Agricultural Sciences in China
March 2006
2006, 5(3): 161-168
Advances on the Responses of Root Dynamics to Increased Atmospheric
CO2 and Global Climate Change
ZHOU Zheng-chao1 and SHANGGUAN Zhou-ping1, 2
State Key Laboratory of Soil Erosion and Dryland Farming on the Loess Plateau, Institute of Soil and Water Conservation, Chinese
Academy of Sciences, Yangling 712100, P.R.China
2 Northwest A & F University, Yangling 712100, P.R.China
1
Abstract
Plant roots dynamics responses to elevated atmospheric CO2 concentration, increased temperature and changed
precipitation can be a key link between plant growth and long-term changes in soil organic matter and ecosystem carbon
balance. This paper reviews some experiments and hypotheses developed in this area, which mainly include plant fine
roots growth, root turnover, root respiration and other root dynamics responses to elevated CO2 and global climate
change. Some recent new methods of studying root systems were also discussed and summarized. It holds herein that the
assemblage of information about root turnover patterns, root respiration and other dynamic responses to elevated
atmospheric CO2 and global climatic change can help to better understand and explore some new research areas. In this
paper, some research challenges in the plant root responses to the elevated CO2 and other environmental factors during
global climate change were also demonstrated.
Key words: elevated CO2, temperature, precipitation, root turnover, root respiration, minirhizotrons, isotope trace
INTRODUCTION
Plant fine roots play an important role in terrestrial ecosystems (Davis et al. 2004; Norby and Jackson 2000).
Roots turn over faster than shoot components, and the
rate of fine root decomposition is often higher than that
of litter decomposition in forest systems (Vogt et al.
1996), thus the fine root turnover is an important component of belowground carbon budget (Noordwijk et
al. 1998). Jackson et al. (1997) estimated that as high
as 33% of global annual net primary productivity was
used for the production of fine roots, which had a short
period of lifetime and then died beginning to decompose.
Some studies suggested that fine root turnover was a
major pathway for carbon (C) and nitrogen (N) cy-
cling in terrestrial ecosystems and most likely sensitive
to many factors of global change (Gill and Jackson
2000; Eissenstat et al. 2000).
Human activities affect many aspects of the Earth.
Atmospheric CO2 concentration has increased from
about 280 to 370 µmol mol-1 since 1800; the temperature, precipitation, and deposition of biologically available N also increased in most regions (IPPC 2001); and
these factors are continuously increasing in present and
future climate change. As researchers try to gain a better
understanding of possible impacts of global climatic
change on C and nutrient cycles in terrestrial ecosystems and their feedback to global climate factors,
increasing attention has been focused on plant root dynamics (Walker and Steffen 1997).
A better understanding of responses of plant root
Received 2 August, 2005 Accepted 2 January, 2006
Correspondence SHANGGUAN Zhou-ping, Tel: +86-29-87019107, E-mail: [email protected]
© 2006, CAAS. All rights reserved. Published by Elsevier Ltd.
162
ZHOU Zheng-chao et al
ecosystems and distribution, especially fine root
ecosystems, to the impacts of global change should be
vital for accelerating research on underground ecosystems and the C and N cycling patterns and process due
to relocation of minimal nutrients from roots during
senescence (Torn et al. 1997; Matamala and Schlesinger
2000). In this paper, we summarize the progresses that
researchers have made in recent years in order to improve understanding of root ecosystems under global
climate change.
METHODS OF STUDYING ROOT SYSTEMS
Root systems are important for plants and terrestrial
ecosystems. Apart from their obvious importance is
known much less about the dynamics of live roots than
about plant shoots, because of the inaccessibility of
root systems, special techniques are needed to investigate standing stock, root distribution and turnover, as
well as to construct underground C budgets (Kùcke et
al. 1995; Vogt et al. 1998). While traditional destructive techniques, such as soil coring, in-growth cores,
whole root system excavation, and trenching, have been
used to investigate root processes. Nondestructive
techniques, including rhizotrons, minirhizotrons and
isotope trace (such as: 13C, 14 C and 15 N), have been
used more recently (Luo 2003; Pierret et al. 2005).
