Annals of Botany 77: 35–45, 1996

Radiation Interception, Partitioning and Use in Grass–Clover Mixtures

O.FAURIE*, J.F.SOUSSANA* and H.SINOQUET† *Fonctionnement et Gestion de l’EcosysteZ me Prairial, INRA-Agronomie. 12 AŠ. du BreT zet, and † PIAF, INRA-Bioclimatologie, Domaine de Crouelle, 63039 Clermont-Ferrand Cedex 2, France

Received: 24 May 1995 Accepted: 29 August 1995

Mixed swards of perennial ryegrass\white clover were grown in competition under controlled environmental conditions, at two temperatures and with different inorganic nitrogen supplies. The swards were studied after canopy closure, from 800 to 1200 mC d cumulative temperatures. Clover contents did not vary significantly during the period. A simulation model of light interception was used to calculate light partitioning coefficients and radiation use efficiencies for both components of the mixture in this controlled environment experiment. Additionally, this same radiative transfer model was applied to the field data from Woledge (1988) (Annals of Applied Biology 112: 175–186) and from Woledge, Davidson and Dennis (1992) (Grass and Forage Science 47: 230–238). The measured and simulated values of light transmission, at different depths in the mixed canopy, were highly correlated (P ! 0n001) with more than 80% of the total variance explained. The daily average of photosynthetically active radiation (PAR) interception in a natural environment was estimated from simulations, for the field and controlled environment data. Under these conditions, white clover captured significantly more light per unit leaf area than perennial ryegrass at low, but not at high, nitrogen supply. In the controlled environment experiment, the radiation use efficiency of the legume was lower than that of its companion grass. For both species, radiation use efficiency was negatively correlated with the mean irradiance of the leaf. The role of a compensation between light interception and light use for stabilizing the botanical composition of dense grass–clover swards is discussed. # 1996 Annals of Botany Company

Key words: Light interception, radiation transfer model, growth analysis, radiation use efficiency, grassland, white clover, perennial ryegrass, Trifolium repens L., Lolium perenne L.

