Palaeogeography, Palaeoclimatology, Palaeoecology 252 (2007) 164 – 175

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Elevated atmospheric CO2 and the delayed biotic recovery from

the end-Permian mass extinction
Margaret L. Fraiser a,⁎, David J. Bottjer b
a
Department of Geosciences, University of Wisconsin-Milwaukee, 3209 N. Maryland Avenue, Milwaukee, WI 53211-0413, USA
b
Department of Earth Sciences, University of Southern California, 3651 Trousdale Parkway, Los Angeles, CA 90089-0740, USA
Accepted 30 November 2006

Abstract

Excessive CO2 in the Earth ocean–atmosphere system may have been a significant factor in causing the end-Permian mass
extinction. CO2 injected into the atmosphere by the Siberian Traps has been postulated as a major factor leading to the end-Permian
mass extinction by facilitating global warming, widespread ocean stratification, and development of anoxic, euxinic and CO2-rich
deep waters. A broad incursion of this toxic deep water into the surface ocean may have caused this mass extinction. Although
previous studies of the role of excessive CO2 have focused on these “bottom-up” effects emanating from the deep ocean, “top-
down” effects of increasing atmosphere CO2 concentrations on ocean-surface waters and biota have not previously been explored.
Passive diffusion of atmospheric CO2 into ocean-surface waters decreases the pH and CaCO3 saturation state of seawater, causing a
physiological and biocalcification crisis for many marine invertebrates. While both “bottom-up” and “top-down” mechanisms may
have contributed to the relatively short-term biotic devastation of the end-Permian mass extinction, such a “top-down”
physiological and biocalcification crisis would have had long-term effects and might have contributed to the protracted 5- to 6-
million-year-long delay in biotic recovery following this mass extinction. Earth's Modern marine biota may experience similar
“top-down” CO2 stresses if anthropogenic input of atmosphere/ocean CO2 continues to rise.
© 2007 Elsevier B.V. All rights reserved.

Keywords: Early Triassic; CO2; Molluscs; End-Permian mass extinction; Biotic recovery; Biocalcification

1. Introduction (coupled with the supercontinent configuration of

Pangea), and the development of a vertically stratified,
Elevated atmospheric CO2 has been hypothesized to low O2, H2S- and CO2-rich deep ocean (Knoll et al.,
have played a critical role in causing the end-Permian 1996; Wignall and Twitchett, 1996; Isozaki, 1997;
mass extinction, the largest Phanerozoic mass extinction Wignall, 2001; Grice et al., 2005; Kiehl and Shields,
(Raup and Sepkoski, 1982; Bambach et al., 2004), by 2005; Kump et al., 2005; Marenco et al., 2005).
facilitating deleterious deep-ocean conditions. In- Widespread incursion of these toxic deep-ocean waters
creased atmospheric CO2 due to volcanism may have onto shelves and into surface waters is currently the
led to global warming, reduced thermohaline circulation best-supported mechanism to have been proposed for
this mass extinction, with certain Permian/Triassic facies
⁎ Corresponding author. (e.g., Wignall and Twitchett, 1996; Isozaki, 1997; Wignall
E-mail addresses: mfraiser@uwm.edu (M.L. Fraiser), and Twitchett, 2002), biota (e.g., Wignall and Hallam,
dbottjer@usc.edu (D.J. Bottjer). 1992), biomarkers (Grice et al., 2005), and geochemical
0031-0182/$ - see front matter © 2007 Elsevier B.V. All rights reserved.
doi:10.1016/j.palaeo.2006.11.041
 M.L. Fraiser, D.J. Bottjer / Palaeogeography, Palaeoclimatology, Palaeoecology 252 (2007) 164–175 165

signals (e.g., Marenco et al., 2005; Algeo et al., 2007-this 2001; Flügel, 2002; Mundil et al., 2004; Fraiser and
volume) cited as evidence of these processes. Bottjer, 2005a). The delayed return of “normal” marine
The end-Permian mass extinction, however, marks communities until the Middle Triassic is exceptionally
only the beginning of a prolonged, 5- to 6-million-year- long compared to recoveries following other mass
long biotic crisis, manifested in low alpha diversity, low extinctions (Hallam, 1991; Schubert and Bottjer, 1995)
ecological complexity, and absence of metazoan reefs, and cannot be attributed simply to poor fossil preserva-
that extended through the Early Triassic in all marine tion (Fraiser and Bottjer, 2005b). Carbon isotopic data
environments (Flügel and Stanley, 1984; Hallam, 1991; demonstrate large negative and positive excursions
Flügel, 1994; Schubert and Bottjer, 1995; Martin et al., throughout the Early Triassic aftermath, indicating

