Carbon dynamics in response to warming and elevated atmospheric CO2 concentration in temperate forest and boreal peatland plant-soil systems

Soils are highly significant to global efforts combating climate change, owing to their capacity to store three times the amount of carbon (C) present in the atmosphere. Concern has been raised over the stability of this vast soil C store as terrestrial ecosystems are already exposed to, and predicted to experience, a strong temperature increase that is likely to exceed 6 °C by the end of the century. An overarching concern is that future climate warming, a consequence of rising atmospheric CO2 concentration, has the potential to destabilize stored soil organic matter (SOM) and accelerate climate change by releasing additional CO2 to the atmosphere. However, given the complexity of the individual impact of either warming or elevated atmospheric CO2 concentration, there is substantial uncertainty about how these two factors combined will impact soil C and the associated feedbacks to climate change. This is because climate and environmental changes are expected to perturb biotic and abiotic processes such as above- and below-ground inputs, and substrate quality and availability and environmental controls such hydrology, potentially altering complex interactions that influence both the supply of organic matter and the microorganisms performing SOM transformations. In this view, the role of biotic and abiotic controls in regulating soil C stability and storage now and in the future merits further attention. Such efforts will lead to construction of accurate predictive models for global C flux and and turnover rates as most existing climate models lack detailed input parameters for C storage. In this context, the overarching goal of this thesis is to assess the potential consequences of climate-driven changes (warming and elevated atmospheric CO2 concentration) on above- and below-ground C inputs and storage and processes responsible for C cycling in temperate forest and boreal peatland ecosystems, two habitats that store large amounts of soil C. The temperate forest study was executed in a functional multi-year whole-soil profile warming experiment, located in the foothills of the Sierra Nevada, USA. The average soil temperature in the warmed plots was elevated by +4 °C to one meter depth above the control plots, while maintaining the seasonality and natural temperature gradient with depth, with the use of buried resistance heater cable. In this experiment, the aboveground vegetation was not warmed. The boreal peatland experiment is located at the southern boundary of the boreal region in northern Minnesota, USA. The experiment adopts a multifactor regression design and incorporates above- and below-ground warming to five warming levels (+0, +2.25, +4.5, +6.75 and +9 °C), which is broader than that used in other warming experiments, repeated at both ambient and elevated CO2 concentrations. The boreal peatland experiment adds a key missing treatment from temperate forest experiment – elevated atmospheric CO2 concentration. Also, the combination of warming and elevated CO2 treatments at a range of increasing temperatures in the boreal peatland experiment allows for the evaluation of C cycling across mild to extreme scenarios for warming. In the temperate forest experiment, 4.5 years of warming led to a decline in fine root mass by 24%, accompanied by preferential loss of plant C inputs and accelerated microbial decomposition of unprotected SOM in the subsoils (20-100 cm), contributing to a loss of 33% of subsoil C stocks and increases in CO2 effluxes. Subsoil C losses were accompanied by a shift in the microbial community towards organisms capable of utilizing complex organic compounds. Soil moisture depletion appears to have been partially responsible for not only reduced plant inputs to SOM and changes in microbial abundance and activity but also the decomposition of SOM in this temperate forest ecosystem. Similarly, 4 years of whole-ecosystem warming accelerated SOM decomposition and altered C storage in the surface aerobic peat layer (acrotelm; 0-30 cm) in the boreal peatland experiment, despite higher aboveand below-ground plant C inputs. Interestingly, warming resulted in a limited drying in the peat surface layer (0-30 cm) and increased fine root biomass and soil CO2 and CH4 efflux, but did not affect microbial communities in this experiment. Thus, the increased soil C decomposition under warmer temperatures is likely fuelled by the resulting oxygenation following lowered water table and increased incorporation of labile C via root growth. Two years of elevated CO2 treatment (ambient temperature) did not alter above- and below-ground C inputs and storage in the boreal peatland experiment, contrary to the expectation that higher CO2 concentrations would lead to an increase in soil C due to higher biomass inputs into SOM. However, warming × elevated CO2 concentration led to higher plant- and microbe-derived C inputs into SOM in this peatland ecosystem. Specifically, warmer temperatures and elevated CO2 treatment stimulated rapid incorporation of plant C inputs into SOM more than warming (C loss) or elevated CO2 treatments (no response) alone, implying that the new C that was assimilated by plants was being re-allocated towards soil C. The source of new C could be root inputs since belowground C inputs have been shown to significantly increase under elevated CO2 concentration in this experiment. However, increases in C turnover, supported by the observed rapid incorporation of new C into SOM in this study cannot be ruled out and is likely limiting the potential for greater soil C storage. In summary, warming evoked contrasting responses in biotic and abiotic processes regulating C stability in temperate forest vs boreal peatland, including changes in the rate of plant inputs and in microbial abundance and activity, and soil moisture, but the overall outcome on C stability was similar in both ecosystems; accelerated SOM decomposition and altered C storage. A likely implication of C loss and increased CO2 emissions observed here is the potential for a strong amplification effect on climate change. Given that warming × higher CO2 concentrations stimulated incorporation of plant inputs into soil C, the observed loss of soil C under warming-only treatment may have overestimated predictions of warming impacts based on observations under ambient CO2 conditions. The counteractive effects of warming and elevated atmospheric CO2 concentration on soil C stability and storage shows that different competing mechanisms can govern C dynamics. Decomposition processes dominate under rising temperature, whereas incorporation of plant inputs into peat C increase when warmer temperatures are combined with elevated greenhouse gases. In this respect, more research is needed to provide an adequate knowledge of C storage capacity and long-term behaviour of these ecosystems under multiple interactive global environmental changes. In conclusion, rising temperatures and atmospheric CO2 concentrations directly changed C cycling in temperate forest and boreal peatland ecosystems by altering SOM inputs, and decomposition parameters that dictate soil C storage within only four years, highlighting the vulnerability of these C rich ecosystems to global change

