1
SUPPLEMENTARY INFORMATION
Supplementary Information:
DOI: 10.1038/NGEO1390
Enhanced weathering by the first land plants caused Late
First
plants
cooled
the Ordovician
Ordovician
global
change
Short title: First plants cooled the planet
Timothy M. Lenton1,2, Michael Crouch2,3, Martin Johnson2, Nuno Pires3,4, Liam Dolan3,4
1
College of Life and Environmental Sciences, University of Exeter, Exeter, EX4 4PS, UK.
2
Earth and Life Systems Alliance, School of Environmental Sciences, University of East
Anglia, Norwich, NR4 7TJ, UK. 3Earth and Life Systems Alliance, Department of Cell and
Developmental Biology, John Innes Centre, Norwich, NR4 7UH, UK. 4Department of Plant
Sciences, University of Oxford, South Parks Road, Oxford, OX1 3RB, UK.
Supplementary Figures
Supplementary Figure 1. Microcosms. Moss growing on granite develops extensive
protonema, gametophores and associated rhizoids: (a) microcosm with moss, (b)
control microcosm.
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2
(a)
(b)
(c)
Supplementary Figure 2. Sensitivity of CO2 results to varying initial conditions by
different means: (a) varying degassing, D, (b) varying uplift, U, (c) varying pre-plant
weathering rate, k15. Dotted lines show solutions with no biological forcing applied.
Solid lines show solutions with biological forcing of silicate and phosphorus
weathering applied.
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3
(a)
(b)
(c)
Supplementary Figure 3. Sensitivity of CO2 results to varying biological forcings: (a)
varying coverage of the land surface achieved by the first non-vascular plants, E, (b)
varying enhancement of silicate weathering achieved by the first non-vascular plants,
W, (c) varying effect on phosphorus weathering, F, of first non-vascular and then first
vascular plants. Dotted line is baseline in the absence of biological forcing. Dashed
lines are for enhancement of silicate weathering only. Solid lines are for
enhancement of silicate and phosphorus weathering.
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4
(a)
(b)
(c)
Supplementary Figure 4. Sensitivity of temperature results to varying the timing of
land colonisation: (a) early start colonisation 490-460 Ma, (b) late finish colonisation
475-445 Ma, (c) fast colonisation 463-458 Ma. Dotted line is baseline in the absence
of biological forcing. Dashed line is enhancement of silicate weathering only. Solid
lines is enhancement of silicate and phosphorus weathering.
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5
Supplementary Figure 5. P. patens exudes organic acids. Malic, citric, glyceric and
succinic acids were identified by GC-MS analysis of exudates from P. patens. Each
panel consists of a chromatogram (below) and m/z spectra (above). There are two
traces on each chromatogram; one trace represents the moss exudate sample (blue)
and the other represents a mock control (black). Above each chromatogram is a pair
of m/z spectra. The upper m/z spectrum corresponds to the blue peak in the
associated chromatogram and the lower spectrum corresponds to an organic acid
standard. In the case of succinic acid, m/z spectra are also shown for the mock
control.
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6
Supplementary Methods
Experiments
Moss preparation and growth conditions. Moss was grown in standard conditions on Petri
dishes1. Moss protonema were grown on Knops media for 5 days and collected when
protonema had covered the surface of the Petri dish, in 5 ml sterile ultrapure H2O. Moss was
then homogenized and washed in 4 further changes of sterile ultrapure H2O. The
homogenized moss was re-suspended in sterile ultrapure distilled H2O to a final volume of 19
ml. 3 ml was used as inoculum for each microcosm. This was either used directly for
inoculation of “moss-containing microcosms”, or filtered using a 0.2 µm filter and the filtrate
used for inoculation of “control microcosms”. Microcosms contained either granite or
andesite that was washed four times with ultrapure H2O and then heat sterilised in a 180 °C
oven for a period of between 16 hours and 24 hours. Rock material was added to screw top
jars to a depth of ~6.5 mm. Inoculated microcosms were incubated at 25 ºC with 16 hours
light 8 hours darkness photoperiod under 100 µmol m-2 s-1 white light for ~130 days in
ambient atmosphere. Moss was removed from the microcosms after ~130 days using forceps
and placed on filter paper to dry for 48 hours and weighed. Liquid from each microcosm was
collected and stored <4 °C prior to analysis.