Fig. 1. Localities and generalized stratigraphy of Lower Triassic strata examined in this study. (A) Early Triassic paleogeography; examined region of
epeiric seaways on western Pangea is within the outlined area. (B) Lower Triassic shallow-marine environments exposed in the present-day western
USA; bold line represents the shelf edge. Smithian Sinbad Limestone Member exposed in Utah (light gray field), Spathian upper member of Thaynes
Formation exposed in Idaho, Utah, and Montana (dark gray field). (C) General stratigraphy of these Lower Triassic strata. Modified from Blakey
(1974), Scotese (1994), Newman (1974), Woods et al. (1999), Martin et al. (2001), and Mundil et al. (2004).
166 M.L. Fraiser, D.J. Bottjer / Palaeogeography, Palaeoclimatology, Palaeoecology 252 (2007) 164–175

changes in biogeochemical cycling not seen since the are recorded during transgressive events in the Smithian
Cambrian and earlier times (e.g., Atudorei, 1999; Payne portion of the Moenkopi Formation and in the Spathian
et al., 2004; Corsetti et al., 2005). portion of the Thaynes Formation (Blakey, 1974;
Heretofore, the prolonged Early Triassic biotic crisis, Newman, 1974). The Smithian Sinbad Limestone
as well as the mass extinction, have been attributed to Member of the Moenkopi Formation, now exposed in
bottom-up effects. Many Lower Triassic sections exhibit south-central Utah, was deposited in shallow subtidal
sedimentological evidence of the influence of toxic marine environments and represents the easternmost
deep-marine waters. On the western coast of Pangea in extension of shallow-marine deposits during the Early
eastern Panthalassa now exposed in the western USA, Triassic in the USA (Blakey, 1974). Later in the
the development of microbialites and the precipitation Spathian the upper member of the Thaynes Formation,
of aragonite fans on the seafloor during the late Lower now exposed in Utah, Idaho, and Montana, was
Triassic in offshore and slope environments are inter- deposited in shallow subtidal and inner-shelf marine
preted to have been facilitated by upwelling of anoxic environments (Newman, 1974).
waters high in alkalinity due to bacterial sulfate To evaluate the roles which bottom-up vs. top-down
reduction (e.g., Woods et al., 1999; Pruss and Bottjer, mechanisms played in causing the prolonged biotic
2004). However, evidence for biotic crisis exists in crisis in shallow-marine environments late in the
many shallow-marine and oxygenated sections where aftermath of the end-Permian mass extinction, we
there is no evidence for deep-ocean influence (e.g., studied the skeletonized benthic invertebrate marine
Schubert and Bottjer, 1995; Fraiser and Bottjer, 2004; biota in fossil accumulations (shell beds) from the
Twitchett et al., 2004). To try to understand the Sinbad Limestone Member and the upper member of the
mechanisms for the Early Triassic biotic crisis recorded Thaynes Formation. Numerical abundance of organisms
in shallow-marine environments, we evaluated the was determined using semi-quantitative visual estimates
paleoecology of two late Early Triassic (Smithian– in the field; for example, in a bivalve-dominated fossil
Spathian) epeiric seaways exposed in the western USA. accumulation, bivalves comprise 60% or more of the
We propose a new hypothesis for the prolonged biotic fossil constituents (60% was chosen rather than 50% to
crisis in shallow-marine environments during the Early ensure that a group was numerically dominant).
Triassic aftermath: elevated atmospheric CO2 was a “top Methods similar to these have been used in previous
down” mechanism that induced a prolonged physiolog- studies of fossil accumulations (Kidwell and Brenchley,
ical and biocalcification crisis in calcareous skeletonized 1994; Li and Droser, 1999), and information contained
benthic marine invertebrates. in shell beds can reveal mechanisms for the prolonged
duration of the Early Triassic biotic crisis (Boyer et al.,
2. Geologic setting and methods 2004). Eighty-two shell beds were evaluated from a
combined thickness of over 120 m from multiple
In the present-day western U.S.A., the aftermath of outcrops of the Sinbad Limestone Member exposed
the end-Permian mass extinction is recorded in over a 3750-km2 area, and 75 shell beds were examined
Griesbachian, Dienerian, Smithian, and Spathian strata from a combined thickness of over 440 m from multiple
deposited along the eastern margin of Panthalassa outcrops of the upper member of the Thaynes Formation
(Fig. 1). Early Triassic shallow-marine environments exposed over a 6762-km2 area (Fig. 1). Twenty bulk

