Download Tracking carbon within the trees

Forum
Commentary
Tracking carbon within the trees
Trees are major players in the cycling of carbon (C) between the
atmosphere and terrestrial biosphere, representing c. 90% of the
world’s biomass C and half of global primary productivity (K€orner,
2003; Beer et al., 2010). Trees take up C through leaf pores (i.e.
stomata) during photosynthesis and convert this C into carbohydrates. These carbohydrates can be stored to support the
maintenance of existing tissues and future growth, or be immediately transported through the tree to form new leaves, woody tissues,
and roots. Within-tree C cycling processes are poorly understood
and are not represented well in current ecosystem C cycling models,
resulting in large uncertainties in the response of tree growth and
whole ecosystem C cycling to future global change (Le Roux et al.,
2001; K€orner, 2003; Millard et al., 2007). In this issue of New
Phytologist, Richardson et al. (pp. 850–861) make substantial
progress in understanding tree growth and within-tree C cycling by
constraining simple hypothesis-driven models with intensive field
measurements of C fluxes, storage pool ages, and stocks. Results
indicated that the average age of carbohydrates was a decade and that
modeled year-to-year variations in tree growth substantially
improved with the incorporation of carbohydrate pools and
reserves. These results have implications for improving tree growth
and ecosystem C cycling models, and understanding whether manmade increases in atmospheric CO2 will stimulate tree growth.
‘… the big within-tree C cycling questions are: how long
are NSC pools physiologically active, and how important
are they for growth and metabolism?’
Nonstructural carbohydrates (NSCs) are the primary class of
carbohydrates used for storage (Chapin et al., 1990; Kozlowski,
1992). Storage of NSCs can be passive, resulting from the
accumulation of photosynthetic C supply when C demand for
growth and maintenance is low, or active, resulting in both
accumulation and the formation of a NSC reserve that occurs at
the expense of growth. Determining which process dominates
has implications for whether trees are C limited under current
atmospheric CO2 concentrations. Proponents of the passive
model argue that NSCs cannot accumulate when growth is C
limited (K€
orner, 2003; Millard et al., 2007), while proponents
of the active model argue that NSC reserve formation can occur
at the expense of growth and has evolutionary advantages by
acting as an emergency reserve during times of stress (Wiley &
No claim to original US government works
New Phytologist Ó 2013 New Phytologist Trust
Helliker, 2012). However, all carbohydrate pools may not be
available for growth (Chapin et al., 1990), and reserve formation may just be a mechanism to avoid down-regulation of
photosynthesis when C demand is low (Millard et al., 2007).
Although views differ in the functional interpretation of NSC
pools, the big within-tree C cycling questions are: how long are
NSC pools physiologically active, and how important are they
for growth and metabolism?
Field studies have demonstrated the importance of storage
reserves for forest C cycling. Eddy covariance-derived gross C
uptake (i.e. photosynthesis) and tree-growth measures are poorly
related at interannual timescales, and suggest that a large carbohydrate pool is decoupling the two processes (Rocha et al., 2006).
Indeed, tree NSC pools have been shown to be large enough to
completely refoliate a tree canopy (W€
urth et al., 2005), while
isotopic labeling studies have demonstrated that remobilization of
late season carbohydrate storage in deciduous trees provides a
substantial amount of C for new leaf growth during the following
spring (Kagawa et al., 2006). Studies have also shown that decade
old C is metabolically available in belowground organs (Vargas
et al., 2009). However, disentangling the relative importance of
newer vs older C for tree growth has been difficult because
assimilation, storage, and accumulation can occur simultaneously
and because there are large uncertainties associated with the degree
of isotopic mixing between current photosynthate, old NSC pools,
and plant tissues (Chapin et al., 1990; Keel et al., 2007).
Richardson et al. provided new insights into within-tree C
cycling processes by directly determining the mean age of the
measured NSC pool, which helped to constrain NSC pool and
tree growth dynamics in later model hypothesis testing. The mean
age of the NSC pool was determined by the carbon-14 (14C)
content of sugars and starches extracted from the outer 2 cm of
stemwood. Atmospheric 14C has declined, as a result of biospheric
uptake and dilution by fossil fuel emissions, since the doubling of
14
C during atmospheric nuclear weapons testing in the 1960s.
