Relation of Phanerozoic stable isotope excursions to
climate, bacterial metabolism, and major extinctions
Steven M. Stanley1
Department of Geology and Geophysics, University of Hawaii, Honolulu, HI 96822
Contributed by Steven M. Stanley, September 10, 2010 (sent for review June 2, 2010)
Conspicuous global stable carbon isotope excursions that are
recorded in marine sedimentary rocks of Phanerozoic age and were
associated with major extinctions have generally paralleled global
stable oxygen isotope excursions. All of these phenomena are
therefore likely to share a common origin through global climate
change. Exceptional patterns for carbon isotope excursions resulted
from massive carbon burial during warm intervals of widespread
marine anoxic conditions. The many carbon isotope excursions
that parallel those for oxygen isotopes can to a large degree be
accounted for by the Q10 pattern of respiration for bacteria: As
temperature changed along continental margins, where ∼90% of
marine carbon burial occurs today, rates of remineralization of
isotopically light carbon must have changed exponentially. This
would have reduced organic carbon burial during global warming
and increased it during global cooling. Also contributing to the δ13 C
excursions have been release and uptake of methane by clathrates,
the positive correlation between temperature and degree of
fractionation of carbon isotopes by phytoplankton at temperatures
below ∼15°, and increased phytoplankton productivity during “ice-
house” conditions. The Q10 pattern for bacteria and climate-related
changes in clathrate volume represent positive feedbacks for
climate change.
paleoclimatology ∣ paleoceanography
M any possible explanations have been advanced for one or
more of the abrupt excursions in the δ13 C of marine carbo-
nates and organic matter that have been documented in the
geologic record (see Fig. 1). Most of these hypotheses have
focused on factors that change the global rate of burial of organic
carbon, which is isotopically light: changes in upwelling and
primary productivity; fluctuations of sea level; changes in ocean
dynamics, including ones affecting the extent of anoxic condi-
tions; changes in carbonate weathering rates; release of methane
from sediments; changes in nutrient input from the land to the
oceans; volcanic degassing; and release of isotopically light CO2
from the deep sea (for literature, see SI Text, Section I). Given the
strong positive correlation between δ13 C and δ18 O excursions in
shallow marine sediments (Fig. 1), however, parsimony suggests
that one or more unifying explanations should be sought to
explain all of these phenomena.
Missing from previous explanations for geologically brief δ13 C
excursions has been a consideration of the role of microbial
processes, even though microbes have an enormous global
biomass and play a prominent role in the exogenic carbon cycle.
Particulate organic matter in ecosystems has three possible fates:
It can be consumed by primary consumers, decomposed by bac-
teria (or fungi, in the case of lignocellulose), or buried. The
relative importance of these fates varies from place to place
and time to time. For example, carbon burial on land increased
markedly during the late Paleozoic, when coal swamps became
widespread (1). In the oceanic realm beyond continental rises,
organic carbon burial plays a minor role in the global carbon
cycle. Owing to consumption by primary consumers and mi-
crobes, less than 1% of particulate organic matter in the upper
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oceanic realm ends up being buried on the deep seafloor (2). In
contrast, continental shelves, slopes, and rises account for ∼90%
www.pnas.org/cgi/doi/10.1073/pnas.1012833107
of global carbon burial in the ocean (3). In these regions, elevated
nutrient levels produce high rates of primary productivity; rivers
and marshes supply large amounts of organic detritus; and high
rates of sedimentation result in the burial and preservation of
∼75% of the organic carbon reaching the seafloor, about half
of this amount being buried in deltaic depositional systems (4).
Temperature has a profound effect on the role of decomposers,
as indicated by the effective fungal destruction of plant debris in
tropical rainforests, which results in very thin, humus-poor soils.
The Arrhenius pattern for chemical reactions, an exponential
increase in rate with temperature, yields a Q10 value: the frac-
tional increase in the rate of a reaction per 10 °C of temperature
elevation (Fig. 2). Bacteria and fungi adhere approximately to
the Q10 pattern because of the effect of temperature on enzymes
utilized in their metabolic processes. For marine and freshwater
sediments above very low temperatures, the average Q10 for re-
spiration is ∼2.2 (Fig. 2) (5). This relationship has been incorpo-
rated into models of the carbon cycle on long time scales (6) but
has not previously been invoked to explain the δ13 C excursions of
Fig. 1, which occurred on short time scales (generally <106 y) and
are distinct from long-term secular isotopic trends (2).
It is true that growth rates of phytoplankton also increase with
temperature, but the net primary productivity of marine phyto-
plankton nonetheless decreases with global warming, which
results in decreased turbulent mixing and upwelling of ocean
waters. With warming, the reduced supply of nutrients exerts a
much stronger negative influence on the productivity of phyto-
plankton than the positive effect of the Q10 relationship (7).
In this paper, I investigate the causes of abrupt δ13 C excursions
that occurred in association with major extinctions. I attribute
these excursions to four factors: first, and perhaps most impor-
tantly, changes in global respiration rates of remineralizing
marine bacteria; second, release or uptake of methane by clath-
rates; third, the positive correlation between carbon isotope frac-
tionation by marine phytoplankton and temperature at relatively
low temperatures; and fourth, changes in the productivity of
phytoplankton and hence in the burial rate of organic carbon,
with changes in global temperature that alter wind stress and
rates of nutrient supply.
Results
A compilation of conspicuous isotopic excursions associated with
major extinctions reveals a close correspondence between δ13 C
and δ18 O excursions throughout Phanerozoic time. Fig. 1 displays
18 plots of δ13 C for carbonates and organic matter in shallow
GEOLOGY
marine stratigraphic sections. These exhibit a total of 26 δ13 C
excursions, each associated with a major extinction. Of these 26,
19 are known to have been accompanied by a δ18 O excursion, and
in every case the paired excursions have both been either positive
or negative. It is common knowledge that δ18 O excursions reflect
Author contributions: S.M.S. designed research, performed research, analyzed data, and
EVOLUTION
wrote the paper.
The author declares no conflict of interest.
1
E-mail: stevenst@hawaii.edu.
This article contains supporting information online at www.pnas.org/lookup/suppl/
doi:10.1073/pnas.1012833107/-/DCSupplemental.
PNAS ∣ November 9, 2010 ∣ vol. 107 ∣ no. 45 ∣ 19185–19189
 Age (Myr)