Table 1
Measures of numerical dominance of skeletonized benthic marine invertebrates in Lower Triassic bulk samples
Rhyn. Inart.
Microgastropods Bivalves brachiopods brachiopods Scaphopods Echinoids
Mean Rank-Order a Sinbad Limestone Member 1.67 1.39 4 2.5 2.5
upper member, Thaynes Fm. 1.57 1.5 2.17 3 3
Breadth of distribution b Sinbad Limestone Member 0.95 0.95 0.16 0.32 0.11
upper member, Thaynes Fm. 0.7 1 0.6 0.1 0.2
a
To determine the rank-orders of organisms from a sample, the most abundant group receives a rank order of 1, the second-most abundant group
receives a score of 2, and so on. To derive the mean rank-order of the organism, the sum of the rank-orders of each organism is divided by the number
of samples in which the group is present.
b
Breadths of distribution are indicated as percentages of the number of samples in which a fossil group occurs.
 M.L. Fraiser, D.J. Bottjer / Palaeogeography, Palaeoclimatology, Palaeoecology 252 (2007) 164–175 167

Fig. 2. Percentages of skeletonized benthic marine invertebrates in Lower Triassic fossil accumulations in the western USA. (A) Constituents of fossil
accumulations in the Smithian Sinbad Limestone Member, and photomicrograph of a microgastropod-dominated shell bed (B). (C) Constituents of
fossil accumulations in the Spathian upper member of the Thaynes Formation, and photo of a bivalve-dominated shell bed (D).

samples from the Sinbad Limestone Member and 10 present (e.g., Patzkowsky and Holland, 1999; Clapham
bulk samples from the upper member of the Thaynes et al., 2006). The Simpson's Index (D) quantifies the
Formation were disaggregated in the lab. diversity of a sample, taking into account the number of
Six metrics common in ecological studies were used different groups of organisms (e.g. species or higher
to further quantify the occurrence of Early Triassic taxonomic groups) present and the abundance of
skeletonized benthic invertebrate fossils at high taxo- organisms in each group (Simpson, 1949). D measures
nomic levels, including mean rank-order, breadth of the probability that two randomly-selected individuals
distribution, the Simpson's Index (D), the Shannon from a sample will belong to the same group. The
Index (H′), evenness, and dominance. Determining the Shannon Index (H′), also known as the Shannon–
mean rank-orders of fossil groups within samples is a Wiener and Shannon–Weaver Indices, is a measure of
means of determining which group is ecologically order (and disorder) of a system (Shannon, 1948);
dominant; the group with the most representatives is in ecological studies, order is characterized by the
considered to have the greatest ecological importance number of individuals in each group of organisms per
regardless of its actual abundance or the number of sample. H′ values are a measure of the uncertainty in
samples in which it occurs (e.g., Baird and Brett, 1983; predicting correctly the species of the next individual
Clapham et al., 2006; see footnotes for Table 1). The collected. Evenness values are measures of how similar
breadth-of-distribution coefficient measures the propor- the abundances of different groups of organisms are and
tion of samples in which a group of organisms was are calculated using the Shannon Index and the number
168 M.L. Fraiser, D.J. Bottjer / Palaeogeography, Palaeoclimatology, Palaeoecology 252 (2007) 164–175

