Tree Physiology 32, 303–312
doi:10.1093/treephys/tps008
Research paper
Patterns of root respiration rates and morphological traits in
13 tree species in a tropical forest
Naoki Makita1,5, Yoshiko Kosugi1, Masako Dannoura1, Satoru Takanashi2, Kaoru Niiyama3,
Abd Rahman Kassim4 and Abdul Rahim Nik4
1Graduate
School of Agriculture, Kyoto University, Kyoto 606-8502, Japan; 2Forestry and Forest Products Research Institute, Ibaraki 305-8687, Japan; 3Tohoku Research
Center, Forestry and Forest Products Research Institute, Morioka 020-0123, Japan; 4Forest Research Institute Malaysia, Kepong, Kuala Lumpur 52109, Malaysia;
5Corresponding author ([email protected])
Received October 11, 2011; accepted January 12, 2012; published online Feburary 23, 2012; handling Editor Douglas Sprugel
The root systems of forest trees are composed of different diameters and heterogeneous physiological traits. However, the
pattern of root respiration rates from finer and coarser roots across various tropical species remains unknown. To clarify how
respiration is related to the morphological traits of roots, we evaluated specific root respiration and its relationships to mean
root diameter (D) of various diameter and root tissue density (RTD; root mass per unit root volume; g cm−3) and specific root
length (SRL; root length per unit root mass; m g−1) of the fine roots among and within 14 trees of 13 species from a primary
tropical rainforest in the Pasoh Forest Reserve in Peninsular Malaysia. Coarse root (2–269 mm) respiration rates increased
with decreasing D, resulting in significant relationships between root respiration and diameter across species. A model based
on a radial gradient of respiration rates of coarse roots simulated the exponential decrease in respiration with diameter. The
respiration rate of fine roots (<2 mm) was much higher and more variable than those of larger diameter roots. For fine roots,
the mean respiration rates for each species increased with decreasing D. The respiration rates of fine roots declined markedly
with increasing RTD and increased with increasing SRL, which explained a significant portion of the variation in the respiration among the 14 trees from 13 species examined. Our results indicate that coarse root respiration in tree species follows a
basic relationship with D across species and that most of the variation in fine root respiration among species is explained by
D, RTD and SRL. We found that the relationship between root respiration and morphological traits provides a quantitative
basis for separating fine roots from coarse roots and that the pattern holds across different species.
Keywords: coarse root, diameter, fine root, primary tropical rain forest, root CO2 efflux, specific root length, tissue density.
Introduction
Tropical forests play an important role in the global carbon (C)
balance, providing approximately half of total terrestrial C production (Houghton 2003, Grace 2004) and representing a
large fraction of the C stock in the terrestrial biosphere (Bonan
2008). There is growing evidence that changes in structural
and functional traits in temperate woody species can affect the
role of the forests as C sinks or sources (Clark 2004). While
the last decade has seen many studies of aboveground traits in
tropical forests (e.g., Reich and Oleksyn 2004, Wright et al.
2004), less is known about the functions and ecosystem consequences of belowground traits related to C sinks or sources
in the forest (e.g., Jackson et al. 1996, Finer et al. 2011). Tree
roots constitute a large fraction of annual net primary production, resulting in a large flux of C and nutrients into the belowground system (Vogt et al. 1996, Högberg and Read 2006).
Root respiration is a major source of CO2 efflux from forest
soils. The contribution of root respiration to total soil respiration ranges from one-third to more than one-half in tropical
© The Author 2012. Published by Oxford University Press. All rights reserved. For Permissions, please email: [email protected]
304 Makita et al.
forests (Hanson et al. 2000, Epron et al. 2001, Bond-Lamberty
et al. 2004). Therefore, knowledge of root respiration in tropical forests is essential for a detailed understanding of the roles
of roots in the C economy of individual trees and the forest
ecosystem as a whole.
