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Photosynthesis Research 77: 209–225, 2003.
© 2003 Kluwer Academic Publishers. Printed in the Netherlands.
209
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Quo vadis C4 ?∗ An ecophysiological perspective on global change and the
future of C4 plants
Rowan F. Sage1,2 & David S. Kubien1
1 Department
of Botany, University of Toronto, 25 Willcocks Street, Toronto, ON MS3B2 Canada; 2 Author for
correspondence (e-mail: [email protected]; fax: +1-416-978-5878)
Key words: C4 photosynthesis, climate warming, elevated CO2 , global change, photosynthesis
Abstract
C4 plants are directly affected by all major global change parameters, often in a manner that is distinct from that
of C3 plants. Rising CO2 generally stimulates C3 photosynthesis more than C4 , but C4 species still exhibit positive
responses, particularly at elevated temperature and arid conditions where they are currently common. Acclimation
of photosynthesis to high CO2 occurs in both C3 and C4 plants, most notably in nutrient-limited situations. High
CO2 aggravates nitrogen limitations and in doing so may favor C4 species, which have greater photosynthetic
nitrogen use efficiency. C4 photosynthesis is favored by high temperature, but global warming will not necessarily
favor C4 over C3 plants because the timing of warming could be more critical than the warming itself. C3 species
will likely be favored where harsh winter climates are moderated, particularly where hot summers also become
drier and less favorable to C4 plant growth. Eutrophication of soils by nitrogen deposition generally favors C3
species by offsetting the superior nitrogen use efficiency of C4 species; this should allow C3 species to expand at
the expense of C4 plants. Land-use change and biotic invasions are also important global change factors that affect
the future of C4 plants. Human exploitation of forested landscapes favors C4 species at low latitude by removing
woody competitors and opening gaps in which C4 grasses can establish. Invasive C4 grasses are causing widespread
forest loss in Asia, the Americas and Oceania by accelerating fire cycles and reducing soil nutrient status. Once
established, weedy C4 grasses can prevent woodland establishment, and thus arrest ecological succession. In sum,
in the future, certain C4 plants will prosper at the expense of C3 species, and should be able to adjust to the changes
the future brings.
Abbreviations: A – the rate of net CO2 fixation; gc – leaf conductance; PNUE – photosynthetic nitrogen use
efficiency; WUE – water use efficiency
Introduction
Human activities around the world have become so
extensive that the global biosphere, hydrosphere and
atmosphere are undergoing significant change. Global
change phenomena are changes that are either global
in nature, or are regional but scale to the global level
because they are widespread and pervasive (Vitousek
1994). The five major categories of global change are
∗ Whither are you going, C ? (after Edwards et al. 2001).
4
1) changes in atmospheric composition, 2) associated
climate warming, 3) landscape conversion by human exploitation, 4) nutrient enrichment of terrestrial
ecosystems (eutrophication), largely by nitrogen pollution, and 5) destruction of ecosystems by invasive,
exotic species (Vitousek 1994; Sala et al. 2001). Atmospheric change and climate warming have received
most attention from the scientific community and the
public; however, bioinvasions, land-use change, and
eutrophication are already having severe impacts in
many biomes (Table 1; Sala et al. 2001).
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Table 1. Five major global change parameters and the associated effects on C3 versus C4 plants. Developed from Vitousek (1994), Sala et al.
(2001) and Sage (2001)
Global change parameter
Time until severe impact
General effects
I. Global in nature
Atmospheric CO2 Rise
50+ years
Global Warming
50+ years
Direct stimulation of photosynthesis (C3 more than C4 )
Direct stimulation of growth (C3 more than C4 )
Reduction in stomatal conductance (C3 and C4 similar)
Stimulates C4 photosynthesis, especially at high CO2 .
Stimulates growth of C4 plants
Increases water consumption and drought probability
II. Regional in nature but scales to global significance
Land Use Change
Ongoing
Terrestrial Eutrophication
30+ years
Bioinvasions
Ongoing
Global change will affect the relative distribution
of C4 to C3 vegetation by affecting the key physiological and ecological parameters that control the success of C4 plant species (Table 1). Because of their
altered physiology, C4 plants respond differently to
temperature, CO2 , light and water availability than C3
plants (Osmond et al. 1982). Extensive research on
the physiology and ecology of C3 versus C4 plants
provides a robust understanding of the mechanisms
controlling photosynthetic response to changing environmental factors, and allows for the generation of hypotheses of how C4 vegetation will respond to future
global change. Because of strong interactions between
the categories of global change, however, responses to
the change must be considered in a synthetic context.
Numerous papers have considered potential responses
of C4 versus C3 vegetation to rising CO2 or warming
(for example, Patterson and Flint 1990; Sage 1994;
Henderson et al. 1994; Wand et al. 1999), but few have
simultaneously considered warming, CO2 , land-use
change and impacts of bioinvasions. Here, we review
the biogeography and environmental physiology of C3
and C4 plants in the context of the primary (temperature and light) and secondary (water and nitrogen)
factors controlling C3 versus C4 plant distributions.
We then discuss C3 and C4 responses to interactions
Alters light availability at the herbaceous layer
Destruction of C3 -dominated forests in tropics and subtropics
Expansion of C4 -grazing land in tropics
Expansion of C3 -shrubland in overgrazed C4 savanna
Conversion of C4 grasslands to crop and timber land
Overcomes C4 advantage in nitrogen use efficiency
Promotes rapid growth of weedy C3 and C4 species
Reduces establishment time of woodland species
Many C4 plants are aggressive weeds and bioinvaders
Tropical C4 grasses increase fire frequency and intensity
Promotes conversion of forest to exotic C4 grasslands
between CO2 enrichment and climate change, land use
change, bioinvasions and eutrophication, and finish
by hypothesizing how global change might alter the
current distribution of C4 vegetation.
Current geography and environmental physiology
of C4 vegetation
It is well recognized that the primary environmental
controls over the distribution of C4 relative to C3 vegetation are temperature and light, with water availability and nitrogen supply having important secondary
effects (Osmond et al. 1982; Sage et al. 1999). Primary
controls are those that must be within a certain range
if C4 species are to occur in an ecosystem; secondary controls become important only when the primary
requirements are met (Sage et al. 1999).