of groups examined. Dominance is the inverse of dominated by bivalves; 57% are dominated by bivalves,
evenness. These metrics represent various ways of microgastropods, or both (Fig. 2C, D). Eighty percent of
determining which (if any) fossil groups are numerically Lower Triassic shell beds formed in shallow-marine
dominant in a sample or many samples. We supple- environments in eastern Panthalassa are numerically
mented our study with data available in the literature on dominated by bivalves, gastropods, or a combination of
Early Triassic paleoecology, Early Triassic environmen- the two groups. Both members contain monospecific
tal characteristics, and Modern invertebrate physiology shell beds that are comprised of 95% of one species of
to evaluate mechanisms for the Early Triassic biotic bivalve (Boyer et al., 2004).
crisis in shallow-marine environments. Bivalves have high mean rank-orders of 1.39 and 1.5,
and microgastropods have high mean rank-orders of
3. The aftermath of the end-Permian mass extinction 1.67 and 1.57 in the samples in which they are present
in shallow subtidal marine environments in eastern from the Sinbad Limestone Member and the upper
Panthalassa member of the Thaynes Formation, respectively
(Table 1). In the Sinbad Limestone Member, bivalves
Our field-based analysis revealed that bivalves and and microgastropods are each found in 95% of the
gastropods are the primary constituents of Lower disaggregated samples (Table 1). In the upper member
Triassic shell beds deposited in shallow subtidal marine of the Thaynes Formation, bivalves are found in 100%
environments in the western USA. Nearly 100% of of the disaggregated samples, and microgastropods are
Sinbad Limestone Member shell beds were comprised found in 70% of them. H′ values were low in both
of bivalves and/or gastropods only: 67% of the fossil members (H′ = 0.034 in the Sinbad Limestone Member;
accumulations are bivalve-dominated, 21% are gastro- H′ = 0.333 in the upper member of the Thaynes
pod-dominated, and 11% are comprised of equal Formation) (Table 2), indicating that individuals were
amounts of bivalves and gastropods (Fig. 2A, B). The not evenly distributed among the fossil groups and were
taxonomic composition of the shell beds is more diverse concentrated primarily among bivalves and gastropods.
(polytaxic) in the upper member of the Thaynes D was high in both members (D = 0.990 in the Sinbad
Formation, but 55% of fossil accumulations are Limestone Member; D = 0.823 in the upper member)
(Table 2), indicating dissimilar abundances of indivi-
duals among the groups. Evenness and dominance
Table 2 values (Table 2) also indicate that the abundances of
Dominance and evenness of skeletonized benthic marine organisms
individuals among the fossil groups were very dissimilar
from Lower Triassic bulk samples
and skewed towards bivalves and gastropods. The
Simpson index (D) a Sinbad Limestone Member 0.990
gastropod-dominated shell beds in the Sinbad Lime-
upper member, Thaynes Fm. 0.823
Shannon Index (H′) b Sinbad Limestone Member 0.034 stone Member are comprised of small-sized adults
upper member, Thaynes Fm. 0.333 termed “microgastropods”; 99% of the gastropods are
Evenness (E) c Sinbad Limestone Member 0.030 smaller than 1 cm in height (Fraiser and Bottjer, 2004)
upper member, Thaynes Fm. 0.240 and the tallest gastropod species is only 1.88 cm in
Dominance d Sinbad Limestone Member 0.969
height (Batten and Stokes, 1986). Though the Sinbad
upper member, Thaynes Fm. 0.759
a
Limestone Member gastropod fauna is the most diverse
The value of D ranges from a minimum value of [1/# of groups of
Early Triassic gastropod fauna known (Nützel, 2005), it
organisms] to a maximum value of 1.0; the larger the value of D, the
lower the diversity and the higher the dominance of only a few groups. reflects a global phenomenon of opportunistic behavior
Sinbad Limestone Member fossils were grouped as molluscs, of microgastropods in normal-marine environments
inarticulate brachiopods, and echinoderms, and groups in the upper during the Early Triassic (Fraiser et al., 2005).
member included molluscs, rhynchnelliform brachiopods, inarticulate
brachiopods, and echinoderms. 4. Discussion
b
H′ values range from a minimum value of 0 to a maximum value of
ln [1/# of groups of organisms] whereby higher numbers indicate that
individuals are distributed more evenly among the groups. 4.1. Early Triassic aftermath in distal versus nearshore
c
Evenness values ranges from 0 to 1.0 whereby higher values marine environments in the western U.S.A.
indicate similar proportions of individuals in the groups, and lower
values indicate dissimilar abundances of individuals among the groups Lower Triassic distal shelf and slope strata exposed
(i.e., some rare and some common groups). Evenness ranges from 0 to
1 (greatest evenness).
in the western U.S.A. exhibit features previously
d
Dominance values range from 0 to 1.0 whereby higher values interpreted as evidence of bottom-up mechanisms. The
indicate dissimilar abundances of individuals among the groups. distal shelf portions of the Griesbachian Dinwoody
 M.L. Fraiser, D.J. Bottjer / Palaeogeography, Palaeoclimatology, Palaeoecology 252 (2007) 164–175 169