The root systems of forest trees are composed of roots of
different diameters and heterogeneous physiological traits and
physical functions. There is now considerable evidence that
root diameter influences respiration (Pregitzer et al. 1998,
Marsden et al. 2008, Makita et al. 2009, Chen et al. 2010). For
most plants, thinner roots are more efficient than larger roots
for water and nutrient uptake, whereas larger roots have higher
transport capacities for water and nutrients because the stele
diameter increases with root diameter (Eissenstat 1992, de
Kroon and Visser 2003). Root diameter is associated with cell
size in the cortex and with thickness of secondary walls in the
exodermis. However, current understanding of the patterns
and controls of root respiration from finer roots to coarser
roots is limited. Furthermore, data on respiration in very fine
roots (<0.5 mm in the diameter) and very large roots (e.g.,
>10 mm in diameter) are limited because no regular chamber
can accurately measure the respiration rates of both small and
large roots.
Comas et al. (2002) reported that the respiration of finer
roots varied among species of temperate tree species but
there were no differences among species for coarser roots.
Makita et al. (2009) showed that root respiration of Quercus
serrata in broad-leaved forests increased with decreasing
root diameter even within 2 mm, suggesting that the differences in developmental process of the root tissues from primary to secondary tissues are affected to the respiration
rates. Thus, the decrease in respiration rate with increasing
diameter would be related to anatomical tissue traits, such as
the deterioration of living parenchymal cortical cells, and the
increase in proportion of dead secondary tissues with individual root age. Given that fine roots and coarse roots have
quite different functional traits, are there different anatomical
relationships with respiration between fine roots and coarse
roots? To answer our question, we applied the model of
Marsden et al. (2008), which is based on the idea that the
respiration rate of root tissues decreases exponentially from
the external part of the root to the central part of the root. If
there is a high correlation between the estimated and measured respiration rates for coarse roots, coarse root respiration will be explained by anatomical tissue traits. In addition,
if the measured respiration rate of fine roots is different from
the estimated respiration rate of fine roots using the model
fitted to the data from coarse roots, fine root respiration will
be explained not only by the proportion of living and dead
tissues of roots but also by the energy requirements of living
cells with high respiration for maintenance, growth and nutrient uptake.
Tree Physiology Volume 32, 2012
The respiration of fine roots (generally defined as <2 mm in
diameter) in forests is metabolically more active and has been
estimated to be higher than that of coarse roots (Pregitzer
et al. 1998, Marsden et al. 2008), although fine root respiration can be highly variable (Makita et al. 2009). Recent studies
have shown that fine root systems are composed of individual
roots with heterogeneous morphological traits and physiological functions (Eissenstat et al. 2000, Pregitzer et al. 2002). To
explain the high variability in respiration within fine roots, it is
necessary to focus on the relationship of respiration with diameter within the <2 mm size class. It is also necessary to determine how the respiration rates of fine roots vary with tissue
density (RTD; g cm−3). Wood tissue density, supported by
broad examinations of stems and branches, partly reflects the
trade-off between growth and survival (Kitajima 1994, Poorter
and Bongers 2006). The tissue density has been related to
growth rate, water storage, mechanical strength and hydraulic
transport efficiency, as well as the resistance against physical
damage by herbivory and pathogens (Jacobsen et al. 2007,
Sperry et al. 2008, Chave et al. 2009). Although it has been
long recognized that the tissue density plays an important role
in the function of individual plants, many questions have
remained unanswered about belowground traits which exhibit
similar associations as those found in aboveground traits
(Comas and Eissenstat 2004, Westoby and Wright 2006). In
addition, there is currently little understanding of RTD variation
and its effects on root respiration rates. Root tissue density is
likely to face physiological and defensive trade-offs that reflect
species-specific traits. An understanding of the relationships
between RTD and root respiration among tree species would
enable a general assessment of root traits across species differences and allow more accurate estimation of stand level root
respiration.
Most studies of the relationships between physiological and
morphological traits of fine roots have focused on individual
species and have generally reported similar patterns in their
relationships. For example, respiration rates tend to be positively correlated with specific root length (SRL) of fine roots
(Reich et al. 1998, Tjoelker et al. 2005, Makita et al. 2009).
Despite the important implications for both morphological and
physiological traits, this general relationship is yet to be evaluated for a large number of species. That is, whether there is
indeed a consistent correlation both within and among species
has yet to be confirmed. We hypothesize that inter-specific proportional relationships between physiology and morphology of
root traits will be quantitatively similar among diverse species,
supporting the idea of convergent evolution. These relationships will be helpful for the evaluation of the root respiration at
the stand scale, because it is difficult in many cases to identify
the roots of each species in mixed tropical forest. If we are able
to use physiological and morphological traits beyond species,
root respiration could be more easily and quickly scaled up to
Root respiration and morphology in a tropical forest 305
the forest stand level using the proportions of each root biomass distribution.