Here, a traditional (i.e., soil coring) and two new methods (i.e., minirhizotron and isotope trace) currently
adopted in root studies are discussed.
Soil coring and in-growth coring
Soil coring was a traditional method in studying fine
root dynamics (Davis et al. 2004; Zhang et al. 2005).
The sampling interval of time and the diameter of soil
core are very critical in soil coring. Fine root dynamics
can be calculated by the following formula (Eq. 1):
PFR = BMAX - BMIN
(1)
Where PFR is annual fine root biomass, BMAX and
BMIN are maximal and minimal biomass in soil core
sampling, respectively.
The fine root biomass calculated by Eq.1 is the minimal biomass because dead roots are not taken into account (Son and Hwang 2003). So some researchers
proposed an in-equation (Eq. 2) (Hendricks et al. 1997)
ｋ
+
ｋ
+
PFR≥ ∑ ｂ ｊ or PFR≥ ∑ (ｂ + ｎ ) ｊ
ｊ=1
Where, ｂ ｊ+
ｊ=1
(2)
is the difference of two consecutive
samplings, ｎ ｊ+ is the dead roots between two consecutive sampling times.
In-growth core is also a commonly used method
adopted in studies of fine root (Son and Hwang, 2003;
Burton et al. 2000). The method for calculating root
biomass in the column of in-growth soil is the same as
soil coring and the amount of soil in the column is relatively less than that in the soil core. But the column of
in-growth soil is also liable to underestimate the annual
root biomass.
Minirhizotron root systems
Minirhizotron is an effective tool to observe and quantify root system dynamics. The individual root segments
can be repeatedly measured during multiple intervals of
time with minirhizotron. Moreover, because it is less
destructive than the soil coring, minirhizotron enables
researchers to minimize soil disturbance as well as the
confounding of spatial and temporal variations associated with other root research methods such as core collection (Makkonen and Helmisaari 1999) and mesh ingrowth bags (Antonio et al. 1985; Ludovici and Morris
1996). Most importantly, minirhizotron allows the production and mortality of fine roots to be measured as
separate processes thus providing direct and independent measurements of these two parameters (Hendrick
and Pregitzer 1996). Alternative methods that are not
taken into account simultaneous production and mortality may underestimate their matters (Chen et al. 2004).
Currently, a minirhizotron system typically consists
of a minirhizotron tube that can be inserted into soil, a
color micro-video camera, a camera control unit to focus the camera and adjust light, a video camera recorder (VCR) for recording root images on video tape,
and a monitor for viewing images as they are collected
(Fig.1).
Isotope trace
The use of isotopes as tracers has become a powerful
tool in ecological research. The isotopes of 13C and 14C
© 2006, CAAS. All rights reserved. Published by Elsevier Ltd.
Advances on the Responses of Root Dynamics to Increased Atmospheric CO2 and Global Climate Change
163
45°
Fig. 1 General set-up of the minirhizotron camera system and the minirhizotron tube for plant root system studies (Johnson et al. 2001). The
minirhizotron system consists of a minirhizotron camera, an indexing handle, a camera control unit, VCR, a monitor, and a microphone. The
users can focus and adjust light levels through the camera control unit. The indexing handle allows users to rapidly and accurately move the
camera from one field-of-view to another. The monitor shows the images, as they are being collected by the camera and recorded by the VCR.
The microphone is used to record camera location, and environmental and observational information on the audio track of the videotape. In
this figure, the minirhizotron tube is inserted into soil at 45° from ground surface and extended 1 m deep beneath the target plants.
have been used to quantify longevity and turnover of
plant roots. In particular, bomb 14C in atmospheric CO2
has been used to estimate mean ages of fine roots in the
deciduous and coniferous forests of the eastern United
States , whic h we re found to be 3-18 yea rs old
(Gaudinski et al. 2001). Similarly, depletion of 13C in
elevated CO2 experiments has also been used to estimate fine root longevity in trees, which was found to
be 4-9 years in a loblolly pine forest (Pendall 2002). In
general, the estimated longevities of fine roots using
the isotope methods are far longer than those estimated
by conventional methods, such as mass balance and
root minirhizotrons.
