Response of mature Norway spruce (Picea abies) to elevated atmospheric CO²

The aim of this thesis was to identify pathways and rates of C allocation in tall forest trees, and to identify effects of elevated CO2 on respiratory processes and root growth. Correspondingly, this thesis is divided into three separate parts:
Chapter 2)
Long-term 13C labeling provides evidence for temporal and spatial carbon allocation patterns in mature Picea abies (published in Oecologia)
Chapter 3)
Respiratory fluxes and fine root responses in mature Picea abies trees exposed to elevated atmospheric CO2 concentrations (published in Biogeochemistry)
Chapter 4)
Photosynthetic enhancement and diurnal stem and soil carbon fluxes in a mature Norway spruce stand under elevated CO2 (published in Environmental and Experimental Botany)
The work was conducted at the Swiss canopy crane (SCC) research site in Hofstetten near Basel, Switzerland, and explored signals produced by free air CO2 enrichment (FACE) in 110-year-old, ca. 37m tall P. abies trees. Chapter 2 capitalizes on the isotopic signal carried by the CO2 gas used for CO2 enrichment, yet does not address effects of elevated CO2 as such, but rather deals with basic questions of C transfer in tall trees. Chapter 3 explores the longer-term CO2 effects on mature P. abies (i.e. 2.5 years), whereas chapter 4 reports short-term (diurnal) responses to elevated CO2. In the following, I will provide a summary of the results of the three chapters of my thesis, extended by a conclusion that links these chapters.
Chapter 2) Long-term 13C labeling of Picea abies
As a side effect, the FACE technique provided the unique opportunity to study C translocation within the tree body using the stable isotope 13C signal the FACE gas carries. Since control trees are not (can not) be similarly labeled with 13C the tree responses to elevated CO2 were not the subject of this chapter. Yet, FACE resembles a continuous 13C labeling of new assimilates. Tracking the fate of these assimilates over a period of 2.5 years in tall trees offers new insights in tree C relations under steady state conditions. We tracked 13C signals in mature P. abies trees at a high spatial and temporal resolution, i.e. from the canopy (needles and branchlets), down to the tree trunk (year rings and stem CO2 efflux), and into the soil compartment (fine roots, fungi, soil CO2 efflux). The following key questions were answered:
1. How long does it take for new C to arrive at a certain tissue type or respiratory flux?
2. What is the proportional contribution of newly assimilated C to concurrent tree tissue production and maintenance?
3. How long does it take until old C is replaced by new C in various tissues?
Generally, we observed a reduction of new assimilate investment with distance from the canopy, which can be explained by a progressive dilution of new C into the existing C storage pools in the tree. New sunlit needles (and adjacent branchlets) exhibited a nearly 100% share of new C, whereas shaded needles also used some older C. Stem wood isotope signals evidenced a complete exchange of old C by new C within 2 years. Fine roots contained only 49-56% new C, hence are using older C pools for a longer period of time. A surprisingly low fraction of novel C (26-43%) was recovered from fungal sporocarps, presumably related to the influence of neighboring trees that were not CO2 enriched. The first appearance of new C in soil and stem CO2 release occurred after 12 days, reflecting a lag due to the long transport distances in these 37m tall trees. The CO2 released by stems was composed of 50% new C already in the first year of FACE. In contrast, only ca. 15% new C contributed to soil CO2 efflux, reflecting the use of older substrates, and the influence of older roots and litter from neighboring trees blown in by wind.
These findings indicate a rapid contribution of new assimilates to tissue formation, and thus, a fast replacement of mobile C reserves with new C, and a progressive signal dilution from treetop to the bottom. The two-year replacement time in stem xylem shows that the storage pool is contributing substantially to tree ring formation. We speculate that the turnover of mobile C pools might be enhanced by elevated CO2, and the metabolic costs of this turnover might compensate for some of the extra C taken up at elevated CO2 concentrations, and thus, may explain the ‘missing C’ at the whole tree level. These metabolic costs are unlikely to produce measurable signals at tissue level, given the large heterotrophic volume of such trees.
Chapter 3) Responses of Picea abies to elevated CO2
Most FACE experiments revealed strong initial growth responses to elevated CO2 that diminished over the first 3 years (Körner 2006). Since growth in natural undisturbed systems is commonly not showing a continued stimulation under altered CO2 for reasons of nutrient supply, a step increase in CO2 concentration should induce overflow responses in terms of enhanced respiration and fine root expansion, the latter in order to forage for nutrients to balance the additional C input. In this web-FACE experiment, established in a natural Central European forest, we investigated mature ca. 110-year-old P. abies trees in their steady state of growth (C cycle coupled to the nutrient cycle; Körner 2006). In this publication we were particularly interested in:
1. Seasonal shifts in assimilate allocation;
2. Locations of C-investment;
3. Residence times (turnover) of mobile C pools.
We tracked the respiratory and fine root growth responses of these trees before and directly after the start of FACE, and for further 2.5 years. The CO2 concentration in the canopy (e.g. 540 ppm) was about twice the pre-industrial level. We anticipated a stimulation of CO2 release, and faster root expansion into root-free soil space (in-growth core method), but we also expected a weaker signal in these mature trees compared to young trees. Seasonal stem CO2 efflux did not show any sign of increase during the 2.5 years under elevated CO2. This result lines up with the lack of any stem radial growth response (ongoing work). Fine roots (<0.5-2 mm) did not accumulate more dry matter in the course of 2.5 years of CO2 fertilization. Interestingly, we observed a slight but significant reduction of CO2 release from the soil despite clear evidence by isotopic signals that novel assimilates arrived in the soil.