Temperature
One of the pronounced biogeographic patterns on
earth is the relationship between growth season temperature and the distribution of C4 biomass. On all
continents save Antarctica, C4 species become less
frequent with increasing latitude and elevation (Sage
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Figure 1. The % frequency of C4 grass species in local floras
of the eastern and western coastal regions of North America as
a function of minimum July temperature. Each point represents
a local flora (usually from parks, counties, government reservations and biopreserves that are less than 2500 km2 in size). The
western region (open symbols) extends from lower Baja California to Alaska and includes sites west of the Sierra Nevada/Cascade
cordillera. The eastern region (filled symbols) extends from Labrador to central Mexico and includes sites east and south of the
Appalachian/Luarentian cordillera. (from Wan and Sage 2001 by
permission).
et al. 1999). The principle environmental variable
correlated with the latitude and altitude patterns is
mid-summer temperature (Figure 1; Teeri and Stowe
1976; Hattersley 1983; Tieszen et al. 1997). In most
locations across the globe, the estimated minimum
summer temperature for C4 grass presence in a flora is
6 to 10 ◦ C, while the estimated minimum temperature
for C4 dominance of a grass flora is 18 to 20 ◦ C (Long
1983). Corresponding average mid-summer temperatures for C4 presence are 13 to 14 ◦ C, and for C4
dominance are 22 to 24 ◦ C (Sage 2001).
The mechanism for the temperature effect on C4
species distribution is largely the temperature response
of net CO2 assimilation (A) in C3 and C4 plants
(Osmond et al. 1982). C3 species typically have a
higher photosynthetic rate at low temperature (below
20 ◦ C) while C4 species have greater A at elevated
temperature (> 25 ◦ C to 30 ◦ C) and current levels
of atmospheric CO2 (Figure 2; Pearcy et al. 1981;
Ehleringer et al. 1997). These differences correlate
with differences in the temperature response of growth
between C3 and C4 plants (Harris et al. 1981; Pearcy
et al. 1981; Ludlow 1985). Numerous groups had
proposed C4 photosynthesis is inherently sensitive to
Figure 2. The temperature response of net CO2 assimilation rate
in Muhlenbergia glomerata (C4 ) and Calamagrostis canadensis
(C3 ) grown at 800 µmol m−2 s−1 and the cool conditions (14 ◦ C
day/10 ◦ C night) that are common in the boreal fen environment
from which the plants originated. Measurements conducted at current CO2 levels and saturating light intensities (Kubien and Sage,
unpublished data). N = 3 − 5, mean ± SE.
low temperature, based on observations of cold lability of C4 cycle enzymes such as PEP carboxylase and
pyruvate-Pi-dikinase in maize and sorghum, and observations that minimum growing season temperature
is best correlated with C4 abundance in a flora (Teeri
and Stowe 1976; Long 1983; Leegood and Edwards,
1996). However, maize and sorghum are adapted to
warm temperatures, and thus are generally intolerant
of cold. The more appropriate species with which to
examine whether the C4 pathway is cold intolerant
are those that naturally occur at the cooler end of
the C4 distribution range. Work with these species
demonstrates C4 cycle enzymes can be stable at low
temperature, and C4 species in cold climates are able
to withstand chilling during the growing season (Leegood and Edwards 1996; Long 1999; Pittermann and
Sage 2001). In one extreme case, the C4 grass Muhlenbergia richardsonis grows in alpine tundra near 4000
m where it regularly experiences temperatures below
zero during the growing season (Sage and Sage 2002).
In the tundra, M. richardsonis only occurs in microsites where leaf temperatures can exceed 25 ◦ C during
the day when photosynthesis is active. By contrast,
low night temperature does not affect its microsite
distribution.
The different temperature responses of photosynthesis have been attributed to 1) increasing inhibition
of A in C3 plants by photorespiration as temperatures
rise, 2) the reduction of CO2 in the chloroplast stroma
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of C3 plants at higher temperature, due to lower CO2
solubility and 3) a low content of Rubisco in C4 plants
that restricts A at low temperature (Ku and Edwards
1977; Sage 2002). In C3 plants, photorespiration is
reduced at low temperature but rises substantially as
temperature increases above 25 ◦ C (Jordan and Ogren
1984). The photorespiratory inhibition of A is over
25% above 30 ◦ C in well-watered C3 plants (Sharkey 1988), and substantially higher where low water
availability causes stomatal closure and a reduction
in intercellular CO2 levels. In C4 plants, by contrast, the CO2 pump concentrates CO2 around Rubisco
to levels where photorespiration is low at all temperatures, typically between 2% to 6% of A (Hatch
1987).
Differences in maximum quantum yield (the initial
slope of the absorbed light response curve) have been
closely correlated with differences in photosynthetic
performance as a function of temperature (Ehleringer
1978; Ehleringer and Pearcy 1983). C3 plants have
a greater maximum quantum yield than C4 plants at
low temperature in current CO2 levels, and a lower
quantum yield above 25 ◦ to 30 ◦ C. The maximum
quantum yield has proven useful for describing distributions of C3 and C4 plants in space and time.
For example, the latitude where C3 dominance shifts
to C4 dominance has been accurately predicted by
models based on quantum yield, and quantum yield
differences have been used to predict CO2 levels and
geological periods when the C4 pathway first became
adaptive (Ehleringer 1978; Ehleringer et al. 1997).
These observations have led to suggestions that the
latitude distribution of C4 plants is directly restricted
by their inferior quantum yields at low temperature
(Ehleringer 1978). This explanation is unsatisfactory,
because maximum quantum yield has no direct effect
on A at high light, where C4 species usually operate
(Long 1999; Sage et al. 1999). However, maximum
quantum yield is an effective index of the relative inhibition of A due to photorespiration, and it is in this
indirect manner that its robustness as a predictor of C3
and C4 dynamics mainly occurs. This is demonstrated
by Equation (1) (derived from Equations (2.18) and
(2.50) in von Caemmerer 2000) and Equation (2):
dAg
0.125 − 0.0625Vo/Vc
=
dIa
1 + Vo /Vc
(1)
dAg /dIa is the maximum quantum yield at an absorbed light intensity, Ia , that is near 0. Vo is the rate
of RuBP oxygenation, and Vc is the rate of RuBP
carboxylation. (The rate of photorespiration equals 0.5
Vo , and the relative photorespiratory inhibition of A
is 0.5Vo/Vc ). The use of Ia indicates spectral quality
and leaf absorbance have been accounted for. Gross
photosynthesis equals
Ag = Vc (1 − 0.5Vo/Vc )
(2)
Equation 1 and 2 show that as Vo increases relative to
Vc , dA/dIa and Ag decline, as does any ratio based on
A, such as water use efficiency (WUE which is A/E,
where E is transpiration) or photosynthetic nitrogen
use efficiency (PNUE, which is A/N, where N is leaf
nitrogen content).