DYNAMIC RESPONSE OF ROOTS TO
ELEVATED CO2
Numerous studies have been conducted to investigate
the root dynamics in field CO2 experiments for forests,
grasslands and agricultural systems (Schlesinger and
Lichter 2001; Pregitzer et al. 2002; He and Bazzaz 2003).
Fundamental differences in these ecosystems and in
their root systems lead to different questions, as well
as different methodological issues. Forests are very difficult to be included in manipulative experiments and
thus available data on root response to elevated CO2 in
forests are limited. However, grassland systems can be
studied as intact ecosystems in manipulative experiments (Fitter et al. 1997). In an annual crop system,
on the other hand, important research questions are
more likely to focus on root distribution and resource
capturing rather than equilibrium responses and C flux
(Dunbabin et al. 2003).
The influence of increased CO2 on forest root
systems
In several CO2 enrichment studies with deciduous trees
© 2006, CAAS. All rights reserved. Published by Elsevier Ltd.
164
and conifers under field conditions, the roots of deciduous trees are more responsive to CO2 enrichment
than those of conifers. Norby et al. (1999) suggested
that fine root density (the mass of roots per unit ground
area) increased from 60 to 140% in elevated CO2, which
was in contrast with conclusion of Tingey et al. (2000)
who reported that fine root density increased more than
leaf area in every case, suggesting that the stimulation
to fine root production was a specific response to elevated CO2. Rasse (2002) used a theoretical model to
analyze fine root dynamics in temperate forests, and
the model simulations indicated that fine roots biomass
increased with elevated CO2 because larger amounts of
assimilates resulting from increased photosynthesis were
available to the growth of plant tissue. Allen et al. (2000)
conducted a free air CO2 enrichment (FACE) experiment in a 15-yr-old Pinus taeda L. in North Carolina,
USA and reported that fine roots were increased 37%
by elevated CO2. In addition, elevated CO2 increased
the absolute fine root turnover (i.e., fine root mortality
+ fine root decomposition) by 26% compared to the
control, but the turnover rate in correspondence to production did not change. The results of elevated CO2
effects on root turnover in field experiments with conifers have showed an increased rate of root loss, but the
response in relative root turnover has been inconsistent
(Tingey et al. 2000). Fine root length, mortality and net
production increase with CO2 enrichment in an Acer
saccharum M.- Acer rubrum M. assemblage in the open
top chambers (Wan et al. 2004). Elevated CO2 also increases the diameter and length of individual roots of
Populus tremuloides M. trees in the open top chambers
(Pregitzer et al. 2000b).
The effect of elevated CO2 on grassland root
systems
Numerous experiments have been conducted to study
root responses to CO 2 in intact native grassland
ecosystems. Arnone et al. (2000) studied the production and mortality dynamics of the roots in calcareous
grasslands at elevated atmospheric CO2 in Switzerland
and reported that after 2-year CO2 enrichment, there
was no difference in either root production or mortality.
However, There was a shift in root distributions with
more roots being found in upper soil in CO2 enriched
ZHOU Zheng-chao et al
plots. They explained that this was probably associated
with the increase in soil moisture under the elevated
CO2 conditions.
The impact of increased CO2 on field crop roots
When discussing the responses of crop roots to elevated CO2, Pritchard and Rogers (2000) emphasized
the importance of cell expansion and cell division. They
also suggested that the key of understanding how root
growth would vary with a CO2 enrichment environment
was to identify how carbohydrates, especially sucrose,
functioned as both substrates for growth and regulatory compounds during plant growth and development.
From this perspective, they summarized the literature
and proposed that roots would be relatively larger and
more highly uptake ability (Pritchard et al. 1999) in a
high CO2 concentration environment. Fitter et al. (1996)
found that wheat showed no changes in root turnover
with enriched CO2 because wheat roots did not or rarely
die until they all die simultaneously at the end of life
cycle. This indicates that root turnover may not be an
important issue to annual crop plants.
