Global Change Biology (1995) 1, 24:^274
Commissioned Review
Terrestrial higher-plant response to increasing
atmospheric [CO2] in relation to the global carbon cycle
JEFFREY S. A M T H O R
Lawrence Liverrtiore National Laboratory, L-256, PO Box 808, Livermore CA 94550 USA
Abstract
Terrestrial higher plants exchange large amounts of CO2 with the atmosphere each year;
c. 15% of the atmospheric pool of C is assimilated in terrestrial-planl photosynthesis
each year, with an about equal amount returned to the atmosphere as CO2 in plant
respiration and the decomposition of soil organic matter and plant litter. Any global
change in plant C metabolism can potentially affect atmospheric CO2 content during
the course of years to decades. In particular, plant responses to the presently increasing
atmospheric CO2 concentration might influence the rale of atmospheric CO2 increase
through various biotic feedbacks. Climatic changes caused by increasing atmospheric
CO2 concentration may modulate plant and ecosystem responses to CO2 concentration.
Climatic changes and increases in pollution associated with increasing atmospheric CO2
concentration may be as significant to plant and ecosystem C balance as CO2 concentration
itself. Moreover, human activities such as deforestation and livestock grazing can have
impacts on the C balance and structure of individual terrestrial ecosystems that far
outweigh effects of increasing COT concentration and climatic change.
In short-term experiments, which in this case means on the order of 10 years or less,
elevated atmospheric CO2 concentration affects terrestrial higher plants in several ways.
Elevated CO2 can stimulate photosynthesis, but plants may acclimate and (or) adapt lo
a change in atmospheric CO2 concentration. Acclimation and adaptation of photosynthesis lo increasing CO2 concentration is unlikely to be complete, however. Plant wateruse efficiency is positively related to CO2 concentration, implying the potential for more
plant growth per unit of precipitation or soil moisture with increasing atmospheric CO2
concentration. Plant respiration may be inhibited by elevated CO2 concentration, and
although a naive C balance perspective would count Ihis as a benefit to a plant, because
respiration is essential for plant growth and health, an inhibition of respiration can be
detrimental. The net effect on terrestrial plants of elevated atmospheric CO2 concentration
is generally an increase in growth and C accumulation in phytomass. Published
estimations, and speculations about, the magnitude of global terrestrial-plant growth
responses to increasing atmospheric CO2 concentration range from negligible to fantastic.
Well-reasoned analyses point to moderate global plant responses to CO2 concentration.
Transfer of C from plants to soils is likely to increase with elevated CO2 concentrations
because of greater plant growth, but quantitative effects of those increased inputs to
soils on soil C pool sizes are unknown.
Whether increases in leaf-level photosynthesis and short-term plant growth stimulations caused by elevated atmospheric CO2 concentration will have, by themselves,
significant long-lerm (tens to hundreds of years) effects on ecosystem C storage and
atmospheric CO2 concentration is a matter for speculation, not firm conclusion. Longlerm field studies of plant responses to elevated atmospheric CO2 are needed. These
will be expensive, difficult, and by definition, results will not be forthcoming for at
least decades. Analyses of plants and ecosystems surrounding natural geological CO2
Correspondence: J.S. AmEhor; fax +1-510-422-6388, e-mail: [email protected]
© 1995 Blackwell Science Ltd.
243
244
J.S. AMTHOR
degassing vents may provide the best surrogates for long-term controlled experiments,
and therefore the most relevant information pertaining to long-term terrestrial-plant
responses to elevated CO2 concentration, but pollutants associated with the vents are a
concern in some cases, and quantitative knowledge of the history of atmospheric CO2
concentrations near vents is limited.
On the whole, terrestrial higher-plant responses to increasing atmospheric CO2
concentration probably act as negative feedbacks on atmospheric CO2 concentration
increases, but they cannot by themselves stop the fossil-fuel-oxidation-driven increase
in atmospheric CO2 concentration. And, in the very long-term, atmospheric CO2
concentration is controlled by atmosphere-ocean C equilibrium rather than by terrestrial
plant and ecosystem responses to atmospheric CO2 concentration.
Keywords: carbon dioxide (CO2), global carbon cycle, global environmental change, photosynthesis, plants, respiration.
Received U May 1995; revision accepted 20 July 1995
360350340-
o
pher
O
oo
330320-
50LU
The atmospheric [CO2I (i.e. [CO2la) of Earth increased
horn c. 280 ppmv (t:. 28 Pa CO2 at sea-level) to c. 360
ppmv (c. 36 Pa CO2 at sea-!evel) during the past 200
years (Friedli et aL 1986; Keeling & Whorf 1994). The
increase in [CO2],i is due mainly to fossil fuel burning
and land-use change processes such as deforestation
(Plass 1956; Houghton et al. 1983; Siegenthaler & Oeschger
1987). Atmospheric [CO2I continues to increase (Fig. 1)
and might exceed 500 ppmv (or more) within the next
100 years.
Although the present increase in [C02la is rapid - the
annual rate of increase during the past several decades
may be unprecedented in Earth's history - present [COila
is low compared with the concentrations existing during
much of Earth's history (Berner 1992, 1994; Kasting 1993).
The primitive (c. 4.6 x lO"* years ago) atmosphere might
have contained as much as 1 MPa CO2, or c. 25 x 10^
times the present atmospheric level (PAL). Atmospheric
[CO2I may have been 14-18 times PAL 450-550 x 10^
years ago, About 300 x 10^ years ago—during a glacial
period of c. 50 X lO*" years—[CO2]a may have been as
low as PAL, but by c. 200 X 10"^ years ago, [COi];, might
have reached four times PAL. Later, during the last glacial
maximum (LGM; c. 18 X lO'' years ago), [CO2],, was as
low as 0.5 PAL So, with a 10^ year time perspective,
[CO2]a is now high (Fig. 2), but with a 10^ year time
perspective, [CO2I., is now low (Fig. 3).
Consequences of the present rapid increase in [CO2la
have been speculated on at length. The main concem is
that increased [CO^J^, and increased concentrations of
other radiatively active gases and aerosols in the atmosphere, will result in an enhanced global 'greenhouse
effect' and global warming (Plass 1956; Manabe 1983).
For example, c. 100 years ago, Arrhenius (1896) calculated
that a 50% increase in [CO2]a - from a then ambient level
of c. 300 ppmv - would cause a 3-4 °C increase in Earth's
Dncent ration (ppm
Introduction
<
Qin.
1
1960
I
I
I
1
1970
1980
Year AD
1
I
I
1990
Fig. 1 Monthly mean atmospheric CO; concentration (ppmv) at
Mauna Loa Obser\^atory (Hawaii; c. MIXi m above MSL) from
March 1958 through December 1994 (Keeling & Whorf 1994;
Keeling i^f al. 1995). Tliis i.s the longest continuous record of
atmospheric CO; concentration and is a rolnist indicator of Ihe
monthly region.il trend in atmospheric CO2 concentration in the
middle troposphere. These data reflect the glob^il atmospheric
C balance on the annual time scale. The abscissa tick marks
correspond to 1 January of the year indicated.
surface temperature, other factore remaining constant.
Using a modern coupled atmosphere-ocean general circulation model (AOGCM), Manabe & Stouffer (1994) predicted that a doubling of lCO2]a would increase Earth's
surface temperature by c. 2.5-3.5 °C. Both Arrhenius and
modem climate models predict that warming duo to
elevated [CO2].i is greater at high latitudes compared
with equatorial regions. An enhanced greenhouse effect
© 1995 Blackwell Science Ltd., Global Change Biology, 1, 243-274
TERRESTRIAL-PLANT RESPONSE TO ATMOSPHERIC [COjl
245
conceritration (ppm
400
mosphleric
o
300- •
280 ppmv
200-
100I
I I mill I I
10-
10^
10'
Years before 1995 AD
Fig. 2 Approximiitf j^k)b<il .itmospheric CO2 cnncentrfition
(ppmv) during the past 220,01)0 years (note logu) abscissa). Pre1956 AD values are from gases extracted from Antarctic ice cores
(Vostok: Barnola et al. 1987; Jouzel et al. 1993; Siple Station:
Neftei et al. 1985; Friedli et at. 1986; South Pole: Friedli el nl.
1984; Nefte! (•( 11I. 1985; Adolie Land: BarnoLi ct al. 1995). PostAD 1956 values are from atmospheric measurements m^de at
Mauna Loa Observatory (see Fig. 1). A reanalysis of the Vostok
ice core for the period 0-160,000 years ago yielded values
similar to those shown here, but with somewhat lower COi
concentrations (several ppmv) during the period 10,000-50,000
years ago, about 120,000 years ago, .ind during the period
I40,000-i50,000 years ago (Barnola et al. 1991). The dashed line
at 280 ppmv indicates the often cited approximate preindustriol
[COi],!, but |CO2]aS varied by c. 10 ppmv during the period
1000-1700 AD (Bamola cf al. 1995).
also cause increased global precipitation and
increased global evaporation, i.e. an intensification of
the global hydrological cycle (Manabe 1983; Manabe &
Stouffer 1994). Changes in regional hydrology resulting
from changes in global atmospheric chemistry are largely
unknown.
So far, however, most predictions of warming exceed
the observed global warming of c. 0.5 °C during the past
100 years Oones et ai 1994). Several factors may contribute
to this discrepancy; e.g. an oscillation in the global
climatic system of period 65-70 years that presently
favours cooling (Scblesinger & Ramankutty 1994), stratospheric ozone destruction (Toumi et ai 1994), and atmospheric sulfur pollution (Taylor & Penner 1994). Indeed,
when sulfate aerosols are included in an AOGCM, predicted global warming matches closely the observed
warming of the past 100 years {Dickson 1995; Murphy
1995). Moreover, recent increases in temperature are wellrelated to increases in [CO:).! (Thomson 1995). In any
D 1995 Blackwell Science Ltd., Global Change Biology, 1, 243-274
600
I
500
10
1
I
400
I
I
300
I
[
200
I
1
T
100
years before 1995 AD
Fig. 3 Mass of COi in the atmosphere, relative to the present
mass of atmospheric CO2, during the past 600 X 10'' years
from the king-term geochemical global C cycle model of Berner
(1994; estimated error is on the order of ± 50%). The most
reliable estimates of past atmospheric CO2 content based on,
e.g. analyses of ancient soils, sediments, and minerals, are in good
agreement with these mt>del predictions (RA Berner personal
communication). The first major plant migration from aquatic
environments to land might have (Kcurred c. 400 x 10" years
ago. The relatively low atmospheric COT content c. 300 x 10*
years ago coincides with a long (on the order of 50 X 10^
years) glacial period. The dashed line approximates present
atmospheric COi content.
case, based on physical principles and available data, it
seems likely that global warming will continue as Earth's
[CO2]a continues to increase, although climatic change at
any location will probably differ from global mean
changes.
Because [CO2]a is important to Earth's energy balance
and climate, and because [CO2la is increasing rapidly, the
global C cycle has become a topic of vigorous study.
Although fossil fuel burning by humans is driving the
present increase in [COil^, several other CO2 fluxes into
and out of the atmosphere are larger in magnitude. These
larger fluxes include those associated with terrestrialplant metabolism (Table 1). The terrestrial C cycle is
central to ecosystem function and its study in relationship
to the productivity and health of ecosystems is important
in its own right, but recent interest in the terrestrial C cycle
follows mainly from concern about increasing lCO2]a and
the global C cycle. It is noteworthy that only about half
the CO2 released in fossil fuel burning during the past
100 years can be accounted for in the observed increase
in [CO2]a/ indicating that large amounts of C are being
stored on land and (or) in the oceans. Knowledge of the
246
J.S. AMTHOR
Table 1 Selected estimates of major confemporar>' C fluxes from land and ocean to the atmosphere, from land to inean, and from
ocean water to ocean sediments. Uncertainties associated with many of these values are large relative to the values themselves.
Carbon exchange
Terrestrial
Terrestrial-plant photosynthesis (gross primary production)^
Terrestrial-plant respiration
Root and mycorrhizal respiration
Terrestrial-plant photosynthesis -I- respiration (NPP)
Litter and soil organic matter decomposition
Litter and soil organic matter decomposition
1982-1992
1982-1992'
1990
1991
1992
Oceanic
Ocean uptake
Ocean release
Submarine volcanos**
Sedimentation
Net ocean-atmosphere exchange
1982-1992
1990
1991
1992
Anthropogenic
Fossil fuel burning
1950
1960
Reference
-90 to -130
Bolin & Fung 1992
Bolin & Fung 1992
Raich & Schlesinger 1992
Box 1975
I.ieth 1975
Whit taker 1975
40-60
18
-38 to -56
-45
^2
-60
-48
-62
50
a)Ot respiration
Herbivory of terrestrial plants (excluding crops)
Burning of terrestrial plants from human and natural causes
Conversion of phytomass to charcoal in fires*^
Caliche formation
Sedimentation on continents
Lake surface = water CO2 release
Terrestrial volcanos"^
Erupting lava
Subaerial volcanos
Chemical weathering of continental nxrks
River transport from land to ocean'"
Dissolved organic C
Particulate organic C
Dissolved inorganic C
Net land-atmosphere exchange
1980-1994
Global flux
^{Pg C per year)
68
76.5
3.5
1.8-4.7
-0.2 to -0.6
-0.02
-0.07
0.14
0.02
0.002
0.01-0.02
-0.24
-076
-0.8
-0.20
Ajtay c(fl/. 1979
Potter et al. 1993
Foley 1994
Raich & Schlesinger 1992
Raich & Schlesinger 1992
Raich & Potter 1995
Whittaker 197S
Crutzen & Andreae 1990
Crutzen & Andreae 1990
Schlesinger 1982
Meybock 1993
Cole et nl. 1994
SN Williams ft al. 1992
Uavitt 1982
Gerlach 1991
Meybeck 1993
Amiottc Suchet & Probst 1995
Siegenthaler & Sarmiento 1993
Meybeck 1993
-O.IO
-0.24
i2.5
-0.3 to -2.8
-0.76 to-1.16
-2,2
-1.8
-1.4
Keeling W «;. 1995
Francey ct al. 1995
Fig. 4 herein
fl/. 1995
-92
90.6
0.01-0.02
-0.2
-1.48
-3.5 to 0.8
-1.0
-2.4
Siegenthaler & Sarmiento
Sifgenthaler & Sarmiento
Gerlach 1991
Siegenthaler & Sarmiento
Siegenthaler & Sarmiento
Francoy c/ ill. 1995
Ciais et al. 1995
1993
1993
1993
1993
-3.1
1.62
2.54
Marland
1995 Blackwell Science Ltd., Ghbat Change Biology, 1, 243-274
TERRESTRIAL-PLANT RESPONSE TO ATMOSPHERIC [COj]
247
Table 1 ami.