Light
As a rule, C4 plants do poorly in deep shade (below about 15% of full sunlight intensity; Sage et al.
1999). They can do well in intermediate light (25%
to 50% of full sun) at warmer temperatures, and are
commonly dominant in warm to hot locations where
they receive > 50% of full sunlight (Weltzin and
Coughenour 1990; Ko and Reich 1993). Because C4
species are largely herbaceous or low stature woody
species, they are susceptible to being overtopped by
tall-stature woody vegetation, which is predominately
C3 (Sage et al. 1999). The inability to tolerate deep
shade therefore means that C4 plants are potentially
excluded from landscapes where woody C3 vegetation
can establish. Hence the critical factors determining
the distribution of C4 -dominated ecosystems are often those that govern the dominance of woody versus
herbaceous species.
A few exceptions are noted in that there over a
dozen shade-tolerant C4 grass species in Brachiaria,
Microstegium, Muhlenbergia, and Setaria and there
is one well-studied C4 understory tree from Hawaii,
Chaemasyce forbsii (Brown 1977; Pearcy and Calkin
1983; Horton and Nuefeld 1998). With the exception of C. forbesii, the degree to which understory
C4 species are true shade plants is unclear, as floristic
descriptions mention they occur along streams, trails
and in small gaps. Instead, they may be gap species
in the sense that they need at least limited exposure
to sunflecks to be ecologically successful (Sage and
Pearcy 2000). In the case of C. forbesii, it has clearly
been shown to occur deep within forests, and it shows
similar light responses of A as adjacent C3 species,
thereby demonstrating the C4 pathway can occur in
plants adapted to deep shade (Pearcy and Calkin 1983;
Pearcy et al. 1985). This unique situation with C. forbsii may result from it having evolved shade tolerance
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in a competitive-free setting early in the history of
Hawaii (Pearcy and Calkin 1983).
Mechanistically, the failure of C4 species in deep
shade is not attributable to any single factor, but instead appears to be the combined effect of numerous
phenomena that individually confer a small difference
in C3 and C4 performance (Sage and Peacy 2000). The
maximum quantum yield is directly significant in that
forest understories tend to be cooler than open landscapes and are not frequently warm enough for C4
species to exhibit a superior quantum yield (Pearcy et
al. 1985). Hence, over a day (which includes cooler
mornings and late-afternoons), C3 understory species
may have a slightly higher average quantum yield,
which means a higher A at the low average light
intensity of a forest interior (Pearcy and Ehleringer
1984). In addition, a major portion of the carbon gain
within forests potentially comes from light-flecks below small gaps in the overstory. The ability to exploit
these gaps is an important contribution to success in
the understory, and C4 plants appear to be less efficient
in utilizing short sunflecks (1 to 10 s) than shadeadapted C3 species (Krall and Pearcy 1993; Sage and
Pearcy 2000). The less efficient use of short sunflecks may reflect an inability of C4 species to properly
coordinate metabolite pools between mesophyll and
bundle sheath tissues during the brief exposure to high
light (Krall and Pearcy 1993).
Water
Water availability is a secondary factor promoting C4
success in that it is important only in warm situations. In cold climate zones, arid grasslands are C3
dominated, and few if any C4 species are present
(Sage et al. 1999). The inability of C4 species to
compete in cold climates explains a marked seasonal
relationship between water availability and C4 abundance. Where precipitation primarily occurs in the cool
months of winter and spring, such as Mediterranean
climate zones and cold deserts, the herbaceous flora
is dominated by C3 plants (Sage et al. 1999). Where
the precipitation primarily occurs during warm to hot
summers, the herbaceous flora outside of woodlands is
dominated by C4 species (Knapp and Medina 1999).
Where there is both cool and warm season precipitation, open habitats exhibit a biphasic flora with
winter-active C3 herbs and summer-active C4 herbs
(Ode et al. 1980; Epstein et al. 1997). In these areas,
the relative dominance of each photosynthetic type
changes in response to short-term climate variation.
Years with dry winters or wet summers promote C4
expansion, while the abundance of C3 plants increases
in years with wet winters and dry summers. (Monson
et al. 1983).
The control of aridity over the distribution of C4
species operates at multiple scales of complexity. Ecologically, dry environments are also fire-prone, and
it is often fire that maintains the C4 -dominated ecosystem (Goldammer 1993; Bond and van Wilgen
1996). In the absence of fire, shrubs and trees can
invade C4 grasslands unless large animal activity or
shallow soils prevent their establishment (Frost and
Robertson 1989; San Jose and Farinas 1991; Dublin
et al. 1990; van Auken 2000). Drought and fire also
interact with the growth rates of plants in that drought
slows tree and shrub growth and increases the time
during which woody species are vulnerable to fireinduced mortality (Bond and Wilgen 1996). In some
cases, severe drought directly kills woody species but
not the grasses that are dormant during dry seasons
(Knapp and Medina 1999). This is most evident where
shallow soils restrict the depth of woody roots. On
shallow soils, the deep roots that permit shrub persistence cannot form, and shrubs must directly compete
with grasses for limited water supplies (Goldstein and
Sarmiento 1987).
Physiologically, C3 and C4 species do not inherently differ in the degree to which they withstand
severe drought, and the main difference in performance in response to aridity is greater water use efficiency of the C4 pathway (Osmond et al. 1982). At the
operating Ci 1 in normal air for non-stressed plants, C4
species have over twice the WUE of C3 plants with an
equivalent photosynthesis rate (Figure 3; Osmond et
al. 1982; Knapp and Medina 1999). This is because
C4 plants can match the CO2 assimilation rate of a C3
plant with about half the stomatal conductance, and
hence half the rate of water loss. Should a C3 plant
reduce stomatal conductance to match the C4 stomatal
conductance and water loss rate, A would be greater
in the C4 plant (by 25% in the comparisons in Figure 3; compare A values on the C3 and C4 curves
at gc = 0.22 and 0.085 mol m−2 s−1 ). As a result,
for a given amount of soil water, C4 species are able
to develop a larger canopy, grow more root mass and
produce more seeds than their C3 competitors (Ludlow
1985; Long 1999). A larger leaf canopy has secondary
effects in that it can shade slower growing C3 species,
while a larger root mass allows C4 species to capture
soil resources before C3 competitors.