ROOT DYNAMIC RESPONSE TO INCREASING TEMPERATURE
Response of root growth to increasing air
temperature
Increased levels of greenhouse gases in atmosphere have
been predicted to cause the increase in average global
surface temperature by 1.4-5.8°C by 2100 (IPCC
2001). As atmospheric temperature increases globally,
soil temperature can be expected to rise concomitantly
(Schlesinger and Andrews 2000). Soil temperature has
a closely impact on the development of plant root
systems. Pregitzer et al. (2000a) discussed the importance of seasonality in root dynamics of perennial plants
and speculated that global warming would result in earlier root growth in spring. Their results suggest that the
flux of C from leaves to roots and then into soil increases with global warming. The analysis of the response of root C flux to global climatic change often
focuses on the root turnover dynamics in controlled
© 2006, CAAS. All rights reserved. Published by Elsevier Ltd.
Advances on the Responses of Root Dynamics to Increased Atmospheric CO2 and Global Climate Change
165
Fig. 2 Relationships between root turnover and mean annual temperature for different vegetation types (P < 0.001, r2 = 0.63 for grasslands;
P < 0.001, r2 = 0.75 for shrub lands; P < 0.03, r2 = 0.10 for forest fine roots) (Gill and Jackson 2000).
temperature. Gill and Jackson (2000) analyzed the relationship between roots turnover and mean annual temperature and suggested that root turnover exhibited
positive exponential relationships with mean annual temperature (Fig.2).
Effect of increase in temperature on the root
respiration
The response of root respiration to future temperature
change will be critical in determining the vegetation responses to global environmental change (Atkin et al.
2000). Chen et al. (2000) concluded that root respiration increased with the increase in temperature and
reached its maximum at 30-40°C, the temperature sensitivity of respiration rate (Q10), defined as (respiration
rate at T+10°C)/(respiration rate at T) was affected by
incubation temperature ranging 5-40°C. And Bryla et
al. (2001) suggested root respiration of citrus trees increased exponentially with the increase in soil temperature (Q10 =1.8-2.0). Atkin et al. (2000) also highlighted
that the temperature sensitivity of respiration changed
with measuring temperature.
high latitudes (IPCC 2001). The annual precipitation
dynamics can affect plant productivity and may influence roots ecosystems. Gill and Jackson (2000) suggested that root turnover was closely and positively
related to the ratio of growing season precipitation to
maximum mean monthly temperature.
Joslin et al. (2000) used the root elongation, observed
by minirhizotron as index of biomass production, to
study the long-term effects of the variation of water
input (a range of 33%) on the forestland with a mature
deciduous forest in Tennessee, USA. A 5-year observation of fine roots in their experiment showed that the
net fine root production of the treatments did not differ
significantly (Fig.3). The periods of lower root production in the dry treatment were compensated by fast
root growth during favorable periods. In the wet
treatment, both the highest production (from 20 to 60%)
and mortality (from 18 to 34%) rates resulted in the
ROOT DYNAMIC RESPONSES TO PRECIPITATION
In recent years, air temperature increases with the increase in greenhouse gases concentration. The increased
temperature should modify global hydrologic budgets,
and thus leading to increase in winter precipitation at
Fig. 3 Mean annual net root growth (elongation) by treatments of
wet, ambient, and dry for each of the 5 yr (Joslin et al. 2000). Net
growth = gross growth - mortality. Error bars indicate S.E. of the
mean. Treatment differences were significant (P < 0.1) only during
1 yr in 1996. Treatments: Closed columns, wet (33% increase in
water input relative to control); Grey columns, ambient (control);
Open columns, dry (33% decrease in water input relative to control).
© 2006, CAAS. All rights reserved. Published by Elsevier Ltd.
166
highest index of fine root turnover, although the differences were not statistically significant. The impact of
water on fine roots differs among plant speciess. For
example, Carolyn et al. (2004) studied the fine root
growth dynamics of four Mojave desert shrubs in terms
of soil moisture and concluded that in Ambrosia
artemisiifolia L. and Ephedra Sinica S. there was a
positive linear relationship among active fine root lengths,
soil moisture, and canopy-below roots. However, there
was a negative correlation among these parameters in
Larrea tridentata C. In addition, it seemed to be an insignificant root/water relationship in Lycium barbarum L.