This large pulse of atmospheric 14C created a large-scale pulse and
chase experiment in which to track the fate of C through the
biosphere (Trumbore, 2006). Determining the 14C content of
sugars and starch was not a trivial task because previous methods
for NSC extraction required the use of methanol, which would
contaminate the 14C concentration in the sample. To avoid this
issue, Richardson et al. developed 14C extraction techniques that
used water for soluble sugar compounds, and ethanol and
repeated rinsing steps for the insoluble starch compounds. The
authors clearly demonstrate that the results from these new
methods were not influenced by methodological contamination,
agreed well with previously established techniques, and had an
ability to resolve NSC ages within 2 yr.
Once the mean age of the NSC pool was determined, hypothesisdriven modeling exercises were conducted to determine which
New Phytologist (2013) 197: 685–686 685
www.newphytologist.com
686 Forum
New
Phytologist
Commentary
model best matched the observational constraints, including yearto-year dynamics in woody biomass increment. Current ecosystem
and canopy level models poorly capture year-to-year variations in
woody biomass increment, and either ignore or crudely incorporate
NSC dynamics in their framework (Le Roux et al., 2001; Misson,
2004). Richardson et al. employed three simple box models to
determine which processes were required to capture year-to-year
woody biomass increment observations. Models were parameterized with actual measurements of canopy, leaf, and soil CO2 fluxes,
soil C, litterfall, leaf area index, and the age and size of the NSC pool
using Monte Carlo model–data fusion. The first model had no
storage pool and a fixed proportion of photosynthate was
immediately used for growth; a representation that is dominant
in current ecosystem C cycling models. The second model
incorporated one storage reserve and accounted for maintenance
and growth respiration. The third model incorporated two
interacting storage pools with different turnover times (i.e. a ‘fast’
and ‘slow’ storage pool), where the fast C pool fueled growth and
metabolism and the slow pool acted as a storage reserve that filled
the fast pool when it was C deficient. Richardson et al. concluded
that the incorporation of both a fast and slow NSC storage pool
performed best in capturing the size and age of the NSC pool and in
predicting woody biomass increment measurements.
Richardson et al. undoubtedly provides novel and important
insights into tree growth physiology, but also leaves several
unresolved questions for future work. The actual age and size of
the NSC pool was likely underestimated in the study because NSC
in roots, leaves, and deep in the heartwood were not sampled. The
actual mobility of the total NSC pools is also unknown, but
anecdotal evidence suggests that recently assimilated C is used
before old C reserves are drawn upon. In Richardson et al.,
starch and sugars were of similar age, which was unexpected as
starches are considered an immobile long-term storage of NSC
(Chapin et al., 1990; Kozlowski, 1992). Starch accumulates in
parenchyma cells whenever high levels of sugars build up, and can
be remobilized and transported outward toward the cambium
when sugar concentrations are low (Kozlowski, 1992). The age
similarity between sugars and starches indicates regular remobilization and recycling of starches within the tree for growth, and
supports the view that trees are not C limited under current
atmospheric CO2 concentrations.
The implications of the study are far reaching and will result in
new questions in tree physiology and evolution, 14C studies,
ecosystem ecology, and ecosystem C cycle models. With regards to
tree physiology, the study provides a new methodology to
understand carbohydrate pools and improve our understanding
of C starvation and limitation in an environmentally changing
world. These techniques can also be used to improve our
understanding of the evolutionary costs and benefits of C storage
and reserve formation. The study also complicates the interpretation of previous 14C studies that have assumed that the 14C
concentrations in plant or mychorrizal tissues reflect current
photosynthate (Trumbore, 2006). Future studies using 14C will
have to take into account the relative functional roles of new and
stored NSC, intermixing between these old and young pools, and
how they are allocated for growth and metabolism within the plant.