Here, we attempted to clarify the species-specific respiration
rates of fine roots (<2 mm diameter) and coarse roots
(2–269 mm diameter) of 13 evergreen broad-leaved species in
14 trees differing in tree height and age in a primary tropical
rainforest in the Pasoh Forest Reserve, Peninsular Malaysia,
Southeast Asia. The variability in respiration rates was examined in relation to mean root diameter (D; mm) of various diameters and the RTD and SRL of fine roots. To accurately measure
the respiration rates of very fine roots and very large roots, nine
sizes of chambers specific to a variety of root sizes were prepared. This study addressed the following three questions: (i) Is
there a strong relationship across species between coarse root
respiration rates and D that follows a model based on an idea
that the coarse root respiration rate decreases e­xponentially
from the external part to the central part? (ii) How do morphological traits, including D, RTD and SRL, determine the respiration rates of fine roots? (iii) Do the relationships between root
respiration and morphological traits exhibit common patterns
across species?
Materials and methods
Study site
The study site was located in the Pasoh Forest Reserve
(2°58′N and 102°18′E, 75–150 m a.s.l.) of the Forest Research
Institute of Malaysia in Peninsular Malaysia. This forest is a lowland mixed tropical rain forest consisting of various taxa:
Shorea spp., Dipterocarpus spp. and Leguminosae spp.
(Manokaran and Kochummern 1993, Niiyama et al. 2010). The
mean leaf area index was estimated to be 6.52 from tree diameter observations. The annual rainfall is ~1800 mm (Kosugi
et al. 2008). Soil temperature at a depth of 2 cm was measured continuously near the tower site with three thermistors
(model 107, Campbell Scientific, Inc., Logan, UT, USA). The
7-year average and standard deviation of daily mean soil temperature was 24.9 ± 0.5 °C (data for 2003–09). The major soil
type at the study site is Ultisol; its fertility is generally low and
the humus layer is thin (0–5 cm) (Yamashita et al. 2003). In
the core area (600 ha) of the reserve (2450 ha), micrometeorological and H2O/CO2 flux data were collected at an observation tower (Kosugi et al. 2008, Takanashi et al. 2010). To
compare the net ecosystem exchange estimated using the
eddy covariance method, CO2 and H2O exchanges of leaves
(Yoda 1978, 1983, Takanashi et al. 2006, Kosugi et al. 2009),
stem CO2 efflux (Yoda 1978, 1983) and soil CO2 efflux (Kosugi
et al. 2007) were previously evaluated at this site. The aboveground and belowground biomasses at the site were estimated
to be 95.9 and 536 Mg ha−1, respectively, from 121 tree census data of 78 species of various sizes (Niiyama et al. 2010).
We investigated four permanent research plots (each
20 × 100 m) established by Niiyama et al. (2010). In each plot,
the size parameters of all living trees (stem diameter at breast
height, DBH >5 cm) were measured in 2009. We selected 14
trees of 13 evergreen broad-leaved species within four plots
with DBH ranging from 0.9 to 29.1 cm and tree height ranging
from 1.8 to 32.0 m (Table 1). The selected species represented a broad range of taxa of the most common woody species in the forests.
Measurements of root respiration
Root sampling was conducted from 31 January to 6 February
2010. The coefficient of variation for mean solar radiation, soil
temperature and soil water content during the each day from
31 January to 6 February were 14, 1 and 2%, respectively, and
did not differ significantly among the days the root samplings
were conducted. We excavated the entire root system of each
tree using a power shovel and then manual shovel. Root samples of each species were identified based on their location of
attachment to larger roots and the appearance of diameter,
branching pattern, color and texture of the root bark or epidermis. The entire root system was carefully isolated from the soil
and organic matter to ensure that it was not damaged and
remained attached to larger roots. It was gently washed with
tap and deionized water to remove the soil.