Rapid loss of complex polymers and pyrogenic carbon in subsoils under whole-soil warming

Subsoils contain more than half of soil organic carbon (SOC) and are expected to experience rapid warming in the coming decades. Yet our understanding of the stability of this vast carbon pool under global warming is uncertain. In particular, the fate of complex molecular structures (polymers) remains debated. Here we show that 4.5 years of whole-soil warming (+4 °C) resulted in less polymeric SOC (sum of specific polymers contributing to SOC) in the warmed subsoil (20–90 cm) relative to control, with no detectable change in topsoil. Warming stimulated the subsoil loss of lignin phenols (−17 ± 0%) derived from woody plant biomass, hydrolysable lipids cutin and suberin, derived from leaf and woody plant biomass (−28 ± 3%), and pyrogenic carbon (−37 ± 8%) produced during incomplete combustion. Given that these compounds have been proposed for long-term carbon sequestration, it is notable that they were rapidly lost in warmed soils. We conclude that complex polymeric carbon in subsoil is vulnerable to decomposition and propose that molecular structure alone may not protect compounds from degradation under future warming

Warming and elevated CO2 promote rapid incorporation and degradation of plant-derived organic matter in an ombrotrophic peatland

Rising temperatures have the potential to directly affect carbon cycling in peatlands by enhancing organic matter (OM) decomposition, contributing to the release of CO2 and CH4 to the atmosphere. In turn, increasing atmospheric CO2 concentration may stimulate photosynthesis, potentially increasing plant litter inputs belowground and transferring carbon from the atmosphere into terrestrial ecosystems. Key questions remain about the magnitude and rate of these interacting and opposing environmental change drivers. Here, we assess the incorporation and degradation of plant- and microbe-derived OM in an ombrotrophic peatland after 4 years of whole-ecosystem warming (+0, +2.25, +4.5, +6.75 and +9°C) and two years of elevated CO2 manipulation (500 ppm above ambient). We show that OM molecular composition was substantially altered in the aerobic acrotelm, highlighting the sensitivity of acrotelm carbon to rising temperatures and atmospheric CO2 concentration. While warming accelerated OM decomposition under ambient CO2, new carbon incorporation into peat increased in warming × elevated CO2 treatments for both plant- and microbe-derived OM. Using the isotopic signature of the applied CO2 enrichment as a label for recently photosynthesized OM, our data demonstrate that new plant inputs have been rapidly incorporated into peat carbon. Our results suggest that under current hydrological conditions, rising temperatures and atmospheric CO2 levels will likely offset each other in boreal peatlands

