Tree Physiology 34, 557–563
doi:10.1093/treephys/tpu030
Commentary
Improving modeling of the ‘dark part’ of canopy carbon gain
Ülo Niinemets1,2,3
1Estonian
University of Life Sciences, Kreutzwaldi 1, 51014 Tartu, Estonia; 2Estonian Academy of Sciences, Kohtu 6, 10130 Tallinn, Estonia;
author ([email protected])
3Corresponding
Received March 14, 2014; accepted March 27, 2014; published online May 8, 2014; handling Editor Danielle Way
Simulating canopy photosynthesis: where do we
stand?
Canopy photosynthesis is the integrated contribution of carbon
gains of all leaves forming the canopy. As the simplest form of
integration, canopy photosynthesis is given as the product of
the number of leaves and the average leaf net assimilation rate.
Although numerically correct, such calculation is wholly impractical as typical moderately dense broad-leaved plant stands
contain thousands and conifer stands contain tens to hundreds
of thousands of leaves per m2 ground area. Furthermore, there
are major environmental gradients, in particular, gradients
in light, temperature and humidity, from canopy top to bottom (for reviews, see Valladares 2003, Niinemets and Anten
2009), such that individual leaves are exposed to vastly different environmental conditions.
As the dependencies of foliar physiological characteristics on key environmental drivers, light and temperature, are
strongly non-linear, the correct daily average leaf photosynthesis rate cannot be obtained using daily average values of
environmental drivers (de Pury and Farquhar 1997, Cescatti
and Niinemets 2004, Niinemets and Anten 2009). Thus, first
of all, canopy models need to provide a reliable description
of canopy environmental conditions as the input for photosynthesis algorithms. There has been much progress since
the pioneering study of Monsi and Saeki (1953) introducing the Lambert–Beer model of light absorption to describe
exponential reduction of light availability with cumulative leaf
area index and the Duncan et al. (1967) model including sunlit and shaded leaf area fractions. Currently available modeling schemes can describe the 3D heterogeneity in foliage
distribution and particularly detailed schemes can even characterize the exact position of single foliage elements (Cescatti
1997, Chelle and Andrieu 1998, Disney et al. 2000, Bittner
et al. 2012). Coupled to soil–vegetation–atmosphere transfer
models, it is further possible to predict within-canopy gradients in temperature, humidity and CO2 concentration (e.g.,
Baldocchi et al. 2002, Akkermans et al. 2012).
A further complication in simulating canopy photosynthesis
is that foliar photosynthetic potentials and respiration rates
vary through the canopy as a result of acclimation to variable
within-canopy environmental conditions (Hirose and Werger
1987, Gutschick and Wiegel 1988, Baldocchi and Harley 1995,
Harley and Baldocchi 1995, Lloyd et al. 2010, Niinemets 2012,
Niinemets and Keenan 2012, Peltoniemi et al. 2012). This
variation has been often ignored when simulating vegetation
carbon gain at scales ranging from canopies to the globe, but
canopy-level studies have conclusively demonstrated that such
variations importantly alter whole-canopy carbon gain (e.g., the
classical studies of Hirose and Werger 1987, Gutschick and
Wiegel 1988, Baldocchi and Harley 1995). Furthermore, recent
modeling studies underscore that even world-scale productivity estimates and spatial mapping can be significantly improved
by considering within-canopy variations in foliar photosynthetic
potentials (Friend 2010, Bonan et al. 2011, 2012).
While within-canopy trait variations have been studied for a
number of temperate ecosystems (see Niinemets 2007 for a
review) and incorporated in large-scale models (Bonan et al.
2011, 2012), information on within-canopy gradients in foliar
photosynthetic traits is particularly limited for the tropics (for
a few studies reporting trait gradients for tropical forests, see
Carswell et al. 2000, Kenzo et al. 2006, Cavalieri et al. 2008,
© The Author 2014. Published by Oxford University Press. All rights reserved. For Permissions, please email: [email protected]
558 Niinemets
Lloyd et al. 2010, van de Weg et al. 2012). All global models predict that tropical rain forests constitute the hotspot of
annual primary productivity due to long growing seasons and
dense canopies, although model-to-model variability is large
(Kumagai et al. 2006, Beer et al. 2010, Friend 2010, Bonan
et al. 2011, 2012, Bastos et al. 2013). Overall high potential
productivity estimates associated with current major uncertainties suggest that an improved understanding of leaf trait
variations in tropical ecosystems is of major significance in
improving worldwide productivity estimates. Thus, the study of
Weerasinghe et al. (2014) reporting within-canopy variations
in photosynthetic characteristics in 12 canopy species and 10
understory species for a northeastern Australian lowland tropical rain forest importantly contributes to filling the major gap in
coverage of within-canopy trait variations in the tropics.