Carbon exchange
Global flux
^(Pg C per year)
1970
198(1
1901
Oil well fires lit in Kuwait in 1991
4.01
5.17
6.03
0.04-0.09
Reference
Watson et al. 1992
•' Positive fluxes are into the atmosphere and negative fluxes are out of the atmosphere
'' The balance of photosynthetic CO2 assimilation with photorespiratory CO; release
' Charcoal has a very long half-life; its formation removes C from the C 'cycle' and places it in long-term storage
•^ Positive values indicate transfer into the atmosphere or oceans
'' Negative values indicate transfer from land to ocean. 'Dissolved inorganic C means dissolved inorganic C coming from atmospheric
and soil COi, rather than from carbonate rocks
' For gross (one-way) terrestrial C flux of 100-120 Pg y"'
^ Inciudes 0.6 Pg C y""' flux from txiean to atmosphere to balance the estimated difference between river input to oceans and
sedimentation out of oceans
(i) magnitude of fluxes of COT from the atmosphere into
oceans and onto land and (ii) responses of the processes
underlying those fluxes to the increase in [CO^la itself,
are both needed to accurately predict future [CO2la's and
therefore future climate.
Terrestrial-plant responses to [CO2]j as they relate to
fluxes and pools of C in terrestrial plants, soils, and the
atmosphere are considered in this review. The emphasis
is on feedbacks on the increase in global [CO^].! and their
role in the global C cycle. Several previous reviews of
terrestrial-plant and terrestrial-ecosystem responses to
[CO:),] '^*"i tie consulted for additional background and
analysis {e.g. Strain & Cure 1985; Eamus & Jarvis 1989;
Jarvis 1989; Bazzaz 1990; Field et al 1992; Bowes 1993;
Ceulemans & Mousseau 1994; Rogers et ai 1994; Allen
& Amthor 1995; Koch & Mooney 19%; Wulischleger
ct ai 1995b).
Terrestrial plants in the global carbon cycle
Plants and microbes in terrestrial ecosystems exchange
large amounts of CO2 with the atmosphere each year
(Table 1), and relative to the amount of C in the atmosphere, the terrestrial biosphere stores large quantities of
C (Table 2). Thus, terrestrial plants are important to
[CO213 and the global C cycle over the course of decades
to centuries, and by extension, global climate. (Although
more C is stored in soils tban in plants, the pathway of
present C transfer from the atmosphere to the soil is
almost entirely through plants.) For example, terrestriaiplant gross primary production [GPP; photosynthesis less
photorespiration (NB photorespiration is not a component
of 'normal' respiration; the two are different processes))
may consume 12-17% of the atmospheric C pool each
year (i.e. [90-130 Pg C y-')/[760 Pg C]; from Tables 1 and
2). Carbon that is assimilated by terrestrial plants is either
© 1995 Blackwell Science Ltd., Global Change Biology, 1, 243-274
(1) released as CO2 in subsequent plant respiration (ii)
released as CO2 during decomposition of dead plant
parts (heterotrophic respiration), or (iii) stored in perennial plant tissues or in soils or in sediments in various
forms for various periods of time. And, because the
associated fluxes are so large, even small changes in GPP,
plant respiration, or plant growth could significantly
affect the global C cycle and the rate of increase of ICO2)aThat said, and acknowledging that uptake and release of
CO2 by the terrestrial biota might affect [CO2]a over the
course of decades to centuries, I add that on longer time
scales [CO2L is determined by atmosphere-ocean C
equilibrium rather than biotic activity in the terrestrial
biosphere (see, e.g. Walker 1991). (In addition to their
direct effects on CO2 exchange between land and the
atmosphere, terrestrial plants also affect tbe terrestrial
hydrologic cycle, land-surface sensible heat exchange,
land-surface momentum exchange, and land-surface radiation balance, all of which are important to atmospheric
circulation and climate.)
Estimates of fossil fuel burning (Keeling 1973; Marland
et ai 1994), which are thought to be accurate, combined
with measurements of [CO2la changes and the isotopic
composition of atmospheric CO2 (i.e. the ratio of '^CO2
to '~CO2) can be used to estimate the amount of CO2
taken up by (or released from) land and taken up by (or
released from) oceans (Keeling et ai 1995). Using this
method, Ciais et ai (1995) estimated tbat, on average, C
was stored on land during the 1980s at a rate of c. 1.5 Pg
per year (and see Table 1). Francey et ai (1995) estimated
that on average c. 1-2 Pg C were stored on land each
year during the period 1982-1992. Our (G Rau, K Caldeira,
J Amthor) work in progress (Fig. 4), however, indicates
that the estimate of Francey et ai (1995) may be too large,
and Keeling et al. (1995) estimated that the terrestrial
biosphere net exchange of C was ± 2.5 Pg y'' during the
248
J.S. A M T H O R
Table 2 Selected estimates of contemporary global C pool sizes. Soil includes litter >.ind mineral soil, but most estimates of soil
organic C are for the top 1 (or less) m of soil only, whereas Nepstad et al. (1994) report that stores ot* C below 1 m depth in an
Amazonian forest exceed C stored in the top 1 m of soil and also exceed C stared in above-ground vegetation. Uncertainties in C
content of ail pools except the atmosphere are large with respect to the estimates themselves.
Carbon pool
C Content (Pg)
Atmosphere (1994 estimate)
Plants
Terrestrial
760
Ocean
Soil organic matter (excluding live roots) + litter^
835 (756)'
560 (490)'^
558 (502)^
< 1
I
2
3
3
1636-2070
1395*^
1511
Litter only
Litter -f- standing dead plants
Coarse woody debris in forests'-'
Peat
Animals
Terrestrial (1970s estimate)
Humans (1995 estimate)
Ocean
Global, including protozoa and invertebrates
Caliche in desert soils
Fossil (recoverable as fuel)
Ocean water'
Reactive marine sediments
Earth's crust
1576
50
60
90
25-180
> 165
455''
0^
0.04
Q3
>aoo
4U01)
37 300
3000
75 000 000
Reference
Whittaker 1975
Ajtaycfw/. 1979
Olson et al. 1983
Whittaker 1975
Olson et al. 1983
Whittaker 1975
Olson c/ii/. 1983
Siegenthaler & Sarmiento 1993
Ajtay el al. 1979
Post ef al. 1982
Schlesinger 1991
Eswaran d al. 1993
Whittaker 1975
Ajtay ct at. 1979
Ajtay et al. 1979
Harmon & Hua 1991
Ajtay cl al. 1979
Corham 1995
Ajtay (•/ ai 1979
JS Amthor unpublished
Whittaker 1975
B<iwen 1966
Schlesinger 1982
Sundquist 1993
Sundquist 1993
Sundquist 1993
Lasaga ft al. 1985
" Values in parentheses account for a reduction in boreal forest phytomass b.isi'd on more recent and statistically appropriate
measurements (Botkin & Simpson IWO) of above-ground phytomass in North Americtin boreal forests
'' Many estimates of soil organic matter and litter cxchulf coarse woody debris and peat
'^ Excludes forest litter
° Only crude estimates of global coarse woody debris C content are available
'• Northern peatlands only
^ Dissolved inorganic C, dissolved organic C, and particulate C
period 1978-1994, rather than being a net uptake each
year (cf. Francey et ai 1995). The analysis of Francey ('( al.
(1995) indicated that terrestrial uptake of CO2 was not a
regulator of [CO2]a during the period 1982-1992, but that
ocean CO2 exchange did control changes in [CO2].,. This
perhaps reflects the nature of oceanic control of [CO2]n
on even short Hmescales (cf. long-term regulation of
[CO2]a by ocean-atmosphere C equilibrium [Walker
1991]), although Keeling et ai (1995) suggest that the
terrestrial biosphere caused most of the slowdown in
global [CO2]i, increase during 1989-1993. The slowdown
in [CO2]a increase ended in 1993, however, so if the
terrestrial biosphere was regulating [COJa- that regulation may have been short-lived.
A complication for estimating annual net storage of C
on land at the global scale is that some ecosystems may
be net sources of CO2, e.g. disturbed tropical forests
(Houghton et ai 1987; Houghton 1995) and 'warm' arctic
tundra (Oechel ct ai 1993). The discrepancy in balancing
known rates of CO2 release from fossil fuel combustion
(Marland et al. 1994), best estimates of net COj releases
from land-use changes (Houghton 1995), assumed (modelled) rates of oceanic CO2 uptake (see, e.g. Sarmiento
& Sundquist 1992), and measured increases in [CO2l,i
(KcMfling & Whorf 1994) is called the 'missing' sink for
anthropogenic CO2 (e.g. Sarmiento & Bender 1994). The
concept of a missing sink arises, in my opinion, from an
indefensible notion that ecosystems free from human
1995 Blackwell Science Ltd., Global Change Biology, 1, 243-274
TERRESTRIAL-PLANT RESPONSE TO ATMOSPHERIC [CO2I
249
error (or that ocean C exchange models are wrong, for
that matter). The 'imbalance' might be accommodated
by C storage in undisturbed ecosystems brought about
by several mechanisms, most notably 'COT fertilization'
and 'N fertilization' resulting from anthropogenic air
pollution (see More on missing sinks below).
The few Pg C y~' apparently stored (net) in the terrestrial biosphere during recent years (see estimates in Table
1) is a large fraction of the C released from fossil fuels,
but it is a small fraction of global terrestrial net primary
production (NPP; GPP less plant respiration) and would
be difficult to measure directly if all the C in question
was stored in plants. Moreover, if the net C stored on
land is sequestered in litter and soil organic matter, that
C pool would be increasing only c. 0.1-0.2% per year.
This would be impossible to measure directly in the short
term (a year to a decade).
It is often assumed that in the absence of human
1984 1986 1988 1990 1992
activities such as deforestation, the terrestrial biosphere
Year AD
would be in a steady state with respect to C. This
assumption, however, 'is far from self-evident' (Hampicke
Fig. 4 Global plant + soil net upt.ikt' of C during the period
1^82-1492 from the budget appro.ich of Francey et al. (1995) for
1980). Even if this were the case over the short term
three different \'alues of the gross flux of C out of (~ into) the
(decades), it is almost certainly untrue over recent millenterrestrial biosphere, Ct (•, 80 Pg C y"'; • , 100 Pg C y"'; and
nia. Between the LGM and c. 1700 AD, the terrestrial
• , 120 Pg C y^'), using a copy of the spreadsheet used by
biosphere apparently accumulated large amounts of C
Francey ct al. (1995) sent to GH Rau by R] Francey. Predicted
[Bird et al. (1994) suggest 310-550 Pg] while temperature
net uptake of C onto land is significantly different across this
and
[COiLi increased. Indeed, northern ecosystems may
range of Gi,s. Francey et al. (1995) used the value 80 Pg C y"'
be still recovering (storing C) from the last ice age.
for each year of the analysis (personal communication to GH
Rau) whereas terrestrial C flux estimates summarized in Table
Undisturbed northern peatlands, for example, are appar1 indicate larger Gi,s. Also, Gf, might change from year to year
ently accumulating C today, although at rates that are
due to regional and global variation in temperature, precipitamuch less than fossil fuel CO2 emissions (Harden et al.
tion, and other environmental factors. With G\., = 100 Pg G y"',
1992; Gorham 1995). The rate of growth of northernour copy of Francey's spreadsheet predicts a nut uptake on land
forest soil C pools, and the rate of production of elemental
of 1.16 Pg C y-' for the period 1982-1992, and with G^ = 120
C (charcoal that has a very long lifetime) during fires in
Pg C y"', the value is 0.76 Pg C y"'. For these calculations we
northern forests (see, e.g., Seiler & Crutzen 1980), are
have not altered the ^^C disequilibria terms of Francey et al.
(1995). Francey ct al. (1995) ascribe typical uncertainties of i 1.7
not known, but might make a significant long-term
Pg G y ' to their estimates of annual net fluxes. NB We do not
contribution to storage of C on land. In any case, oceans
obtain the values shown in Francey et al. (1995)'s fig. 2b with
were probably a considerable source of C to the atmoour copy of their spreadsheet. In any case, I suggest that Francey
sphere and to land since the LGM; perhaps c. 650 Pg C
t'f al. (1995) overestimate net uptake of G by land because Ct, in
were released from oceans. Accumulation of C on land
their analysis is too small. A reduction in G uptake on land is
even while atmospheric [CO2]a increased since the LGM
exactly matched by increased G uptake by oceans in this analysis.
reflects a lack of strong control on [COi]., by terrestrial
ecosystems; the atmosphere-ocean C equilibrium was
the main regulator of [CO2la over the course of the last
disturbance are in an annual steady state with respect to
several millennia (and see Walker 1991).
C. This results in an underestimation of recent net C
The amount of new land made available for terrestrial
storage by undisturbed terrestrial ecosystems. The anaecosystems during the last deglaciation was perhaps
lyses of land-use change by, e.g. Houghton (1995), only
about equal to the amount of land inundated by ocean
apply to areas that are altered by human land uses,
expansion. One assumption that follows from this is that
not the entire terrestrial biosphere. That estimates of
the amount of C stored on land did not increase due to
C exchanges associated with land-use change - which
the availability of new land area for plant growth because
include C uptake during regrowth of previously disthe net change in land area was near zero. This assumpturbed forests - do not balance modelled ocean C uptake,
tion is not true if a significant fraction of the biomass C
fossil fuel C releases, and atmospheric C accumulation is
on the inundated land is still stored on the continental
not evidence that the land-use related C releases are in
© 1995 Blackwell Science Ltd., Global Change Biology, 1, 243-274
250
J.S. A M T H O R
shelves in, e.g. sediments, or if the new land was more
productive since the LGM than the inundated land
was during the last glacial period. In those cases, the
inundated land need not be a large C source, but the
new land has clearly been a large C sink, with the net
result being a large new land sink for C as a direct result
of deglaciation.
Though some understanding of the past and the present
C balances of terrestrial plants and ecosystems exists, the
question at hand is; How will terrestrial plants respond
to elevated [CO2]a in the future? The answer to this
question has implications for the net effect of human
activities on [CO2I.1 and global climate during the coming
decades to centuries. Assessments of plant responses to
increasing [CO2]a must be based on either (i) experimental
treatment of plants or ecosystems with elevated [CO2]a
or (ii) mathematical models of pIant-CO2 interactions.
Observed relationships between |CO2]^ and plant processes during the past 200 years might be used to assess
plant--CO2 interactions, but it is unknown whether the
'shape' of CO2-plant relationships is the same below and
above present lCO2la. Also, few quantitative measures of
plant processes spanning the past 200 years are available.
In any case, the focus herein is on experimental treatments
of plants and ecosystems with elevated [CO2]a. Explanations of experimental observations, and therefore a predictive capability with respect to future higher-[CO2j.,s,
come from knowledge of underlying biochemical, physiological, and ecological processes and linkages.