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Figure 3. The response of net CO2 assimilation rate to intercellular CO2 partial pressure of Amaranthus retroflexus and Capsicum annuum.
Supply functions are shown for leaf conductances (gc ) of C. annuum in normal air (gc = 0.54 mol m−2− s−1 ), A. retroflexus in normal air (gc =
0.22 mol m−2 s−1 ) and assuming stomatal closure to conserve water (gc = 0.085 mol m−2 s−1 ). Gray arrows indicate CO2 saturation points.
Inset: WUE corresponding to each supply function, where WUE was calculated as A/E assuming a vapor concentration difference between leaf
and air of 30 mmol water mol1 air. Data from Sage (2002 and unpublished). Supply function terminology after Farquhar and Sharkey (1982).
Nitrogen
Because of their greater nitrogen (N) investment in
Rubisco and photorespiratory enzymes, C3 plants
have lower nitrogen-use efficiency of photosynthesis
(PNUE) than C4 plants (Brown 1978; Sage and Pearcy
1987, 2000). The ecological consequences of greater
C4 PNUE have been studied to only a limited degree.
In the temperate grasslands of North America, the
greater PNUE of C4 grasses allows them to grow at
lower soil N availability than C3 grasses (Wedin and
Tilman 1993, 1996; Sage et al. 1999). Hence, when
soils are low in N, C4 species are superior competitors and will dominate a plot. When soils become
N-enriched, the advantage in NUE is offset and the
C3 species can match the photosynthetic potential of
C4 species, and thereby increase in cover (Brown
1978; Sage and Pearcy 1987; Wedin and Tilman 1993,
1996). With high N fertilization, temperate grasslands
become dominated by C3 grasses (Gibson et al. 1993;
Wedin and Tilman 1996).
One important ecological interaction between N
supply and vegetation is the relationship between biomass C:N ratio and decomposition. High C:N ratios
usually reduce decomposition rates, such that proportionally more N on a site may reside in the soil
organic matter pool (Ball 1997). C4 grasses have significantly higher C:N ratios than C3 grasses, and thus
soil N availability often declines when a C4 -dominated
sward replaces C3 vegetation (Brown 1978; Wedin and
Tilman 1993; Reich et al. 2001). Establishment of C4
vegetation also increases fire frequency, which volatilizes N and reduces site N availability (Kaufmann et
al. 1995). In tropical soils, the reduction in soil nitrogen availability that follows C4 grass establishment
reduces the probability that woody C3 plants will return. Lower N availability also reduces the growth
rates of C3 species, thereby increasing the time during which the woody plants are vulnerable to fire and
lethal drought stress (Aide and Cavelier 1994; Johnson
and Wedin 1997).
C4 plants and global change
Atmospheric CO2 enrichment
Photosynthesis of C3 species is generally increased
20% to 50% by a doubling of atmospheric CO2 , while
photosynthesis in C4 species increases by 0% to 25%
(Cure and Acock 1986; Patterson and Flint 1990).
Simple extrapolation from these results indicates C3
plants will be favored over C4 plants in CO2 enriched
environments of the future. A problem with such an
interpretation, however, is that the range of conditions
in which most measurements have been conducted are
215
relatively narrow and usually do not fully consider
the environment where C4 species are currently active. Once comparisons are made between C3 and C4
species in natural settings (typified by warmer, less
humid conditions where C4 species are common), the
difference in CO2 responses are less than expected
(Owensby et al. 1996; Wand et al. 1999; Morgan et al.
1998; 2001; Ghannoum et al. 2001). For example, using a meta-analysis of non-cultivated grass responses
to elevated CO2 , Wand et al. (1999) noted that growth
of C4 grasses was increased 33% by exposure to elevated CO2 , compared to a 44% growth enhancement of
C3 grasses.
The common explanation for the low response of
C4 plants to CO2 enrichment is the relatively low CO2
saturation point of A in C4 relative to C3 species (Figure 3; Osmond et al. 1982; Sage 1994). In C4 plants,
the photosynthetic response to intercellular CO2 consists of a steep initial slope of A versus rising CO2 ,
and a plateau where A is CO2 saturated. By contrast,
C3 species have a higher CO2 compensation point,
a lower initial slope, and a relatively high CO2 saturation point (Figure 3). At moderate temperatures,
the CO2 saturation point in C4 plants roughly corresponds to the operating Ci in the current atmosphere, so
that increasing atmospheric CO2 above current values
should have little effect. At elevated temperature, however, C4 photosynthesis can develop significant CO2
sensitivity, particularly at the low humidity associated
with hot days in semi-arid regions of the world.
Temperature has a slight effect on the initial slope
of the A/Ci response in C4 plants, but stimulates the
CO2 -saturated plateau at a Q10 of 2 or more up to
the photosynthetic thermal optimum (Figure 4). As a
result, the CO2 saturation point increases with temperature, and once the operational Ci falls below the CO2
saturation point, C4 photosynthesis becomes sensitive
to slight increases in CO2 (Figure 4; Sage 1994; Sage
and Pearcy 2000).). Also, at elevated temperature, stomata conductance often declines in response to lower
relative humidity, particularly in drier environments
(Schulze and Hall 1982). In C4 plants, stomatal closure in response to low humidity will reduce Ci . If the
reduction in Ci is sufficient to keep it in the initial slope
region of the CO2 response curve, then C4 plants will
remain CO2 sensitive to higher ambient CO2 levels.
For example, in Amaranthus retroflexus, the operating
Ci falls on the initial slope at 32 ◦ C when plants exhibit
a normal leaf conductance of 0.2 mol m−2 s−1 (Figure
4). If gc declines 50%, the operating Ci falls on the
initial slope at 24 ◦ C as well, and the increase in the
CO2 sensitivity of A with rising temperature is dramatically enhanced (inset, Figure 4). For these reasons, C4
photosynthesis has greater CO2 sensitivity at warmer
than cooler temperatures. The CO2 sensitivity of C3
plants also increases with temperature (Figure 4, inset;
Sage et al. 1995), and C3 plants are likely to remain
CO2 sensitive at higher ambient CO2 levels than C4
species. For example, CO2 increases above about 500
µbar should saturate C4 photosynthesis in most cases,
while C3 photosynthesis should continue to respond
to CO2 increases above 500 to 700 ppm at warmer
temperatures (Lecain and Morgan 1998; Ghannoum et
al. 2000). However, acclimation effects can reduce the
CO2 responsiveness of plants, such that the degree to
which CO2 enhances productivity in C3 relative to C4
plants in field situations is uncertain.