In simulating canopy carbon gain, there has been traditionally
much more attention given to carbon gain and much less to carbon loss, although there is a general understanding that respiratory losses of carbon do significantly alter the net canopy carbon
gain (Van Oijen et al. 2010), especially under stress conditions
that strongly curb photosynthesis, but affect much less the respiration rates (Flexas et al. 2005). Furthermore, modeling respiration in canopy photosynthesis schemes is often simplistic, and the
study of Weerasinghe et al. (2014) further makes a general point
that the within-canopy patterns in respiration can be much more
complex than traditionally thought, calling for improved parameterization of respiration in within-canopy modeling schemes.
Consideration of respiration in simulating canopy
photosynthesis
Traditionally, leaf net assimilation rate, An, in canopy models
is simulated according to the Farquhar et al. (1980) steadystate photosynthesis model that considers photosynthesis as
a minimum of the potential rates of ribulose-1,5-bisphosphate
(RuBP) carboxylation determined either by Rubisco in RuBPsaturated conditions (Wc) or by RuBP regeneration in RuBPlimited conditions (Wj):
(
)
An = (1 − Γ * /Cc )min Wc ,Wj − RL ,
(1)
where Cc is the chloroplastic CO2 concentration, RL is the nonphotorespiratory respiration rate during photosynthesis (the
light respiration rate) and Γ * is the chloroplastic CO2 compensation point in the absence of RL. The capacity of Wc is
determined by the maximum carboxylase activity of Rubisco
(Vcmax) and the capacity of Wj is determined by the rate of
photosynthetic electron transport rate (Jmax). Both Vcmax and
Jmax increase with increasing light availability in plant canopies
(for reviews, see Kull 2002, Niinemets 2007), as the study of
Weerasinghe et al. (2014) further demonstrates for the southeastern Australian tropical rain forest (Figure 1a).
Tree Physiology Volume 34, 2014
While the physiological knowledge of variations in Wc
and Wj is relatively mature for reliable incorporation in models (von Caemmerer et al. 2009), the nature of RL is much
Figure 1. ​Average maximum carboxylase activity of Rubisco (Vcmax)
and average daily integrated carbon gain (a), and fraction of daytime (light period) gross carbon gain respired (R L,int/Ag,int, b) in the
lower and the upper canopy and in the understory of a northeastern
Australian lowland tropical rain forest (Daintree Rainforest Observatory
(16°07′S, 145°27′)) simulated using the data of Weerasinghe et al.
(2014) for a representative clear day on 15 September. In the simulations, diurnal variation in above-canopy quantum flux density was
simulated according to Campbell and Norman (1998), while leaf temperature was varied from 19 °C in the morning to 28 °C at mid-day
corresponding to average values of air temperature for the month of
September at Cairns (http://www.weatherzone.com.au). Estimates of
Vcmax were derived from values of net assimilation rate and light respiration (R L) using inverse modeling as in Niinemets et al. (1999),
and correspond to averages for 12 canopy species sampled from both
the lower and the upper canopy and for 10 understory species in the
study of Weerasinghe et al. (2014). In the derivation of Vcmax estimates
and in the photosynthesis simulations, temperature dependencies of
Rubisco kinetic characteristics and Vcmax were from Niinemets and
Tenhunen (1997), and the capacity for photosynthetic electron transport, Jmax, was taken as 2.5Vcmax, while the intercellular CO2 concentration at different canopy positions and the temperature relationships
of the respiration rate were from Weerasinghe et al. (2014). Values of
R L to Vcmax ratio (R L/Vcmax) at 29 °C were derived from the data, and
the simulations were conducted using an average value of R L/Vcmax of
0.0142 (constant R L/Vcmax simulation) and with values of 0.0182 for
the upper canopy, 0.0103 for the lower canopy and 0.0148 for the
understory (variable R L/Vcmax simulation).
Improving modeling of the ‘dark part’ of canopy carbon gain 559
less understood due to difficulties of its estimation in photosynthesizing leaves. As a first approximation, the respiration
rate measured in darkness, RD, is considered as a proxy of
RL (e.g., Lenz et al. 2010, Groenendijk et al. 2011, Smith and
Dukes 2013). Although RL and RD are closely associated, RD
typically becomes inhibited in light (Sharp et al. 1984, Brooks
and Farquhar 1985, Villar et al. 1994, 1995, Atkin et al. 1997,
Pärnik et al. 2007, Weerasinghe et al. 2014):
RL = kRD ,
(2)
where k is the fraction of dark respiration remaining in light.