Methods of studying plant responses to [CO2]a
Experimental techniques used to study plant responses
to ICO2la were outlined by, e.g. Allen ['( al. (1992). In
brief, individual-leaf chambers are commonly used, often
within the laboratory, to study short-term (seconds to
hours) photosynthetic responses to elevated lCO2]n, but
they (and branch chambers) also can be used for longterm elevated-CO2 treatments. Most whole-plant experiments are conducted in laboratory con trolled-environment chambers ('growth chambers') and glasshouses
with varying degrees of control on, and monitoring,
environmental conditions. Most of those studies involve
potted-plants, and light levels are often low compared
with conditions out-of-doors. Open-top field chambers,
such as those used to study plant responses to air
pollution, also are used to treat whole plants with elevated
[CO2I.,. Often, but not always, open-top field chamber
experiments use plants growing in the ground rather
than in pots. Portable and permanently situated closedtop chambers -'small greenhouses'- also can be used to
treat plants growing in the ground with elevated [CO2la.
During the past few years, free-air CO2 enrichment
methods were used to elevate [CO2]a across large areas
(e.g. 500 m^) of plants and soil not encumbered in
chambers or other structures. As with open-top chambers,
the use of free-air CO2 enrichment techniques follow
methods used earlier to study effects of air pollutants on
plants and ecosystems (McLeod 1993).
Each of the methods now in use (e.g. leaf cuvettes,
branch chambers, growth chambers, glasshouses, opentop field chambers, and free-air CO2 enrichment facilities)
has advantages and disadvantages compared with the
other techniques. That is to say, no single present method
is best for addressing all types of research related to plant
and ecosystem responses to elevated [CO2I,,. Indeed, a
combination of methods is often desirable. For example,
long-term free-air CO2 fumigation experiments can
include short-term measurements of leaf photosynthesis
and respiration using leaf cuvettes and short-term measurements of canopy CO2 exchange rate using portable
closed-top chambers (e.g. Hileman et al. 1994). In general,
it is important to focus attention on studies in the
field with unchambered plants and ecosystems because
'chamber effects' can be large relative to effects of elevated-CO2 on plants (e.g. Owensby et al. 1993a). Chamber
experiments are, nonetheless, important in the study
of mechanisms underlying plant responses to elevated
[CO2]a, and in any case, most data are from chamber
experiments.
Plants might acclimate and (or) adapt to changes in
[CO2la- Acclimation is a phenotypic adjustment to a shortterm, e.g. seasonal, change in the environment whereas
adaptation is a genotypic adjustment to a change in
prevailing environmental conditions, e.g. a millennialscale increase in [CO2]a or enhanced greenhouse warming. Acclimation may not become apparent for days to
weeks or even months, so very short experiments may
miss important acclimatory responses. Adaptation is a
(very) long-term process, so experiments with a duration
less than many plant life cycles will be unsuccessful in
assessing adaptation to elevated |CO2]a. On the other
hand, concern for effects of elevated [COTLI during the
next several decades to a century lessens somewhat the
need for immediate knowledge of potential adaptation
because adaptation will not occur in nature ftir many
long-lived plants for some time. A related experimental
problem is that [CO2]a is increasing gradually (c. 1.21
ppmv per year during the period 1958-1994; see Fig. 1)
whereas experimental treatments involve large and
instantaneous increases in ICO2la- It is unknown whether
plants respond differently to the continuing gradual
increase in lCO2]a compared with the rapid CO2 increase
used in experiments.
Questions of acclimation and, especially, adaptation to
elevated [CO2]fl raise the issue of truly long-term elevatedICO2]a treatments. A 25-year experiment started today,
for example, obviously would not be completed for
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T E R R E S T R I A L - P L A N T R E S P O N S E TO A T M O S P H E R I C [ C O , ]
25 years. The need exists therefore for elevated-[CO2l.,
treatments that were started long ago. Although far from
ideal 'experiments,' natural geological COT springs or
degassing vents have in some cases exposed terrestrial
ecosystems to elevated [COil;, for centuries or even
millennia. The main henefit of natural COT springs as
research tools is the long history of elevated |CO2la in an
otherwise (mostly) natural environment (Miglietta el ai1993b). This provides the potential to study (i) plants
acclimated and adapted to elevated ICO^la (ii) interspecies
competitive outcomes within elevated [CO2ld, and (iii)
changes in ecosystem biogeochemistry in response to
elevated [CO2],, (Koch 1993). Drawbacks of natural CO2
springs are the possibility of large fluctuations in ICOJI^T
on many time scales, and the lack of quantitative knowledge of past ICO^ljS. Nonetheless, natural CO2 springs
have the potential to provide information concerning
long-term plant and ecosystem responses to elevated
ICO2I., that cannot be obtained in any other way.
Although natural CO2 springs are imperfect as experimental tools, and the 'results' from long-term exposures
of plants to elevated [CO2]i,s near COT springs are only
beginning to be analysed. Nature has nonetheless
'spoken' about terrestrial-plant response to long-term
elevated [CO^lo- 1 visited several natural CO2 springs,
and I collected first-hand accounts concerning plant and
ecosystem processes and states around other CO2 springs,
in an attempt to understand what it is that Nature has
'said' about modem-plant responses to long-term CO2
enrichment. In all cases with which I am familiar, plant
communities surrounding CO; springs are not significantly more productive than communities more distant
from CO2 springs (the 'controls'). Elevated ICOJLT - more
than twice present [CO2]n in many cases - did nol result
in 'super vegetation' forming dense jungles of phytomass
(see, e.g., Korner & Miglietta 1994). Carbon dioxide
springs can enhance tree and herb growth under some
circumstances, as indicated by comparison of tree ring
widths and plant sizes near to and distant from CO2
springs (e.g. Miglietta ('(ai. 1993a; F Miglietta, C Korner &
S Hattenschwiler, personal communication), and elevated
ICO2],i might enhance soil C pool sizes (this has yet to
be quantified near CO2 springs), but clearly, a long-term
doubling (or more) of [CO2la near CO2 springs does not
cause a doubling of general plant size. Indeed, long-term
growth stimulations near CO2 springs may be modest in
comparison with growth responses obtained in shortterm ( s 10 years) experiments using chambers or freeair CO2 fumigation methods. But, even modest changes
in global terrestrial NPP might be equivalent to significant
fractions of C released during fossil fuel burning (Table
1). In any case, studies of plants near natural CO2 springs
have important implications for knowledge of overall
long-term terrestrial-plant responses to elevated
© 1995 Blackwell Science Ltd., Global Change Biohgi/, 1, 243-274
251
The corollary is that not too much should be made
of short-term elevated-CO2 experiments-especially those
involving chambers and (or) young plants-with respect
to rates of and amounts of long-term ecosystem-level C
flux and C storage, respectively.
Photosynthesis (CO2 assimilation)
Plants assimilate atmospheric CO2 ii^ th^ process of
photosynthesis, which uses solar radiation in the c. 400700 nm wave band as its source of energy (McCree 1981).
Terrestrial higher plants can be divided into three broad
categories with respect to their biochemical pathways of
photosynthesis: (i) C3, (ii) C4, and (iii) crassulacean acid
metabolism (CAM) (see, e.g., Edwards & Walker 1983;
Ting 1985). All three types of plant use the C3 pathway
of photosynthesis - which forms two molecules of glycerate-3-phosphate from one molecule each of ribulose-1,5bisphosphate and CO2 - but C4 and CAM plants use
additional, preliminary CO2 assimilation reactions that
concentrate CO2 inside plants. In general, Qy, C4, and
CAM plants are adapted for different environments
(Osmond et ai. 1982; Ehleringer & Monson 1993). Plant
species numbers are dominated by C3 plants - on the
order of 95% of higher-plant species are C3 - and C3
plants are generally more sensitive to [CO2]a than are C4
and CAM plants (Bowes 1993). Nonetheless, C^ plants
make a significant contribution to photosynthesis in
grasslands (and a few other ecosystems), and grasslands
are globally widespread and important to the global C
cycle (Ajtay ct ai. 1979) so C4 photosynthesis is more
significant to the contemporary global C cycle than is
indicated by species counts.
The enzyme ribulose-l,5-bisphosphate carboxylaseoxygenase (rubisco) is central to C3 photosynthesis. It is
a large, sluggish enzyme with a low affinity for CO2
(Miziorko & Lorimer 1983; Bowes 1991). It is generally
believed that rubisco is the most abundant enzyme on
Earth, at least in terms of mass (Ellis 1979), and it is an
important global biospheric pool of N. More importantly,
the carboxylase function of rubisco catalyses the carboxylation reaction of the photosynthetic reductive pentose
phosphate (PRPP) cycle, globally involving more than
100 Pg C each year.
In the present atmosphere, perhaps 10-30% of the C
assimilated in photosynthesis by C3 plants is almost
immediately released as CO2 in the process of photorespiration', which involves the oxygenase activity of rubisco. An increase in [CO2I,, has the potential to stimulate
net CO2 assimilation (photosynthesis less photorespiration) in C3 plants because (i) the Michaelis constant of
rubisco for CO2, ^^M(CO2), is high relative to present
[CO2]a (ii) CO2 competitively inhibits photorespiration,
and (iii) CO2 is required for the activation of rubisco
252
).S. AMTHOR
(CO2 molecules used in rubisco activation are not the
CO2 molecules assimilated during photosynthesis by that
activated rubisco) (Sage & Reid 1994). The first two
points, (i) and (ii), may be the most significant with
respect to a stimulation of global photosynthesis by
elevated ICO2l,i in C3 plants. But note that the response
of C^-plant CO2 assimilation rate to ICO2],, is concave
down, i.e. the first derivative of the photosynthetic rate
decreases as lCO2]a increases.
Many factors such as temperature, light, and water
supply, affect the response of leaf and canopy photosynthesis to lCO2],i (e.g. Radin el al. 1987), Based on the
biochemical kinetics of rubisco, an increase in lCO2]a
from 360 to 720 ppmv might be expected to enhance CO2
uptake by C3 plants on the order 10-100%, with a small
relative response at low temperature and a large relative
response at high temperature (Long 1991; Kirschbaum
1994). The interaction with temperature is related to the
positive relationship between r» and temperature (see
footnote 1) and has important implications for global
photosynthesis with concomitant global increases in
|CO2ln and temperature. Predictions of photosynthetic
stimulation by elevated ICO2I.1 are consistent with the
few canopy-level CO2-exchange measurements made to
date (e.g. Drake & Leadley 1991; Pinter et al. 1995).
Although elevated lC02la stimulates^ photosynthesis
under many circumstances, the fate of the 'extra' C taken
up by plants in elevated ICO2I.1 is not obvious. The extra
C could be added to plant structure in additional growth,
or respired by the plant, or added to soil C pools via
'The ratio of photorespiration (PR) to photosynthesis (P) can be
estimated from P^ / P ^ T. / ICO2I,- where V. is the [CO:1 in
chloroplasts at which photosynthetic carboxylation matches
photorespiratory decarboxylation and [CO2IC is the ICO2I inside
chloroplasts. (In this notation, CO2 concentrations in chloroplasts
are the equiiibrium gas phase concentrations.) The value of P.
depends on temperature. Based nn (ordiin & Ogren (1984), F- is
c. 20 ppmv CO2 at 5"C .md c. 54 ppmv CO2 at 30"C (see also
Woodaiw & Berry 1988). At present ICO2L, [COi]^. may be in
the range 180-270 ppm CO2 during much of the day for many
Ci plants (see, e.g., Caemmerer & Evans 1991; Lloyd et ai. 1992;
Loreto et al. 1992). Thus, the ratio PR / P may normally be in
the range 0.1O-0.30 at present [CO2I., in C3 plants. Due to their
CO2-concentrating prtKesses, C4 and CAM plants have low rates
of photorespiration at present ICO2]a.
Contrary to a positive response of leaf CO2 assimilation rate to
increased ICO2].,, there are several well documented cases of
short-term inhibition of photosynthesis caused by 'supraoptlmal'
CO2 levels (e.g., Woo & Wong 1983 and other references in
Harley & Sharkey 1991). Such an inhibition of photosynthesis
caused by CO2 may occur at tCO2]j's only slightly greater than
present global iCO2la- It is possible that this response to elevated
CO2 is related to reduced recycling of C in the photorespiratory
cycle, i.e., a lack of glycerate entry into chloroplasts (Harley &
Sharkey 1991). The significance of such a phenomenon to the
global C cycle has not been assessed.
enhanced exudation from roots or accelerated root growth
and death, i.e. root turnover. Some combination of these
fates may be the most likely outcome, although the fate
of extra assimilated C may change over time in response
to acclimation, adaptation, and feedback processes. And,
the photosynthetic response to elevated tCO2l., and the
assimilation of extra C may itself changeover time, owing
to acclimation of photosynthesis to elevated [CO2laPhotosynthefic acclimation to elevated lCO2]a
Long-term (weeks to years) CO2-enrichmcnt often, but
not always, results in reduced amounts of photosynthetic
pigments and enzymes such as rubisco in leaves of C3
plants (Bowes 1991, 1993; Rowland-Bamford ct ai 1991;
Van Oosten ft ai. 1992; Webber el ai. 1994; Wilkins cl al.
1994; Jacoh et ai. 1995). A downregulation (acclimation) of
photosynthetic capacity in response to long-term elevated
[CO2I.1 can limit the photosynthetic response of C^i plants
to elevated [CO2],i (Sagec^?/. 1989;Gunderson & WuUschleger 1994; Sage 1994). Downregulation of photosynthesis
has important positive implications for resource-use efficiency by plants; that is to say, downregulation may have
more positive impacts on plant N balance and growth
than it has a negative effect on photosynthetic CO2
assimilation (Sage 1994). Plants grown in small pots or
with low nutrient availability, i.e. plants having significant
limitations to growth other than photosynthetic C assimilation, may show the greatest degree of photosynthetic
downregulation when grown in elevated ICO2L (Arp
1991; Hogan et ai. 1991; Thomas & Strain 1991; Sage
1994). This is a potential artifact of some studies using
potted plants and is probably related to the balance
between C source activity and C sink activity, although
results to date are somewhat contradictory (Pettersson &
McDonald 1994). Even plants growing in the ground,
however, may generally show some degree of photosynthetic downregulation in response to long-term elevated
[CO2L (Webber t'ffl/. 1994; Jacob I'/rt/. 1995). It is significant
that recent biochemical studies show possible photosynthetic acclimation in plants grown in elevated |CO2],i
but for which previous reports suggested a lack of
photosynthetic downregulation. For example, leaf CO2exchange measurements indicated a lack of photosynthetic acclimation in Citrus aurantium trees grown in
elevated compared with ambient [CO2L1 (Idso & Kimball
1991), but later biochemical studies revealed a decrease
in leaf soluble protein levels-an indication of downregulation - in those same trees (Webber et ai. 1994; and see
Jacob fM/. [19951 ^or a similar chain of events with Scirptis
olneifi elevated-1CO21.T research). And, leaves of Quereiis
trees growing near natural CO2 springs, which are presumably adapted to a higher-[CO2la environment, may
also downregulate photosynthetic capacity compared
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T E R R E S T R I A L - P L A N T R E S P O N S E TO A T M O S P H E R I C [CO2]
with leaves on trees growing more distant from CO2
springs (CL Hinkson, WC Oechel, F Miglietta & A Raschi
personal communication). Tlie downregulation of
QmTL"i/s-leaf photosynthesis near CO2 springs is observed
in old leaves rather than in young leaves.