Analysis. To analyse elemental content in moss material 10 ml of 30% HNO3 and 30% H2O2
was added to dried moss from each microcosm and heated to 70 °C for 30 minutes with
intermittent shaking. This was then filtered using a 0.2 µm filter and the filtrate used for
analysis. To measure the elements present in the bathing solutions in the microcosms
(“control” and “moss-containing”), 10 ml ultrapure H2O was added to each microcosm and
shaken for 30 minutes. Then 10 ml sample was taken and filtered using a 0.2 µm filter and
HCl added to 10% final volume. Abundance of elements was measured by Inductively
Coupled Plasma, Atomic Emission Spectrometry (ICP-AES) (Varian Inc., Palo Alto,
California, USA). Phosphorus content was determined from microcosm liquid samples by
using a Skalar Sanplus System Nutrient Auto Analyser (Skalar Analytical B.V., Breda, The
Netherlands). Phosphorus weathering was estimated as follows: The mean moss biomass was
16.5 ± 8.5 mg for the granite microcosm experiments in which phosphorus was measured
(control n = 33; moss n = 31). Review of the literature (e.g. ref 2) indicates that phosphorus
typically constitutes ~0.1 % of dead moss biomass. Hence an estimated ~0.53 ± 0.28 µmol is
weathered into the moss on average, compared to 0.06 ± 0.03 µmol in biotic microcosm
water, and 0.01 ± 0.01 µmol in the controls. This gives a total phosphorus weathering
enhancement of 0.58/0.01 = 58.
Detection of organic acids. Organic acids were detected using gas-chromatography mass
spectrometry (GC-MS). For this analysis, 6 week-old P. patens plants with well developed
protonema and gametophores were incubated in water; mock treatment consisted of water
only. The incubation solutions were collected after 4 days, supplemented with 1 µg of ribitol
as an internal quantitative standard, evaporated in a speedvac and stored at -80°C. Sample
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7
derivatization and GC-MS analysis was performed following the protocol described by Lisec
et al.3. GC-MS analysis was performed with a Varian EZ-Guard CP0913 column and an
Agilent 5975C MSD. Chromatograms and mass spectra were evaluated using the Enhanced
MSD ChemStation D.01.02 software (Agilent Technologies) and the NIST Mass Spectral
Search Program version 2.0 (National Institute of Standard and Technology, USA). Mass
spectra of eluting acids were identified using mass spectra libraries and by comparison with
pure standards of malic, citric, glyceric and succinic acids.
Modelling
COPSE model. The Carbon Oxygen Phosphorus Sulphur Evolution (COPSE) model is
described in full in ref 4. We made the following changes to the structure of the baseline
model: (a) Atmospheric CO2 was made proportional to the square of the total amount of
carbon in the ocean and atmosphere following ref 5. This makes no difference to steady state
CO2 predictions, but the total amount of carbon in the Paleozoic ocean and atmosphere is
much reduced, allowing greater transient variations in CO2 (e.g. in response to peaks of
organic carbon burial). (b) The nitrogen cycle was removed and new production made
proportional to phosphate concentration (without altering their initial values). This makes no
difference to the predictions (as phosphate concentration was determining nitrate
concentration and new production anyway), but it allows a much longer time step of 10,000
years to be used. (c) Selective phosphorus weathering forcing (F) was introduced as a
normalised parameter multiplying the phosphorus weathering flux (equation 25 of ref. 4).
Forcing scenarios. We used three different runs, in which we altered the forcing of the
model, to isolate the effects of early plants (all forcings are normalised to 1 at the present
day): (1) Geological forcings were held constant at Ordovician values of; degassing, D = 1.5
(enhanced volcanic activity) and uplift, U = 1.0 (Taconic orogeny). The original biological
forcings and changing solar luminosity were retained. (2) Biological forcings of silicate (and
carbonate) weathering were altered to capture the effects of non-vascular plants; evolution
and colonisation, E = 0 up to 475 Ma then linear rise to E = 0.15 at 460 Ma, constant
thereafter; enhancement of weathering, W = 0 up to 475 Ma then linear rise to W = 0.75 at
460 Ma, constant thereafter. (3) Additional forcing of phosphorus weathering was introduced
to capture the transient effects of non-vascular plants and the first vascular plants; F = 1 until
460 Ma, linear rise to F = 2 at 458 Ma, linear decline to F = 1 at 456 Ma, constant until 447
Ma, linear rise to F = 3 at 445 Ma, linear decline to F = 1 at 443 Ma, constant thereafter.