Neogene
A 33 B
Ma Eoc.
57.2
Ma C D

Paleog.
Oligoc. Olig. M. Trias.
A 34
13
δ C δ O
18
Eoc. Ma
50 Paleoc. 57.4
Paleoc. B Eoc. Ma Jur. E. Trias.
18
δ O
13
δ C 13
δ C δ O
18
13
δ C
Late Trias.

Cretaceous
0 1 20 1 2 -1 0 1 2 -2 -1 0
1 2 3 4 5 -2 -1 0 1 2
100 -1 0 1 2 3 4 7 8
Trias.
δ C
13 Yabeina Loping.
Early Eδ 13
C Perm.δ
18
O
zone
Guad.
Neoschw.
-2 -1 0 1 2 3 4 -7 -6 -5 -4 -3 -2 -1 zone G
150 Late F Early
Jurassic

Serp. Guad. 18
δ O
13
Middle δ C
13
H δ C Visean 18
δ O 3 4 5 6 7 -3 -2 -1 0 1 2 3 4 5 -7 -6 -5 -4 -3
Early
Mississippian
200 C
Tournais.
I
Triassic

Late Famennian
0 1 2 3 4 5 6 19 20 21 22 23 δ C
13 18
δ O
Middle Famenn.
250
Early D E
Late 1 2 3 4 5 6 7 -8 -7 -6 -5 -4 -3 -2 -1 0
Permian

Middle
G F 13
Frasn. K δ C Devon.
18
δ O
18
Early
δ C
13 δ O
300 J Silur.
Penn. Givet. -3 -2 -1 0 1 2 3 4 -10 -9 -8 -7 -6 -5 -4
H 0 1 2 3 -6 -5 -4 -3
Wenl.
Miss. M
350
I L δ C
13 18
δ O Llandov.
18
δ O
13
Ludlow δ C
Late J
Devonian

Wenlock
-1 0 1 2 3 4 5 6 -6 -5 -4 -3 -2 -1
Middle 0 1 2 3 4 5 6 7 -6 -5 -4 -3 -2
400 Silurian
Early sedgwickii
Mohawk
Late L
K 13
δ C
zone O Ordovician
? Chazyan
Cambrian Ordovician Silur.