Acclimation to elevated CO2
When plants are grown at elevated CO2 , the value
of A shifts with time, a process known as photosynthetic acclimation (Sage 1994). In C3 plants, A often
declines in the weeks after elevated CO2 exposure,
and can even decline to equal the value exhibited by
plants growing at current levels of CO2 (Stitt 1991;
Lee et al. 2001). Photosynthetic acclimation to high
CO2 is largely controlled by the production of regulatory signals in response to elevated carbohydrate
levels; these signals reduce the expression of major
photosynthetic enzymes, notably Rubisco (Moore et
al. 1999). C3 plants are prone to high carbohydrate
accumulation in elevated CO2 conditions for two major reasons. First, they may be adapted to low CO2
conditions of the recent geological time, and as a result
may have limited ability to utilize enhanced supplies
of carbohydrate (Sage and Coleman 2001). For over
95% of the past 420,000 years, CO2 levels were below
280 µbar, and carbon acquisition potentials were correspondingly less (Sage and Coleman 2001). Second,
most natural ecosystems are deficient in mineral nutrients, and these limitations reduce a plant’s capacity to
utilize carbohydrates. Thus, although C3 plants have
the potential to show large responses to rising CO2 , the
degree to which this potential is realized is restricted
by acclimation responses. (Diaz et al. 1993; Koch and
Mooney 1996).
Acclimation to CO2 enrichment also occurs in C4
plants (Tissue et al. 1995; Watling et al. 2000; Lee
et al. 2001), although there are numerous exceptions
(Sage 1994). When acclimation occurs, C4 photosynthesis adjusts to high CO2 by slightly reducing both
216
Figure 4. The response of C4 photosynthesis to intercellular CO2 partial pressure at four leaf temperatures. Supply functions corresponding to
leaf conductances (gc ) of 0.2 and 0.1mol m−2 s−1 are shown in gray. Inset: the corresponding % CO2 sensitivity as a function of temperature
for A. retroflexus at supply functions of 0.2 (filled circles) and 0.1 (inverted triangles) mol m−2 s−1 ; best-fit regression lines are shown as black
lines. For comparison, the % CO2 sensitivity at a supply function of 0.2 mol m−2 s−1 of the C3 plants Chenopodium album (open circles)
and Capsicum annuum (diamonds) are shown with fitted regressions lines in gray. % CO2 sensitivity is expressed as the relative increase in net
photosynthesis that occurs when atmospheric CO2 is doubled from 360 µbar assuming constant gc . Data from Sage (2002; A. retroflexus, C.
album) and unpublished (Capsicum annum).
Figure 5. The CO2 responses of C4 photosynthesis in sorghum
plants grown at current (black line) or 700 µbar (dashed line) partial
pressures of atmospheric CO2 . (from Watling et al. 2000 by permission). Arrows indicate intercellular CO2 content corresponding to
the ambient or elevated growth CO2 levels.
the initial slope and CO2 -saturated A (Figure 5; Tissue
et al. 1995; LeCain and Morgan 1998; Ghannoum et
al. 2000; Watling et al. 2000; Snowdon et al. 2002).
PEPCase activity declines in nutrient-deficient Pan-
icum antidotale plants grown at elevated CO2 , but
not in plants grown at high CO2 and full nutrition
(Ghannoum et al. 2000), demonstrating acclimation is
promoted by nutrient deficiency in C4 plants as well.
Sorghum, maize and C4 Flaveria species also exhibit
significant reductions in PEPCase but not Rubisco
content (Watling et al. 2000; Gascoigne-Owens et al.
2002; Snowdon et al. 2002), indicating acclimation
may preferentially reduce C4 cycle capacity.
Where nutrients are limiting, productivity depends
upon the rate at which nutrients are released through
decomposition and the inherent nutrient use efficiency
of the plants (Hungate 1999). In this regard, the PNUE
advantage of C4 plants is a key feature that may enable C4 species to remain competitive in high CO2
situations. Nitrogen is limiting in most soils, and if
the nitrogen supply rate to a plant is less than the carbon supply rate from photosynthesis, carbohydrates
accumulate and a reduction in photosynthetic capacity
occurs. Where nitrogen supply rate has high control over productivity, species with higher PNUE can
maintain greater productivity, and thus are more likely
to dominate a site (Wedin and Tilman 1996). Elevated
CO2 enhances PNUE in C3 plants, but not to a de-
217
gree that allows them to match the PNUE of C4 plants
(Sage and Pearcy 1987).
Stomatal responses to CO2
Increasing CO2 causes a reduction in stomatal conductance in both C3 and C4 species. Average reductions in stomatal conductance in fully watered C4
plants following a doubling of atmospheric CO2 vary
widely but are usually 20% to 50% (Knapp et al. 1996;
Lecain and Morgan 1998; Wand et al. 1999; Ghannoum et al. 2001; Anderson et al. 2001; Maherelli et
al. 2002), which is roughly similar to or greater than
what is observed in C3 species (Sage 1994; LeCain
and Morgan 1998; Anderson et al. 2001; Ghannoum
et al. 2001; Reich et al. 2001). The consequence of
the lower stomatal conductance is water status in both
C3 and C4 plants improves at any given point in a
growing season, and growing seasons are prolonged
because soil water reserves are exhausted less rapidly
(Owensby et al. 1996, 1997; Ghannoum et al. 2001;
Morgan et al. 2001; Polley et al. 2002). This effect is
more significant for C4 plants because they tend to be
active in hot, drought prone situations where growing
seasons are curtailed by late-season drought.
Climate change
The global temperature of the Earth has increased
more than 0.5 ◦ C in the last century and is expected
to rise an average of 2 ◦ to 4 ◦ C in coming centuries as greenhouse gas concentrations increase in the
atmosphere (Houghton et al. 2001). The common expectation is C4 plants will be favored by global warming alone, although CO2 enrichment complicates this
picture because C3 photosynthesis also becomes more
CO2 responsive with increasing temperature (Long
1991; Sage et al. 1995). When CO2 and temperature
increase, a common response is for growth to increase
in both C3 and C4 plants (Patterson 1995; Grise 1996).
When both are grown in mixed stands where competition occurs, the faster growing C4 species can still
suppress the slower growing species, so that narrowing
of differences in plant size that is often observed in
monocultures is less in mixed cultures (Grise 1996).