To examine the sensitivity of our results to uncertain initial conditions and parameter choices,
we performed a thorough model sensitivity analysis.
Sensitivity to initial conditions. Uncertain initial conditions are the background
concentration of atmospheric CO2 (in PAL), and the corresponding global mean temperature,
in the absence of the first non-vascular plants. These are determined internally by the model
as a function of its structure, parameter choices, and the constraint of matching present values
under present boundary conditions. Available proxy constraints on atmospheric CO2 during
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8
the Ordovician are summarised in Figure 1 of the main paper; 14-22 PAL at ~460 Ma (the
start of the Late Ordovician), 7.5-14 PAL at ~453 Ma, and 14-18 PAL at ~440 Ma. With the
default parameter settings, CO2 = 15.8 PAL at 460 Ma, i.e. at the lower end of the range.
Initial CO2 is sensitive to the assumed geological forcing factors; degassing D, and uplift U.
The default values of these (D = 1.5, U = 1.0) were based on the relevant interval of existing
Phanerozoic forcing scenarios4, simplified to fixed values to isolate the effects of colonisation
by non-vascular plants. In the original forcing scenarios (upon which the chosen values are
based), during the interval 480-440 Ma degassing D rises from 1.50 to 1.57 and uplift U
drops from 1.08 to 0.84. However, we judged that the inferred drop in uplift, U, based on a
significant drop in the 87Sr/86Sr composition of seawater in the Mid to Late Ordovician, is
flawed. This drop in seawater 87Sr/86Sr is now thought to be due to extensive weathering of
basalt with low 87Sr/86Sr composition6, at a time of significant ongoing uplift associated with
the Taconic orogeny.
For the sensitivity analysis we varied the fixed values of both D and U over a factor of 1.5,
centred on the default values, hence we varied D over 1.2–1.8, and U over 1.2–0.8. For
comparison, over the whole of Phanerozoic time, the estimated range4 in D is 0.98-1.73, and
in U is 0.53-1.17. The resulting ranges in CO2 at 460 Ma are 13.5-17.9 PAL for varying D
and 13.9–18.4 PAL for varying U. These span the lower end of the range from the one proxy
estimate at 460 Ma. We find that a value of CO2 ~22 PAL cannot be produced simply by
varying the geological forcing factors within reasonable bounds.
Initial CO2 is also sensitive to the assumed pre-plant weathering rate, determined by the
parameter k15 (= 0.15 by default), where 1/k15 (~7 by default) is the amplification of
weathering by today’s land plants relative to abiotic levels. The value of k15 is more uncertain
than that of U or D, so we vary it by a factor of 2, over k15 = 0.1–0.2 (corresponding to a
factor of 5–10 amplification), which gives CO2 = 12.7–21.1 PAL at 460 Ma. This roughly
corresponds to the range of the one proxy estimate at ~460 Ma.
The effect on the results when altering the initial conditions as outlined here, and then
applying the default forcing scenarios, is shown in Supplementary Figure 2 and summarised
in Supplementary Table 1.
Sensitivity to biological forcing factors. Key uncertain parameters determining the forcing
scenarios are: (1) The percentage coverage of the land surface achieved by the first nonvascular plants (relative to present coverage) – determined by model parameter E. (2) The
enhancement of silicate weathering achieved by the first non-vascular plants – determined by
model parameter W. (3) The additional forcing of phosphorus weathering – determined by
model parameter F.