In some cases (Curtis & Teeri 1992), elevated ICO2la
may increase leaf longevity, which will in part mitigate
effects of photosynthetic downregulation on seasonal
CO2 assimilation in ele\ated ICO2I.,, but in other cases
(Pinter I'f til. 1996) elevated |CO21.T may reduce leaf life
span. And, an exception to photosynthetic downregulation may exist in N2-fi>;ing plants. For example, rubisco
capacity was apparently increased in leaves of black aider
[Aitnts glutinosa) plants grown in elevated compared with
present ambient |CO2].T (Vogel & Curtis 1995).
Photosynthetic acclimation to elevated [CO2I,, might
be temperature dependent, but this has been rarely
studied. In Medica^o saliva leaves, downreguiation of
photosynthesis in elevated LCO2I,, was observed at 30 "C
but not at lower temperatures, whereas in Dactylus glomeraln lea\t's, photosynthetic acclimation was apparent at 15
and 20 ''C but not at 25 or 30 °C (Ziska & Bunce 1994a).
This is an important aspect of plant response to combined
increases in global [CO2]a and temperature that needs
further study.
A common result of exposure of plants to elevated
ICO2I.1 is increased accumulation of nonstructural carbohydrates in leaves (Wong 1990; Hendrix ct ai. 1994;
Komer & Miglietta 1994), which results from enhanced
photosynthesis. TTie accumulation of nonstructural carbohydrates, and in particular soluble sugars, may be the
trigger for acclimation of photosynthesis in response to
elevated [CO2l,v Sugars, e.g. glucose and sucrose, can
repress photosynthetic gene expression and lead to reductions in the amount of photosynthetic pigments and
PRPP cycle enzymes, including rubisco (Sheen 1990,1994;
Stitt et al. 1990; Krapp ct ai. 1991, 1993; Cheng ct ai. 1992;
Schafer et al. 1992; Harter et al. 1993; Van Oosten et ai.
1994; Webber ct ai. 1994). Repression of photosynthetic
genes by sugars (i.e. photosynthetic end-product repression) may underlie photosynthetic acclimation to elevated
[CO2la, and probably plays a role in maintaining a balance
between carbohydrate source and sink activities (Sage
1994; Webber et ai. 1994). Repression of photosynthetic
genes by sugars might be most extensive when N supply
is limited, in part as a mechanism of increasing carbohydrate sink activity by mobilizing N in mature leaves and
making it available to growing organs (Paul & Stitt 1993;
Webber ct ai. 1994).
Two of thf most important questions relating leaf
physiology to the global C cycle are: Will enhanced
photosynthesis in a future, higher-[CO2]., world lead
to downregulation of photosynthesis at the ecosystem,
regional, and global scales? If so, to what extent? General
253
answers to these questions, i.e. answers that can be
applied globally, may be slow in coming. In the meantime,
the weight of the evidence indicates that photosynthetic
acclimation to elevated [CO2]j is common, but that the
acclimation is rarely complete.
Feedback inhibition of photosynthesis
In addition to long-term acclimatory responses to an
accumulation of nonstructural carbohydrates in leaves,
i.e. downregulation of photosynthesis, an increase in the
size of leaf nonstructural carbohydrate pools may result
in short-term end-product feedback inhibition of photosynthesis (Azcon-Bieto 1983). This end-product inhibition
of photosynthesis may be related to inorganic phosphate
cycling in leaves (Herold 1980; Foyer 1988). It may be
most important in the short term, e.g. during the course
of a single day, as com pared with seasonal photosynthesis.
Tlius, both short-term and long-term negative feedbacks
on photosynthesis from leaf nonstructural carbohydrate
pools can exist in an elevated-[CO2i environment.
So although the stimulation of photosynthesis caused
by elevated ICO2]a is a negative feedback on the increase
in global [CO2L1, there are also negative feedbacks on the
response of photosynthesis to ICO2L- The magnitudes of
each of these feedbacks are unknown, although present
annual CO2 emissions associated with fossil fuel use are
equivalent to only c. 5% of the annual balance of terrestrial
higher-plant photosynthesis and photorespiration, i.e.
GPP, so small changes in global photosynthesis might
have large effects on fossil-fuel-driven [CO2U increases.
But, many long-term and multi-life-cycle experiments
must be conducted in order to sort out likely higherplant photosynthetic responses to increasing [CO2]j over
the decadal to century time scale, and again, over the
very long-term, ocean-atmosphere C equilibrium will
control
Growth
One potential result of stimulated photosynthesis is
enhanced plant growth. That is, 'additional' photosynthate can be used in the biosynthesis of 'additional'
plant structural dry matter (sensu Penning de Vries et al.
1979) such as membranes, enzymes, and cell walls. A
change in plant growth or C accumulation over a year
or 'season' is in many ways the most meaningful measure
of plant response to elevated [CO2].,. It is a more significant assessment of the effect of plants on [CO2L than
measurements of either photosynthesis or respiration.
Effects of elevated [CO2la on plant growth have been
studied, and reviewed, frequently (Lawlor & Mitchell
1991; Ceulemans & Mousseau 1994; Rogers et ai. 1994).
In general, growth of C3 plants is positively related to
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254
J.S. AMTHOR
a- Growth of C4 plants can also be enhanced by
elevated [C02la, but the magnitude of response is generally less than that observed with Ci species. The differential growth response of C3 compared with C4 plants
is presumably related to the stronger response of C3
photosynthesis to elevated [CO2I,,. Forest-tree species
mean response to a doubling of |CO2h, was a 32','.. increase
in dry mass accumulation (Wullschleger et ai. 1995b).
(Forest growth, and any changes in forest growth due to
increasing ICO2I.1, are especially important to the global
C cycle; Ajtay et al. [1979] suggest that as much as 40%
of global terrestrial NPP occurs in forests.) Whereas
elevated [CO2]a has the potential to enhance forest tree
growth, it often has been suggested that when N or
water are limited, plant growth will not be significantly
stimulated by elevated ICO2I., (e.g. Kramer 1981; who is
frequently cited in support of this view). Available data,
however, indicate that the relative increase in tree growth
brought about by elevated ICO2].i is about the same with
and without N deficiency and with and without water
limitation (Wullschleger ct al. 1995b). But, available data
are all of a short-term nature, i.e. from experiments lasting
a few years at most. Long-term enhancement of forest
tree growth with N deficiency is only possible if plant
N/C ratio decreases, which may in fact tKcur in elevated
[CO2L, (Field et at. 1992).
Unfortunately, almost all studies with forest tree species
are limited to seedlings or saplings growing in chambers,
often growing in pots, rather than large trees growing
naturally for long periods of time. It is not known whether
seedling/sapling responses to elevated [CO2ln reflect the
response of large trees to [CO2]a. Moreover, it has been
suggested that plants grown in pots have a limited
growth response to elevated lCO2]a because they are
grown in pots. To the extent that this is true, pot studies
underestimate growth response to elevated [CO2I.1 by
plants in the field. In at least one case (one of only two
direct studies of pot-size effects on growth response to
elevated [CO2].i?), however, the relative stimulation of
growth by elevated [CO2]j was greater in 'small' compared with 'large' pots (Thomas & Strain 1991). But, in a
comparison of growth in 270 vs. 350 ppmv CO2, growth
of plants in large pots responded positively to ICO2L
whereas growth of plants in small pots did not (Thomas
&c Strain 1991). The (only?) other direct study of pot-size
effects on growth responses to elevated [CO2la indicated
that pot size per sc need not influence growth in elevated
[CO2L) and that soil nutrient concentrations may be more
important than pot size in affecting growth response to
[CO2la (McConnaughay et al. 1993b; Bemtson ct ai. 1993).
The issue of pot size is far from resolved, however. Both
studies addressing it were of short duration (4 weeks
and 10 weeks, respectively). Both studies used what I
would call small and very small pots, not small and large
pots. Thus, the long term effects of truly large (fieldlike) and small rooting volumes on growth responses to
elevated [CO2I., ha\ e not been addressed. As prt'\ iously
noted, however, plants in nature 'do not have unlimited
below-ground resources with which to maximize growth
in a CO2-rich world' (McConnaughay et ai. 1993a),
although they commonly have access to at least more
volume than they do in most pots used for research.
And, the assertion that small pots iieeii not limit growth
responses to elevated ICO2I., is not the same assertion as
small pots do not limit growth responses.
There is special concern for the effects of increasing
ICO2la on the growth of crops. Both the potential stimulation of crop growth by elevated [CO2].i and the effects of
CO2-related climatic change on crop productivity are of
interest. Most data indicate that crop yield Is enhanced
by elevated ICO2]a, but only a relatively few experiments
were conducted under field conditions. Economic yield
in C3 crop species responds to a doubling of [CO2ia vv'ith
on average an c. 33% increase - remarkably similar to
the relative stimulation of dry mass accumulation by
forest tree species in doubled [CO2].i - and C4 crop species
respond with an e. 10% increase in economic yield (Rogers
ct ai. 1994; see also Lawlor & Mitchell 1991; Pinter ct ai.
1996). But, I suggest that effects of future increases in
[CO2I.1 will have only a minor impact on overall agricultural productivity, The reason for this is that developments in technology and management have resulted
in large increases in productivity over time and large
increases due to technology (which includes breeding)
might be anticipated in the future, whereas by comparison, effects of increasing |CO2l,i on crop growth are
minor. An estimate of the relative effect of |CO2l,i compared with technology on wheat yield can be obtained
by comparing wheat growth in different ICO2LS with
historic changes in wheat yield. Using data presented by
Polley ct al. (1993), I calculated that wheat (cv. Yaqui 54)
above-ground dry mass at maturity was increased e. 447o
by growth in 350 compared with 280 ppmv CO2 in CO2depletion experiments. By contrast, using U.K. mean
wheat yield data for the period AD 1200-1993 summarized
in Amthor & Loomis (1996, e.specially our fig. 2), I
estimate that wheat yield has increased c. 800"''.. (!) as
[CO2] of the actual atmosphere increased from 280 to 350
ppmv during the past c. 300 years. Although this analysis
is not overly rigorous (e.g. Polley ct at. [1993] reported
above-ground biomass and we summarized grain yield),
it indicates that only c. 5% of the increase in U.K. wheat
yield that has occurred during recent centuries can be
attributed to increasing [CO2].v That is to say, increases
in crop productivity are driven mostly by technology
and management (see, e.g. Evans 1993) rather than by
environmental changes, and effects of continued increases
in ICO2la may have small effects on productivity com© 1995 Blackwell Science Ltd., Global Change Biology. 1, 243-274
T E R R E S T R I A L - P L A N T R E S P O N S E TO A T M O S P H E R I C [CO2]
pared with continued improvements in management and
breeding. For example, according to Evans (1993 [p. 307]),
'there is no indication that the genetic yield potential of
any of the major crops is reaching its limit. Indeed, for
wheat [Triticum aestivum], barley [Hordeitm vitigare] and
maize [Zca mai/s\ in some environments, the rate of
improvement is accelerating.' At the same time, the
relative crop growth response to increasing [CO2]a will
diminish as |C02].,s increase, i.e. the relationship between
crop growth and [CO2]a is concave down. A similar
analysis can be carried out for rice {Otyza sativa) using
growth, yield, and [CO2],i data in Baker ct al. (1992) and
Amthor & Loomis (1996). Moreover, from the perspective
of the global C cycle, much of the C assimilated in
crops is oxidized and released as CO2 within a year of
assimilation during feeding of humans and livestock (this
is not, however, true for lint harvested from cotton
[Gosfiijpiuin iursutimt]). And, crops probably contain less
than T'fi of the C in terrestrial plants (Ajtay cl at. 1979),
so even a doubling of crop phytomass would have
a negligible impact on the global plant-C pool size.
Agricultural-soil C pools may be enhanced by elevated
|CO2li, due to increased organic-C inputs from roots and
stubble, but conversion of land to agriculture from more
natural vegetation in the first place generally results in a
loss of soil C (Houghton 1995). On the whole, increased
crop productivity due to increasing ICO2l.i is likely to
have no more than minor effects on the global C cycle;
changes in land use associated with changes in geographical patterns of agriculture due to continued increasing
human population and to climatic changes will probably
have more significance effects on global terrestrial C
pools and fluxes than will changes in crop productivity.
A simple way to summarize the effects of [CO2I., on
plant growth, i.e. NPP, is the empirical coefficient p used
as follows (e.g. Gifford 1980; Goudriaan 1993)
NPP, = NPPo [1 + p In (C,/Q,)l
NPPo ^ 0; C,, Co > 0,
(1)
where NPPg is NPP at a given atmospheric CO2 concentration C,v NPPii is NPP at a reference or baseline atmt>
spheric CO2 concentration CQ, and In (-t) is the natural
logarithm of x. Note that p applies to the primary effects
of a change in ICO2IJ on plant growth, not any secondary
effects mediated through climatic change. This p, and
similar parameters, is called the 'biota growth factor' and
the 'biotic growth factor' (Bacastow & Keeling 1973;
Gifford 1980). The logarithmic response of NPP to ICO2I.,
used in (1) was questioned by Gates (1985), who suggested that P might be better calculated with a MichaelisMenten expression, but Gifford (1980) and Goudriaan
et ai. (1985) adequately defended the use of (1), at
least for moderate (a few hundred ppmv) changes in
atmospheric
© 1995 Blackwell Science Ltd., Globai Change Biology. 1. 243-274
255
A P value [sensu (1)] of unity represents a 69% increase
in NPP with a doubling of [CO2]a whereas P is c. 0.43
if doubled [CO2];, increases plant growth by 30% (cf.
summaries for forest tree seedlings and crops outlined
above). Several values of p were used in assessing the
effects of increasing ICO2l,i on the global C balance with
simple models of the terrestrial biosphere (summarized
in Wullschleger et at. 1995b). For example, Rotmans &
den Elzen (1993) were able to 'balance' the global C
budget with P = 0.4 in their model when effects of
temperature on NPP and heterotrophic respiration
(decomposition) were also considered. Other typical
values of p used in global C cycle models are in the
range 0.2-0.5 (Wullschleger t'f at. 1995b), which are consistent with experimental data summarized in Amthor &c
Koch (1996) and WuUschieger ct ai. (1995b). In a recent
survey of the literature (and some unpublished datasets),
however, we could find no measurements of NPP in
intact, non-crop ecosystems treated with elevated [CO2ld;
abovc-gromid NPP was estimated a few times, and wholeecosystem CO2 exchange (including decomposition) was
measured in a few cases, but effects of elevated ICO2L
on NPP in natural ecosystems have not been rigorously
studied (Amthor & Koch 1996). Thus, we are mostly in
the dark with respect to knowledge of NPP responses by
natural ecosystems to increasing [CO2],,To put into perspective any plant growth (NPP) stimulation that might occur with increasing |C02]a/ a 10%
increase in present global terrestrial NPP is about equivalent to present fossil fuel C emissions (though opposite
in 'sign'—see Table 1). This means that a 1O''.> increase in
present global terrestrial NPP would about balance present fossil fuel C emissions. But, could the C associated
with extra NPP be stored in the biosphere over the long
term, or would it be returned to the atmosphere in
short order during subsequent litter production and
decomposition? Some of the C associated with increased
NPP resulting from increased ICO2I,-, would probably
remain in the biosphere, but not all of it. The nature of
the terrestrial C cycle is such that NPP does not represent
permanent C storage; only a small fraction of the C in
terrestrial-plant NPP subsequently enters C pools with
lifetimes of 1000 or more years. Most of the C in NPP is
much more labile.