One of the advantages that C4 plants have over
many C3 species is that they are already adapted to
elevated temperature, whereas C3 species tend to
prefer cooler periods of the day and growing season
(Patterson 1995). C4 species are also more tolerant of
heat stress that may accompany episodic heat events,
which are predicted to increase in the future (White
et al. 2000, 2001). Meristematic regions of C4 plants
are also stimulated at high temperatures that are often inhibitory for growth in C3 plants (Ghannoum et
al. 2000; Morgan et al. 2001). As a consequence,
C4 species may be better able to respond to warming
in a manner that promotes rapid canopy growth, root
proliferation, and colonization of disturbed patches.
In natural systems, the significance of climate
warming for C4 vegetation depends less on the mean
increase in global temperature, and more on the spatial and temporal variation of the temperature increase.
In New Zealand, for example, episodic heat events
inhibit C3 plants more than C4 grasses, and as a
result, facilitate C4 grass invasion of C3 -dominated
grasslands (White et al. 2000, 2001). On a broader
scale, most climate warming is predicted to occur at
high latitudes and during the winter (Kattenberg et al.
1996), that is, when and where C3 biomass is currently favored. In temperate zones, if climate warming
acts to moderate severe winter cold such that the cool
growing season is lengthened, then the range of C3
species could expand. A recent increase in C3 biomass at the expense of C4 biomass in southern Alberta,
Canada, may be the result of moderating winter and
spring cold (Peat 1997). If climate warming also leads
to greater summer aridity and thus reduces the length
of the summer growing season, C4 species could be
inhibited. Alternatively, if warming extends the warm
season, C4 species should expand their ranges, and at
higher latitude where summers sufficiently warm, C4
species could begin to invade climate zones where they
are currently excluded. The expansion of Spartina into
higher latitude salt marshes of western Europe in recent decades (Long 1999) may be a reflection of the
warming following the termination of the little ice age.
Notably, this has occurred during a period when CO2
levels rose over 25%.
If precipitation patterns change, C4 species should
be favored where the increase in precipitation occurs
during the warmer months of the year, while C3 species should be favored if precipitation increases during
the cool months of the year (Sage et al. 1999). Likewise, reductions in summer precipitation will likely
suppress C4 species, and reduction in winter precipitation will suppress C3 species (Monson et al.
1983).
Paramount to predicting changes in C3 and C4
distribution will be predicting the response of disturbance regimes as the climate warms, notably storm
damage and fire. Warming inevitably increases fire fre-
218
quency and intensity, and increased burning reduces
the area of woodlands in favor of grasslands, which
at lower latitudes will be C4 -dominated (Goldammer
1990; Flannigan et al. 2000; Clark et al. 2001). A
key component associated with climate warming is the
more rapid drying of surface fuel, such that an ecosystem will be flammable for a longer period of the
year. Once started, fires burn with greater intensity in
warmer climates, and are more likely to kill woody
species and open the canopy. Once a canopy is opened
by an ecological disturbance, the penetration of solar
radiation to the ground accelerates drying of litter, further increasing fire probabilities (Uhl and Kaufmann
1990; Cochrane et al. 1999). After a forest canopy
is sufficiently opened, C4 grasses are able to invade
woody biomes, and they promote further burning by
rapidly producing highly flammable litter that readily
burns in the presence of an ignition source.
Land-use change
Land-use change includes all human activity that directly affects the vegetation cover on the terrestrial
surface. The important aspects of land use change
from the perspective of C3 and C4 dynamics are the
use of fire, conversion of natural landscapes to agriculture, and degradation of land due to overexploitation, usually from overgrazing and logging (Vitousek
1994).
Humans employ fire as a land management tool,
and many if not most of the C4 biomes on the planet
have significantly benefited when humans first entered
a landscape. For example, most warm-temperate to
low-latitude grasslands and savannas on the planet
expanded when humans appeared (Schüle 1990). In
North America, the tall grass prairie biome extended
hundreds of kilometers eastward into the deciduous
woodlands of the Mississippi basin because of aboriginal burning practices (Kucera 1992). In Australia,
the large savannas of the continent are a response to
widespread use of fire by aborigines after their arrival 75,000 years ago, and most of the grasslands
on Pacific islands are derived from human use of fire
in the past few thousand years (Schüle 1990). Fire
is an important land-management tool in traditional
societies for clearing bush and driving game, and is
now an integral part of modern management practices
for maintaining grassland ecosystems (Pyne 1990). In
recent years, human population pressure has often increased burning of landscapes, and this has fueled
the loss of forests in many tropical regions as the in-
creased burning has accelerated forest removal beyond
regeneration rates (Mueller-Dombois and Goldammer
1990). In Nigeria, for example, forests have retreated
500 km since 1960 and have been replaced by C4 dominated savanna grasslands (Hopkins 1983).
In the future, higher CO2 levels could accelerate
land conversion by increasing fuel loads and reducing fuel recovery times, such that fire cycles can
be shortened where ignition sources are frequent and
fire suppression ineffective (Sage 1996; Bond and
Midgley 2001). Where fire control is effective, higher
CO2 should favor succession to woodlands because
woody seedlings show pronounced responses to CO2
enrichment (Polley et al. 1994; Polley 1997; Hoffmann et al. 2000; Dijkstra et al. 2002). In addition to
establishing faster from seed, woody plants resprout
more rapidly following fire injury in high CO2 environments, and thus may be able to overtop the grass
canopy in less time (Bond and Midgely 2001). Once a
woodland canopy forms above the grasses, the growth
of the C4 grasses is directly suppressed by shade,
and the cooler, wetter conditions in the woody plant
understory further reduce fire probabilities.
In forested regions of the tropics, C4 grasslands
are expanding because of extensive logging, which is
often followed by further clearance for farming and
pasture (Goldammer 1993; Maas 1995). At low latitude, C4 grasses are planted where pasture is created,
and invasive C4 grasses aggressively seed into abandoned farm plots and recently cut or burned lands
(Uhl and Buschbacher 1985; D’Antonio and Vitousek
1992; Sage 2001). Most of the C4 grasses are fireadapted and promote burning because they rapidly
develop a dense canopy that dries following a few days
of little or no rain (Uhl and Kaufmann 1990). Following each fire, the grasses aggressively recover and
advance into forest boundaries where a previous burn
damaged trees and opened gaps into which C4 grasses
can establish (Cochrane and Schulze 1999). Frequent
burning also reduces nitrogen levels in grassland soils,
while stimulation of C:N ratios by elevated CO2 could
reduce soil fertility and further favor persistence of C4
grasses (Frost and Robertson 1987; Aide and Cavelier 1994; Johnson and Wedin 1997). Eventually, C4
grasslands become a permanent fixture on the landscape because of regular burning, reduced soil fertility,
warmer, drier microclimates, and a lack of seed rain
from forest species.