Middle M 18
P 13
δ C
δ O
13
Early N N convolutus
zone δ C
O
450 Late P -31-30-29-28-27 0 1 2 3 4 5 6 -5 -4 -3 -2 -1 0 -3 -2 -1 0 1 2 3 4
Middle Sunwapt. Marj.
Early Delam.
Stept. Stept.
Q 13 18
δ O
500 Late
13
Marj. Rδ C
Middle
R
Marj. δ C Q
18
δ O
E. Cam.
Early -10 -9 -8 -7 -6
-3 -2 -1 0 1 2 3 4 5 -3 -2 -1 0 1 2 -11-10 -9 -8 -7 -6 -5 -4

Fig. 1. Stable isotope excursions that have been documented in shallow marine strata and are associated with mass extinctions. Eighteen intervals (A–R) contain
a total of 26 such δ13 C excursions. Corresponding to these, and trending in the same direction, are 19 published δ18 O excursions, which are displayed in the
plots to the right of those depicting δ13 C. Temporal positions of excursions are indicated by encircled letters on the left. Blue indicates association with
global cooling and red with global warming; black indicates the absence of published evidence of associated climate change. Horizontal scales represent
magnitudes of δ13 C and δ18 O excursions in parts per thousand. Light δ13 C in N is for organic carbon rather than carbonates, and heavy δ18 O in H is for conodonts
rather than bulk or skeletal carbonate. Ordinates represent stratigraphic positions of samples and are neither precisely linear with respect to time nor scaled
the same for all graphs. (See SI Text, Section II for sources of figures and for citations of literature on isotope excursions, climate change, and major extinctions.)

global temperature changes and sometimes expansion or contrac- It is inevitable that changes in mean global temperature will
tion of glaciers, which preferentially accumulate 16 O. Among the alter the δ13 C of seawater via the Q10 relationship for microbes.
global extinctions associated with the 26 δ13 C excursions depicted Although the total rate of net primary productivity and total rate
in Fig. 1 are four of the five most severe Phanerozoic mass of respiration in the ocean are similar (2), an increase in the rate
extinctions: those of the Late Ordovician, Late Devonian, Late of bacterial respiration would reduce but not eliminate carbon
Permian, and Late Triassic. Of the 17 positive δ13 C excursions of burial along continental margins, where ∼75% of organic carbon
Fig. 1, 16 have been identified as being associated with climate reaching the seafloor is buried today. The flux of remineralized
change and, in every case, the change entailed global cooling. In carbon from modern continental shelf/margin sediments is 3.72 ×
complementary fashion, all six of the nine negative excursions 1014 g∕y (6). The amount of dissolved inorganic carbon in the
for which there is evidence of simultaneous climatic change were modern ocean is larger by a factor of almost exactly 105 ð3.74×
associated with global warming. The implication is that climate 1019 gÞ (9). A temperature increase of 5° would elevate the
changes have been connected to carbon and oxygen excursions flux of remineralized carbon by ∼40% (Fig. 2). For marine
and, as indicated by a variety of other evidence (8), have also organic carbon remineralized in shelf/slope sediments, δ13 C
played an important role in major extinctions. Excluded from is ∼ − 23‰, which is slightly more negative than that for marine
Fig. 1 are exceptional positive δ13 C excursions during three Me- organic matter because of an admixture of isotopically light
sozoic intervals of global warming when massive amounts of or- carbon derived from terrestrial organic detritus (10). It would
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ganic carbon were buried under widespread anoxic conditions in be difficult to estimate the time that would be required for a
the ocean. I will discuss these episodes in the Discussion section. 40% increase in the rate of remineralization along continental