The parameter E (= 0.15 by default) is uncertain because we do not know whether the first
non-vascular plants were restricted to permanently wet habitats (wetlands) or whether they
could flourish in seasonally wet habitats. Furthermore, the extent of these habitats in the MidLate Ordovician is uncertain. We identified the locations of early fossil cryptospore
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9
occurrences on the relevant paleoclimate reconstructions of Christopher R. Scotese
(http://www.scotese.com). The first cryptospores7 ~472 Ma appear on the eastern margin of
Gondwana (Argentina today) in a then arid climate belt. Some of the next cryptospore
occurrences8 ~463 Ma are from the western margin of Gondwana (Saudi Arabia today) in a
then warm temperate climate belt. Whilst the cryptospores had to have been washed into
freshwaters to have been preserved, they are not obviously located in what were then the
wettest climate belts. Furthermore, early miospore occurrences are of a similar composition
throughout the world and the plants that produced them “are interpreted as being able to
survive in a wide range of climates”9. Hence as an upper limit we use E = 0.45, implying
widespread colonisation of only seasonally wet areas. As a lower limit we use E = 0.05
corresponding to restriction of the first non-vascular plants to wetlands, based on these
comprising ~5% of today’s vegetated land surface. This range spans a factor of 3 in either
direction, or nearly an order of magnitude in total.
The parameter W (= 0.75 by default) is based on the results of our experiments, which show
that a non-vascular plant can cause comparable weathering amplification to vascular plants.
We use W = 1.0 as an upper limit as it implies equivalent amplification of weathering as
today’s vascular plants (factor of 6.7), where present. For the lower limit, we use W = 0.1,
which is equivalent to a factor of ~1.6 amplification of weathering where present, close to the
experimental values obtained for weathering of Ca and Mg from granite. The range in W
spans an order of magnitude. The global amplification factor for silicate weathering is
determined jointly by E and W, which are multiplied together and by (1 – k15) within an
overall silicate weathering function4. E = 0.15 and W = 0.1 implies only a factor of 1.085
global amplification of weathering (8.5% increase), whereas E = 0.15 and W = 1.0 implies a
factor 1.85 global amplification (85% increase).
The parameter F is highly uncertain, and our experimental results of a ~60 fold increase in
phosphorus weathering could allow for much higher values than used. Hence we took the
approach followed in previous work4, of attempting to reproduce the observed carbon isotope
excursions (GICE and HICE), and then examining their effects on CO2 and temperature.
However, there is uncertainty in the magnitude of the GICE and HICE, and to capture that
here we consider a range in peak values of F of 1.5–3 (default = 2) for the GICE and 2–4
(default = 3) for the HICE.
The effect on the CO2 results when altering the biological forcing factors E, W, and F, as
outlined, is shown in Supplementary Figure 3 and summarised in Supplementary Table 2.
Sensitivity to timing of land colonisation. The timing of land colonisation by the first plants
is uncertain, and has been the subject of considerable debate. Our default scenario assumes
colonisation occurring over 475–460 Ma, spanning two key cryptospore finds7,8.
However, recent evidence of at least 5 genera of cryptospores present in eastern Gondwana
~472 Ma, suggests an “Early Ordovician or even Cambrian, origin of embryophytes”7. A
Cambrian origin has also been suggested based on palynomorphs from Laurentia (both
eastern and western USA today), which are interpreted as cryptospores10,11, although others
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10
argue they belonged to freshwater algae9. As an ‘early start’ scenario we consider 490 Ma in
the Late Cambrian, with completion again at 460 Ma.
The completion of colonisation by non-vascular plants at 460 Ma is based on the presence of
cryptospores on east and west sides of Gondwana7,8 by ~463 Ma, and the fact that most
subsequent cryptospore morphologies are found in the ~463 Ma assemblage, indicating “very
slow”9 evolution from then until the early Silurian. However, given the very limited data,
colonisation by non-vascular plants may have been a more drawn-out affair. As a ‘late finish’
scenario we assume colonisation started at 475 Ma but continued until 445 Ma (Hirnantian).
These slow scenarios have colonisation spread over 30 Myr, with the default over 15 Myr.
For completeness, we also consider a 5 Myr fast colonisation scenario. Previous authors6
have invoked a 25% increase in weatherability of the continents 463-459 Ma to explain the
pronounced drop in seawater 87Sr/86Sr that starts at this time and continues until ~450 Ma.
