Ecophysiological mechanisms involved in competition in C3/C4 mixed
stands
Lattanzi F. A. and Schnyder H.
Lehrstuhl für Grünlandlehre, Technische Universität München, Am Hochanger 1, 85350 FreisingWeihenstephan, Germany.
Abstract
We analyze the role of structural and physiological differences between a C3 (Lolium perenne L.) and a
C4 grass (Paspalum dilatatum Poir.) in determining the carbon economy of individuals growing in
mixtures. Further, we assess to what extent such differences are intrinsic or size-mediated (allometric).
C3/C4 mixtures were grown at 15ºC and 25ºC, to produce C3- and C4-dominated stands, respectively.
Daily whole-plant carbon gain was estimated using steady-state 13C-labelling. Light capture was
estimated from profiles of incident light and leaf area measured down the canopies. The dominant
species –Lolium at 15ºC, Paspalum at 25ºC– had higher relative photosynthesis rates and proportionally
lower respiratory losses than their subordinate neighbours. Therefore, at both temperatures, the mixtures
were becoming more dominated by the dominant species. At 15ºC, subordinate C4 plants were as
efficient as their dominant C3-neighbours in capturing light, but had a lower light use-efficiency. At
25ºC, subordinate C3 plants had similar light use-efficiency but captured less light than dominant
C4-neighbours. Hence, changes in the C3/C4 balance were related to physiological determinants at
15°C, but to structural characteristics at 25°C.
Keywords: coexistence, light, carbon, use-efficiency, allometric analysis.
Introduction
C3 and C4 species co-occur in many temperate and subtropical grasslands. However, an understanding
of the mechanisms determining the balance between C3 and C4 species is only emerging, with models
able to estimate light capture and photosynthesis of individual plants being used to assess the
relationship between structure/productivity of individuals and the coexistence of species (Anten and
Hirose, 2003). Here we analyzed the consequences of differences in structural and physiological
characteristics between a C3 (Lolium perenne L.) and a C4 grass (Paspalum dilatatum Poir.) for the
carbon economy of individuals growing in mixed stands. Instead of modelling C gain, we directly
measured it with a novel labelling approach. Since structural parameters are often correlated with plant
size (Niklas, 1994), we assessed to what extent differences were intrinsic or allometric.
Materials and methods
Mixed C3/C4 stands grew undisturbed at 15ºC or 25ºC for ~2 months, to produce C3- and
C4-dominated canopies, respectively. Daily whole-plant C gain was estimated using steady-state 13CO2
labelling (Schnyder et al., 2003). Simultaneously, light capture by each species was estimated from the
profiles of incident irradiance (I) and leaf area (F) measured down the canopies. Extinction coefficients
(K) were estimated as the slope of log (I/I0) = K F (0.49 at 15°C, 0.57 at 25°C), where I0 is the
irradiance at the top of the canopy (550 µmol m-2 s-1). Light capture by each species was a direct
function of its contribution to F at each canopy layer. Finally, light capture per unit mass (Φmass) and per
unit area (Φarea), and light use-efficiency (Plight, C fixed per unit captured light) were calculated.
Allocation between leaf parts (sheath/blade), and the relationship between blade mass and area (i.e.
specific leaf area, SLA) were analyzed allometricaly (Niklas, 1994). Briefly, the scaling exponent (α)
and the scaling coefficient (β) in Y1 = β (Y2)α were obtained from reduced major axis regression of
log(Y1)= log b + a log(Y2).
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Results and Discussion
The dominant species –Lolium at 15ºC, Paspalum at 25ºC– had higher relative photosynthesis rates and
proportionally lower respiratory losses than their subordinate neighbours. Therefore, at both
temperatures, the dominant species had higher relative growth rate (RGR, Table 1). This implies that the
mixtures were not at equilibrium, but were becoming more dominated by one of the species. The
reasons for these displacements of the C3/C4 balance differed between the C3- and C4-dominated
stands.
Table 1. Relative rates of photosynthesis (RPR), respiration (RRR) and growth (RGR); proportion
(BWR), specific area (SLA) and average N content (nL) of blades; and average irradiance (IL), light
capture per unit area (Φarea) and mass (Φmass) and light use-efficiency (Plight) of C3 (Lolium) and C4
(Paspalum) individuals growing in mixtures at 15°C or 25°C.