Climate warming and elevated CO2 alter peatland soil carbon sources and stability

Peatlands are an important carbon (C) reservoir storing one-third of global soil organic carbon (SOC), but little is known about the fate of these C stocks under climate change. Here, we examine the impact of warming and elevated atmospheric CO$_{2}$ concentration (eCO$_{2}$) on the molecular composition of SOC to infer SOC sources (microbe-, plant- and fire-derived) and stability in a boreal peatland. We show that while warming alone decreased plant- and microbe-derived SOC due to enhanced decomposition, warming combined with eCO$_{2}$ increased plant-derived SOC compounds. We further observed increasing root-derived inputs (suberin) and declining leaf/needle-derived inputs (cutin) into SOC under warming and eCO$_{2}$. The decline in SOC compounds with warming and gains from new root-derived C under eCO$_{2}$, suggest that warming and eCO$_{2}$ may shift peatland C budget towards pools with faster turnover. Together, our results indicate that climate change may increase inputs and enhance decomposition of SOC potentially destabilising C storage in peatlands

Whole-soil warming decreases abundance and modifies the community structure of microorganisms in the subsoil but not in surface soil

The microbial community composition in subsoils remains understudied, and it is largely unknown whether subsoil microorganisms show a similar response to global warming as microorganisms at the soil surface do. Since microorganisms are the key drivers of soil organic carbon decomposition, this knowledge gap causes uncertainty in the predictions of future carbon cycling in the subsoil carbon pool (> 50 % of the soil organic carbon stocks are below 30 cm soil depth). In the Blodgett Forest field warming experiment (California, USA) we investigated how +4 ∘C warming in the whole-soil profile to 100 cm soil depth for 4.5 years has affected the abundance and community structure of microorganisms. We used proxies for bulk microbial biomass carbon (MBC) and functional microbial groups based on lipid biomarkers, such as phospholipid fatty acids (PLFAs) and branched glycerol dialkyl glycerol tetraethers (brGDGTs). With depth, the microbial biomass decreased and the community composition changed. Our results show that the concentration of PLFAs decreased with warming in the subsoil (below 30 cm) by 28 % but was not affected in the topsoil. Phospholipid fatty acid concentrations changed in concert with soil organic carbon. The microbial community response to warming was depth dependent. The relative abundance of Actinobacteria increased in warmed subsoil, and Gram+ bacteria in subsoils adapted their cell membrane structure to warming-induced stress, as indicated by the ratio of anteiso to iso branched PLFAs. Our results show for the first time that subsoil microorganisms can be more affected by warming compared to topsoil microorganisms. These microbial responses could be explained by the observed decrease in subsoil organic carbon concentrations in the warmed plots. A decrease in microbial abundance in warmed subsoils might reduce the magnitude of the respiration response over time. The shift in the subsoil microbial community towards more Actinobacteria might disproportionately enhance the degradation of previously stable subsoil carbon, as this group is able to metabolize complex carbon sources

Warming promotes loss of subsoil carbon through accelerated degradation of plant-derived organic matter