As the physiological basis of the light inhibition of RD is not
yet fully understood and the values of k have not been routinely estimated, models often use a constant estimate of
k = 0.5 to account for inhibition of RD in light (e.g., Harley and
Tenhunen 1991, Falge et al. 1996, Niinemets and Tenhunen
1997). However, experimental estimates of k vary from ~0.2
to 1.3 across the species and under different environmental
conditions (Brooks and Farquhar 1985, Villar et al. 1994,
1995, Hurry et al. 1996, 2005, Atkin et al. 1997, Tcherkez
et al. 2005, Pärnik et al. 2007, Way and Yamori 2014). It is
currently unclear how large the variability in k can be among
species growing intermixed in the same canopy, and further it
is unknown to what extent k can vary within the canopy of the
same species. In eight rain forest species, Weerasinghe et al.
(2014) observed a range of variation in k of 0.23–0.89 across
species and canopy positions (whole-canopy average of 0.68),
although the within-canopy variation in k was not significant
across the species. Ecosystem-scale estimates demonstrate
that the inhibition of RD during the day can importantly alter
whole-ecosystem carbon balance (Wohlfahrt et al. 2005), and
the large interspecific variability in k observed in Weerasinghe
et al. (2014) underscores the importance of better parameterization of respiration in the photosynthesis models even when
intending to apply the model to any given multispecies forest
stand.
Scaling respiration within the canopy
The important question in simulating canopy photosynthesis is
how to scale RL for different leaves in the canopy? There are
often basic positive interspecific correlations among respiration
rate, leaf nitrogen content and photosynthetic capacity, typically better on a leaf mass than on an area basis (Wright et al.
2004, 2006, Slot et al. 2013, Westoby et al. 2013). These correlations are indicative of greater maintenance requirements,
for example for protein turnover, of physiologically more active
leaves with greater nitrogen contents. There is further a strong
intraspecific variability in RD within the canopy accompanying
photosynthetic acclimation to within-canopy light gradients
(Niinemets et al. 1998, Mitchell et al. 1999, Griffin et al. 2001,
Tissue et al. 2002, Turnbull et al. 2003, Cavalieri et al. 2008,
O’Grady et al. 2008, van de Weg et al. 2012). Differently from
across-species relationships, the within-canopy trait variations
are often stronger on a leaf area basis, reflecting the lightdependent accumulation of biomass with a similar physiological activity per unit leaf area (Niinemets et al. 1998, Mitchell
et al. 1999, Griffin et al. 2001, Cavalieri et al. 2008, van de
Weg et al. 2012).
Different strategies have been employed to incorporate
within-canopy variations in RD in canopy photosynthesis
schemes. Hirose and Werger (1987) have used individual
regressions to link the light-saturated net assimilation rate and
RD to the leaf nitrogen content, and this approach has been
further widely used in modeling canopy photosynthesis (e.g.,
Harley et al. 1992, Anten 1997, Hikosaka and Hirose 1998,
Pons and Anten 2004). On the other hand, given the correlations among photosynthetic and respiratory characteristics,
already classical canopy modeling studies have attempted to
link the leaf respiration rate directly to the assimilation characteristics, initially to gross light-saturated assimilation rate, Ag
(e.g., Tooming 1967):
RD =ηAg ,
(3)
where η is the proportionality factor. As Ag depends on the
availability of CO2 for photosynthesis (Eq. (1)), RD is more frequently linked to Vcmax in contemporary canopy models, i.e.,
RD = κ Vcmax, where κ is another proportionality factor (Amthor
1994, Niinemets and Tenhunen 1997, Niinemets et al. 1998,
Groenendijk et al. 2011).
While linking the respiration rate to leaf photosynthetic
potentials provides a simple means to incorporate respiration
in the Farquhar et al. (1980) photosynthesis model (Eq. (1)),
within-canopy variations in η and κ factors have seldom been
assessed. The study of Weerasinghe et al. (2014) demonstrates that the fraction of carbon gain respired in the upper
canopy was consistently much larger than that respired in the
lower canopy (on average, a 2-fold greater RL/Ag and a 1.8-fold
greater RL/Vcmax in the upper canopy). As leaves in the upper
canopy have higher photosynthetic capacities and intercept
more light, the question is how significant is the within-canopy
variation in RL/Vcmax for daily carbon gain? Indeed, the daily
average RL/Ag ratio increases with decreasing light availability
(Figure 1b), and upper canopy photosynthesis is only moderately affected by within-canopy changes in RL/Vcmax (Figure
1a). However, the simulation analysis suggests that the effects
are particularly relevant for the lower canopy (Figure 1a).