25°C
RPR, d-1
15°C
Lolium
Paspalum
Lolium
Paspalum
0.046 ±0.015
0.116 ±0.008
0.086 ±0.022
0.047 ±0.012
RGR, d-1
0.026 ±0.010
0.097 ±0.010
0.065 ±0.021
0.011 ±0.008
RRR, d-1
0.020 ±0.005
0.019 ±0.002
0.021 ±0.001
0.036 ±0.004
BWR, kg C (kg C)-1
0.72 ±0.00
0.64 ±0.01
0.59 ±0.07
0.75 ±0.03
SLA, m2 (kg C blade)-1
73 ±3.4
89 ±2.0
55 ±0.3
112 ±2.8
nL, mmol m-2
96 ±0.6
69 ±2.9
80 ±0.3
75 ±6.5
IL, µmol (m blade)-2 s-1
52 ±7.8
132 ±7.9
125 ±5.7
73 ±5.4
2.8 ±0.27
-2
Φarea, mol quanta m
1.9 ±0.34
4.8 ±0.29
4.4 ±0.31
Φmass, mol quanta (kg C)-1
86 ±13
186 ±1
153 ±24
144 ±2
Plight, mmol CO2 (mol quanta)-1
42 ±7.5
50 ±3.7
44 ±4.5
26 ±6.3
Mean ±SD (n = 2 growth chambers, 4 to 10 plants)
(i) The disproportionately greater respiratory burden of subordinated individuals contributed
substantially to differences in RGR at 15°C, but less so at 25°C. If subordinate plants would have had
the same proportional respiratory losses of their dominant-neighbours, differences in RGR would
decrease by 40% at 15°C, but only 13% at 25°C. Insufficient down-regulation of respiration as plants
become shaded seems to stem from maintenance requirements (Lötscher et al., 2004) (ii) Differences in
relative photosynthesis rates were associated with differences in Plight at 15°C, but not at 25°C (Table 1).
The low Plight of the C4 at 15°C was related to a failure of the CO2 concentrating mechanism, as
suggested by higher 13C discrimination: 2.1‰ at 25°C vs. 4.8‰ at 15°C. Whether this was a low
temperature- or shade-related effect is not clear. In any case, nL did not limit C gain in these plants
(Table 1). At 25°C, P light was similar in both species, as also found in a C4 dominated grassland (Anten
and Hirose, 2003). Therefore, these results only partially support the role of Plight at low irradiances in
determining the C3/C4 balance proposed by Ehleringer (1978). (iii) Differences in relative
photosynthesis rates were related to differences in Φmass at 25°C, but not at 15°C (Table 1). Subordinate
C4 plants were as efficient as their dominant Lolium-neighbours in capturing light per unit mass because
higher BWR and SLA compensated for a lesser and less advantageously disposed leaf area (i.e. lower
Φarea). Conversely, at 25°C, subordinate C3 plants were not able to develop this response to the same
extent and had lower Φarea and Φmass than dominant C4-neighbours. Therefore, competition for light was
asymmetric in this case, as bigger plants captured disproportionately greater amounts of light.
Adjustments in BWR and SLA are common responses of subordinate plants in dense stands, which can
be adaptive or size-mediated (Schwinning and Weiner, 1998; Anten and Hirose, 2003). Scaling
exponents of blade/sheath and area/mass relationships were always lower than unity (Fig. 1). This
means that, as plants got bigger, (proportionally) less C was allocated to blades, and less area was
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produced per unit C invested in blade tissue. This often-described trade-off is believed to arise from
greater requirement of support tissue in taller plants (Schwinning and Weiner, 1998). In this study,
higher BWR and SLA in subordinate plants were mainly allometric effects, i.e. they had higher BWR
and SLA because they were smaller than dominant plants. In fact, Paspalum had lower scaling
coefficients (p<0.05, Fig. 1A), and thus intrinsically lower amounts of blade per unit sheath, both at
15°C and 25°C. In both species, scaling exponents of the area vs. mass relationship were higher (close
to 1) in subordinate plants (p<0.05, Fig 1B). Thus, shading did trigger a morphological response,
allowing these plants to become (relatively) taller with minor changes in SLA.
10 3
(A)
y1 =6.8 y2 0.77
0.81
y1 =6.4 y2
10 1
10 3
10 2
y1 =2.3 y2
0.90
y1 =1.2 y2
10 1
10 3
10 2
y1 =1.4 y2 0.93
y =3.0 y 0.80
y1 =4.1 y2 0.77
10 1
10 1
10 2
Sheaths, mg C
10 3
0.97
y1 =2.1 y2 0.84
2
Blades, mg C
(B)
10 2
10 2
Blades, cm
10 3
1
10 1
10 1
10 2
2
10 3
Blades, mg C
Figure 1. Allometric analysis of allocation of C to sheaths vs. blades (A), and between blades mass vs.
area (B) in C3 (circles) and C4 (triangles) individuals growing in mixed stands at 15°C or 25°C, and
thus in dominant (open symbols) and subordinate (closed symbols) hierarchical positions. Equations
are: Y1 = β Y2 α.
Morphological responses in subordinate Paspalum at 25°C were sufficient to reach a similar Φmass than
taller and greater Lolium-neighbours. Why were they not in Lolium at 15°C ? One possibility is that
Kranz anatomy of C4 leaves allows thinner/lower density blades, and thus maximum attainable SLA is
inherently lower in C3 than in C4 species. In conclusion, different structural and physiological
parameters were responsible for the displacement of the C3/C4 balance at low and high temperature.
C3 dominance was based on high Plight and proportionally low respiration of Lolium. But C4 dominance
was based on high efficiency in capturing light of Paspalum.
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