Formation exhibit finely laminated, dark gray, pyritic

shales and micrite (Wignall and Hallam, 1992); a fauna
comprised of low-O2-adapted paper pectens (Claraia)
and the disaster taxon Lingula (Rodland and Bottjer,
2001); and low ichnogeneric diversity, low depth and
extent (ii2) of bioturbation, and small trace fossil burrow
diameters (Twitchett and Barras, 2004), all previously
interpreted as the result of marine anoxia. Buildup of
alkalinity in low-O2 deep-marine water by bacterial
sulfate reduction is hypothesized as the cause of black
calcareous shales and seafloor carbonate fans in
Smithian–Spathian strata in slope-deposited sections
of the Union Wash Formation (Woods et al., 1999; Woods
et al., 2007-this volume) and microbialites in offshore
sections of the Spathian Virgin Limestone Member
Fig. 4. [CO2−
3 ] as it varies with pCO2; modified from Orr et al.
(Schubert and Bottjer, 1992; Pruss and Bottjer, 2004). (2005). [CO2−
3 ] for average surface waters in the tropical ocean, the
The shallow-marine environments in which the Southern Ocean, and the global ocean calculated assuming
Sinbad Limestone Member and the upper member of thermodynamic equilibrium between CO2 in the atmosphere and
the Thaynes Formation were deposited were predicted surface waters at their in situ alkalinity, temperature and salinity.
to have provided refuges for marine invertebrate Flat dotted lines indicate the [CO2−3 ] for seawater in equilibrium
with aragonite and calcite.
organisms from the toxic conditions of the Early
Triassic deep ocean. However, millions of years after
the end-Permian mass extinction, bivalves and gastro- Sinbad Limestone Member or in the upper member of
pods numerically dominated communities in these the Thaynes Formation, but the composition of their
shallow-marine environments, and pre-extinction eco- shell beds indicates stressful conditions. No reefs with
logical complexity had not returned. Monospecific shell calcified colonial metazoans are known from the Early
beds like those found in these Lower Triassic shallow- Triassic, and metazoan reef-building resumed only in
marine strata are extremely rare in the fossil record and the Middle Triassic (Anisian) after a millions-of-years
are interpreted to indicate stressful environmental hiatus (Flügel and Stanley, 1984; Flügel, 2002). The
conditions (Boyer et al., 2004). No sedimentological combination of numerical dominance of bivalves and
evidence of bottom-up mechanisms is present in the small-sized adult gastropods and the absence of
metazoan reefs in shallow-marine environments is
unique in the Phanerozoic history of the Earth (Flügel
and Stanley, 1984; Flügel, 2002; Fraiser et al., 2005).
Therefore, the hypothesis that bottom-up disturbances
were the only mechanism for the Early Triassic biotic
crisis must be reevaluated, especially for shallow-
marine environments. It is likely that a different
mechanism delayed biotic recovery in shallow-marine
environments after the end-Permian mass extinction.

4.2. Elevated atmospheric CO2 as a top-down mechan-

ism for the delayed biotic recovery from the end-
Permian mass extinction

The early Paleozoic was characterized by high levels

of atmospheric CO2 that dropped to low levels during
the Carboniferous–Permian (Berner, 2004). Compared
to the late Paleozoic and the Late Triassic, atmospheric
Fig. 3. Permian–Triassic atmospheric CO2 300–200 Ma. RCO2 is the
CO2 levels were elevated during the latest Permian
ratio of reconstructed CO2 concentration to a preindustrial level of through Early Triassic for several million years by
300 ppm; modified from Berner and Kothavala (2001). perhaps 1000 to 1500 ppm (Berner and Kothavala,
170 M.L. Fraiser, D.J. Bottjer / Palaeogeography, Palaeoclimatology, Palaeoecology 252 (2007) 164–175

Table 3
Estimated changes in ocean chemistry as the atmospheric concentration of CO2 increases; modified from Raven et al. (2005)
2× 3× 4× 5× 6×
Pre-industrial Present day pre-industrial pre-industrial pre-industrial pre-industrial pre-industrial
Atmospheric concentration of CO2 (ppm) 280 380 560 840 1120 1400 1680
H2CO3 (mol/kg) 9 13 19 28 38 47 56
HCO−3 (mol/kg) 1768 1867 1876 2070 2123 2160 2183
CO2−
3 (mol/kg) 225 185 141 103 81 67 57
Average pH of surface oceans 8.18 8.07 7.92 7.77 7.65 7.56 7.49
Calcite saturation 5.3 4.4 3.3 2.4 1.9 1.6 1.3
Aragonite saturation 3.4 2.8 2.1 1.6 1.2 1 0.9
Models from the International Carbon-cycle Model Intercomparison Project Phase 3 (OMIP3) were used. Assumptions in model include: Total
alkalinity = 2324 mol/kg, temperature = 18°C.