Whilst they attribute this to an abiogenic pulse of volcanic weathering, an alternative is that
the first plants colonised easily-weathered and non-radiogenic volcanic rocks at the time. To
represent this we assume that the effect of the first plants on weathering increased over 463458 Ma.
The timing of increases in phosphorus weathering was roughly based on the appearance of
the first non-vascular plants and then the later appearance of the first vascular plants, but set
more precisely to produce the approximate timings of the GICE and HICE. There are
uncertainties in the dating of these events, and their timing in the model can be readily moved
by altering the timing of the forcing. However, to produce the GICE event appears to require
a delay between the onset of non-vascular plant effects on silicate weathering and their
effects on phosphorus weathering. To explain this we hypothesise that increasing effects on
phosphorus weathering evolved over time, as phosphorus limitation became more acute and
symbiotic partnerships with mycorrhizal fungi were formed. As an alternative, the fast
colonisation scenario involves both silicate and phosphorus weathering reaching their
maximum effects at 458 Ma. We also considered a variant of this where increases in silicate
and phosphorus weathering are tied together over 463-458 Ma (results not shown).
The effects on the global temperature results of altering the timing of land colonisation and
effects on weathering are shown in Supplementary Figure 4.
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11
Supplementary Tables
Supplementary Table 1. CO2 results of sensitivity analysis varying initial conditions.
Run
Parameter
D
U
k15
0.15
0.15
CO2 (PAL)
Initial
condition
(460 Ma)
15.8
13.5
Si–only
weathering
(460 Ma)
8.4
7.1
Si & P weathering
GICE
HICE
(458 Ma)
(445 Ma)
6.2
4.5
5.2
3.7
Baseline
Reduced
degassing
Increased
degassing
Reduced
uplift
Increased
uplift
Weaker abio.
weathering
Stronger abio.
weathering
1.5
1.2
1.0
1.0
1.8
1.0
0.15
17.9
9.7
7.2
5.4
1.5
0.8
0.15
18.4
9.9
7.4
5.7
1.5
1.2
0.15
13.9
7.4
5.3
3.8
1.5
1.0
0.1
21.1
9.1
6.7
5.0
1.5
1.0
0.2
12.7
7.8
5.7
4.1
Supplementary Table 2. CO2 results of sensitivity analysis varying biological forcing.
Run
Forcing parameter
E
W
F
Baseline
0.15
0.75
2
3
CO2 (PAL)
Si–only
Si & P weathering
weathering
GICE
HICE
(460 Ma)
(458 Ma)
(445 Ma)
8.4
6.2
4.5
Less
colonisation
More
colonisation
Weaker Si
weathering
Stronger Si
weathering
Weaker P
weathering
Stronger P
weathering
0.05
0.75
2
3
11.7
9.0
6.8
0.45
0.75
2
3
5.3
3.5
2.5
0.15
0.1
2
3
13.2
9.8
7.2
0.15
1.0
2
3
7.6
5.6
4.1
0.15
0.75
1.5
2
8.4
7.2
6.1
0.15
0.75
3
4
8.4
4.6
3.3
458 Ma
445 Ma
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Supplementary Discussion
Model sensitivity analysis
We discuss the results of the sensitivity analysis with particular reference to the climate
model-derived threshold for Late Ordovician glaciations of CO2 ~8 PAL. This threshold
value carries some uncertainty, and could be somewhat higher or lower based on existing
model studies12-14 and their assumptions about sea level, ocean heat transport and orbital
forcing, but seems unlikely to have been >10 PAL.
Sensitivity to initial conditions. Varying the initial conditions by varying either degassing D
or uplift U has similar effects on the results (Supplementary Figure 2a, b, Supplementary
Table 1). With reduced degassing or increased uplift, and the default enhancement of silicate
weathering, CO2 falls below 8 PAL at the start of the Late Ordovician, and with additional
enhancement of P weathering, CO2 falls to <4 PAL in the simulated HICE event.
Alternatively, with increased degassing or reduced uplift, and the default enhancement of
silicate weathering, CO2 falls to ~10 PAL at 460 Ma, but additional phosphorus weathering
forcing is sufficient to take it to ~5-7 PAL in the GICE or HICE events.
