Global suppression of photorespiration during the 20th century
Global changes in the photorespiration to photosynthesis ratio during the 20th century were assessed by comparing the D6S/D6R ratios of modern and ≥100 years old Sphagnum tissues. Modern Sphagnum samples were retrieved from surface peat (top 0-2 cm) formed at contemporary atmospheric CO2 levels (ca. 400 ppm). Conversely, historical Sphagnum tissues were retrieved from peat layers ≥ 30 cm below the surface, with an approximate age of 100 years or more (Table S1). Thus, the historical Sphagnum tissues were formed when atmospheric CO2 concentrations were ≤ 300 ppm. The D6S/D6R ratio of modern Sphagnum was 0.860 ± 0.004 (average ± SE, range: 0.810-0.927), while that of historical Sphagnum was 0.901 ± 0.005 (average ± SE, range: 0.858-0.971, Figure S1). Thus, the D6S/D6R ratio of modern Sphagnum was significantly lower (t-test, p < 0.001) compared to ≥100 years old Sphagnum, indicating that photorespiration is suppressed relative to photosynthesis.
The peat samples differed with respect to their depth below the surface (which is related to the atmospheric CO2 concentration when the Sphagnum biomass was formed), the Sphagnum subgenus, the present WT depth, and the geographical location (site). Effects of differences in the site are related to differences in climate, and are investigated later on. Therefore, we performed a three-way analysis of variance (ANOVA) to test the effects of atmospheric CO2, WT and subgenus on the D6S/D6R ratio (Table 1). Atmospheric CO2 and subgenus had a significant effect and explained 39% and 8% respectively (p<0.001 and p=0.002, respectively). A significant interaction was found between CO2 and WT (p < 0.001), indicating that the effect of CO2 on the D6S/D6R ratio is dependent on the WT depth.
Table 1
Three-way ANOVA models of effects of atmospheric CO2, water table (WT) and Sphagnum subgenus (Subg.) on the D6S/D6R ratio.
Factor
|
Df
|
F
|
p
|
R2 (%)
|
CO2
|
1, 62
|
64.7
|
<0.001
|
39.1
|
WT
|
n.s.
|
Subg.
|
2, 62
|
6.9
|
0.002
|
8.4
|
CO2 x WT
|
4, 62
|
5.5
|
<0.001
|
13.2
|
CO2 x Subg.
|
n.s.
|
WT x Subg.
|
n.s.
|
CO2 x WT x Subg.
|
n.s.
|
Df, degrees of freedom of the model and residues. Non-significant factors/interactions with p > 0.1 are denoted as n.s. |
The effect of atmospheric CO2 on the D6S/D6R ratio clearly depended on the present WT depth. For samples where the WT was < 10 cm below the moss surface, the D6S/D6R ratios were not significantly different (t-test, p = 0.199) between modern and historical Sphagnum, with means of 0.893 ± 0.01 and 0.905 ± 0.009 (SE), respectively. Conversely, for samples with WT depth of 10-40 cm, the D6S/D6R ratios of modern and historical Sphagnum clearly differed (p < 0.001), having means of 0.850 ± 0.004 and 0.910 ± 0.007 (SE), respectively (Figure 1 and S1). For the WT >40 cm group, the difference between modern and historical samples was again not significant (p = 0.073), with means of 0.860 ± 0.007 and 0.873 ± 0.004 (average ± SE), respectively.
The Sphagnum subgenus had a clear effect: the mean D6S/D6R ratios for modern and historical samples of ACUTIFOLIA species were 0.858 ± 0.004 and 0.906 ± 0.007 (SE), respectively (p < 0.001), while those for species of the subgenus SPHAGNUM were 0.846 ± 0.006 and 0.885 ± 0.006 (SE), respectively (p < 0.001). The D6S/D6R ratio was thus generally lower for species of the subgenus SPHAGNUM than for ACUTIFOLIA species. Modern and historical samples of CUSPIDATA species had higher mean D6S/D6R ratios of 0.911 ± 0.008 and 0.921 ± 0.009 (SE), respectively, with no significant difference (p = 0.211) between modern and historical samples (Figure 1 and S1).
The differences in the D6S/D6R ratio between modern and historical Sphagnum were normalized based on the linear relationship between the D6S/D6R ratio and 1000/[CO2] previously reported by Ehlers et al. (2015), to account for variations in atmospheric CO2 concentrations due to differences in peat depth and/or age. To this end, the regression slope of this linear function was calculated as the change in the D6S/D6R ratio per unit change in 1000/[CO2] between modern and historical Sphagnum samples (denoted ΔD6S/D6RN). ΔD6S/D6RN thus represents the degree of suppression of photorespiration; its mean was 0.044 ± 0.008 (SE) and it varied between 0.000 and 0.094 (Figure 1). ΔD6S/D6RN varied with the WT depth: it was 0.010 ± 0.005 (average ± SE) for WT depths < 10 cm below the moss surface, 0.066 ± 0.006 (average ± SE) for WT depths between 10 and 40 cm, and 0.016 ± 0.010 (average ± SE) for WT depths >40 cm (Figure 1). These results indicate that a WT between 10 and 40 cm below the moss surface is optimal for suppressing photorespiration in response to increased atmospheric CO2.