ZHOU Zheng-chao et al
sponses to elevated atmospheric CO2 and global climatic change. Therefore, it is promised to see a much
clearer picture of the basic mechanisms of root dynamics in the future global change.
Acknowledgements
This research was supported by the National Natural
Science Foundation of China (90502007, 30270230),
the Program for New Century Excellent Talents in
University, China (NCET-04-0955), and the United
Scholar’s Item of Talent Training Program in West China
of CAS and the Program for Outstanding Talents in
Northwest A & F University.
CONCLUSIONS
References
Plant fine roots are the major components of terrestrial
ecosystems, which affect the C and N cycling in the
ecosystems. Investigations of the effects of elevated
CO2 and global climatic change on root dynamics can
help better understanding of C sink and source of the
greenhouse gases in the terrestrial ecosystems.
Many researchers have contributed a great amount
of effective work to study root dynamic responses to
elevated CO2 and other environmental factors during
global climatic change. However, there still have not
been enough experiments with sufficient durations or
spatial scales attempted to allow proper conclusions in
the effects of elevated atmospheric CO2, the increase
in temperature and change in precipitation on root dynamics to be made. Thus, there are insufficient data to
support any generalizations about effects of enriched
CO2 on root turnover, the consequence of root turnover,
and the C flux to long-lived soil C pools. The root responses to increased temperature and changed precipitation are obscured by the corresponding acclimation.
Therefore, the challenges are to solve serious methodological and analytical problems and to obtain more
comprehensive data along with sufficient ancillary data,
so that the differences among ecosystems can be
explained. A new conceptual and predictive model of C
partitioning in plants should be developed so that environmental influences on leaves can be transformed into
the responses taking place in roots. Fortunately, different research groups are conducting intensive research
to clarify the mechanisms of root turnover, root
respiration, root decomposition, and C partitioning re-
Allen A S, Andrews J A, Finzi A C, 2000. Matamala R, Richter
D D, Schelsinger W H. Effects of free air CO2 enrichment
(FACE) on belowground processes in a Pinus taeda forest.
Ecological Applications, 10, 437-448.
Antonio F, Persson H Å, Steen E. 1985. Growth dynamics of
superficial roots in Portuguese plantations of Eucalyptus
globules Labill. Studied with a mesh bag technique. Plant
and Soil, 83, 233-242.
Arnone J A, Zaller J G, Spehn E, Niklaus P A, Wells C E, Korner
C H. 2000. Dynamics of root systems in native grasslands:
effects of elevated atmospheric CO2. New Phytologist, 147,
73-85.
Atkin K O, Everard J D, Beth R L. 2000. Response of root
respiration to changes in temperature and its relevance to
global warming. New Phytologist, 147, 141-154.
Bryla D R, Bouma T J, Hartmond U, Eissenstat D M. 2001.
Influence of temperature and soil drying on respiration of
individual roots in citrus: integrating greenhouse observations into a predictive model for the field. Plant, Cell and
Environment, 24, 781-790.
Burton A J, Pregitzer K S, Hendrick R L. 2000. Relationships
between fine root dynamics and nitrogen availability in
Michigan northern hardwood forests. Oecologia, 125, 389399.
Carolyn S W, Joseph W F, George C J F, Robert S N. 2004. Fine
root growth dynamics of four Mojave Desert shrubs as related
to soil moisture and microsite. Journal of Arid Environment,
56, 129-148.
Chen H, Mark E H, Robert P G, William H. 2000. Effects of
tem perature and moisture on carbo n respired from
decomposing woody roots. Forest Ecology and Management,
138, 51-64.
Chen W J, Zhang Q F, Cihlar J, Bauhus J, Price D T. 2004.
© 2006, CAAS. All rights reserved. Published by Elsevier Ltd.