The negative feedback on the increase of ICO2]d mediated through enhanced photosynthesis (GPP) and plant
growth (NPP) cannot, by itself, reverse the upward trend
in ICO2I.-, because increased GPP and NPP depend on
increasing [CO2LT It can, however, slow it. Increased area
of land covered by vegetation, or major changes in
vegetation type brought about by, e.g. large-scale afforestation, couid halt or even reverse the increase in ICO2I.,
through significant increases in C storage on land if fossil
C releases are significantly reduced (see also Sarmiento
256
J.S. AMTHOR
et ai. 1995), but this is unlikely for at least many decades,
and if oceans do not then become significant sources of
atmospheric CO2. Most estimates are that the oceans are
now sinks for atmospheric CO2 (Sarmiento & Bender
1994) so they are absorbing fossil C and limiting the
increase in
An extreme view
A minority view (Idso 1991a) was that the 'real-world P
factor may well be three to four or possibly even five
times greater than what has heretofore been believed.'
Idso (1991a) claimed that large values for p can be found
from 'all the available physical and biological evidence,'
but in point of fact, the lion's share of the relevant data
were summarized in Wullschleger ct ai. (1995b) and
Amthor & Koch (1996) and these summaries indicate that
real-world p is probably about 'what has heretofore been
believed li.e. P = 0.3-0.7].' Idso (1991b) also claimed that
'increases in atmospheric CO2 result in growth rate
increases of trees five times greater than growth rate
increases of nonwoody plants' (italics added), yet data
from hundreds of elevated-CO2 experiments summarized
in, e.g. Lawlor & Mitchell (1991), Ceulemans & Mousseau
(1994), Rogers et al. (1994), and Wullschleger ct al. (1995b),
make it impossible to objectively conclude that trees
generally respond much more positively to elevated
[CO2la than do herbaceous plants. While 1 reserve judgement on the ratio of tree to herbaceous plant growth
responses to elevated ICO2l,i in nature, the data now
available to Idso and to me indicate that herbs and trees
differ by much less than a factor of five, if they differ at
all, in their growth responses to elevated [CO2|,T Kohlmaier ct al. (1989, 1991) clearly outlined other difficulties
with Idso's inflated P that do not need to be repeated here.
Some of Idso's notions of extreme positive tree growth
responses to elevated [CO2L come from his relatively
long-term experiments with Citrus aurantium growing in
the ground in open-top chambers (e.g. Idso & Kimball
1993). In that experiment, photosynthesis and growth
were greatly stimulated by elevated ICO2]a- Is the basis
for such a large positive response to [CO2]., by Citrus
known? Maybe. The mesophyll or internal leaf conductance to CO2 transfer in C. aurantium leaves can be very
low compared with other plants (Loreto et al. 1992) and
this tends to result in low CO2 concentrations inside
chloroplasts (see also Lloyd ct al. [1992] with respect to
C. paradisi and C. iimon). The outcome is that the CO2
concentration 'seen' by rubisco is very low in Citrus
leaves, and this leads to a relatively strong response to
an incremental increase in the supply of CO2 because the
photosynthesis vs. ICO2] function is generally increasing,
but is concave down. Thus, C. aurantium should respond
strongly-in relative terms-to elevated [CO2]j, at least
with respect to photosynthesis, and it 'is probably not a
good plant from which to generalize about CO2 responses
given that its Imesophyll conductance! can be so low'
(Loreto ct ai. 1992), but that is just what Idso (1991b) did.
Although the C. aurantium experiment of Idso & Kimball (1993) was 'designed to o\ ercome the problems that
have plagued most prior tree experiments,' it unfortunately succumbed to what are the most serious problems
with such experiments: the plants were (/) grown outside
their native habitat (Phoenix, Arizona is nt)t by nature a
forest of Citrus) so its applicability to natural ecosystems
is possibly lost, (//) flood-irrigated instead of heing subjected to natural precipitation, and {iii) fertilized instead
of allowed to grow on naturally available soil nutrients.
That is to say, the plants were grown as a horticultural
crop rather than as natural vegetation. The experimental
results, however, were extrapolated to "earth's 'global
forest'" (Idso & Kimball 1993; p. .^51), although the
experiment is unlike any of Earth's forests. And, as
mentioned above. Citrus is expected to respond more
strongly to elevated [CO2],, than do Earth's forests, especially when Citrus is grown in the warm (often hot)
conditions of a plastic chamber in Phoenix, Arizona- In
a more realistic experiment - with a forest tree species
growing in a forest soil - elevated ICO2]., compared with
present ambient lCO2la did not significantly enhance tree
dry mass accumulation over the course of three years
(Norby ct at. 1992).
In another case of exaggeration, tdso & Kimball (1993)
wrote that, with respect to their single experiment with
irrigated and fertilized C. aurantium and one analysis of
the seasonal cycle of [CO2la at Mauna Loa by Pearman
& Hyson (1981; cf. Kohlmaier W at. 1989), 'it would appear
to make it almost impossible for one to derive any other
conclusion than that which looms so obvious from this
comparison, namely, that /(// ofEartit's trees, in the mean,
likely respond to atmospheric CO2 enrichment to the
same phenomenal degree 12.8 times as much growth in
655 compared with 355 ppmv CO2I that sour orange trees
|did in our single experiment]' (italics added). Not only
is it possible, but it is necessary to come to a much
different conclusion. Based on available data, forest tree
species respond to atmospheric CO2 with a P of perhaps
0.3-0.7, or c. 1.2-1.5 times as much growth at 700 compared with 350 ppmv CO2 (Amthor & Koch 1996). That
is what the data say. Although, as stated above, only <i
poor understanding of the effects of increasing lCO2]fl on
NPP in the 'real world' exists, this is not justification to
disregard the facts that are at hand in favour of wild
claims of 'phenomenal' growth responses by aii of Earth's
forests. The honest scientific view musi be more guarded.
For as Idso (1991c) wrote, 'when faced with a conflict
between someone's theory and many other people's
measurements, it is usually wisest to go with the measure© 1995 Blackwell Science Ltd., Global Change Biology, 1, 243-274
TERRESTRIAL-PLANT RESPONSE TO ATMOSPHERIC ICO.]
ments.' Idso's {1991b) published theory was lhat P was
2.9 Ifrom (1): P = 1.8/In (655/355) « 2.91 for 75% of
Etirth's terrestrial vegetation, i.e. the trees, whereas a
summary oi all the measurements with forest tree species
indicates a |i of c. 0.3-0.7 {Wulischleger ef ai 1995b),
which is about the estimate of P obtained for nonwoody
plants and ecosystems (Amthor & Koch 1996); so, the
wild theory that 'increases in atmospheric CO2 result in
growth rate increases of trees five times greater than
growth rate increases of nonwoody plants' {Idso 1991b)
is gone and 'many other people's measurements' {summarized in, e.g. Amthor & Koch 1996; Wulischleger et ai
1995b) remain.
Respiration
The rate of plant respiration {i.e. glycolysis, oxidative
pentose phosphate network, tricarboxylic acid cycle, and
related mitochondrial electron transport and oxidative
phosphorylation) is presumably often controlled by the
rate of growth and maintenance processes through classic
respiratory control mechanisms (Beevers 1970,1974). That
is to say, respiration slows when respiratory products
(i.e. ATP, NAD(P)H, and C-skeleton intermediates) accumulate in cells, and respiration proceeds when respiratory
products are consumed, through a series of feedback
mechanisms. This implies that respiratory responses to
elevated ICO2I., rnay result mainly from changes in plant
growth {and therefore metabolic costs of growth) and
plant size (and therefore metabolic costs of maintenance);
bigger plants are generally more expensive to grow
and to maintain, which results in faster whole-plant
respiration (Beevers 1970; McCree 1970; Thornley 1970).
This is not, however, the same as faster whole-plant
specific {per unit dry mass) respiration rate.
Indirect effects of elevated ICO^Ja on respiration
One link between ICO2]., and respiration rate is likely to
be via nonstructural carbohydrates. An increase in the
amount of nonstructural carbohydrates may stimulate
growth and related activities, and this would likely pull
growth respiration along at a faster pace {Amthor 1994a).
But in order for respiration {and growth) to proceed at a
faster rate, respiratory capacity might need to increase as
well. Indeed, it appears that {i) growth processes, (ii)
respiratory capacity, {iii) futile cycling and respiratory
activity that may consume 'excess' nonstructural carbohydrates, and (iv) related reactions, may be positively
related to tissue sugar concentrations {Baysdorfer & Van
Der Woude 1988; Bingham & Farrar 1988; Wenzler et al.
1989; Stitt et al. 1990; Williams & Farrar 1990; Farrar &
Williams 1991; Geigenberger & Stitt 1991; Cheng et ai
1992;Schafer(*/rt/. 1992; JHH Williams eh;/. 1992; Bingham
© 1995 Blackvvx-ll Scic-nce Ltd., Global Change Biology. 1, 243-274
257
& Stevenson 1993; Krapp & Stitt 1994). These responses
to carbohydrate concentration, which all are directly or
indirectly related to respiratory metabolism, would be
expected to contribute to a balance between carK)hydrate
production and carbohydrate use in different lCO2laS (or
across other environmental gradients that affect the rate
of carbohydrate production). Thus, an increase in [CO;].,
can stimulate photosynthesis {see abo\'e), which can
enhance levels of nonstructural carbohydrates, which
can stimulate (or induce) growth and other processes
consuming respiratory products, which would tend to
then stimulate respiration. This chain of events is an
imiirect effect of elevated 1C02],, on respiration because
any factor other than tCO2lj that also stimulated photosynthesis and increased the rate of production of nonstructural carbohydrates might elicit the same respiratory
response (Amthor 1991).
A change in plant (bio)chemical composition brought
about by elevated [CO2Ja might affect rates of respiration
independent of any changes in plant growth and size.
For example, plant soluble protein concentration may be
negatively related to ICOi]., {Ziska & Bunce t994a; Jacob
['/ al. 1995) and this might be expected to cause a reduction
in specific maintenance respiration rate because respiration
associated with protein turnover can be a significant
fraction of total maintenance respiration {Penning de
Vries 1975; De Visser et al. 1992; see also Amthor 1994b;
Bouma et al. 1994). There is evidence that elevated ICO2],,
can in fact reduce specific maintenance respiration rate
{Silsbury & Stevens 1984; Bunce & Caulfield 1991;
Wulischleger & Norby 1992; Wulischleger et ai 1992;
Ziska & Bunce 1993; Bunce 1995a). There are also reports
of increased leaf specific maintenance respiration rate
{Thomas ct ai 1993; Thomas & Griffin 1994), but I have
shown {Amthor 1996) that, in those particular cases, the
stimulation of leaf respiration caused by elevated lCO2]a
was probably due to increased leaf respiration to support
increased phloem loading and transport, resulting from
increased photosynthesis, rather than being due to an
increase in the rate of leaf maintenance processes.
Growth costs {i.e. CO2 released in processes associated
with growth per unit C added to new plant structure)
also may be affected by a change in plant composition.
When an increase in lCO2].i causes a reduction in plant
protein concentration, or an increase in carbohydrate
concentration, it might then reduce growth costs and
therefore growth respiration per unit of plant growth
(based on Penning de Vries et ai 1974). Data from
the few experiments addressing this issue indicate that
elevated ICO2IJ does not affect, or causes a slight decline
in, the C costs of plant growth (Silsbury & Stevens 1984;
Loomis & Lafitte 1987; Baker et al. 1992; Wulischleger &
Norby 1992; Wulischleger ct ai 1992; Griffin ct al. 1993;
258
J.S. AMTHOR
Thomas et ai 1993; Amthor et ai 1994; Thomas & Griffin
1994; Wulischleger et ai 1995a).
Changes in respiration brought about by changes in
plant composition also are indirect effects of lC02]d
because any other factor that caused the same change in
composition would be expected to cause a similar change
in respiration. A simultaneous increase in plant growth
and decrease in plant protein concentration (not necessarily whole-plant protein content) might cause a decline in
whole-plant specific respiration rate {moi CO2 kg"' s"')
without a change in, or perhaps even an increase in,
respiration per plant (mol CO2 s"' per plant) or plant
respiration per unit ground area {mol CO2 m"^ s"').
Direct effects of ICOzJa on respiration
In addition to the indirect effects of lCO2la on respiration
mediated through growth and maintenance processes,
there are several reports of a direct inhibition of respiration
by elevated [CO2L that may be independent of respiratory
control processes {Gale 1982; Reuveni & Gale 1985; Bunce
1990, 1995a; Amthor et ai 1992; Byrd 1992; Mousseau
1993; Qi et ai 1994; Downton & Grant 1994; Thomas &
Griffin 19Q4; Villar et al. 1994; Ziska & Bunce 1994b;
Teskey 1995). The apparent direct inhibition of respiration
by elevated ICOi],! may, however, be due to effects on
non respiratory metabolism, e.g. stimulated dark CO2
fixation and organic acid synthesis {Amthor 1996).
In a simple analysis, a reduction in respiration improves
a plant's C balance, but it must be remembered that plant
growth and maintenance each require respiration. Thus,
a limitation on respiration might in turn limit growth
and the maintenance processes required for plant health.