calculate light partitioning between grass and clover and INTRODUCTION thus to compare their light interception efficiencies in the Temperate perennial grasses and legumes differ with respect mixed canopy. to radiation interception and conversion efficiencies. In White clover leaves have high photosynthetic capacities monocultures, light is fully intercepted at a lower leaf area (Woledge, Dennis and Davidson, 1984; Dennis and index with legumes than with grasses (Brougham, 1958); on Woledge, 1985) and even in situ in the sward, where grass the other hand, the radiation use efficiency of C$ grasses was dominant (nitrogen fertilized plots), clover laminae had "% tends to be higher than that of legumes (Gosse et al., 1986). a greater assimilation rate of CO# per unit leaf area than Competition for light is considered to be important in grass (Woledge, 1988). This was also reported for simulated determining whether grass or legumes dominate in mixed mixed swards grown in a controlled environment (Davidson swards (Haynes, 1980). With perennial ryegrass (Lolium and Robson, 1985). perenne L.) and white clover (Trifolium repens L.) mixtures, The balance between species within the mixed sward long regrowth periods in conditions more favourable to depends upon the relative growth rate of each component grass growth (low temperatures, high availability of mineral (Woledge, 1988). The net assimilation rate of the leaf nitrogen) lead to strong competition for light and quite surface is not the only factor determining the plant relative often to a decline in the proportion of clover (Frame and growth rate; respiratory losses (Haystead et al., 1980; Ryle, Newbould, 1986). Arnott and Powell, 1981) and biomass partitioning between White clover has a greater proportion of its leaf lamina in organs (Ko$ rner, 1990) can be of overwhelming importance. the upper, well lit, layers of the canopy than grass (Dennis As a result, clover radiation use efficiency may be lower, in and Woledge, 1985; Woledge, 1988; Woledge et al., 1992). mixed swards, than that of the grass. Yet, there is little It seems therefore unlikely, even in nitrogen fertilized evidence of a lower radiation use efficiency of the legume in mixtures (Woledge, 1988), that the enhancement of grass a mixed sward. Models of radiation interception are needed growth could cause it to overtop and shade the clover. Yet, to calculate the efficiencies of photosynthetically active in nitrogen fertilized permanent grasslands, the small radiation (PAR) capture and of PAR use for species grown proportion of white clover was thought to be due to the in mixture. By using such a model, Sinoquet et al. (1990) large leaf area of the other species at heights which white calculated that the radiation use efficiency of white clover clover could not attain (Schwank, Blum and No$ sberger, was lower than that of the tall fescue in a nitrogen-fertilized 1986). However, in these reports, no attempt was made to mixture. However, some simplifications were made: (a) the 0305-7364\96\010035j11 $12.00\0 # 1996 Annals of Botany Company 36 Faurie et al.—Light Partitioning and Use in Grass–CloŠer Swards canopy was only one horizontal layer, which did not (NIR, above 700 nm)—in which optical properties are account for differences in the vertical distribution of leaf assumed to be constant and incident radiation equally area between grass and clover; (b) leaf lamina angles were distributed (50% in each band, Varlet-Grancher, 1975, assumed to be constant. Moreover, as with most field amongst others). In this study, leaf transmittance was studies, the radiation use efficiency was presumably under- assumed to be 0n10 for both grass and legume species in the estimated as the root biomass was not taken into account PAR band, and 0n47 and 0n49 in the NIR band for tall fescue (Russell, 1993). and white clover, respectively (Nijs and Impens, 1993; In the present study, a similar light model, but using Varlet-Grancher, pers. comm.). several horizontal layers of leaves, was applied to the field data reported by Woledge (1988) and by Woledge et al. Controlled enŠironment experiment (1992) and to results from a controlled environment experiment with mixed grass-clover swards. Light par- Plant cultiŠation. Seeds of white clover (Trifolium repens titioning was calculated and, for the controlled environment L., cv. Grasslands Huı$ a) and perennial ryegrass (Lolium experiment, a growth analysis technique based on the whole perenne L., cv. Pre! fe! rence) were germinated in the dark at plant growth rate, allowed separate calculation of grass and 20 mC. After 3 d, the seedlings were transferred to an aerated clover radiation use efficiencies. basal nutrient solution (Faurie and Soussana, 1993) and grown in a controlled environment cabinet at 500 µmol # " PAR m− s− with a 14-h photoperiod at 20\16 mC, day\night MATERIALS AND METHODS temperature, respectively. Ten days after sowing, the clover seedlings were inoculated with Rhizobium leguminosarum Radiation interception model bv. trifolii USDA 2063. One week later, simulated grass– The simulation model of radiation interception computes clover swards were made by transplanting 21 plants of each the terms of the radiation balance of horizontally homo- species (in six alternate grass–clover rows) to a container # geneous, mixed crops. Most details of the model have been (0n40i0n60) m surrounded with reflective side panels. For previously given (Sinoquet et al., 1990), thus only the main each species, five development classes were made, according features are summarized here. The model is based on the to the leaf number and to the leaf length, and plants from turbid medium analogy (see Ross, 1981). In the version used the two medium classes were distributed at random among in the present study, the canopy is divided into horizontal the replicate containers. After transplantation, the simulated layers containing foliage of either a single or the two species. mixed swards were grown, under the same conditions, either Each layer is characterized by the leaf area index (LAI), at (20\16) mC(Tj)orat(12\9) mC(Tk) day\night mean inclination and leaf scattering coefficient of each temperature, until a cumulative temperature sum of 1200 mC species present in the layer. Other model inputs are the sun d was reached, 65 (Tj) or 100 (Tk) d after sowing. The elevation, the direct and diffuse radiation at the top of the swards were rotated twice weekly around the growth cabinet. canopy, and the soil reflectance. Radiation interception for Two successive experiments were carried in the same growth each sky direction is computed from Beer’s law adapted to cabinet, one at Tj and one at Tk. partition light between species in mixed layers (Sinoquet The basal liquid medium was renewed twice weekly and and Bonhomme, 1991). This is used to derive interception of supplemented every 2 d with Ca(NO$)#. Two amounts of N direct radiation (i.e. coming from a single sun direction) supply (Nk,Nj) were compared at the two temperatures − and diffuse light (i.e. assumed to come from a finite set of (Tk,Tj). A total of 50 and 200 mg N-NO$ per plant at sky directions). Scattering is characterized by exchange Nk and Nj, respectively, was supplied to the mixed coefficients between each pair of vegetation layers, which swards during their growth after transplantation. As nitrate combines scattering on leaf surfaces, assumed to be supply was based on the thermal time, the amounts supplied lambertian, and interception of scattered radiation. The every 2 d were smaller at Tk than Tj. radiation balance of the canopy, i.e. coupling between To avoid inhibition of clover N# fixation by excess nitrate interception and multiple scattering is solved using a method (Faurie and Soussana, 1993), nitrate supply was adjusted to similar to the ‘radiosity’ method (Ozisik, 1981). This the mean growth rate of the mixed sward, determined in − consists of expressing the radiation fluxes intercepted by preliminary experiments (Faurie, 1994). Thus, NO$ supply each component (i.e. each species foliage in each vegetation varied from 0n82 to 170 (Nk) or from 3n3 to 710 (Nj) µg − −" layer) as a linear combination of the fluxes coming from the N-NO$ mCd per plant. This N supply mode, derived radiation sources: (a) direct and diffuse incident radiation from the relative addition technique (Ingestad, 1982), was weighed by the interception probabilities; (b) fluxes scattered compared, at Tj, to a constant N supply of 56 (Nk) or 225 − −" by the canopy components weighed by the above exchange (Nj) µgN-NO$mCd per plant, resulting in the same coefficients. This makes a system of linear equations where total N supply over the growth period. intercepted fluxes are the unknown and which is iteratively Canopy structure, growth analysis and radiatiŠe balance solved (Sinoquet and Bonhomme, 1992). Radiation trans- simulation. After canopy closure, from approx. 800 to mitted below each vegetation layer and absorbed by each 1200 mC d cumulative temperature sums—that is from 38 to species in each layer is thus computed. Because of changes 65 (Tj) or from 64 to 100 (Tk) d after sowing—sward in optical properties of leaf and soil surface, a simulation measurements were carried out on four occasions, approxi- has to be run for each waveband. The solar spectrum is split mately weekly. At each harvest, one simulated sward per into two domains—PAR (400–700 nm) and near infra-red treatment was taken at random. Light (photosynthetic Faurie et al.—Light Partitioning and Use in Grass–CloŠer Swards 37 T 1. Mean total sward biomass, mean percentage cloŠer content in total biomass and in leaf area in simulated mixed swards after canopy closure, at the beginning (800 mC d after sowing) and at the end (1200 mCd)of the controlled enŠironment experiment