Varying the initial conditions by varying pre-plant weathering (k15) has remarkably little
effect on the results of weathering forcing by the first land plants (Supplementary Figure 2c,
Supplementary Table 1). Despite an initial range of CO2 ~13-21 PAL, under the default
forcing of silicate weathering, CO2 levels converge to 8-9 PAL at the start of the Late
Ordovician ~460 Ma. With the additional forcing of phosphorus weathering, they drop to 6-7
PAL in the GICE and 4-5 PAL in the HICE. The reason for the convergence is that nonvascular plants come to dominate the total weathering functional response, despite
contributing only around half of the weathering flux.
Sensitivity to biological forcing factors. Varying E, the extent of colonisation by the first
non-vascular plants, W, the enhancement of weathering achieved by the first non-vascular
plants, or F, the additional forcing of phosphorus weathering, significantly alters the CO2
levels achieved but does not alter the central result (Supplementary Figure 3, Supplementary
Table 2).
Lowering E, with colonisation restricted to wetlands, CO2 drops from ~16 to ~12 PAL with
the amplification of silicate weathering, probably insufficient to trigger glaciations. However,
additional enhancement of phosphorus weathering lowers CO2 to ~9 PAL in the GICE and ~7
PAL in the Hirnantian (the most pronounced interval of glaciations). Increasing the extent of
colonisation, E, means that with enhanced silicate weathering alone, CO2 falls to ~5 PAL,
below the threshold for glaciations. Additional phosphorus weathering can then lower CO2 to
2.5-3.5 PAL.
Lowering W, the enhancement of weathering achieved by the first non-vascular plants, such
that they achieve only 10% of the weathering enhancement of modern vascular plants, CO2
levels drop from ~16 to ~13 PAL at the start of the Late Ordovician, likely insufficient to
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13
trigger glaciations. However, additional phosphorus weathering lowers CO2 to ~7 PAL in the
Hirnantian, sufficient for glaciations. Increasing W, if we assume that silicate weathering
enhancement by non-vascular plants matches that due to modern vascular plants, CO2 is
drawn <8 PAL at the start of the Late Ordovician, and additional phosphorus weathering can
lower it to ~4 PAL in the Hirnantian.
Notably, the effect on CO2 of the first plants enhancing phosphorus weathering is greater if
their effect on silicate weathering is weaker, and the CO2 level is correspondingly higher
(Supplementary Figure 3a, b).
Lowering F, the additional forcing of phosphorus weathering, causes CO2 to drop to ~7 PAL
in the GICE and ~6 PAL in the HICE, still likely sufficient to cause glaciations in both cases.
However, the corresponding δ13C increases of ~1.5 ‰ (GICE) and ~3 ‰ (HICE) are smaller
than observed (results not shown). Increasing F produces δ13C increases of ~5 ‰ (GICE) and
~7.5 ‰ (HICE), at the upper end of observations, and CO2 drops to ~4.5 PAL and ~3 PAL
respectively. Global temperature drops to a minimum of ~12 °C in the Hirnantian.
Sensitivity to timing of land colonisation. Whilst uncertainty in the timing of land
colonisation clearly alters the timing of predicted effects on CO2, temperature and other
variables in the model, it does not significantly alter the final magnitude of those effects. If
we assume an early start to colonisation in the latest Cambrian 490 Ma and that it was largely
completed by 460 Ma (Supplementary Figure 4a), this produces a good fit to the pattern of
Early-Mid Ordovician cooling, followed by temperature stabilisation, inferred from oxygen
isotopes of conodonts15 (data in Figure 1 of the main paper). If instead we assume a late
finish to colonisation around 445 Ma this produces a progressive cooling to the Hirnantian
(Supplementary Figure 4b), which is more consistent with traditional views of Late
Ordovician temperature history. Alternatively, if we assume a fast colonisation over 463-458
Ma, this produces a corresponding abrupt CO2 drop and cooling (Supplementary Figure 4c).
Tying this abrupt increase in silicate weathering to a corresponding increase in phosphorus
weathering produces a longer δ13C excursion (GICE) of unaltered magnitude (results not
shown), but δ13C data do not support such an early start for the GICE.
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14
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