These data suggest that such mature trees do not even show a transient stimulation of respiration to a step increase of CO2, as was observed in other FACE experiments using much younger trees (Norby et al. 2010). Other growth-limiting factors appear to prevent more vigorous tree growth and thus, metabolism at high CO2 (Norby & Zak 2011). N limitation can be excluded at our site because of high N-deposition. A part of the extra C taken up by needles at elevated CO2 might have been allocated belowground, however, not to fine roots. Conversely, slightly reduced rather than increased rates of soil CO2 efflux implies that respiration of roots and/or soil organisms declined under elevated CO2, implying an overall reduced C allocation into the rhizosphere. We assume that extra C absorbed by foliage is either retained within the tree body (stored carbohydrates), recycled by respiration rates below detection limit across all heterotrophic plant tissues, or lost through enhanced leaching of dissolved organic or inorganic carbon (DIC/DOC).
In summary, we conclude that mature P. abies trees at our site are roughly C saturated at current CO2 concentrations. We find no indication of stimulated belowground metabolic activity (fine roots and soil CO2 efflux).
Chapter 5) Diurnal courses in P. abies under elevated CO2
Leaf-level photosynthetic stimulation in trees following a step increase of atmospheric CO2 was commonly observed in CO2 enrichment experiments, however, mostly without corresponding growth stimulation. Hence, the fate of this additional C input in tree still is not fully resolved, but C overflow mechanisms such as respiratory C losses might account for this C surplus. Since these potential variations in C fluxes might not be detectable on a daily basis, a response may emerge on shorter timescales (i.e. on a diurnal basis). This chapter (co-authorship) explored the diurnal variations in C fluxes (i.e. net photosynthesis, and CO2 efflux from the forest floor and the from stem) in mature P. abies trees exposed to elevated CO2 in the SCC web-FACE experiment. We tracked the diurnal variations of these fluxes on a summer day shortly before the onset of FACE, and twice during the FACE periods in summer 2009 and 2010.
Results from this study confirmed a CO2-induced photosynthetic stimulation shortly after the onset of FACE, and a change in magnitude throughout the day. Intriguingly, this stimulation of Anet diminished in the second year under FACE, indicating photosynthetic downregulation in these trees. The respiratory fluxes from P. abies stems, as observed on a seasonal basis (chapter 4), were not affected by high levels of CO2 whereas soil CO2 efflux decreased slightly with prolonged exposure to elevated CO2. Further, the diurnal patterns of CO2 release (stems and soil) were not altered by CO2 enrichment.
In conclusion, despite larger C input into the tree system in the first year of FACE, respiratory overflow mechanisms could not be observed even on a diurnal basis, corroborating our results obtained in chapter 4. Additionally, the photosynthetic downregulation observed at high CO2 confirms the assumption that these trees are C saturated.
Final conclusions
Stimulatory effects of elevated CO2 on tree growth are constrained by several growth-limiting factors, mainly availability of nutrients and other resources, and the developmental stage (age) of a tree. This thesis for the first time illuminates the current (chapter 2) and future (chapters 3 and 4) C balance of mature evergreen conifers subjected to prospective CO2 levels of 540 ppm in a near-natural forest in Switzerland. Isotopic labeling of fresh assimilates successfully depicted the pathways of C in these trees, thus provided basic insights into how P. abies trees handle the distribution of assimilates. We observed remarkable tree-specific variations in all pre-treatment measurements, emphasizing the importance of recording baseline conditions prior to any experiment. At current CO2 levels, all investigated tissues (except for needles in the sun), and respiratory fluxes depended only partly on new assimilates. The further away from the upper tree canopy, the greater the role of old C stores for new tissue formation and respiration. Since no aboveground growth stimulation was observed (ongoing works) despite higher but transient rates of photosynthesis, and since stem CO2 efflux remained unaffected by elevated CO2, we assume that the extra C assimilated in the first year is dissipated via respiration associated with C turnover (phloem) at rates below detection limit. These processes seem to be too small to be detectable but their accumulated rate along the entire phloem system might account for the unresolved ‘missing C’ at elevated CO2. We found no evidence for increased C investment belowground at elevated CO2 that might also account for some of the higher leaf-level C input at elevated CO2.
References
Körner C (2006) Plant CO2 responses: An issue of definition, time and resource supply. New Phytologist 172:393-411
Norby RJ, Warren JM, Iversen CM, Medlyn BE, McMurtie RE (2010) CO2 enhancement of forest productivity constrained by limited nitrogen availability. Proceedings of the National Academy of Sciences of the United States of America 107:19368-19373.
Norby RJ, Zak DR (2011) Ecological lessons from free-air CO2 enrichment (FACE) experiments. Annual Review of Ecology, Evolution, and Systematics 42:181-203