19186 ∣ www.pnas.org/cgi/doi/10.1073/pnas.1012833107 Stanley

 0.4
Respiration rate (mg O-1 L-1 day-1)
0.35
0.3
Community
respiration rate
0.25 (Q10 = 2.2)
0.2 40%
0.15
Specific
0.1 growth
rate
0.5
0 0
5 10 15 20 25
Temperature (°C)
Fig. 2. Relationship to temperature of respiration rate and specific growth
rate (fractional increase in cell mass per unit time) for freshwater and marine
benthic bacteria (data from ref. 5). An increase in mean temperature from
15–20 ºC results in an increase in respiration rate of ∼40% (stippled area).
margins to shift δ13 C for dissolved inorganic carbon in the ocean
from its present value of ∼ − 2‰ to −6‰ (a 4‰ excursion,
which is a typical magnitude for the excursions illustrated in
Fig. 1). The complicating factor is that, although less isotopically
light carbon would be buried, a negative feedback would be trig-
gered: Dissolved inorganic carbon would become progressively
isotopically lighter, and so would the carbon of phytoplankton
and, therefore, of buried carbon. Also, to the degree that warm-
ing or cooling of the climate has been protracted, δ13 C excursions
will also have been protracted. In fact, this pattern is evident in
Fig. 1, where gradual shifts of δ18 O are paralleled by gradual
shifts of δ13 C.
The bacterial mechanism I am proposing is also consistent with
the observation that many carbon isotope excursions, such as
those of the Late Ludlow (Fig. 1L) (11) and Late Permian
(Fig. 1E) (12), began at about the time of the associated major
extinction, when a global climate shift occurred, and peaked
slightly later. The high-resolution record for the Eocene/
Oligocene transition shows the associated δ13 C excursion to have
begun slightly (<10;000 y) after the associated δ18 O excursion
(13). These patterns are understandable, given the exponential
response of respiration rate to temperature change (Fig. 2).
Changes in global rates of bacterial respiration at times of
CO2 -induced climate change have represented positive feedbacks
because changes in bacterial respiration rates as a function of
temperature are accompanied by little change in the fraction
of acquired carbon that is respired (14). Every rapid global shift
of δ13 C for shallow marine sediments has been reversed at some
point, however, either by one or more negative feedbacks, such
as a change in terrestrial weathering rates, or by a reversal of
whatever factor or factors produced the initial climate change.
In fact, many intervals of glacial expansion and contraction have
been quite brief. For example, the Late Ordovician Hirnantian
interval and its δ13 C and δ18 O excursions were confined to just
0.5–1 Myr (15).
Three additional factors have presumably also contributed
to the δ13 C excursions associated with climate change. The co-oc-
currence of positive global δ13 C and δ18 O excursions is compati-
ble with the possibility that sequestration or release of methane
hydrates in marine and terrestrial settings has been partly respon-
sible for the δ13 C excursions (16). However, quantitative evalua-
tions have concluded that release of methane hydrates from the
seafloor cannot fully account for the Paleocene/Eocene (17) or
terminal Permian (18) negative δ13 C excursions; one or more po-
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sitive feedbacks are required. The response of bacterial respira-
tion to climatic warming would have been one such feedback.
Stanley
2.0 -10
1.8
Specific growth rate (day-1)
1.6 -15
1.4
-20
1.2
1.0
13
0.8 δ C -25
(0/00)
0.6
0.4 -30
0.2
-35
30
-40
-4 0 4 8 12 16 20 24 28 32
Temperature (°C)
Fig. 3. Positive correlation between temperature and δ13 C of marine
particulate organic matter, including phytoplankton cells, for temperatures
below ∼15 °C (after ref. 19).
Another, secondary factor contributing to the δ13 C excursions
of Fig. 1 would have been the positive correlation between tem-
perature and the δ13 C of phytoplankton and particulate organic
carbon for temperatures below ∼15 °C (Fig. 3) (19). During
“greenhouse” intervals of the past, seawater temperatures were
above 15 °C throughout the photic zone, except at relatively high
latitudes. The degree to which this condition would have elevated
the global average δ13 C of buried organic carbon above its level
during icehouse times is difficult to quantify, but temperature
changes equatorward of high-latitude regions would have had
no effect.
A third, secondary factor contributing to the δ13 C excursions
would have been the strong turbulent mixing and upwelling that
characterize icehouse oceans, which elevate the supply of nutri-
ents and therefore enhance phytoplankton productivity (7) and
burial of isotopically light carbon.
Discussion
Not all carbon isotope excursions of Fig. 1 have configurations
closely resembling those of the associated oxygen isotope excur-
sions, presumably because of second-order regional and global
influences. Relative magnitudes of excursions are difficult to
interpret. It is puzzling, for example, that the terminal Eocene
excursions were small despite having been associated with sub-
stantial global cooling.
During three Mesozoic intervals of global warming when
vertical mixing of the ocean weakened and anoxia became wide-
spread, black muds were deposited over broad areas. At each of
these times, massive burial of isotopically light carbon overrode
the reduction of carbon burial via increased bacterial reminera-
lization in areas that were better oxygenated. The result was
a positive excursion for δ13 C. At the end of the Cenomanian,
for example, a positive global δ13 C excursion coincided with a
GEOLOGY
negative global δ18 O excursion (20). Thus, a pulse of global
warming quickly reduced vertical mixing of the ocean to provide
widespread anoxia. A different pattern, however, is observed
throughout the world for oceanic changes in the mid-Toarcian
and late early Aptian (21). At the latter time, a sudden negative
δ13 C excursion of ∼2‰ coincided with a negative δ18 O excursion
of ∼3‰, in keeping with the standard pattern for global warming
EVOLUTION
(Fig. 1). Only after the widespread burial of organic-rich
sediment began was there a strong positive shift of δ13 C (Fig. 4).
Similarly, a 4–7‰ negative shift in mid-Toarcian time was
followed by a positive shift after deposition of dark mud began;
Hesselbo et al. (21) interpreted the negative excursion as a result
PNAS ∣ November 9, 2010 ∣ vol. 107 ∣ no. 45 ∣ 19187