In the past two centuries, humans have intensively
exploited temperate-zone landscapes for row crop agriculture, pasture, and timber. Because C4 grasslands
219
occurred on some of the most productive biomes of the
planet, or themselves were viewed as valuable grazing
sites, the C4 -dominated biomes of the temperate zone
have been converted if not altogether destroyed (Sage
et al. 1999). In North America, the tall-grass prairie in
the center of the continent, and the wiregrass savanna
of the southeastern region, are largely destroyed because of conversion to row crop agriculture, pasture
and timber plantations (Means 1997). In the southwestern region of the North America, and in large
areas of Africa, Australia, and South America, semiarid C4 grasslands have been converted to thornscrub
by overgrazing from sheep and cattle (van Auken
2000). Landscape conversion caused by overgrazing
largely occurred at a time when CO2 levels were much
lower than today, and rising CO2 is not considered
a major reason for the initial conversion from C4 dominated grasslands to C3 shrubland (Archer et al.
1995). The higher CO2 of the current era tends to
favor C3 shrub establishment in the presence of continued grazing, however, and should hinder reversion to
grassland (Bond and Midgley 2001). In addition to accelerated growth rate, elevated CO2 can promote shrub
growth by reducing transpiration in the grass canopy.
This allows more water to percolate to deeper soil layers where the roots of the shrubs are active (Polley
1997). C4 grasses have shallow roots as opposed to the
deep tap-roots of woody dicots. Thus by reducing transpiration, elevated CO2 increases the water available
to the shrubs.
Bioinvasions
Bioinvasions occur when exotic species successfully
establish in novel landscapes (Vitousek 1994). Most
concern has focused on the limited number of invasive
species that escape biological controls and aggressively spread across landscapes to the detriment of the
native flora and fauna. C4 plants are noted bioinvaders,
and many are listed as the most noxious weeds on the
planet (Patterson 1995). Nearly all grass floras of the
warmer regions of the planet have a suite of exotic
C4 species. Although most are associated with agricultural habitats, a number have become major threats
to natural ecosystems.
C4 bioinvasions are of greatest concern where they
act in concert with local burning practices to establish
runaway fire cycles that convert a landscape from a
forest or shrubland into a low-diversity C4 grassland
(Figure 6; D’Antonio and Vitousek 1992). Because
the alien grasses often escape the natural predator
and disease control of their native ranges, their introduction into a landscape can be a novel element
that overwhelms the regeneration ability of a forest
or shrubland (Baruch et al. 1985; D’Antonio and Vitousek 1992; Knapp and Medina 1999). Moreover, the
high photosynthetic potential associated with the C4
pathway allows for the rapid production of grass biomass that readily dries to form a highly flammable
tinder. As a consequence, after a C4 invader becomes
established, relatively modest fire regimes can intensify and often develop a positive feedback mode
where fire frequency and intensity accelerate until a
low-diversity C4 grassland dominates the landscape
(Figure 6; Cochrane et al. 1999). This often occurs
within a decade or two after the invader is introduced.
Once established, the C4 grassland is often resistant
to encroaching trees and brush because of frequent
burning, low soil fertility and direct competition from
the dominant grasses (D’Antonio and Vitousek 1992).
In New Caledonia, for example, there is little in the
way of endemic C4 grasses. C4 grasses became common on the western, drier half of the island as a result
of pasture creation by French colonists in the last
two centuries. In recent decades, fires and alien C4
grasses have invaded rainforests in the central highlands, and now large tracts of grassland are found
(Figure 7). Despite the damage to forests, fire cycles
are difficult to control, often for reasons unrelated to
the natural ecology of the region. For example, one
New Caledonian noted that it was common evening
entertainment in rural areas to gather in the countryside, drink beer and set a hillside on fire (H. Reeves,
personal communication).
Terrestrial eutrophication
Through fertilizer production, extensive planting of
legumes, fossil fuel combustion, and automobile exhaust, humans have more than doubled the natural
rate at which biologically useful forms of nitrogen are
produced (Vitousek et al. 1997). As a consequence,
widespread areas of the planet are becoming enriched
in soil nitrogen, or eutrophied. Higher soil N favors C3
species over ecologically similar C4 species in temperate zone settings. However, weedy tropical C4 grasses
also show pronounced growth responses to N enrichment, such that temperate zone patterns may not apply
at low latitude (Wedin and Tilman 1993; Knapp and
Medina 1999).
An uncertainty associated with C3 and C4 responses to rising CO2 is the effect of increased carbon
220
Figure 6. Grass-fire cycles and forest replacement by invasive C4 grasses. Disturbance of woody vegetation would normally be followed by
succession back to rainforest, as seeds from adjoining forest disperse into open patches (indicated by the ‘natural cycle’). In the presence of
C4 grasses, an autocatalytic cycle promoting repeated burning can occur, because the grasses, in combination with ignition by humans and
microclimate aridification of the grass layer, promote repeated burning. With each burn, the grass patch increases and forest extent decreases,
until forests become isolated fragments and the grassland dominates the landscape. As forest fragmentation increases, seed rain of forest species
declines while the seed rain of grasses increases. With each cycle, the probability of forest regeneration declines, while the probability of more
fire and grass expansion increases. In time, the grass-fire cycles spiral out of control until the forest is completely replaced by a grassland that
is sustained by regular burning (based on D’Antonio and Vitousek 1992 and Cochrane and Schulze 1999).
flow into soils. Plants at elevated CO2 enrich soil carbon by injecting carbohydrates into the soil as root
exudates, and by putting more leaf, root and stem
litter into the soils as plant tissues die (Ball 1997).
In high CO2 conditions, litter injected into soils has
greater C:N ratios and thus decomposes more slowly.
In grassland soils of limited N, elevated CO2 thus can
cause a reduction in N availability, which should favor
C4 grasses due to their higher PNUE. Eutrophication
overcomes effects of high CO2 on soils by providing sufficient N to compensate for greater C:N ratios
in the litter and accelerate nutrient cycling (Hungate
1999). Eutrophication also favors C3 plants by providing the nutrients required for C3 species to sustain high
growth responses to elevated atmospheric CO2 (Stitt
1991).