The entire root system was then divided by diameter class to
separate roots into their respective size classes. We firstly classified small roots (containing an intact network of root segments comprised primarily of first-, second- and third-order
roots; see Pregitzer et al. 2002) and large roots based on
diameter size. For small roots, one thickest point of the segment was excised for measuring root respiration. For large
roots, the samples were cut into lengths of 10–15 cm. The
excised point of the root segment was sealed with silicone and
polyethylene film to reduce the influence of root excision and
wound respiration.
The root respiration rate was measured using a closed
dynamic chamber system equipped with an infrared gas analyzer (IRGA: LI-840, LI-COR, Lincoln, NE, USA) immediately after
sampling a root in the early afternoon (12:00–16:00) in the field.
The most suitable chamber was selected from nine size patterns
(volume = 0.12, 0.21, 0.34, 0.48, 0.94, 1.45, 2.17, 11.60, or
22.50 l) to measure the respiration rates of small roots and
larger roots. We enclosed a root sample in the chamber and
measured CO2 concentration in the chamber for 180 s. During
the time of measurement, a lid of the chamber was sealed by a
rubber and closed with four locks (up, down, left and right), not
allowing air to pass in or out. The air was circulated in a loop
between the chamber and an IRGA within the system at a flow
rate of 1.0 l min−1 using a pump (MP-15CF, Shibata, Tokyo,
Japan). In a closed dynamic chamber, root respiration rate was
calculated from the slope of the CO2 ­
concentration increase
Tree Physiology Online at http://www.treephys.oxfordjournals.org
306 Makita et al.
Table 1. ​Characteristics of the 14 evergreen broad-leaved trees that were evaluated for root traits. The DBH and tree height were measured
directly for each tree on the harvesting day during the first week of February 2010.
Species name
Shorea acuminata Dyer
Shorea leprosula Miq.
Hypobathrum racemosum (Roxb.) Kurz
Shorea multiflora (Burck) Sym.
Pentaspadon motleyi Hook.f.
Aporosa bracteosa P. & H.
Blumeodendron tokbrai (Bl.) J.J.Smith
Anaxagorea javanica Bl.
Galearia maingayi Hook.f.
Aglaia odoratissima Bl.
Dacryodes rugosa (Bl.) H.J. Lam
Aglaia exstipulata (Griff.) Theob.
Shorea multiflora (Burck) Sym.
Sterculia macrophylla Vent.
Abbreviation
SA
SL
HR
SM1
PM
AB
BT
AJ
GM
AO
DR
AE
SM2
StM
Family
DBH (cm)
Dipterocarpaceae
Dipterocarpaceae
Rubiaceae
Dipterocarpaceae
Anacardiaceae
Euphorbiaceae
Euphorbiaceae
Annonaceae
Pandaceae
Meliaceae
Burseraceae
Meliaceae
Dipterocarpaceae
Dipterocarpaceae
29.1
25.6
18.9
16.7
9.2
8.5
5.7
3
1.6
1.4
1.2
1.1
0.9
0.9
Tree height (m)
29.7
32
23.7
20.2
16.5
13.5
10
5.9
3.1
3.3
1.8
2.8
1.9
1.6
Number of root samples
Fine root
Coarse root
27
23
20
9
11
9
6
5
3
4
3
3
3
3
33
27
19
21
11
11
5
6
7
6
6
7
5
7
l­inearly within the chamber. The temperature of the roots was
directly measured with a copper constantan thermocouple.
These procedures were repeated for 300 samples from 14
trees. Root respiration rates were expressed on a mass basis
(nmol CO2 g−1 s−1) by the dry mass of the sample.
Following the respiration measurements, samples of coarse
roots were immediately measured for morphological traits. The
fine root samples were wrapped in moistened tissue paper,
placed on ice and transported within hours to the laboratory
for morphological analysis.
data to mean soil temperature (25 °C) in the field, we used a
fixed Q10 temperature coefficient, defined as the proportional
increase in root respiration for each 10 °C rise in temperature.
At the biochemical level, the measured Q10 for root respiration
is usually ~2.0 (Luo and Zhou 2006); therefore, this value was
used for all data. By normalizing all the respiration data with
Q10, the simulated respirations at 25 °C were 74.0 ± 5.6%
(mean ± SD; n = 300) of measured respiration rates in the
field.