Advances on the Responses of Root Dynamics to Increased Atmospheric CO2 and Global Climate Change
167
Estimating fine-root biomass and production of boreal and
cool temperate forests using aboveground measurements: a
new approach. Plant and Soil, 265, 31-46.
Davis J P, Bruce H, David C, Hendrick R. 2004. Fine root
dynamics along an elevational gradient in the southern
Appalach ian Mountains, USA. Forest Ecolog y and
Management, 187, 19-34.
Kùcke M, Schmid H, Spiess A. 1995. A comparison of four
methods for measuring roots of field crops in three contrasting
soils. Plant and Soil, 172, 63-71.
Ludovici K H, Morris L A. 1996. Responses of loblolly pine,
sweet gum and grass roots to localized increases in nitrogen
in two watering regimes. Tree Physiology, 16, 933-939.
Luo Y Q. 2003. Uncertainties in interpretation of isotope signals
Dunbabin V, Diggle A, Rengel Z. 2003. Is there an optimal root
architecture for nitrate capture in leaching environments?
Plant, Cell and Environment, 26, 835-844.
Eissenstat D M, Wells C E, Yanai R D, Whitbeck J L. 2000.
Building roots in a changing environment: implications for
root longevity. New Phytologist, 147, 33-42.
Fitter A H, Graves J D, Wolfedden J, Self G K, Brown T K,
Bogie D S, Mansfield T A. 1997. Root production and
for estim atio n of fine roo t lo ng evity : th eo retical
considerations. Global Change Biology, 9, 1118-1129.
Makkonen K, Helmisaari H S. 1999. Assessing fine-root biomass
and production in a Scots pine stand comparison of soil core
and root ingrowth core methods. Plant and Soil, 210, 43-50.
Matamala R, Schlesinger W. 2000. Effects of elevated
atmospheric CO2 on fine root production and activity in an
intact temperate forest ecosystem. Global Change Biology,
turnover and carbon budgets of two contrasting grasslands
under ambient and elevated atmospheric carbon dioxide
concentrations. New Phytologist, 137, 247-255.
Fitter A H, Self G K, Wolfenden J, van Vuuren M M I, Brown T
K, Williamson L, Graves J D, Robison D. 1996. Root
production and mortality under elevated atmospheric carbon
dioxide. Plant and Soil, 187, 299-306.
Gaudinski J B, Trumbore S E, Davidson E A. 2001. The age of
6, 967-979.
Noordwijk M V, Martikainen P, Bottner P, Cuevas E, Rouland
C, Dhillion S. 1998. Global change and root function. Global
Change Biology, 4, 759-772.
Norby R J, Jackson R B. 2000. Root dynamics and global change:
seeking an ecosystem perspective. New Phytologist, 147, 312.
Norby R J, Wullschleger S D, Gunderson C A, Johnson D W,
fine root carbon in three forests of the eastern United States
measured by radiocarbon. Oecologia, 129, 420-429.
Gill R A, Jackson R B. 2000. Global patterns of root turnover
for terrestrial ecosystems. New Phytologist, 147, 13-31.
He J S, Bazzaz F A. 2003. Density dependent responses of
reproductive allocation to elevated atmospheric CO 2 in
Phytolacca americana L., New Phytologist, 157, 229-239.
Hendrick R L, Pregitzer K S. 1996. Applications of minirhizotrons
Ceulem ans R. 1999. Tree respon ses to risin g CO2,
im plicatio ns for the future forest. Plant, C ell a nd
Environment, 22, 683-714.
Pendall E. 2002. Where does all the carbon go? The missing sink.
New Phytologist, 153, 199-211.
Pierret A, Christopher J M, Doussan C. 2005. Conventional
detection methodology is limiting our ability to understand
the roles and functions of fine roots. New Phytologist, 163,
to understand root function in forests and other natural
ecosystems. Plant and Soil, 185, 293-304.
Hendricks J J, Nadelhoffer K J, Aber J D. 1997. A 15N tracer
technique for assessing fine root production and mortality.
Oecologia, 112, 300-304.