New Phytologist (2013) 197: 685–686
www.newphytologist.com
Lastly, this study demonstrates that incorporating C storage pools
in ecosystem models is critical in predicting woody growth
increment. It remains to be determined if incorporating storage
and reserve pools will better represent tree response to extreme
climatic events or mortality. Understanding these fundamental
processes in tree physiology will improve C cycle models and help
constrain the large uncertainties surrounding the response of the
terrestrial biota to future global change (Friedlingstein et al., 2006).
Adrian V. Rocha1,2
1
Department of Biological Sciences, University of Notre Dame,
Notre Dame, IN, USA;
2
Environmental Change Initiative, University of Notre Dame,
Notre Dame, IN, USA
(tel +1 574 631 6552; email [email protected])
References
Beer C, Reichstein M, Tomelleri E, Ciais P, Jung M, Carvalhais N, Rodenbeck C,
Arain MA, Baldocchi D, Bonan GB et al. 2010. Terrestrial gross carbon dioxide
uptake: global distribution and covariation with climate. Science 329: 834–838.
Chapin FS, Schulze ED, Mooney HA. 1990. The ecology and economics of storage
in plants. Annual Review of Ecology and Systematics 21: 423–447.
Friedlingstein P, Cox P, Betts R, Bopp L, von Bloh W, Brovkin V, Cadule P, Doney
S, Eby M, Fung I et al. 2006. Climate–carbon cycle feedback analysis: results from
the C4MIP model intercomparison. Journal of Climate 19: 3337–3353.
Kagawa A, Sugimoto A, Maximov TC. 2006. Seasonal course of translocation,
storage and remobilization of 13C pulse-labeled photoassimilate in naturally
growing Larix gmelinii saplings. New Phytologist 171: 793–804.
Keel SG, Siegwolf RTW, Jaggi M, K€orner C. 2007. Rapid mixing between old and
new C pools in the canopy of mature forest trees. Plant, Cell & Environment 30:
963–972.
K€orner C. 2003. Carbon limitation in trees. Journal of Ecology 91: 4–17.
Kozlowski TT. 1992. Carbohydrate sources and sinks in woody plants. Botanical
Review 58: 107–222.
Le Roux X, Lacointe A, Escobar-Gutierrez A, Le Dizes S. 2001. Carbon-based
models of individual tree growth: a critical appraisal. Annals of Forest Science 58:
469–506.
Millard P, Sommerkorn M, Grelet G-A. 2007. Environmental change and carbon
limitation in trees: a biochemical, ecophysiological and ecosystem appraisal. New
Phytologist 175: 11–28.
Misson L. 2004. MAIDEN: a model for analyzing ecosystem processes in
dendroecology. Canadian Journal of Forest Research 34: 874–887.
Richardson AD, Carbone MS, Keenan TF, Czimczik CI, Hollinger DY, Murakami
P, Schaberg PG, Xu X. 2013. Seasonal dynamics and age of stemwood
nonstructural carbohydrates in temperate forest trees. New Phytologist 197: 850–861.
Rocha AV, Goulden ML, Dunn AL, Wofsy SC. 2006. On linking interannual tree
ring variability with observations of whole-forest CO2 flux. Global Change Biology
12: 1378–1389.
Trumbore S. 2006. Carbon respired by terrestrial ecosystems – recent progress and
challenges. Global Change Biology 12: 141–153.
Vargas R, Trumbore SE, Allen MF. 2009. Evidence of old carbon used to grow new
fine roots in a tropical forest. New Phytologist 182: 710–718.
Wiley E, Helliker B. 2012. A re-evaluation of carbon storage in trees lends greater
support for carbon limitation to growth. New Phytologist 195: 285–289.
W€
urth MKR, Pelaez-Riedl S, Wright SJ, K€orner C. 2005. Non-structural
carbohydrate pools in a tropical forest. Oecologia 143: 11–24.
Key words: carbon limitation, maintenance and growth respiration, model–data
fusion, net primary productivity, nonstructural carbohydrates, plant ecophysiology,
radiocarbon, tree growth.
No claim to original US government works
New Phytologist Ó 2013 New Phytologist Trust