2001; Berner, 2002) (Fig. 3). Outgassing from conti- (e.g., Seibel and Fabry, 2003; Feely et al., 2004) (Fig. 4,
nental flood basalt province (CFBP) volcanism in Table 3).
Siberia is considered a major source of elevated Organisms possess mechanisms for coping with
Permian–Triassic CO2, as Siberian Trap volcanism cellular acid–base imbalances induced by elevated
correlates well with elevated atmospheric CO2 and with environmental pCO2, such as the abilities to transport
the end-Permian mass extinction (Wignall, 2001; acid–base equivalent ions across cell membranes, to
Courtillot and Renne, 2003). The Siberian Traps emitted suppress metabolism, and to passively buffer intra- and
between 2 and 3 million km3 of material over 1 million extracellular fluids (such as via shell dissolution) (e.g.,
years spanning the P/T boundary, including between Seibel and Fabry, 2003). Organisms with low metabolic
7 × 1012 and 4.8 × 1013 g of CO2 (Renne et al., 1995; rates (e.g., rhynchonelliform brachiopods) have a low
Berner, 2002; Reichow et al., 2002). The increase in capacity to buffer and transport acid–base equivalents
CO2 would have led to global warming, the release of and are therefore more sensitive to hypercapnia than
methane in methane hydrates, and a short-term increase organisms with high metabolic rates (e.g., molluscs)
in CO2 as CH4 oxidized (Wignall, 2001; Krull et al., (James et al., 1992; Seibel and Fabry, 2003). Metabo-
2004). Sustained elevated levels of atmospheric CO2 are lism may be suppressed in organisms if compensation of
hypothesized to have resulted from terrestrial extinc- acid–base imbalance is not achieved, which in turn may
tions that moved the major locus of organic carbon lead to reduced growth and reproductive potential
deposition from the continents to the oceans and caused because expensive processes, like protein synthesis,
global burial rate of organic matter to decrease (Berner, are halted (Guppy and Withers, 1999; Riebesell et al.,
2002). Concomitantly with the increase in CO2, 2000). Some organisms (crustaceans, cephalopods, and
atmospheric O2 levels plummeted to some of the lowest fish) experience large decreases in oxygen affinity with
levels of the Phanerozoic (Berner, 2002), and it has been decreasing pH; others, like gastropods, experience
hypothesized that hypoxia (a top-down mechanism) led increased oxygen affinity with a decrease in pH, an
to the Late Permian terrestrial extinctions (Huey and affinity likely to be adaptive in hypercapnic environ-
Ward, 2005) and adversely affected marine organisms as ments (e.g., Seibel and Fabry, 2003). Growth rates and
well (Wignall, 1992; Wignall and Hallam, 1992). Global
warming may have affected some Early Triassic marine Table 4
invertebrates (Wignall, 2001), but the increased atmo- Changes in calcification rate in various marine organisms due to
spheric CO2 has not been fully explored as a mechanism increased pCO2
for the prolonged biotic crisis in the marine realm. 2× pre-industrial 3× pre-industrial
In Modern times the atmospheric CO2 concentration
Organism pCO2 pCO2
has risen continuously since the Industrial Era, from 280 ±
Coccolithophores −9 to − 29 −18 to − 66
10 ppm to 380 ppm observed today, and it is projected to
Foraminifera −4 to − 8 −6 to −14
reach 540–970 ppm by the end of this century due to Scleractinian corals 0 to − 50 no data
anthropogenic input (Prentice et al., 2001). This addi- Coralline red algae −25 no data
tional atmospheric CO2 is diffusing into the oceans Numbers indicate approximate % change in rate of calcification at 2×-
creating H2CO3, decreasing pH and [CO32−], and therefore and 3×-pre-industrial pCO2 (280 ppm). Based on field and laboratory
also decreasing the CaCO3 saturation state of seawater studies; modified from Feely et al. (2004).
 M.L. Fraiser, D.J. Bottjer / Palaeogeography, Palaeoclimatology, Palaeoecology 252 (2007) 164–175 171

abundances of marine phytoplankton decrease progres- as is observed in Modern invertebrates; a similar