Indeed, it was suggested on several occasions {Gale 1982;
Reuveni & Gale 1985; Amthor 1991; Wulischleger et ai
1992) that to the extent that elevated [CO2]., causes a
direct inhibition of respiration, elevated ICOj]^ may be
detrimental to growth and {or) maintenance processes.
This view is supported by the short term experiments of
Gale {1982) and also by the 21-day experiments in which
soybean seedlings were exposed to elevated [CO2]a during the night, but not the day (Bunce 1995b). A direct
inhibition of respiration - or more correctly, CO2 efflux
in the dark - does not always, however, occur as a result
of elevated 1CO2].T {Bunce 1990; Byrd 1992; Ryle et ai
1992a,b; Mousseau 1993; Ziska & Bunce 1994b).
Available evidence indicates that the ratio of plant
respiration to photosynthesis usually remains constant
or declines in elevated ICOj],, {Hughes & Cockshull 1972;
Gifford 1977; Silsbury & Stevens 1984; Du Cloux et al.
1987; Gaudillere & Mousseau 1989; Bunce 1990; Ryle et ai
1992a,b; Reid & Strain 1994; but see Nijs et al. 1989 and
Den Hertog et ai 1993 for reports of increases in the ratio
respiration/photosynthesis caused by elevated
This implies that the C-use efficiency or growth efficiency
{sensu Yamaguchi 1978) is unaffected or increased by
elevated [CO2I,,. Either of these responses to elevated
lC02]j cause a carry through from stimulation of photosynthesis by elevated lCO2]a to a comparable stimulation
of growth by elevated [CO2]., because growth is related
to the difference between photosynthesis and respiration.
Thus, much of the pertinent literature indicates that plant
respiratory responses to ele\ated ICO2I,, could reinforce
a negative feedback on the rate of increase of ICO2I., that
might be brought about by faster terrestrial higherplant photosynthesis. But, increasing temperature has the
potential to stimulate plant respiration rate at any given
lCO2]a - although plant respiration can acclimate and
adapt to short-term and long-term changes in temperature
{Amthor 1994a) - and the impact on global plant respiration of increasing lCO2la in combination with global
warming is unclear.
Any effects of increasing [CO2]a and (or) increasing
temperature on the amount of COi released to the
atmosphere during plant respiration at the global scale
is important to the global C cycle because about 10 times
as much CO2 is released each year by plant respiration
as is released by fossil fuel burning {Table I). Moreover,
changes in plant respiration carry with them significant
consequences for all other aspects of plant metabolism
because plant health and growth depend on plant respiration.
Stomatal conductance and plant water use
A short-term {minutes to hours) doubling of (CO2la often
causes a reduction in stomatal conductance (i.e. the
conductance of gas flux through leaf surfaces via stomatal
pores) of order 30-50% due to stomatal pore closure
(Morison 1987). Stomatal conductance is not always,
however, markedly affected by elevated [CO2]., (Radin
et ai 1987; Eamus & Jarvis 1989; Bunce 1992; Gunderson
et al. 1993), although the ratio of water transpired to CO2
assimilated In/ individual leaves is nearly always positively
related to lCO2la {e.g. Eamus 1991). When elevated tCO2l.i
causes stomatal closure, it is appaR'ntly the intercellular
[CO2I {i.e. [CO2L) that is of significance, rather than
[CO2la or the [CO2I at the leaf surface {Mott 1988).
Stomata in Ci and C4 leaves may be about equally
sensitive to a change in ICO2I, (Morison & Gifford 1983).
In addition to stomatal closure following short-term
increases in lCO2]j, stomata! density (stomata per m^
leaf) can be affected by long-term changes in JCO2I.V An
inverse relationship between lCO2la and stomatal density
was observed over the 200-350 ppmv CO2 concentration
range in (i) experiments (Woodward 1987), {ii) leaves of
herbarium specimens collected during the last 200-250
years (Woodward 1987; Pefiuelas & Malamala 1990; Van
© 1995 Blackwell Science Ltd., Global Change Biology, 1, 243-274
T E R R E S T R I A L - P L A N T R E S P O N S E TO A T M O S P H E R I C ICO2I
der Burg et ai 1993; but Komer 11988] did not find an
effect of [CO2I3 during the past 100 years on stomatal
density), (iii) leaves preserved in pack rat middens for
thousands of years (Van de Water ct al. 1994), and {i\')
Quaternary fossil leaves {Beerling & Woodward 1993).
Thus, stomatal density might have declined as [CO2l.i
increased since the LGM. Such a response could be
related to optimization of water lost per C gained by
individual leaves.
When ICO2]., is increased above 350-360 ppmv in
experiments, stomatal density remains constant or
decreases {Woodward 1987; Woodward & Bazzaz 1988;
Estiarte ct al. 1994; Ferris & Taylor 1994; Beerling &
Woodward 1995). These experiments were short-term less than the life cycle of the plants studied - so effects
of long-term elevated (CO2LT on adaptation processes
that might influence stomatal density were not addressed.
In any case, effects of future increases in [CO2la on
stomatal density are unclear. But, stomatal conductance
may be reduced in the future by increasing [CO2la,
perhaps in part as a result of smaller stomala (Miglietta
& Raschi 1993) and due to stomatal ckisure.
One result of a negative relationship between [CO2I.1
and stomatal conductance is a somewhat conservative
2l,, ratio. Thus, across a range of [CO2l.iS,
may be about constant, although many
exceptions are known. Data available indicate no general
acclimation of stomata to elevated [CO2]a during the
course of days to months, i.e. lCO2]i/[CO2la does not
change consistently with time (Sage 1994). Applicable
data are limited, however, and Ehleringer & Cerling
(1995) concluded that [CO2li/[CO2l.i 'will remain constant
in some species and vary in others' as [C02]j continues
to increase during the coming decades to centuries.
Although stomatal closure can reduce transpiration at
the single leaf level, effects of stomatal closure on regional
and global transpiration are unclear because of feedbacks
from the atmosphere - specifically, the planetary boundary layer (PBL) - to canopy transpiration {Jarvis &
McNaughton 1986; Jacobs & De Bruin 1992). When
stomatal closure occurs at the regional scale, as might be
the case for regional and global lC02],i increase, the
tendency for reduced transpiration would itself tend to
reduce tbe vapour pressure of the PBL. This in turn
would tend to stimulate transpiration because of an
increased vapour pressure gradient from inside leaves to
the atmosphere. This feedback on regional transpiration
is an important, but often overlot)ked, aspect of terrestrialplant and terrestrial-ecosystem responses to elevated
[CO2],,. Regional transpiration therefore may be less
affected by an increase in global [CO2lfl than is transpiration by small field plots treated with elevated [CO2]
because the PBL vapor pressure is unaffected by elevated
e plot scale. The same applies to plants treated
© 1995 Blackwell Science Ltd., Glohal Change Biology, 1, 243-274
259
with elevated [CO2I in controlled environment chambers
with constant vapor pressure. These facts are important
in the interpretation of measured water use in elevatedCO2 experiments conducted in chambers and free-air
CO2 enrichment plots.
Another result of reduced stomatal conductance,
brought about by reduced stomatal aperture and {or)
reduced stomatal density in elevated lCO2l,v is the potential for elevated leaf and canopy temperature due to
reduced latent heat exchange. Thus, even without a
general increase in global temperature, canopy temperature may be increased by elevated lCO2],i. This would
increase the vapour pressure gradient from inside leaves
to the atmosphere and therefore stimulate transpiration
(and limit the effect of elevated-lCO2la-induced stomatal
closure on transpiration).
Stomatal responses to lC02]a are important to the C
cycle in part because CO2 assimilation {photosynthesis)
is controlled by stomatal conductance, at least slightly
{Farquhar & Sharkey 1982). Changes in the ratio of C
assimilated to water transpired, however, may be the
most important effect of stomatal responses to ICO2I,, on
the C cycle. The general decline in stomatal conductance
and increase in photosynthesis with a short-term increase
in [CO2];, leads to a marked increase in water-use efficiency by C3 plants. Water-use efficiency of C4 plants is
also increased by CO2 enrichment, but mainly due to
reduced transpiration rather than the combination of
stimulated photosynthesis and reduced transpiration. In
addition, over the long term, several non-stomatal plant
responses lo elevated [CO^l.i may influence stomatal
conductance. For example, increased whole-plant growth
or altered root/shoot ratios can affect plant and soil
water status and therefore influence stomatal conductance
via whole-plant water relations and water use. To the
extent that elevated ICO2],, enhances the depth of root
growth and thus the depth in the soil from which water
can be extracted, elevated ICO2IJ may increase water use,
especially in dry soils for which all (most) water would
be extracted from the surface soil in any [CO2la.
Even though effects of increasing lCO2la on plantcommunity water use have been speculated on at length
for many years, there is only one set of field experiments
not involving chambers that directly addresses this issue:
the free-air CO2 fumigations {at c. 550 ppmv CO2) of
cotton and wheat in Arizona {Pinter (•( ai 1996).
(Chambers have significant effects on canopy energy
exchange. In particular, the ratios of longwave radiation
exchange, sensible heat exchange, and latent heat
exchange are usually different inside chambers compared
with natural conditions. Chambers will generally have
larger effects than elevated [CO2la tltws on energy
exchange, and the effects are confounded through a
series of interactions with transpiration and wind. Thus,
260
J.S. AMTHOR
transpiration within chambers is unlikely to reflect transpiration outside chambers and effects of elevated ICO2],,
on water use by chamber-grown plants may bear little
relevance to global plant responses to increasing lCO2]a )
In cotton amply supplied with water in free-air CO2
enrichment experiments, elevated [CO^],, had no effect
on transpiration compared to ambient [CO2]a plots
{Dugas et ai 1994). With either ample irrigation or deficit
irrigation, cotton-crop water use, i.e. transpiration plus
soil evaporation, was not affected (Hunsaker i-f (?/. 1994),
or perhaps even increased {Kimball ct til. 1994), by
elevated ICO2]., compared with present ambient ICO2I.T
For wheat amply supplied with water, elevated [CO2L,
decreased water use over two seasons by c. 4.5%, but
with limited irrigation, elevated [CO2l,, increased crop
water use c. 3"/.. (Pinter et ai 1996). So in spite of significant
speculation concerning important impacts of elevated
lCO2]a on water use, the only data directly addressing
the issue indicate no, or only small, effects of [CO2]d
on whole-plant transpiration and whole-crop water use
(volume of water evaporated per unit area of crop).
Nonetheless, water-use efficiency (CO2 assimilated per
unit water evaporated) was increased in both cotton and
wheat by elevated lCO2la.
Effects of ICO2L, on the ratio of plant growth to water
transpired has implications for the global C cycle. In
elevated [CO2la- more C can be assimilated for a given
amount of water transpired, and this has the potential to
enhance plant growth per unit of precipitation. Increased
plant growth for a given amount of precipitation may
lead to increased C storage - in both living plants and
soil C pools - in terrestrial ecosystems that are presently
'limited' by water availability. This could result in a net
transfer of C from the atmosphere to arid and semi-arid
land now occupied by plants. Moreover, increased plant
growth per unit precipitation in elevated [CO2],i has the
potential to increase the geographical range of plants in
arid and semi-arid regions. This in turn could lead to C
storage in plants and soils in areas not now occupied by
plants, leading to further net transfers of C from the
atmosphere to land. Thus, increased plant growth per
unit precipitation may function as a negative feedback on
the increase in ICOaJa, although the magnitude of such
a negative feedback has not been properiy evaluated.
To the extent that stomatal closure increases canopy
temperature, stomatal response to elevated lCO2la niay
represent a posithv feedback to warming and climatic
change. And, although the only appropriate data available
indicate that elevated tCO2]a does not affect water use
by crops, climatic change - in particular warming - has
the potential to increase water use, although precipitation may also be intensified by an enhanced greenhouse effect.
C3 vs. C4 plants
The time of the evolution of C4 photosynthesis is not
precisely known, but it may have been as recently as
15 X 10^ years ago (Morgan ct al. 1994a), as compared
with the far more distant past for tbe emergence of C^
photosynthesis. It was suggested that low [CO2la {e.g.
near PAL) was 'the primary selecti\'e factor influencing
the evolution of C4 photosynthesis' {Ehleringer t'/d/. 1991)
because C;^ photosynthesis is limited by lC02la near PAL,
but other factors may also have been important. The
global expansion of C4-dominated ecosystems 5-7 X UV'
years ago may have occurred in response to declining
[CO2L (Cerling et ai 1993), but again, otber factors may
also have been important (Quade et al. 1989; Morgan
et ai 1994b).
Since C4 photosynthesis is nearly CO2-saturated at
present [CO2]a whereas C-^ photosynthesis is operating
well below optimal ICO2I at PAL of CO2, it is often
suggested that the present increase in lCO2].i should
favour Cl plants compared with C4 plants. To quote
Kirschbaum (1994)
Enhanced photosynthetic capacity of C^ plants lin elevated
COj] is of immediate significance for the competition betjoeen
C3 and Cj plants. At a particular location wtiere C.i and Cj
plants co-exist, tlieif must be competing for other limiting
resources, such as tvater, nutrients or access to light. Increasing
COi concentration confers a selective advantage on the C3
plants, and puts them into an increasingly favourable competitive position. Increased C gain by C3 plants iwyuld allow them
to either increase root growth and compete more successfully
with their C4 neighbours for nutrients, or increase foliage
production to compete more successfully for available light.
This leads to the typical experimental observations on mixed
C1JC4 stands that the C3 components gain an increasing
biomass share with increasing CO2 concentration...although
the complexities of plant/plant interactions are such that results
are not ahcays consistent...Where differences are obserz'cd
within a single generation, these are likely to be further
compounded over successive generations. The continuously
improving photosynthetic performance of Qi plants...should
put great competitive pressure on neighbouring C4 plants.
especially in warmer regions xvhere the improvements in the
performance o/Ci p'lants should be mosi marked.
As expected, several experiments support this straightforward conclusion concerning effects of elevated lCO2la
on mixtures of Cy and C4 plants. For example, in a
Chesapeake Bay {MD, U.S.A.) wetland mixed community
of C3 sedge and C4 grasses, elevated lCO2]a resulted in
an increase in C^plant above-ground dry mass and a
concomitant decrease in C4-p!ant above-ground dry mass
at 'mid-season' (Drake 1992).
From the LGM to several hundred years ago, C:i
1995 Blackwell Science Ltd., Glottal Change Biology, 1, 243-274
THRRESTRTAL-PLANT RESPONSE TO ATMOSPHERIC ICO2I
vegetation replaced C4 vegetation in some locations while
[CO2la increased from c. 180 to c. 280 ppmv. It was
suggested 'that the increase in global CO2 concentration...aiH/n'/n/M/ directly to the shift from C4 to C3 vegetation' at one such site (italics added; Cole & Monger 1994),
but other en\'ironmental factors must also be considered
and the replacement of C4 vegetation with C-, vegetation
was not global as was the increase in lC02]a (Boutton
ctal. 1994).