One of the critical impacts of CO2 enrichment will
be on nitrogen fixing organisms. As CO2 increases,
nitrogen fixation rates increase in a diversity of plants
that have mutualistic associations with N-fixing bacteria (Tissue et al. 1997; Dakora and Drake 2000).
Grasses and sedges develop close associations with
many free-living nitrogen-fixing bacteria, and the extra carbohydrate from elevated CO2 is passed to these
bacteria, increasing N-fixation. In the Chesepeake Bay
salt marsh (eastern USA), the C3 sedge Scirpus olneyi
exhibited a 73% increased acqusition of fixed N, while
in the nearby C4 grass Spartina patens, incorporation
of fixed N rose only 23% (Dakora and Drake 2000).
Nitrogen-fixation in legumes and alders is particularly
responsive to elevated CO2 , with increases over 100%
commonly following a doubling of CO2 (Tissue et al.
221
2002). Because soil N levels in many areas are now
well elevated, the conversion to C3 shrublands may be
permanent as the soil N supports rapid recolonization
of shrub species following a major disturbance (van
Auken 2000).
Some predictions of how global change will effect
the future of C4 plants
Figure 7. Forest fragmentation in New Caledonia. A) Exotic grass
incursion into forest habitat following burning of a hillside. Note the
patch of grass extending beyond the grass front into the forest (white
arrow). B) A rainforest fragment in the central highlands of New
Caledonia, surrounded by a C4 -grass dominated vegetation. Trees
killed in a recent fire are visible in the foreground. Note the predominance of grasslands on former forested land in the background
(photo by R. Sage).
1997; Vogel et al. 1997; Schortemeyer et al. 2002).
One of the few plant groups that are successful in C4
dominated grasslands are the legumes, perhaps in part
because their ability to fix nitrogen allows them to escape competition from C4 plants (Ludlow 1985). If N
fixation in legumes increases at elevated CO2 , then the
native legumes in tropical grasslands could begin to
eutrophy these systems, initially to the benefit of the
legumes themselves, but perhaps to the later benefit of
other C3 species. This effect may have already contributed to the conversion of semi-arid C4 grasslands
to C3 thornscrub. Many of the shrubs that establish
in degraded C4 grasslands are legumes, such as mesquite (Prosopsis spp.) and Acacia spp. (Polley et al.
1994). Once established, leguminous shrubs inject significant quantities of nitrogen into the soil, supporting
further establishment of woody species (Polley et al.
1994; Archer and Stokes 2000; Schortenmeyer et al.
The future of the C4 flora on the planet is not simply
a matter of CO2 and warming. Land-use change, eutrophication and introduction of alien C4 species will
strongly interact with CO2 and warming to produce
shifts in patterns of C3 and C4 dominance. Because
bioinvasions and land use are more immediate in terms
of their impacts, they will tend to constrain the type of
responses that may follow as changes in climate and
CO2 intensify. In any case, certain trends between the
global change parameters appear likely, as they are
clearly evident today. Below, we list five scenarios
that appear likely given our understanding of current
trends.
1. Widespread deforestation of tropical forests will
continue, with replacement of the forests by C4
grasslands. While the destruction of forests will
often be intentional, unintentional forest loss will
be exasperated by runaway fire cycles driven by
invasive C4 grasses. Elevated CO2 and warming
will promote these trends where fire management
is ineffective.
2. As temperate climates warm, C4 species will migrate to higher latitudes due to warmer summers,
and the increased number of heat and dry spells
that will harm existing C3 vegetation. Elevated
CO2 will enhance the growth of C4 grasses and
their water status, thereby increasing their ability to exploit novel habitats following natural and
anthropogenic disturbance. Increased fire that is
associated with warmer, drier conditions, and
clearcutting of forests, will promote the expansion
of C4 habitat.
3. Where the summer monsoon shifts to new locations, C4 species will be favored because their
growing season will improve. The Mojave and
Great Basin Deserts in western North America,
for example, are predicted to receive more summer moisture from a stronger summer monsoon,
and thus should have a more active C4 flora (Lin
et al. 1996). In semi-arid regions where summers
become drier (the high plains of Colorado and
222
Wyoming, for example), C4 species will become
less prevalent.
4. C3 species will be favored where a woody canopy
can establish, either by active afforestation (as occurs in Brazil where savanna has been converted
to timber production; Soares 1990), by fire control, or by overgrazing. Elevated CO2 will interact
strongly where there are enough nutrients in the
soil to allow for increased growth of woody seedlings. C4 grasslands in wetter climates may become dominated by C3 woody species because the
greater precipitation and higher CO2 level could
allow establishment of a woodland canopy. This
is occurring in the southeastern US, where woodlands are establishing in former wiregrass savanna
(Means 1997).
5. Eutrophied landscapes of the temperate zone will
likely convert to C3 grasslands and woodlands because the higher N in the soil will allow C3 plants
to overcome the NUE advantage of C4 plants and
reverse the immobilization of soil N caused by
high C:N ratios. High nutrients will also enable
C3 species to maintain high CO2 responsiveness
in a CO2 enriched world, and will speed the establishment of woody species into C4 grasslands,
thereby disrupting fire cycles. Much of the C3 advantage will arise from their ability to exploit the
cool growing season and develop a dense canopy
on N-enriched soils. The dense canopy is then able
to shade C4 grasses that become active later in the
year (Sage et al. 1999).
In conclusion, there is little reason to suspect that
the C4 functional type will be threatened by global
change, although many C4 species will be at risk of extinction for the same reason that C3 species are at risk
– land use change, bioinvasions and eutrophication
are producing widespread destruction of habitat and
simplification of biotic diversity. By acting as major
disturbance agents driving global change, humans are
creating more environments where the primary conditions for C4 photosynthesis are met. While high CO2
and eutrophication will offset the benefits of global
change for C4 plants in many instances, there should
be an abundance of niche space to allow C4 species to
evolve in concert with future change.
Quo vadis C4 ?
Omnia mutantur, nos et mutamur in illis.
Acknowledgements
We thank Jarmila Pittermann for some of the gas
exchange analyses, and Danielle Way, Sandor D.
Nagy and James Havey for assistance in preparing the
manuscript.
Note
1 Operating C refers to the intercellular partial pressure corresi
ponding to a given level of atmospheric CO2 .
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