Measurements of root morphology
To determine whether there are different anatomical relationships with respiration between fine roots and coarse roots, we
applied the model of Marsden et al. (2008), which is based
on the idea that the respiration rate of root tissues decreases
exponentially from the external part of the root to the central
part of the root. The following model relating coarse root respiration per dry weight to D was fitted to the experimental
data:
Root morphological traits (RTD (g cm−3) and SRL (m g−1) of fine
root samples and D (mm) of all samples) were measured for
the same samples used for the respiration analysis. The root
volume, length and mean diameter of small root samples were
determined using WinRHIZO Pro 2007a (Regent Instruments,
Quebec, Canada), which is an image analysis system specifically designed for root measurement. The diameter of each end
of the large root samples was estimated as the mean of two
measurements using a vernier scale and ruler. After measuring
the morphological traits, all root segments were dried at 70 °C
for 48 h and weighed. RTD, SRL and D from the total root volume, length and dry mass of the samples were calculated.
Temperature sensitivity; Q10 value
Because it was difficult to control the temperature of our
­measurement chambers in the field, the temperatures of the
sample roots varied (29.4 ± 1.1 °C (mean ± SD); n = 300).
­
Temperature changes result in an immediate change in respiration rates by a direct effect on enzyme activity, so that it is
important to normalize the respiration rates at field temperature for comparing all root samples. To normalize the r­ espiration
Tree Physiology Volume 32, 2012
Model of coarse root respiration
α

2
D
 ( − k( D /2))

R = Rm  2
+ k − 1  (1)
2 e
2

 k (D / 2) 
where R represents the respiration rate on a measured
weight basis, Rm (nmol CO2 g−1 s−1) is the maximum respiration rate, i.e., the respiration rate of the tissues containing the
highest proportions of living cells, supposedly localized close
to the surface, k is the exponential coefficient (mm−1) and α is
an empirical power coefficient. These parameters in the model
were fitted based on the data. Marsden et al. (2008) have
provided detailed information regarding this model. The fit
was performed using the IGOR Pro6.0 (Wave Metrics, Inc.,
Root respiration and morphology in a tropical forest 307
Lake Oswego, OR, USA) function, which estimates the coefficients of a non-linear regression using least-squares
estimation.
value of the k parameter was 8.3 mm−1 and the corresponding
value of Rm was 16 nmol g−1 s−1.
Data analysis
The range in D for the 129 fine root samples (D < 2 mm) from
the 14 trees used for measurement was 0.23–2.0 mm. The
fine root respiration rates varied widely from 0.52 to 24 nmol
CO2 g−1 s−1.
When the model (Eq. (1)) was fitted to the data from coarse
roots, the measured respiration rate of fine roots was higher
than the estimated respiration rate of fine roots (Figure 1). For
roots <2 mm, there was a significant power relationship
between D and the respiration of every fine root sample
(r = 0.75, P < 0.001, n = 129; Figure 2a) and of the mean for
each species (r = 0.78, P < 0.01, n = 14; Figure 2b). Fine root
respiration rates increased with decreasing D.
The mean RTD of fine roots for each species ranged from
0.26 to 0.73 g cm−3. The mean SRL of fine roots for each
­species ranged from 0.55 to 29 m g−1. When pooling data for
every fine root sample and averaging the data for each
­species, there was a significant correlation between the
­respiration rate and RTD or SRL (Figures 3a, b, and 4a, b). The
respiration rates of fine roots declined markedly with increasing RTD for every fine root sample (r = −0.73, P < 0.001,
n = 129; Figure 3a) and across the 14 trees (r = −0.68,
P < 0.01, n = 14; Figure 3b). The SRL was used to evaluate
whether fine root respiration rates were significantly related to
combinations of D and RTD. There was a clear increase in the
respiration rates with increased SRL that explained a significant portion of the variation in respiration for every fine root
sample (r = 0.58, P < 0.001, n = 129; Figure 4a) and across
the 14 trees (r = 0.73, P < 0.01, n = 14; Figure 4b).
The D, RTD and SRL of fine roots explained a high proportion of the variability in the specific rates of fine root respiration
among all sampled species in the forest.