Woody C3 vegetation 'invaded' C4-dominated grasslands in some locations during the past 200 years when
global [CO21.1 increased from c. 280 to c. 360 ppmv. This
was attributed by some {see references in Archer et ai
1995) to the increase in lCO2]j itself or to recent climatic
change, but the most objective analyses of this phenomenon indicate that the main cause of recent C3 invasit)ns
was livestock grazing (Archer et al. 1995). But even though
CT, invasions of C4-dominated communities during the
past 200 years were probably unrelated to global changes
in [CO2la, effects of further increases in [CO2la might
significantly influence future C3/C4 competitions.
Although C4 photosynthesis is nearly CO2-saturated at
PAL of CO2, C4 plants can respond positively to elevated
ICO2],,. As mentioned above, stomatal closure in C4 plants
exposed to elevated [CO^l^ leads to improved water-use
efficiency, and there are direct observations that C4-plant
growth can be stimulated by elevated [CO2l,i (Rogers
et al. 1983; Amthor ct ai 1994; reviewed by Poorter 1993).
Moreover, in mixed C3-C4 communities, growth of C4
plants may be stimulated by elevated ICO?];, when at the
same time growth of C3 plants is not affected, at least
during drought {Owensby et al. 1993b; cf. Drake 1992).
As stated by Henderson ct ai {1994), 'precisely which
trait, or which combination of traits, is most relevant to
the relative fitness of C3 and C4 species remains baffling.'
Indeed, Henderson ct ai {1994}—focusing on Australian
plants—suggest that because additional warming and
other climatic changes are likely to accompany the continuing increase in
...it is by no means clear that C^ plants ivill uniformly exploit
accelerated CO2 fixation in the long term. In fact C^ plants
face an array of limitations on translocation and utilization of
assimilates, of respiration at elevated temperatures and of
unpredictable reproductive outcomes...that may constitute
larger threats to fitiwss than they do to C4 plants. We
[Henderson et al,/ are tempted to conclude that the outcomes
ofthe contest between plants with the C^ and C4 photosynthetic
pathways [in] elevated CO2 will depend more on the extent of
advantages gained by the former than on those surrendered by
the latter.
Indeed, when considering the increase in temperature occurring with increasing COj... zve [Henderson et al.] conclude that
there may well be a significant Increase in the representation of
© 1995 Blackwell Science Ltd., Glohal Change Biology, 1, 243-274
261
C4 grasses in the Australian flora. Tlie southerly and easterly
expansion in the range of C4 grasses in Australia may match
the northerly expansion of the range of North American grasses
such as Eclnnochloa...[And\ it may be more appropriate to ask
not whether C4 grasses will be endangered by global climatic
change, but zvhether C,i grasses will be endangered, especially
in Australia.
There is divergence of thought concerning relative
effects of global environmental change on C3 and C4
plants. With other factors unchanged, increasing [CO2I.,
tends to enhance the competitive advantage of C3 plants
over C4 plants, except perhaps in dry environments, but
overall effects of global environmental change on the
C3/C4 balance is not obvious. Time, and discerning
observation and experimentation, may tell. It also is
unclear how a change in the C3/C4 balance per se would
affect the global C cycle and
Plant-Utter production and decomposition
Both the rate of transfer of C from plants to soils and the
quality {chemical composition) of plant litter affect C
cycling in soils, and key links, perhaps the key links,
between terrestrial-plant responses to lCO2].i and the
global C cycle are the amount and the quality of plant
litter produced. This is because the amoimt of plantderived C in soil and litter is thought to significantly
exceed the amount of C in living plants (Table 1) and,
depending in part on chemical composition, some fractions of soil C have lifetimes in excess of 1000 years
{Trumbore 1993). Moreover, the potential for additional
C storage on land as a result of increasing [CO^la is
probably greater in the litter and soil organic matter
pools compared with the living-plant C pools because
organic C can accumulate on {in) soils without significant
requirements of heat, nutrients, light, water, and structure;
these are critical requirements for the maintenance of
large pools of living-plant C.
The amount of plant litter produced is clearly related
to plant growth, at least in the long term. Thus, inputs
of organic C to soil are expected to be positively related
to tCO2lj to the extent that elevated ICO2],, enhances
plant growth. Present ecosystem soil and litter C content,
however, may be unrelated to rates of C input from
plants, at least according to data from the forests and
grasslands summarized by Cebrian & Duarte (1995).
Instead, soil organic-C ptKi! size may be negatively related
to plant turnover rate, i.e. positively related to plant
lifetime {Cebrian & Duarte 1995). It is unknown if such
a relationship exists in other terrestrial ecosystems or If
increasing [CO2la will affect such a relationship.
Since the N / C ratio {and related properties) of leaves
was altered in several elevated-CO2 experiments (e.g.
262
J.S. AMTHOR
Wong 1979; Norby et ai 1986, 1992; Williams et ai 1986;
Curtis et al. 1989; Kuehny et ai 1991), there was concern
that litter decomposability will be reduced as a result of
an increase in [CO2I., (see O'Neill & Norby 1996). A
related concern is that reduced litter decomposability
could reduce tbe rate of nutrient cycling in soils which
could in turn affect plant physiology and growth. Litter
quality (and amount) could also be affected by elevated
lCO2].i to the extent that species composition of terrestrial
ecosystems is changed because different species can differ
with respect to qualities, rates of decomposition, and
amounts of litter produced (Kemp et al. 1994; O'Neill &
Norby 1996).
But what evidence addresses the concems about effects
of elevated [CO2I., on litter quality? The short answer to
this question is: Very little. O'Neill & Norby (1996)
reviewed the limited data and made the important conclusion that, with respect to litter quality - as with many
other factors - pljmts growing in pots, often in 'growth
chambers,' differ from plants growing in the 'field.'
Moreover, it is the quality of naturally abscised leaves
and dead stems and roots that is relevant to decomposition. Most speculation concerning effects of elevated
ICO2I., on decomposition, however, is based on green
rather than senesced and naturally abscised leaves and
the chemical composition of green leaves may differ
significantly from the composition of naturally abscised
leaves {Curtis ct al. 1989).
Generalizations that can be made presently for plants
groiving in the groutni with noniial senescence processes
are (see O'Neill & Norby 1996): (i) leaf litter chemical
composition is unaffected, or only slightly altered, by
elevated [CO2],, (ii) decomposability of leaf litter is unaffected by the [COi]^ to which plants producing the litter
were exposed, and {iii) amount of litter production can
be positively related to ICO2].,. {Pot-grown plants can give
different results—O'Neill & Norby 1996.) Nonetheless,
Drake {1992) reported that elevated lC02la slowed decomposition in a Cl {Scirpus olnci/i) community but did not
affect decomposition in a C4 (Spartina patens) community
in the field. It is unknown whether elevated [CO2la
has a direct effect on decomposition per se in intact
ecosystems.
Additional effects of [CO2hT on decomposition rate
might be mediated through climatic change. Both soil
temperature and moisture affect decomposition, so
changes in either factor brought about by CO2-induced
climatic change could influence decomposition rate (Anderson 1992; Schlesinger 1995). 'First principles' and available data Indicate that warming might stimulate
decomposition rates and increase CO2 release from soils
in a positive feedback on the lCO2lfl increase (e.g. jenkinson ('/ al. 1991), but the N cycle may modulate such a
response {e.g. Schimel ct ai 1994). As outlined by, e.g.
Field ['/ ai (1992), warming that increases the rate of
decomposition can release to the soil 1 mol N for every
c. 10-20 mol of CO2 produced. For woody vegetation, 1
mol N might support the storage of c. 100-200 mol C,
because of the large C/N ratio of wood. Thus, increased
decomposition of organic matter in forest soils can potentially store more C in wood than is lost from soil because
of N cycling. For nonwcxidy vegetation, such a link
between soil organic matter dect)mposition and storage
of additional C in plants does not exist or is not as strong.
And e%'en in forests, which may contain c. 25% of global
soil organic matter {Ajtay (•( al. 1979), 'this mechanism
can persist only until the pcxil of soil organic matter
reequilibrates at a new size' {Field t'f ai 1992). The global
terrestrial {plant plus soil) C pool will be affected by such
a mechanism to the extent that 'additional' C stored in
wood offsets 'additional' C lost from all soils, not just
forest soils.
Carbon dioxide and N are not the only products of
decomposition that are important to global environmental
change. Although C released in CH4 during organic
matter decomposition plays only a small role in the
present global C cycle - c. 0.5% of atmospheric C is in
CH4 (DIugokencky et ai 1994) - CH4 is a much stronger
greenhouse gas than is CO2 {Leiieveld & Crutzen 1992), so
any changes in CH4 production resulting from increasing
ICO2]., might have significant implications for climatic
change. Natural and agricultural wetlands are major
sources of atmospheric CH4, and primary production in
wetlands is positively related to CH4 production (Whiting
& Chanton 1993). Thus, increasing [CO2].i may stimulate
CH4 production by stimulating wetland productivity.
Indeed, for Scirpus olneifi communities grown in elevated
[CO2]., in the field, CH4 production was stimulated, at
least during the four nights of measurements {Dacey et al.
1994). It has yet to be determined whether an incremental
increase in wetland primary production caused by an
incremental increase in lCO2la will weaken or strengthen
global greenhouse warming; stimulated primary production will function as a negative feedback on the [CO2la
increase, but enhanced CH4 production may accelerate
warming. Dryingof wetlands with global warming might
reduce CH4 production, if drying iKCurs.
The link between elevated lCO2la and litter production
and decomposition needs much more study because it is
quantitatively important to the global C cycle and because
so few data are available from plants growing in the
ground in different ICO2I.1S. Analyses of soil C pool sizes
and qualities near natural CO2 springs may be the best
available measures of effects of long-term elevated [CO2I.,
on litter production and decomposition. Any experiment
that can be conducted, using any technique, is of short
duration compared to the time scale of soil C turnover
in many {or perhaps all) ecosystems. And, the 'step
© 1995 Blackwell Science Ltd., Glottal Change Biology, 1, 243-274
T E R R E S T R I A L - P L A N T R E S P O N S E TO A T M O S P H E R I C ICO2]
change' in lCO2],i that is used in experiments may cause
different plant and ecosystem responses to [CO2I.1 than
the responses that are occurring with the present gradual
increase in global
More on missing sinks
There is confusion in the literature concerning the definition of the 'missing' sink of anthropogenic C. The annual
gUibal anthropogenic-C balance is often written in a form
equivalent to
where F is CO2 released in fossil fuel burning (Pg C
y"'), D is net CO2 released from land disturbed by
humans and includes COT released from wood removed
from forests {Pg C y"'), O is oceanic net CO2 uptake {Pg
C y~'), A is atmospheric CO2 increase {Pg C y^'), and M
is the missing C sink (Pg C y"'). Values of F are summarized in Marland et al. (1994; and see Table 1), Houghton
(1995) gives 1.6 i 0.7 Pg C y"' for the 1980s value of D,
estimates of O are given in Table 1 and Francey et ai
(1995), and A can be derived from Fig. 1 along with the
relationship 1 ppmv CO2 = 2.12 Pg C. In most analyses
M is greater than zero.
The anthropogenic-C balance equation above is not in
the correct form, however. It should be
F + D-O-A-U
= 0,
where il is net CO2 uptake by all land not directly disturbed
In/ humans (Pg C y"'). The difference LI - D is annual
global terrestrial ecosystem net CO2 uptake (Pg C y"') (it
could be negative). A comparison of these two anthropogenic-C balance equations indicates that M = U, although
this point is often unappreciated. Recent year-to-year
variation in tJ - D inferred by, e.g, Francey et ai (1995)
and Keeling et ai {1995), may be related to interannual
variation in weather, but there are mostly questions rather than answers - concerning year-to-year changes
in rates and controls of global CO2 exchange by terrestrial
ecosystems.
Two assumptions commonly made when considering
the missing C sink M are that (i) regrowth of disturbed
forests, either from logging or previous conversion to
agriculture, is the missing C sink and (ii) the annual net
C uptake by land not disturbed by humans U is zero.
Assumption {i) is false by definition, and assumption {ii)
may be false in actuality. The missing C sink, and
distinctions among D, M, and U, are discussed further
by Houghton {1995; and references therein).
It is well known that many forests, particularly those in
northern temperate and boreal regions, are accumulating
phytomass C. The northeastern U.S. is a good example:
it contains extensive area of aggrading {sensu Bormann
© 1995 Blackwell Science Ltd., Global Change Biology, 1, 243-274
263
& Likens 1979) forest now accumulating C {e.g. Armentano & Ralston 1980). Although this forest growth has at
times been assigned to the missing sink M {assumption
Ii]), much of that C accumulation occurs in previously
cleared or logged forests and is therefore a component
of D. Indeed, Houghton (1995) includes that forest
regrowth in his estimates of D and it cannot be simultaneously assigned to U or M. In short, C accumulating in
previously disturbed forests is a component of D, not of
M {see Houghton 1995 for further discussion), and it
is included in estimates of global D. A point worth
consideration with respect to increasing [CO;].i and reforestation and afforestation programmes - reforestation
and afforestation are human activities included in D - is
that in many areas Eucalyptus is planted {e.g. Seiler &
Crutzen 1980) and the growth response of Eucalyptus to
elevated tCO2la may be particularly strong {Wulischleger
ct ai 1995b).
Assumption {ii) can be evaluated by solving the anthropogenic-C balance equation for U. To the extent that O
is known {see Francey et ai 11995] & Keeling et ai 119951
for estimates of O that vary considerably from year to
year), U can be found because f and A are well quantified
and D can be taken from Houghton {1995). Available
data indicate that the terrestrial biosphere is presently a
net sink for on the order of 0-3 Pg C y"' {e.g. Conway
et ai 1994; Winn et ai 1994; Francey ct ai 1995; but see
also Keeling et al. 1995). U U - D is 1.5 Pg C y"' (see
Table 1) and D is 1.6 ± 0.7 Pg C y"' {Houghton 1995), U
is 3.1 ± 0.7 Pg C y-'. Can this be the case? Not if
ecosy.stems undisturbed by humans are in steady state
with respect to C. As mentioned above, however, some
undisturbed northern forests and peatlands may be accumulating C, primarily in peat and soil C pools, as they
continue to 'recover' from the last glacial cycle. Changes
in natural disturbance cycles might also affect U, and
there is evidence that during recent decades Canadian
forests accumulated C for that reason {Kurz et al. 1995).
