the composition of floral assemblages in organic carbon iso-
present material includes morphological modifications of taeniae (paral- tope (δ13Corg) composition and the distribution of the teratomorphic and
lel strips of exine) in bisaccate pollen grains. Other gymnosperm pollen darkened sporomorphs might provide leads to substantiate the effects of
grains show modifications in their shapes and wall structures. the events around the PTB on terrestrial plants (see below).

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 Teratomorphic sporomorphs can be traced throughout the studied marine collapse in East Greenland (Twitchett et al., 2001), but prior to the
section. Severely affected assemblages, documented by the consider- “spore spike.” Floral phase B indicates still-proliferating gymnosperms
able number of teratological forms, existed already in the latest Permian (Hochuli et al., 2010). The onset of high abundances of darkened sporo-
Tempelfjorden Group (phase A). The highest numbers of abnormal pollen morphs co-occurs with the onset of the “spore spike” (phase D). Compiled
grains (up to 40%) occur in the topmost samples of this group (phases data from East Greenland show co-occurring extinctions of bryozoans,
B–C), coinciding with the onset of the negative δ13Corg shift, prior to the brachiopods, and bivalves (Stemmerik et al., 2001). The next maximum
“spore spike.” Assemblages are largely dominated by gymnosperms up in teratomorphic forms co-occurs with the third Hg spike (Fig. 1) and the
to this level. Because pteridophyte spores are rare in the lower part of main marine extinction pulse in Meishan, China (Jin et al., 2000). By
the section (phases A–C), tetrads are essentially absent from this interval. this time, gymnosperm recovery was already underway (phase G) (Fig.
This association is replaced by the assemblages of the “spore spike,” 1). Unfortunately, U-Pb and Ar-Ar dating of Siberian Traps magmatism
dominated by a few species of lycopod spores (phase D). The number of is currently less precise than dating of the extinction interval (Burgess et
teratological forms is still elevated (~30%). At the onset of this spike, a al., 2014). Thus, it is currently impossible to correlate the presented floral
considerable number of darkened sporomorphs (~10%) and small numbers events with concrete pulses of Siberian Traps magmatism.
of tetrads occur. The tetrad numbers increase to ~10% toward the end The reason for the darkening of parts of the organic matter remains
of the “spore spike” (phases D and E), half of them showing abnormal enigmatic. Normally, dark-colored palynomorphs are associated with
features. This event is accompanied by a continued negative δ13Corg shift the burial history of the sediments in which they are contained or their
(Hochuli et al., 2010). proximity to igneous dikes. This would affect all palynomorphs in the
In phase F, along with the recovered dominance of gymnosperms there sediment. Most of the palynomorphs in the studied section show bright
is a considerable reduction of spores, tetrads, and darkened sporomorphs. yellow, translucent colors indicating that the thermal maturation of this
However, the percentage of the teratomorphic forms remains constant. material is low (immature) (thermal alteration scale; after Batten, 1982).
The continued gymnosperm recovery in phase G coincides with another However, numerous dark-brown or opaque, black, or opaque black sporo-
distinct negative shift in δ13Corg. The lower part of this phase shows slightly morphs represent a striking difference from these immature conditions in
lower percentages of teratomorphic forms (~20%) and only a few dark- about half of the studied samples. The most obvious explanation for the
ened forms (~2%). Its middle part is marked by an abrupt increase in observed heterogeneous preservation would be reworking (see Mangerud,
the latter forms, reaching as much as 10%. This level corresponds to the 1994). However, for the studied section, reworking can be excluded. Firstly,
onset of another, although minor, negative shift in δ13Corg, which reaches the species composition does not differ between the thermally altered
minimum values of −31‰ just above this level. There is, however, no and the unaltered forms (e.g., both dark- and normal-colored specimens
corresponding increase in teratomorphic forms; they peak in one sample of Uvaesporites imperialis occur in the same sample). Secondly, most of
near the top of the section. The percentage of darkened forms remains the observed darkened sporomorphs would reflect temperatures beyond
relatively high (~8%) up to the top of the section, with higher values the oil window (e.g., >120 °C). In the tectonic setting of the innermost
accompanying the peak of the abnormal forms. parts of the Finnmark Platform, reworking from such strongly altered,
essentially coeval sediments can be excluded. Noteworthy is the fact
DISCUSSION that among the very numerous acritarchs, no dark-colored specimens
On heavily polluted industrial sites, morphological changes in sporo- have been found, and only terrestrial forms (spores, pollen grains, and
morphs have been recorded up to abundances of ~40%–60% (Dzyuba, fungal remains) are affected. Thus, other reasons for the modified col-
2006; Dzyuba and Tarasevitch, 2002). Agents causing these teratomorphic ors had to be envisaged. In situ darkening of spores is also known from
features are radioactive radiation and contamination with heavy metals, the so-called Triletes beds in TJB sections of the Germanic Basin (e.g.,
arsenic, acid rain (SO2), and benzo[a]pyrene from industrial emission/ Mariental; van de Schootbrugge et al., 2009). There, it has been explained
exhaust gases (Dzyuba, 2007; Beerling et al., 2007) by soil acidification from sulfuric acid deposition during the activity of
The morphological modifications documented from these sites are the Central Atlantic Magmatic Province. In contrast to the samples from
comparable to and are found in similar abundances as our findings in the the Finnmark sections, all sporomorphs from this specific bed seem to
Permian-Triassic successions on the Finnmark Platform. This suggests be affected. Hence, processes causing this color change were probably
that environmental impact or atmospheric pollution during the Permian- different in the two cases, or the darkened Finnmark sporomorphs have
Triassic interval was comparable to that from modern heavy industrial been transported from distant polluted surfaces and admixed with locally
sites. Sulfur, chlorine, and fluorine have been measured from Siberian unaffected floras. Our experiments exposing recent sporomorphs to sul-
Traps melt inclusions (Black et al., 2012), and models concerning the furic acid remained inconclusive.