The relationships between morphological traits (D, RTD and
SRL) and root respiration rates were examined by regression
analysis. Exponential and power equations have been used to
describe the relationship between D and the respiration rate of
fine roots. To evaluate the relationship between D and the respiration rate of fine roots, we chose to fit the power relationship because it had the highest r 2 value. The relationships
between RTD and SRL and the respiration rate of fine roots
were examined by linear regression analysis. The D, RTD and
SRL of fine roots in each species were calculated by pooling
data for every fine root sample and also by averaging the data
for each species.
Results
Coarse root respiration
The range in D of 171 coarse root samples (D > 2 mm) in the
14 measured trees was 2–269 mm. Coarse root respiration
rates per dry weight ranged from 0.025 to 5.6 nmol CO2 g−1 s−1
(Figure 1). Root respiration rates increased markedly with
decreasing D, suggesting that the smaller roots had higher respiration rates than the larger roots. For coarse roots, we found
a strong relationship between the respiration and D of coarse
roots and a good fit of Eq. (1), which explained 53% of the
observed variability. The parameter α was 0.95, the estimated
Fine root respiration
Discussion
Figure 1. ​Relationships between mean root respiration rate per dry
weight at a reference temperature of 25 °C. Open circles (n = 129)
show roots <2 mm in diameter, and closed gray circles (n = 171) show
roots 2–264 mm in diameter. The solid line represents the fit of the
Marsden model (Eq. (1)) data for roots of 2–264 mm (roots <2 mm
excluded) that were pooled across 14 tropical trees of 13 species.
Our results demonstrate that root respiration rates are determined by root morphological traits in tropical rain forests.
Specifically, the respiration rates increased significantly with
decreasing root diameter size (Figure 1). The range and consistency of the respiration rates in this study were in ­accordance
with several previous studies (Desrochers et al. 2002, Burton
and Pregitzer 2003, Marsden et al. 2008, Makita et al. 2009,
Chen et al. 2010).
When the model (Eq. (1)) was fitted to the data from the
coarse roots (>2 mm), the measured respiration rates of the
coarse roots agreed with the estimated respiration rates with
mean root diameter >2 mm. This suggests that coarse root
respiration rates followed the same pattern as a function of
the diameter in all species examined. Previous studies also
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308 Makita et al.
Figure 2. ​Relationship between fine root respiration rate and mean root diameter (D) in 14 tropical trees of 13 species in Malaysia. Species abbreviations are as in Table 1. (a) Each point represents an individual fine root sample. (b) Each point is a mean value (± standard error) for samples
within a tree. The regression line shows the respiration–D relationship (a: r = 0.75, P < 0.001, n = 129., b: r = 0.78, P < 0.01, n = 14).
Figure 3. ​Comparison of fine root respiration rate per weight for 14 tropical trees of 13 species in relation to root tissue density (RTD). Species
abbreviations are as in Table 1. (a) Each point represents an individual fine root sample. (b) Each point is a mean value (± standard error) for
samples within a tree. The regression line shows the respiration–RTD relationship (a: r = −0.73, P < 0.001, n = 129., b: r = −0.68, P < 0.01, n = 14).
Figure 4. ​Relationship between fine root respiration rate and specific root length (SRL) in 14 tropical trees of 13 species in Malaysia. Species
abbreviations are as in Table 1. (a) Each point represents an individual fine root sample. (b) Each point is a mean value (± standard error) for
samples within a tree. The regression line shows the respiration–SRL relationship (a: r = 0.58, P < 0.001, n = 129., b: r = 0.73, P < 0.01, n = 14).
reported a decreasing exponential relationship between root
respiration and diameter for coarse root samples (Yoda 1978,
1983, Ryan et al. 1996, Marsden et al. 2008, Chen et al.
Tree Physiology Volume 32, 2012
2010). In addition, CO2 efflux from a stem segment also
showed a negative relationship with diameter and was closely
related to the respiration rate of the living tissues (phloem,
Root respiration and morphology in a tropical forest 309
cambium and xylem) in the segment (Ceschia et al. 2002,
Cernusak et al. 2006, Kim et al. 2007). Levy and Jarvis (1998)
suggested that the stem respiration rate is mainly due to tissues located close to the stem surface. This implies that the
distribution of living tissues may partly explain the radial variations in the respiration rates and that the respiratory potential
decreased from the inner bark to the sapwood and the heartwood (Ceschia et al. 2002, Spicer and Holbrook 2007).