As a result of within-canopy changes in RL/Vcmax, the lowercanopy leaves lose much less of their potential carbon gain
due to respiration than they would have lost for invariable RL/
Vcmax. Similarly to the study of Weerasinghe et al. (2014), RD/
Ag increased from the bottom toward the top of the canopy
Tree Physiology Online at http://www.treephys.oxfordjournals.org
560 Niinemets
in Nothofagus fusca (Hook. f.) Oersted (Griffin et al. 2001)
and in a tropical forest canopy (Cavalieri et al. 2008), and RD/
Ag became large with increasing site nutrient limitations and
site openness along a soil chronosequence in New Zealand
temperate rain forests (Turnbull et al. 2005). However, such
patterns in RD/Ag are not always observed (for qualitatively
different patterns among species, see Niinemets et al. 1998,
Posada et al. 2009).
What can be the physiological basis for disproportionally
larger respiration rates in the upper canopy? First of all, relatively higher respiration rates in the upper canopy can suggest higher rates of protein turnover at the given overall protein
content. Given that leaves in the upper canopy are exposed
to a greater photoinhibition stress (e.g., Niinemets and Kull
2001, Werner et al. 2001a, 2001b), higher protein turnover
can be considered as the price the leaves pay for photosynthesizing at higher light. Alternatively or complementarily to
this hypothesis, the coordination between photosynthetic and
respiratory activities can change depending on respiratory
substrate availability. Leaf sugar concentrations vary during the
day (e.g., Hüve et al. 2006, Lewis et al. 2011, Chi et al. 2013),
and the daily photosynthetic production of leaves at higher
light in the upper canopy is greater than in leaves in the lower
canopy (Figure 1a). In fact, daytime sugar concentrations do
often reach higher values in upper-canopy leaves (Niinemets
1995, Turnbull et al. 2002, Lewis et al. 2011). There is further
evidence that sugar content (Griffin et al. 2001, Tissue et al.
2002, Turnbull et al. 2003) and daytime sugar accumulation
(Lewis et al. 2011) correlate with the respiration rate, but not
always (Chi et al. 2013). Although the respiration rate per area
was correlated with the sugar content per area in the study of
Weerasinghe et al. (2014), the proportionality factor between
respiration and photosynthesis, η (Eq. (3)), was not associated
with sugar content in their study.
Higher respiration rates can also be associated with greater
respiration costs due to active phloem loading as observed in
herbaceous species (Sovonick et al. 1974). However, phloem
loading in woody species is thought to be mainly passive and
is thus driven by sugar concentration gradients between mesophyll cells and phloem cells (Turgeon and Wolf 2009, Turgeon
2010, De Schepper et al. 2013), although there seems to be
a continuous evolutionary spectrum in phloem structure and
function across plant functional types (Gamalei 1989, 1991,
Turgeon et al. 2001). Nevertheless, intermediary, companion
and transfer cells of phloem are entirely or partly heterotrophic (e.g., see Voitsekhovskaja et al. 2006 for evidence of the
presence of leucoplasts rather than chloroplasts in companion
cells), and greater sugar concentrations in higher light conditions are expected to support higher respiration rates in these
cells. Furthermore, it has been demonstrated that increases in
light availability are associated with a greater density of minor
veins and a greater number of sieve elements and support cells
Tree Physiology Volume 34, 2014
within veins (Adams et al. 2013, 2014), further possibly increasing the respiratory activity of phloem tissues. Clearly, more data
are needed on the respiratory activity of phloem and on how
the phloem respiratory activity is regulated by sugar concentration in tree species with predominantly passive phloem loading.
In contrast to the hypothesis of sugar control of respiration,
there is experimental evidence indicating that glycolysis and the
use of glucose in respiration become strongly inhibited in light
(Tcherkez et al. 2005). In fact, chloroplastic pyruvate decarboxylation may dominate the respiratory fluxes in light (Tcherkez
et al. 2005, 2012). If so, this could explain the relatively higher
RL in the upper canopy where pyruvate availability is likely
higher. Application of isotopic techniques (Pärnik et al. 2007,
Hüve et al. 2012, Tcherkez et al. 2012) might allow insight to be
gained into within-canopy variations in respiratory metabolism.
In summary, the study of Weerasinghe et al. (2014) highlights several important understudied aspects of canopy carbon gain. Clearly, more experimental work is needed to gain
insight into the mechanisms and the overall range of variation
of within-canopy gradients in RL/RD and RL/Vcmax. While consideration of respiration in the canopy models has been intuitively
simple, such simple modeling strategies do not do justice to
the observed within-canopy variations in respiratory carbon
fluxes in vegetation.
Conflict of interest
None declared.
Funding
Author’s work on plant biology is supported by the Estonian
Ministry of Science and Education (institutional grant IUT-8-3),
and the European Commission through the European Regional
Fund (Center of Excellence in Environmental Adaptation).
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