IPPC. 2001. Third Assessment Report. In: Houghton J T, Ding
Y, Griggs D J, Noguer M, Linden P J van der, Dai X, Maskell
K, Johnson C A, eds, Climate Change. The Scientific Basis.
135-143.
Pregitzer K S, DeForest J L, Burton A J. 2002. Fine root
architecture of nine North American trees. Ecological
Monographs, 72, 293-309.
Pregitzer K S, King J S, Burton A J, Brown S S. 2000a. Responses
of tree fine roots to temperature. New Phytologist, 147, 105115.
Pregitzer K S, Zak D R, Maziasz J, DeForest J, Curtis P S,
Cambridge University Press, Cambridge. pp. 1-94.
Jackson R B, Mooney H A, Schulze E D. 1997. A global budget
for fine root biomass, surface area, and nutrient contents.
Proceedings of the National Academy of Sciences, USA, 94,
7362-7366.
Johnson M G, Tingey D T, Phillips D L, Storm M J. 2001.
Adv ancing fine root research with m inirhizo tron s.
Environment and Experimental Botany, 45, 263-289.
Lussenhop J. 2000b. Interactive effects of atmospheric CO2
and soil N availability on fine roots of Populus Tremuloides.
Ecological Applications, 10, 18-33.
Pritchard S G, Rogers H H, Prior S A, Peterson C M. 1999.
Elevated CO2 and plant structure: a review. Global Change
Biology, 5, 807-837.
Pritchard S G, Rogers H H. 2000. Spatial and temporal
deployment of crop roots in CO2 enrichment environments.
Joslin J D, Wolfe M H, Hanson P J. 2000. Effects of altered
water regimes on forest root systems. New Phytologist, 147,
117-129.
New Phytologist, 147, 55-71.
Rasse D P. 2002. Nitrogen deposition and atmospheric CO2
interactions on fine root dynamics in temperate forests: a
© 2006, CAAS. All rights reserved. Published by Elsevier Ltd.
168
ZHOU Zheng-chao et al
theoretical model analysis. Global Change Biology, 8, 486503.
Schlesinger W H, Andrews J A. 2000. Soil respiration and the
global carbon cycle. Biogeochemistry, 48, 7-20.
Schlesinger W H, Lichter J. 2001. Limited carbon storage in soil
and litter of experimental of forest plots under increased
atmospheric CO2. Nature, 411, 466-469.
and indirect methods for estimating root biomass and
production of forests at an ecosystem level. Plant and Soil,
200, 71-89.
Vogt K A, Vogt D J, Palmiotto P A, Boon P, O’Hara J, Asbjornsen
H. 1996. Review of root dynamics in forest ecosystems
grouped by climate. Plant and Soil, 187, 159-219.
Walker B, Steffen W. 1997. An overview of the implications of
Son Y H, Hwang J H. 2003. Fine root biomass, production and
turnover in a fertilized Larix leptolepis plantation in central
Korea. Ecological Research, 18, 339-346.
Tingey D T, Phillips D L, Johnson M G. 2000. Elevated CO2
and conifer roots: effects on growth, life span and turnover.
New Phytologist, 147, 87-103.
Torn M S, Trumbore S E, Chadwick O A, Vitousek P M,
Hendricks D M. 1997. Mineral control of soil organic carbon
global change for natural and managed terrestrial ecosystems.
Conservation Ecology. http://www.consecol.org/Journal/
voll/iss2/art2/index.html
Wan S Q, Norby R J, Pregitzer K S, Ledford J, O’Neill E G.
2004. CO 2 enrichment and warming of the atmosphere
enhance both productivity and mortality of maple tree fine
roots. New Phytologist, 162, 437-446.
Zhang L Z, Cao W X, Zhang S P, Zhou Z G. 2005. Characterizing
storage and turnover. Nature, 389, 170-173.
Vogt K A, Vogt D J, Bloomfield J. 1998. Analysis of some direct
root growth and spatial distribution in cotton. Acta
Phytoecology Sinica, 29, 266-273. (in Chinese)
(Edited by ZHANG Yi-min)
© 2006, CAAS. All rights reserved. Published by Elsevier Ltd.