Increasing global temperatures have the potential to stimulate decomposition and alter the composition of soil organic matter (SOM). However, questions remain about the extent to which SOM quality and quantity along the soil profile may change under future warming. In this study we assessed how +4 °C whole-soil warming affected the quantity and quality of SOM down to 90 cm depth in a mixed-coniferous temperate forest using biomarker analyses. Our findings indicate that 4.5 years of soil warming led to divergent responses in subsoils (>20 cm) as compared to surface soils. Warming enhanced the accumulation of plant-derived n-alkanes over the whole soil profile. In the subsoil, this was at the expense of plant- and microorganism-derived fatty acids, and the relative abundance of SOM molecular components shifted from less microbially transformed to more transformed organic matter. Fine root mass declined by 24.0 ± 7.5% with warming over the whole soil profile, accompanied by reduced plant-derived inputs and accelerated decomposition of aromatic compounds and plant-derived fatty acids in the subsoils. Our study suggests that warming accelerated microbial decomposition of plant-derived inputs, leaving behind more degraded organic matter. The non-uniform, and depth dependent SOM composition and warming response implies that subsoil carbon cycling is as sensitive and complex as in surface soils

Warming and elevated CO2 induced shifts in carbon partitioning and lipid composition within an ombrotrophic bog plant community

Plant carbon (C) allocation is a key process determining C cycling in terrestrial ecosystems. In carbon-rich peatland ecosystems, impacts of climate change can exert a strong influence on C allocation strategies of the dominant plant species, with potentially large implications for the peatland C budget. However, little is known about plant C allocation into various secondary biosynthetic metabolites and whether different plant species vary in C allocation strategies in response to climate change. Here, we report species-specific leaf chemistry and secondary metabolism in trees (Picea mariana and Larix laricina), shrubs (Rhododendron groenlandicum and Chamaedaphne calyculata), and Sphagnum mosses (Sphagnum angustifolium and Sphagnum magellanicum) in response to whole-ecosystem warming (+0, +2.25, +4.5, +6.75 and +9 °C) and elevated CO2 manipulation (ambient or +500 ppm) in an ombrotrophic peatland. We show that warming and elevated CO2 substantially altered leaf chemistry and cuticle composition, including increases in leaf nitrogen, shifts in lipid composition and dependence on new photosynthates, although results varied by species. Shrub species lowered the saturation of their membrane fatty acids and increased their leaf nitrogen and C concentrations, while tree species increased their wax concentrations under higher warming treatments. Using isotopic labeling to trace the fate of newly-assimilated C, we observed an unexpectedly low fraction of new C in tree and shrub species (∼50% and ∼70% respectively). This suggests the combined use of newly-assimilated and older C reserves stored in plant organs for plant functional processes and CO2 originating from peat degradation and even more so in response to warmer temperatures and elevated CO2 concentrations. Under higher temperatures, Sphagnum mosses increased their leaf nitrogen but decreased their leaf C concentrations and the fraction of experiment-derived C (by 20%); suggesting an increasing C allocation to osmotic compounds that aid in maintaining high water retention capacity, albeit at the cost of other metabolites. Our results indicate species-specific shifts in plant chemistry and cuticular lipid composition, which could strongly moderate and shape boreal peatland ecosystem response to climate change in the future

Climate warming and elevated CO2 alter peatland soil carbon sources and stability

Abstract Peatlands are an important carbon (C) reservoir storing one-third of global soil organic carbon (SOC), but little is known about the fate of these C stocks under climate change. Here, we examine the impact of warming and elevated atmospheric CO2 concentration (eCO2) on the molecular composition of SOC to infer SOC sources (microbe-, plant- and fire-derived) and stability in a boreal peatland. We show that while warming alone decreased plant- and microbe-derived SOC due to enhanced decomposition, warming combined with eCO2 increased plant-derived SOC compounds. We further observed increasing root-derived inputs (suberin) and declining leaf/needle-derived inputs (cutin) into SOC under warming and eCO2. The decline in SOC compounds with warming and gains from new root-derived C under eCO2, suggest that warming and eCO2 may shift peatland C budget towards pools with faster turnover. Together, our results indicate that climate change may increase inputs and enhance decomposition of SOC potentially destabilising C storage in peatlands