amounts and effects of released volatiles demonstrate the potential of
the Siberian Traps as a trigger for environmental pollution (Black et al., CONCLUSIONS
2014). Documentation of plant damage after the Laki eruption on Iceland Despite the fact that no considerable loss of higher plant taxa is
(A.D. 1783) shows the effects of volcanically induced acid rain (Grattan recorded for the PTB, plant assemblages were seriously afflicted by a
and Charman, 1994; Thordarson and Self, 2003). It is assumed that heavy series of events during this interval.
metals played a role during the PTB events (Bond and Wignall, 2014). The present study demonstrates the first evidence of unusual rates
Three anomalies of the toxic metal mercury (Hg) have been documented of teratological pollen grains in the late Permian succession of Norway.
in the PTB succession in northern Canada (Sanei et al., 2012). Correlation Their number reaches a maximum near the top of the Tempelfjorden
of Canadian and Norwegian carbon isotope data places the first Hg peak Group and at the base of the Havert Formation. There are no associated
immediately prior to the first negative δ13Corg shift, the second peak co- darkened sporomorphs observed in this part of the succession. However,
occurring with the intermittent stable δ13Corg values, and the third peak co- teratological and darkened sporomorphs co-occur above the onset of the
occurring with the second δ13Corg negative shift (Fig. 1). Comprehensive “spore spike.” This suggests that the agents causing morphological dam-
qualitative and quantitative pollutant data sets are still missing. However, age on the sporomorphs and those causing the darkening were different
heavy metal enrichment in snow and laboratory rinses of fresh tephra and and did not necessarily act simultaneously.
lava after modern volcanic eruptions is known from Iceland (Hong et al., The teratological features observed on the sporomorphs (e.g., mal-
1996; Ragnarsdottir et al., 1994). Here, the first maximum of teratomor- formation of the protective cover of the male gametes and malformed
phic forms occurs subsequent to the first Hg spike and the onset of the and malfunctioning tetrads) most likely afflicted sexual reproduction of

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 plants over a long time. The process of the darkening of the sporomorphs
remains enigmatic, however, because only part of the material is affected;
we consider direct contact of the sporomorphs with the darkening agent.
The Siberian Traps are assumed to have been the source of the polluting
agents such as heavy metal ions, arsenic, organohalogens, and acid rain
(SO2). The continuous record of teratomorphic sporomorphs documented
in the present study reveals that plants suffered from continuous stress
during the PTB. Three distinct events emerge from the record where
harmful effects were probably most vigorous: (1) exceptionally high per-
centages of teratomorphic forms; (2) induced changes to the composition
of the plant assemblages, associated with the appearance of numerous
darkened sporomorphs; and (3) a second peak of darkened forms. Impor-
tantly, there is no evidence that these events led to the extinction of major
plant groups; only relatively few species disappeared within the interval
Mangerud (1994). The possibility for plants to survive over long times
in cryptic stages like spores, seeds, or roots, and the frequent occurrence
of vegetative reproduction, give plants a much higher survival potential
than animals. This might explain the lack of clear evidence for a plant
extinction event across the PTB.
ACKNOWLEDGMENTS
Access to the shallow stratigraphic cores 7128/12-U-1 and 7129/10-U-1 was granted
by SINTEF Petroleum Research, Trondheim, Norway. Research was supported
by the Swiss National Science Foundation project 20021-135446/1 to H. Bucher.
We thank two anonymous reviewers for comments.
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Manuscript received 6 July 2017
Revised manuscript received 13 September 2017
Manuscript accepted 18 September 2017
Printed in USA