sively with lower pH (Yoo, 1991; Hinga, 2002). phenomenon of reduced shell size due to high
Experiments on Modern marine eukaryotic inverte- atmospheric CO2 levels is observed in Early Jurassic
brates indicate that the degree and rate of calcification megalodontoid bivalves (Hautmann, 2004). Early
among corals and coral reef communities (e.g., Kleypas Triassic bivalves also may have possessed a unique
et al., 1999; Leclercq et al., 2000), coccolithophores ability to secrete a shell in conditions of low CaCO3
(e.g., Riebesell et al., 2000), and foraminiferans (e.g., saturation, similar to the proliferation of Lithiotis facies
Barker and Elderfield, 2002) decrease as the CaCO3 bivalves during the Early Jurassic and to rudist bivalves
saturation state of seawater decreases (Table 4). during the Cretaceous when atmospheric CO2 levels
Calcareous skeletons weaken, dissolve, and become also were elevated (Fraser et al., 2004). Metazoan reef-
increasingly difficult to secrete in these surface-ocean builders (Flügel, 2002) and larger gastropods (Fraiser
conditions; the species composition and succession of and Bottjer, 2004) reappear when atmospheric CO2
coral communities and phytoplankton are likely to be levels decreased in the Middle Triassic. Bivalves and
altered if anthropogenic atmospheric CO2 continues to gastropods were competitive dominants during the Early
rise (Kleypas et al., 1999). Though the ocean is Triassic probably because they were the best-adapted
potentially a large sink for increasing amounts of skeletonized organisms for the conditions.
atmospheric anthropogenic CO2 (Sabine et al., 2004), Elevated atmospheric CO2 possibly also contributed
these effects on the shallow-marine calcareous biota to the end-Permian mass extinction in a top-down
have been detected and measured after modest changes manner. Benthic invertebrate species that formed
in seawater chemistry, even when the aragonite and massive carbonate skeletons, aragonite- and high-
calcite saturation indices of seawater are above 1.0 and magnesium calcite-secreting organisms, and all major
CaCO3 precipitation is favored (Feely et al., 2004). A groups of reef organisms suffered large losses during the
physiological and biocalcification crisis for Earth's end-Permian mass extinction (Flügel and Kiessling,
calcareous marine biota is being observed today because 2002; Knoll, 2003). Increased CO2 may have contrib-
of increases in anthropogenic atmospheric CO2. uted to other aspects of Early Triassic paleoecology as
Because even small changes in seawater pH and well, such as the small body size of many benthic and
CaCO3 saturation state affect the marine biota (e.g., nektonic invertebrate marine groups (Twitchett, 2005)
Raven et al., 2005), the elevated level of atmospheric and preservation style of calcareous marine invertebrate
CO2 during the latest Permian-Early Triassic likely had shells (Fraiser and Bottjer, 2005b).
detrimental effects on the physiology and biocalcifica- The end-Permian mass extinction and the prolonged
tion of Earth's shallow-marine biota. Based on clues biotic crisis were likely caused by a combination of
provided by the high numbers of bivalves and gastro- mechanisms, and we propose here that elevated
pods, we propose that elevated atmospheric CO2 was an atmospheric CO2 was an additional causal mechanism
important top-down mechanism in prolonging biotic for the biotic crisis from the top-down. The interplay of
crisis and delaying biotic recovery in shallow-marine perturbations to the global atmosphere and ocean
environments after the end-Permian mass extinction. triggered by CFBP volcanism and the breakup of
Bivalves and gastropods have rapid metabolisms that Pangea was complex and manifested in different ways in
likely enabled them to quickly transport acid–base various parts of the globe, as demonstrated by spatially
equivalent ions across cell membranes and to passively and temporally varied phenomena. For example, while
buffer intra- and extracellular fluids in conditions of evidence outlined here indicate that surface waters in
elevated environmental pCO2 (Seibel and Fabry, 2003). much of the world's oceans could have experienced a
The increased respiratory protein oxygen affinity that slight decrease in the CaCO3 saturation state during the
gastropods experience with a decrease in pH could have late Permian-Early Triassic, large seafloor carbonate
been another attribute beneficial in such ocean condi- precipitates (e.g., Woods et al., 1999; Baud et al., 2005;
tions (Seibel and Fabry, 2003). The protracted absence Woods et al., 2007-this volume), microbialites (e.g.,
of colonial metazoan reefs and reef organisms through- Pruss and Bottjer, 2004), and oolites (e.g., Assereto and
out the Early Triassic (Flügel and Stanley, 1984; Flügel, Rizzini, 1975; Groves and Calner, 2004) are present in
1994, 2002) perhaps can be attributed to a biocalcifica- many Lower Triassic sections. Lower Triassic carbonate
tion crisis caused by decreased CaCO3 saturation state in sediments may indicate that some parts of the world's
shallow seawater. The small size of adult gastropods oceans experienced CaCO3 supersaturation during some
during the Early Triassic may have been an adaptation intervals due to bacterial sulfate reduction in anoxic
for the increased energetic costs for carbonate secretion ocean water (e.g., Woods et al., 1999, 2007-this volume),
172 M.L. Fraiser, D.J. Bottjer / Palaeogeography, Palaeoclimatology, Palaeoecology 252 (2007) 164–175