Effect of changes in water table, temperature and precipitation during the 20th century
The relationship between ΔD6S/D6RN and the present WT depth assumes that hydrological conditions were relatively stable over the 20th century. To support this assumption, we estimated changes in WT depth based on available testate amoebae reconstruction data (Table 2). Data were obtained for peat cores with WT depth >10 cm only (and site 1, WT = 8 cm). In cases where data were not available for the sampled mires, data were acquired for mires from the same region (Table 2 and S2), assuming that the similarities in regional climate would result in similar changes in WT depth 37. Additionally, variations in other climate parameters such as temperature and precipitation may have affected the suppression of photorespiration (ΔD6S/D6RN). Therefore, we also estimated changes in temperature and precipitation during the 20th century using available climate models 33,34,35 (Table 2).
Table 2
Historical changes in water table (WT) depth, mean annual air temperature (MAT) and total annual precipitation (TAP) during the 20th century at the sites shown in Figure 1.
Site
|
Δ WT (cm)
|
Δ MAT (⁰C)
|
Δ TAP (%)
|
Reference (WT)
|
1
|
≈ 0
|
+ 3.1
|
+ 9.9
|
38
|
2, 3
|
+ 4
|
+ 0.2
|
- 6.7
|
39, 40
|
4
|
- 40*
|
- 1.7
|
- 32.6
|
41
|
5
|
≈ 0*
|
+ 2.8
|
+ 19.1
|
37
|
6
|
- 5*
|
+ 1.3
|
+ 11.1
|
37, 42
|
7, 8
|
- 11*
|
+ 0.4
|
+ 12.5
|
37
|
9
|
- 6
|
+ 1.6
|
+ 25.0
|
43
|
10
|
- 30*
|
+ 0.1
|
+ 15.1
|
44
|
Changes in TAP are specified in percent change. (-) indicates a decrease and (+) indicates an increase. WT data were obtained only for peat cores with WT >10 cm, and for site 1 (WT = 8 cm), n = 30. (*) indicates WT data for another mire in the same region as the relevant site (Table S2).
Changes in WT during the 20th century were generally small (between +4 and -11 cm), except in southern Argentina and Australia, where the WT depth decreased by 40 and 30 cm, respectively (Table 2). To determine whether changes in historical climate data contribute to the ΔD6S/D6RN-response, we performed a three-way ANOVA, with WT, mean annual air temperature (MAT), and total annual precipitation (TAP) as factors. No significant effect of WT, MAT and TAP could be detected (p > 0.2). However, a significant interaction was found between WT and MAT (R2=0.16, F=53.8, p=0.028). Further, we tested if specifically the mean summer air temperature (MSAT) or the total summer precipitation (TSP) effect the ΔD6S/D6RN–response by performing a three-way ANOVA with WT, MSAT and TSP as factors. Again no significant effect could be detected (p > 0.2), except for an interaction between WT and MSAT (R2=0.17, F=53.3, p=0.029). Thus, a small part of the variation in ΔD6S/D6RN (17%) of Sphagnum may be explained by combined changes in WT and temperature during the 20th century.
Sphagnum δ13C as proxy for changes in water table depth
The carbon isotopic signature (δ13C) of Sphagnum peat has been proposed as proxy for surface moisture 27,36,45,46. Therefore, we tested the use of δ13C as a potential indicator of changes in WT depth by measuring the δ13C of both modern and ≥100 years-old whole-Sphagnum tissues. Regression analysis revealed a highly significant correlation between δ13C in modern Sphagnum and the present WT depth (R2=0.67, p <0.001, Figure 2) confirming that δ13C reflects changes in WT depth. The δ13C values became more negative (i.e. more depleted) with increasing WT depth, from -25.8 ± 0.2‰ (average ± SE) at WT depths < 10 cm to -30.3 ± 0.5‰ (average ± SE) at WT depths > 60 cm below surface. For ≥100 years-old Sphagnum, δ13C also correlated significantly with the present WT depth (R2 = 0.40, p < 0.001). Both modern and historical Sphagnum showed the same trend (with slopes of 0.07 and 0.06, respectively, Figure 2), indicating that the WT depth ≥100 years ago was similar to that today. The δ13C of modern Sphagnum was more negative than that of historical Sphagnum (average difference 1.9 ± 0.9‰ SD) in all peat cores bar one that showed an increase (2.9‰, site 9, Figure S2), and was excluded from the regression in Figure 2.