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Supplementary Information:

Enhanced weathering by the first land plants caused Late 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

1College of Life and Environmental Sciences, University of Exeter, Exeter, EX4 4PS, UK. 2Earth 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.

First plants cooled the Ordovician

© 2012 Macmillan Publishers Limited. All rights reserved.

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(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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(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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(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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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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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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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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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 non-vascular 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 Mid-Late Ordovician is uncertain. We identified the locations of early fossil cryptospore


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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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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 463-458 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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Supplementary Tables

Supplementary Table 1. CO2 results of sensitivity analysis varying initial conditions.

Parameter CO2 (PAL) Si & P weathering

Run D U k15 Initial

condition (460 Ma)

Si–only weathering (460 Ma)

GICE (458 Ma)

HICE (445 Ma)

Baseline 1.5 1.0 0.15 15.8 8.4 6.2 4.5 Reduced degassing

1.2 1.0 0.15 13.5 7.1 5.2 3.7

Increased degassing

1.8 1.0 0.15 17.9 9.7 7.2 5.4

Reduced uplift

1.5 0.8 0.15 18.4 9.9 7.4 5.7

Increased uplift

1.5 1.2 0.15 13.9 7.4 5.3 3.8

Weaker abio. weathering

1.5 1.0 0.1 21.1 9.1 6.7 5.0

Stronger abio. weathering

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.

Forcing parameter CO2 (PAL) F Si & P weathering

Run E W

458 Ma 445 Ma

Si–only weathering (460 Ma) GICE

(458 Ma) HICE (445 Ma)

Baseline 0.15 0.75 2 3 8.4 6.2 4.5

Less colonisation

0.05 0.75 2 3 11.7 9.0 6.8

More colonisation

0.45 0.75 2 3 5.3 3.5 2.5

Weaker Si weathering

0.15 0.1 2 3 13.2 9.8 7.2

Stronger Si weathering

0.15 1.0 2 3 7.6 5.6 4.1

Weaker P weathering

0.15 0.75 1.5 2 8.4 7.2 6.1

Stronger P weathering

0.15 0.75 3 4 8.4 4.6 3.3


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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 non-vascular 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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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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doi: 10.1038/ngeo1390 supplementary information: enhanced ... · anglia, norwich, nr4 7tj, uk....

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