and/or that perhaps a switch to inorganic and microbial history (Fraiser and Bottjer, 2004), and megalodontoid
precipitation occurred in some regions (Baud, 1998; bivalves reduced shell size during the Early Jurassic
Pruss et al., 2006). These changing regional and (Hautmann, 2004). In some sections marine carbonate
temporal patterns could be related to a highly stratified production was also temporarily suppressed after the end-
ocean that was subject to varying patterns of incursion of Triassic mass extinction, and the preservation of shells
deep water into shallow environments and sea-level changed from body fossils to molds (Ward et al., 2001;
fluctuations related to impingement of superplumes and Hautmann, 2004). Nannoplankton exhibited a decrease in
CFBP volcanism (Hallam and Wignall, 1999), for which size, absolute abundance, and calcification during the
the precise relationships still must be deciphered. The early Toarcian (Mattioli et al., 2004). Elevated atmo-
specific influence of some of the various mechanisms for spheric CO2 is also hypothesized to have caused
the Permian–Triassic biotic crisis may be discerned, extinction and dissolution of calcareous benthic micro-
such as the effects of global warming evidenced by organisms during the Paleocene–Eocene Thermal Max-
migration of warm-water invertebrates to high latitudes, imum (e.g., Zachos et al., 2005).
the loss of high latitude floras, and development of low-
latitude paleosols at high latitudes (see references in 5. Conclusions
Wignall, 2001; Kiehl and Shields, 2005). However, the
particular effects of individual mechanisms may never be The kill mechanisms for the end-Permian mass
discerned or separated-out from each other because the extinction were likely from the bottom-up; however,
mechanisms are interconnected and likely caused a we present evidence that elevated atmospheric CO2 was
cascade of effects. Furthermore, it was likely that the perhaps a more important mechanism for sustained
combination of top-down and bottom-up mechanisms ecological degradation in Early Triassic shallow-marine
could be responsible for the prolonged biotic crisis and environments. Elevated atmospheric CO2 is a top-down
the observed paleoecological patterns. More quantitative environmental stress hypothesized to have affected
Early Triassic paleoecological data and comparisons to Earth's marine biota during other times in Earth's
Modern experimental and field studies may demonstrate history whose potentially wide-ranging effects during
the particular roles of these top-down and bottom-up the Permian–Triassic should be investigated further. We
mechanisms. must understand and remember the Earth's past as
Elevated atmospheric CO2 has been proposed as a we anticipate its future, and studies of the duration and
mechanism from the top-down for other biotic crises in scope of the biotic effects resulting from elevated
Earth's history, and thus it is not far-fetched to propose atmospheric CO2 will help us predict the future of the
that it played some role in the prolonged Early Triassic Earth's marine biota if the input of anthropogenic
biotic crisis. During the last 300 million years, some of the atmospheric CO2 continues.
highest atmospheric CO2 levels have been recorded
during the early and middle Mesozoic (McElwain et al., Acknowledgements
1999; Berner and Kothavala, 2001; Retallack, 2001;
Beerling and Berner, 2002; Rothman, 2002) (Fig. 3), and Support was provided by The Paleontological Society
they have been hypothesized to have had a key role in and the USC Department of Earth Sciences to MLF, and
extinction at the Triassic/Jurassic boundary and during the by the USC Women in Science and Engineering (WISE)
early Toarcian (e.g., Hautmann, 2004; Mattioli et al., Program to DJB. We thank T. Algeo, P.Wignall, and an
2004; Huynh and Poulsen, 2005). Metabolically slow anonymous reviewer for comments on earlier versions of
organisms (rhynchonelliform brachiopods and bryozo- this manuscript.
ans) experienced large extinctions during the end-Triassic
and early Toarcian extinctions (Taylor and Larwood, References
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