These mechanisms may not be sufficient to support the
required value of U, however. Other causes of positive
U {as compared with an undisturbed terrestrial biosphere
that is in steady state with respect to C content) that have
been proposed include global warming, increased N
deposition on land, and CO2 fertilization of terrestrial
plants.
Potential effects of warming on increased N mineralization, associated with increased soil organic matter
decomposition, and subsequent net C storage in wood
were outlined by Field et ai {1992). Some evidence
indicates that warming during the past 200 years stimulated boreal forest productivity relative to preindustrial
times {Jozsa & Powell 1987). Warming might have
increased growing season length, and therefore annual
264
J.S. AMTHOR
plant growth, in temperate, boreal, and tundra ecosystems.
Plant growth responses to increased N deposition,
resulting from air pollution, might also enhance C storage
in terrestrial ecosystems {Field et ai 1992). Increased N
deposition is probably greatest in northern temperate
ecosystems, where air pollution is greatest, and its effects
might therefore be largest in northern ecosystems. It was
proposed that 0.6 Pg C might be stored in terrestrial
ecosystems each year due to fertilization from anthropogenic N releases {Schimel 1995). This is not sufficient to
account fully for the estimate of U above.
How and where might increasing [CO2la increase U?
The main mechanism is probably stimulated photosynthesis, although increased water-use efficiency may also
be important. The interaction between temperature and
[CO2Ja with respect to Cij photosynthesis indicates that
increasing [CO2l.,-iriclLiced photosynthetic enhancement
might be most significant in tropical (and other warm)
areas {Kirschbaum 1994). Direct effects of [CO2lfl on
respiration might increase or decrease 11, depending on
which metabolic processes are affected and whether they
are essential for plant growth and health. As outlined
above, plant growth is probably stimulated, to some
degree, by increasing lCO2]a- and plant growth responses
to increasing lCO2la could be spread throughout the earth
because CO2 is well mixed in the atmosphere; increasing
lCO2la is not limited to areas of CO2 emission. The
parameter U includes CO2 exchange by plants and soils,
however, so knowledge of plant response to lCO2la is
not sufficient to quantify the response of U to ICO2].,.
Carbon dioxide flux measurements made over an
undisturbed tropical rain forest in Brazil during 55 days
were used to estimate annual whole-ecosystem C
exchange {Grace et al. 1995). The estimated annual wholeecosystem C exchange rate so obtained was c. 0.24 |imol
CO2 m"^ s"' {units used by leaf physiologists) or c. 91 g
C m"'^ y"^ {units used by ecologists). Carbon uptake
cannot be so precisely measured with the methods used,
i.e. the annual rate obtained cannot be distinguished from
zero with great confidence, and that value was obtained
by extrapolation from 55 measurement days to 365 days.
Nonetheless, the result indicates annual net C uptake by
an undisturbed forest. If those measurements represent
an actual net uptake of C by the forest that is sustained
over many years, they could be indicative of a response
to increasing [CO2la- Or, the C gain might be due to
normal year-to-year fluctuations between C net loss and
C net gain with a net-gain period studied by chance,
because it is unlikely that the C balance of any ecosystem
is exactly zero during any 365-day period. Unfortunately,
there is little direct data concerning annual net C exchange
by other undisturbed terrestrial ecosystems.
Other factors may also be important to the present
apparent C sink activity of the terrestrial biosphere. Deep
roots {up to 18 m or more) in Amazonian forests (Nepstad
et ai 1994) not only increase the size of the soil (and
plant) pools of C compared with values listed in Table 2,
but deep roots also increase the potential C sink strength
of tropical forests in response to increasing [CO2l,i. This
may be particularly important if increasing [CO2].i is
causing an increase in root/shoot ratio (see Rogers et ai
1994 for qualifications). Carbon also may be accumulating
below-ground, independently of any change in [CO2i.,,
in tropical savannas that were subject to the introduction
of deep-rooted grasses {Fisher ct al. 1994) - a land-use
change factor not included in D by Houghton (1995). In
addition, increasing ICO2I,, may be enhancing water-use
efficiency, NPP, and C storage in both managed and
unmanaged tropical savannas.
Carbon that accumulates in undisturbed terrestrial
ecosystems may do so in living plants, in litter and dead
wood, or in soil humus. Some 'additional' C storage
in all of these C pools is likely. After analysing soil
chronosequences, Schlesinger {1990) concluded that only
c. 0.4 Pg C y"' are likely to be stored in soil humus under
natural vegetation globally, and noted that agriculture
generally results in a net loss of soil C compared witb
the same soil prior to cropping. This implies that soil
organic matter is not a likely sink for large quantities of
C; 0.4 Pg C y"' is much less than the 3.1 Pg C y"' estimate
of U above. But, Schlesinger's (1990) analysis is based on
historic trends, not on ecosystem processes occurring
with present, relatively high ICO2].,, with present N
deposition, and with present, relatively warm climate.
Moreover, all tbese factors are likely to continue to change
for decades. Thus, a convincing case has not been made
for a low C storage potential of soil today and into
the future when environmental conditions, and plant
productivity, may differ from those of the past several
thousand years; a possible rapid soil-C accumulation rate
should not be ignored. Also, litter and dead wood globally
contain large amounts of C {not considered by Schlesinger
[1990]), and those pools could be increasing in size as a
result of recent stimulations of plant photosynthesis and
growth. The limits to global living wood C content are
unknown, and could be greater than present stocks, so this
C pool too could increase in size over the coming decades.
Increased monitoring of spatial and temporal gradients
of ICO2];, and the atmospheric '•*CO2/'^CO2 ratio are key
to resolving general locations of today's (probably broadly
distributed) terrestrial net sink for C (Ciais 1'/ al. 1995;
Keeling et al. 1995). To the extent that C is accumulating
on land across large areas, it cannot be accurately and
directly measured at the individual ecosystem scale. In
the extreme case that 3.1 Pg C was added uniformly to
Earth's land surface each year, C accumulation rates
would be only 0.055 pmol CO2 m"^ s"' or 21 g C m"~ y"'
1995 Blackwel! Science Ltd., Global Change Biology, I, 243-274
T E R R E S T R I A L - P L A N T R E S P O N S E TO A T M O S P H E R I C ICO2]
lr>creased water-use
eflidency
Photosynlhetk: repression
(long term)
Feedback inhibition
(short lerm)
Stimulated
plxjtosynthesis
More nonstructurai
cartwhydrate
•
265
More C storage in
presently vegelated
arid and seml-and areas
Expansion ol vegetalion into, arxl
sidTsequeni C storage in.
runvegetated arid srxj semi-arid areas
on of N in
photosynlhetic apparatus
COn
More
gnswth'
More mairitertance_
respiration (7)
. Transport of N
to C sinks
Larger
planis
More C input
10 soil
-»-More waler used (?)
Mom C stored in plants,
most impoiiantty in wood
Fig. 5 Proposed main terrestrial hij^her-plant responses to elevated [C02ta that may be of quantitative importance to the global C
cycle. Elevated [C02]a stimulates photosynthesis, much more so in C3 plants compared vi/ith C4 plants, which in tum may increase
plant nonstructural cirbohydrate concentration (Bowes 1993). Accumulation of nonstructural carbohydrates can inhibit (Azcon-Bieto
19H3; Foyer 19KiS) or repress (Sheen 1994; Webber ct ill. 1994) photosynthesis, but it might also enhance growth and growth R'spiration
(Farrar & Williams 1991). Repression of photosynfhesij; may be related to the mobilization of N in photosynthetic enzymes and
pigments, and that mobilized N might be used for additional plant growth (Webber et ul. 1994), which could be significant for plants
growing in N-deficient soils. Increased maintenance respiration, normally resulting from larger plant size, may be mitigated by changes
in plant composition, i.e. reduced N/C ratio, that in tum reduce specific maintenance costs (Amthor 1991). And, respiration may be
directly inhibited by elevated [COT]., (not shown; Amthor 1996). Enhanced plant growth in tum could lead to enhanced C storage in
perennial plant tissues, most importantly wood, and enhaticed inputs of litter (both above-ground and below-ground) to soil C pools.
An increase in root growth or size might also increase C inputs to the soil via exudation. Enhanced input of C to soil could lead to
an increase in soil C content.
In addition to stimulated photosynthesis per sc, elevated ICOij., can potentially increase whole-plant water-use efficiency, which in
turn can enhance growth of plants in arid and semi-arid areas now containing some vegetation. Increased water-use efficiency might
also allow the expansion of vegetation into presently unvegetated arid and semi-arid areas. Increased plant growth in arid and semiarid areas would enhance organic-C inputs to soil in those areas, which might lead to larger soil C ptwis.
Plant responses to elevated [COi],, shown here tend to act as negative feedbacks on the rate of increase of ICOi]^, but all the links
in this scheme are subject to modification by ciimatic change accompanying the increase in ICOi]^. And, effects of human activities
(other than fossil fuel burning) have a greater impact on the C balance of many individual ecosystems than do increasing [CC>2la and
global warming.
(four times smaller than the annual value proposed by
Grace et ai 11995] for an undisturbed tropical rain forest).
Such a rate of C accumulation would be deep within
the noise of measurements of ecosystem C exchange.
Ecosystem and global C cycle models now in use are
inadequately tested (or not tested at all!) against measured
terrestrial C fluxes - so little significance can be attached
to their predictions - and point measurements of CO2
exchange in the field may be ttw geographically specific
to be useful in quantifying regional and global scale
processes. Thus it may be some time before a reasonable
assessment of the C sink activity of the terrestrial
biosphere can be obtained hy ground-based measurements.
An issue related to the future glohal C cycle is the
potential displacement (or migration) of biomes caused
by climatic change and (or) elevated lCO2Ja- Changes in
the area of individual biomes caused by environmental
1995 Blackwell Science Ltd., Glohal Change Biology, 1, 243-274
change might alter terrestrial ecosystem C fluxes proportionally, at least in the long term. For example, if boreal
forest replaces some tundra as a result of warming, CO2
assimilation and C storage in the 'new' boreal forest
might exceed values in the 'old' tundra because boreal
forest photosynthesis can exceed tundra photosynthesis.
On the other hand, warming of tundra could cause
significant releases of CO2 due to changes in the water
table leading to accelerated decomposition (Oechel et al.
1993) if drying is not prevented by increased precipitation
due to an enhanced global greenhouse effect (Manabe &
Stouffer 1994). Such changes are difficult to evaluate
because the early phase of transition from one biome to
another at a particular site might result in a net release
of CO2 due to reduced NPP and continuing decomposition, but this might be followed in time by increased
NPP and soil C storage. The extent and timing of future
hiome migrations (if any) is unknown.
266
J.S. AMTHOR
Summary
Aside from its potentially negative impact on climate, it
is easy to think of elevated [COolj as a good thing for
plants. The most obvious and immediate effect of elevated
[C02ia on terrestrial Ci higher plants is a stimulation of
photosynthesis. And because terrestrial-plant photosynthesis assimilates about 20 times as much CO2 as is
released in fossil fuel burning each year, even a small
increase in photosynthesis has the potential to significantly affect the fate of fossil C released by human
activities.
Stimulated photosynthesis initiates a string of process
responses that can affect nearly all aspects of the C cycle
of terrestrial higher plants and ecosystems (Fig. 5), Most
immediately, stimulated photosynthesis may lead to the
accumulation of nonstructural carbohydrates, which may
reduce photosynthetic capacity (downregulation) and
photosynthetic rate (inhibition) in a series of negative
feedbacks. The interaction between N availability (or N
concentration in a plant) and [CO^],, may play a role in
the degree of photosynthetic acclimation to elevated
[CO2la although this issue remains unresolved. Accumulation of nonstructural carbohydrates may also stimulate
capacities and rates of respiration, biosynthesis, and
related reactions that consume photoassimilate in a series
of positive feedforwards in plant metabolism. A common
response of C3 plants to elevated ICOoJa in experiments
is enhanced growth, but growth of C4 plants also can be
stimulated by elevated [COT].,.
In addition to effects on terrestrial-plant photosynthetic
metabolism and subsequent growth, elevated [CO2]a can
cause partial stomatal closure, although whole-ecosystem
water use may, at the same time, be unaltered. In any
case, elevated [COjJa generally increases the ratio of the
amount of COT assimilated (or amount of plant grown)
to the amount of water transpired. As a result, more
growth is possible for a given amount of precipitation or
soil moisture. One possible effect of this increased wateruse efficiency is an expanded range of plants in arid and
semi-arid regions as well as enhanced growth by plants
already occupying arid and semi-arid areas. This could
lead to the storage of additional C in plants and soils of
these regions. Increasing [CO2]a may benefit C3 plants
more than it benefits C4 plants, but climatic change
accompanying increasing [CO2l,i may confer relative
advantages to C4 plants, so the overall impact of global
environmental change on competition between C3 and
C4 plants is unknown. And, the long term (decadal)
growth responses of perennial plants to elevated [CO^la
are unclear.
To the extent that an increase in [CO2]a causes an
increase in plant growth and (or) an increase in the
geographical range of plants, the amount of plant litter
produced will increase globally, i.e. the input of plant C
to the global soil C pool will increase. Because the
chemical composition of dead leaves allowed to senesce
and abscise naturally was not significantly affected by
ICO2la in the few experiments germane to this issue, it
must presently be concluded that the net effects of
increased leaf growth (if any) caused by elevated [CO2la
will result in larger soil C pools if other factors such as
climate remain sensibly constant. Little is known of the
effects of elevated [COTI,, on root or (woody) stem litter
quality, so although it is likely that rates of C input to
soil from roots and stems will increase with an increase
in [CO2].v effects of elevated [CO2],, on whole-plant litter
decomposition rate are unknown. In general, increasing
[CO2I., may lead to greater input of organic C to soils,
but warming might cause increased rates of soil organic
matter decomposition.^
Although most plant responses to [COil,, act as negative
feedbacks on the increase in [CO^la, those plant responses
cannot end the increase in [CO2]a in the next several
decades. Inputs of CO2 to the atmosphere from fossil fuel
combustion are too large, and it is unlikely that reductions
in fossil fuel use will be significant - or occur at all during the next several decades. Moreover, further climatic change associated with increasing [CO2I.1 may be
more of a detriment to C storage on land than a benefit,
at least in the long term. Therefore, whtile-ecosystem
responses to continued global environmental change and
human land-use changes may be as likely to stiniuUite
tho future increase in (CO2]n as they are to dampen it.
Acknowledgements
This paper is dedicated to Spike Gixxibody. He made critical
contributions to the manuscript, but died just as it was completed. My financial support for the prt'paration of this paper
came from Lawrence Livermore National Laboratory's Laboratory Directed Research and Development I'rogram (9!i-D!-(X15)
under the auspices of the U.S. Department of Unergy, Environmental Sciences Division (contract No. W-7405-Eng-48).
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