Late
OAE
Aptian
Early
Black shale
Marly limestone 0 1 2 3 4 -3 -2 -1 0 1
and marlstone 13
δ C (0/00)
18
δ O (0/00)
Limestone
Fig. 4. Excursions of δ13 C and δ18 O near the end of the early Aptian recorded
in strata of northwestern Sicily and displaying a global pattern: Both isotopic
ratios shifted in a negative direction when global warming began (lower
arrow), but the δ13 C trend was reversed when anoxic conditions produced
widespread burial of organic carbon (upper arrow) (after ref. 31). OAE, ocea-
nic anoxic event.
of massive dissociation of gas hydrate, but elevated bacterial
remineralization via climate warming may largely account for it.
A sudden negative δ13 C excursion following the terminal
Cretaceous mass extinction, which, perhaps uniquely, was caused
by an extraterrestrial impact, was unrelated to factors discussed
in the present paper, having resulted from a brief annihilation
of marine phytoplankton populations that resulted in a drastic
reduction of organic carbon burial (22).
During the Pleistocene, global δ13 C did not follow the tem-
perature-related pattern of earlier intervals discussed herein: It
declined slightly during glacial maxima and rose slightly during
glacial minima; the mean value for the ocean was 0.32‰ more
negative than today during the most recent glacial maximum (23).
One contributing factor must have been the transfer to the ocean
of a large amount of isotopically light terrestrial organic carbon
during the shrinkage of forests (24), which contracted to about
35% of their present global area during the last glacial maximum
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(25). It is also possible that increased burial of organic material
along continental margins during eustatic sea level rises reduced
½PO4
in the ocean, and hence phytoplankton productivity and
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have significantly reduced the δ13 C of seawater.
Of the four consequences of global climate change identified
here, which in some combination can account for the δ13 C excur-
sions depicted in Fig. 1, three must be of concern with regard
to future global warming: increased respiration by bacteria along
continental margins, release of methane by clathrates, and
reduced assimilation of CO2 by phytoplankton. All of these
processes represent significant feedbacks that will enhance
global warming that results from human-induced increases in
the partial pressure of atmospheric CO2 .
Methods
The δ13 C excursions depicted in Fig. 1 are the set of excursions associated
with major extinctions that were encountered in a literature survey. Where
multiple plots were encountered depicting a particular excursion, one was
selected for Fig. 1. The remainder are cited in SI Text, Section II.
ACKNOWLEDGMENTS. I thank Robert A. Berner, A. Hope Jahren,
Fred T. Mackenzie, Isabel Montañez, and Neil Tabor for their critical
reading of my manuscript and Jennifer Engels for her clerical assistance.
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Stanley PNAS ∣ November 9, 2010 ∣ vol. 107 ∣ no. 45 ∣ 19189