Because roots with secondary radial development are similar
in stem anatomical structure, most of the large diameter roots
of tropical trees are comprised of dead tissue and most of
their living tissue is in the few outer rings of root anatomical
structure. Thus, the coarse roots might show an exponential
decrease in the proportion of living tissues with increasing
root diameter, resulting in exponential decrease in the root
respiration from the external part to the central part of coarse
roots.
We found a high correlation between the estimated and
measured respiration rates for coarse roots. Conversely, when
the model (Eq. (1)) was fitted to the data from coarse roots,
the measured respiration rate of fine roots was higher than the
estimated respiration rate of fine roots (Figure 1). Although
leaves and branches are viewed as different functional groups,
the functional groups within roots are not well understood
(Pregitzer et al. 1998, 2002). This result suggests that fine
roots, which appear to be analogous to leaves, have additional
different functions than coarse roots.
Coarse roots of forest trees have higher transport capacities
for water and nutrients, whereas fine roots perform important
physiological functions including water and nutrient uptake and
synthesis of certain growth hormones (de Kroon and Visser
2003). Despite the widespread recognition that the functional
role of fine roots and coarse roots differs, few studies have
quantitatively compared the respiration rates between fine and
coarse roots (Comas et al. 2002). Our results suggest that respiration from fine roots is higher than that from coarse roots,
and that estimations of fine root respiration are not directly
applicable to models of coarse root respiration (Figure 1). The
comparison between respiration rates and diameter using the
model in this study explains not only the differences in proportions of living and dead tissue of the coarse roots but also the
specific functional role of fine roots, because the main tissues
in the cortical cells and vascular cylinder of roots in primary
growth are living cells with a high respiration for maintenance,
growth and nutrient uptake (Evert 2006).
Fine root respiration rates were highly variable among the
14 trees of 13 woody species examined from the tropical rain
forest. However, the respiration rates were dependent on root
diameter within 2.0 mm. Our detailed measurements of diameter of fine root segments revealed a strong relationship
between D and respiration rate (Figure 2a and b). The respiration rates of the root segments <1.0 mm in diameter were sub-
stantially higher than those of larger diameter roots. Additionally,
the respiration rates were more highly variable for roots
<1.0 mm than for those of larger diameters. Our results showed
that cut-off for ‘fine roots’ should be categorized <1.0 mm in
diameter in this study, but the diameter should not be considered at all for what are truly ‘fine roots’ as a functional category. These findings suggest that fine roots should be evaluated
based on not only diameter but also other morphological traits,
such as RTD and SRL, which indicate the physiological function
of roots (Eissenstat et al. 2000, Pregitzer et al. 2002, Makita
et al. 2009).
We found high RTDs under conditions of relatively low respiration rates, whereas lower RTDs occurred at relatively high
respiration rates (Figure 3a and b). We determined that most of
the variation in fine root respiration among species in the forest
was highly explained by RTD. This pattern is consistent with
that of stem and branch respiration (Ceschia et al. 2002,
Cernusak et al. 2006, Kim et al. 2007).
Wood tissue density is a key functional trait of tree species
and reflects characteristics of life history. For example, longlived climax species tend to have high wood density, while
pioneer species have low wood density (Muller-Landau 2004,
Chave et al. 2009). Each tree species has developed specific
strategies to alter the tissue density; i.e., an increase in tissue
density provides benefits of greater strength but requires
higher construction costs and slower growth. Larjavaara and
Muller-Landau (2010) recently reported that tissue density is
interconnected with the maintenance cost of woody maintenance respiration. They showed that high wood density is
associated with lower maintenance costs of respiration due to
lower trunk surface area, given that trunk surface area correlates with stem maintenance respiration. This advantage could
explain why the fine roots, which exhibit lower respiration
rates, show high tissue density. It is clear that variations in
RTD could have consequences for the hydraulic, mechanical
and physiological performance of a tree, which may explain
how root anatomical development alters root respiration.
We also found a strong positive correlation between SRL and
fine root respiration (Figure 4a and b), in agreement with the
results of several previous studies (Tjoelker et al. 2005, Makita
et al. 2009). Specific root length is a complex parameter that
includes variations in D and RTD. The composite response of
mean D and RTD in different species with differing anatomical
traits and environmental stresses can reflect SRL values. It
appears that the SRL is closely correlated with species-specific
traits, such as different strategies of nutrient acquisition,
metabolism capacity, nutrient absorption and growth (Ryan
et al. 1996, Pregitzer et al. 1998, Comas et al. 2002). Comas
and Eissenstat (2004) showed that the SRL in 11 temperate
tree species of differing potential growth rates was higher in
fast-growing than in slow-growing species. Therefore, the variation in respiration rates of fine roots might reflect different
Tree Physiology Online at http://www.treephys.oxfordjournals.org
310 Makita et al.
growth strategies among species, which could have specieslevel effects on C and nutrient cycling. The finding that SRL is
strongly correlated with root respiration supports that root
morphology reflects physiological function (Eissenstat et al.
2000, Makita et al. 2009). Thus, SRL appears to be an important morphological parameter for evaluating fine root
respiration.
Although our results indicated that morphological traits
explain the variation in root respiration rate, other factors also
affect root respiration rates. For example, the contribution of
individual sources to root respiration varies strongly, depending on biotic factors (tree species, root age, tissue nitrogen
concentration and total non-structural C concentration) and
abiotic factors (temperature, soil water content, solar radiation
and season) (Moyano et al. 2009). Moreover, the metabolism
of C by leaves has been suspected to affect root respiration
rates (Högberg and Read 2006, Kuzyakov and Gavrichkova
2010). In terrestrial ecosystems, C assimilated by photosynthesis is generally allocated to plant organs, where it can be
used as building material for structural biomass and storage
or as substrate for autotrophic respiration. As result, photosynthetic activity supplying carbohydrates from leaves to roots
via the phloem is a key driver of root respiration (Högberg and
Read 2006, Mencuccini and Hölttä 2010). In our study, the
respiration rates were measured during daytime (12:00–
16:00) in the field, so that the photosynthetic activity and
other biotic and abiotic factors might affect the levels of root
respiration. Although the root samples in our study were taken
in similar weather conditions and times during the measurement periods, the effects of different measurement days and
times on the variation of root respiration remain an open question. If specific root respiration rate based on morphological
traits is considered in combination with other biotic and abiotic factors, we can evaluate real root respiration rates through
the above- and belowground continuum. These results would
provide more precise scaling-up values of root respiration and
could help to explain spatial and temporal variation in soil
respiration.
Our hypothesis was that relationships between physiological and morphological traits will be quantitatively similar
among diverse species. This proved to be true. Our findings
provide evidence of the generality and specificity of root respiration from very fine roots to coarse roots in relation to
their ­
morphological traits across species. Examining root
respiration is a time consuming and difficult endeavor
because it requires excavating and identifying the roots of
each species in mixed tropical forest. In practice, if it is possible to use physiological and morphological traits beyond
species, root respiration could be more easily and quickly
scaled up to the forest stand level, such as by using the proportions of root biomass distributions for fine and coarse
roots in the field. Understanding the relationships between
Tree Physiology Volume 32, 2012
the respiration rates and morphological traits of roots in a
wide variety of tropical forest species has critical implications. For example, it provides a quantitative basis for separating fine roots from coarse roots, and for evaluating
patterns of species differences. Overall, we propose to combine the respiration rates and morphological traits of roots
separated into detailed diameter size classes, linking with
accurate and consistent estimates of belowground C effluxes.
In particular, for fine roots, the relationship between tissue
density and respiration should be incorporated to gain
insight into the physiological and ecological variations among
species, including growth rates, successional position and
whole-plant life strategies. Knowledge of the relationships
between respiration and morphological traits is necessary to
further improve our understanding of belowground C cycling
in terrestrial ecosystems.
Acknowledgments
We gratefully acknowledge the staffs of the Pasoh Station of
Forest Research Institute, Malaysia, for helping with field
observations. Dr Katsunori Tanaka and Mr Syuuhei-Woods
Kanemitsu helped wash roots and measure root respiration in
the field. We also thank Mr Takehiko Haruta, Dr Shoji Noguchi
and Dr Tamon Yamashita for their valuable help in the field and
the editor and two anonymous reviewers for their insightful
comments.
Funding
This study was funded in part by the Japanese Ministry of
Education, Culture, Science, Sports, and Technology (Grant-inAid for Scientific Research (A) 20255010).
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