Tk Tj

Nk Nj Nk Nj

Thermal time (mC d) RA RA C RA C RA

Total sward 800 330 610 300 270 330 290 # biomass (g d. wt m− ) 1200 980 1440 840 720 900 870 Clover content in 800 24 11 49 69 51 53 total biomass (%) 1200 23 14 59 75 46 49 Clover content in 800 33 13 56 76 52 57 leaf area (%) 1200 33 20 66 78 36 48

ANOVA Total sward biomass Clover content in total biomass Clover content in leaf area

Factor Tk Tj Tk Tj Tk Tj N supply * ** * * * ** N supply mode — * — * — * Factor Nk Nj Nk Nj Nk Nj Thermal time ** ** NS NS NS NS Temperature NS * ** ** ** *

(Tk), (Tj), temperature; (Nk), (Nj), N supply; (C), (RA), constant or relative addition of N (see Materials and Methods). (*, **) denote, respectively, a significant (P ! 0n05) and a highly significant (P ! 0n01) effect (ANOVA). The effects of the N supply and of the N supply mode were tested by ANOVA for each temperature. The effects of the thermal time and of the temperature were tested by ANOVA for each N supply with the relative addition N supply mode. photon flux) extinction profile was measured using a sunfleck technique (Warren-Wilson, 1959, 1963) and calculated the ceptometer (Decagon Devices Inc, Pullman, WA, USA) vertical distribution of foliage area for both species. These placed at different depths within the canopy (every 2 or data were used as inputs for the radiative transfer model. 3n5 cm at the top and thereafter every 7 cm), hence delimiting Since no measurements of leaf laminae angles were reported, horizontal canopy layers. Canopy geometrical structure was we assumed (a) a clover leaf lamina angle of 25m, as this then described for each of these horizontal layers. First, mean value was found to be constant over a wide range of clover and grass leaf lamina angles were recorded (30 growth conditions in the controlled environment study; (b) replicates each). The plastic sheet supporting the sward was that, for a given canopy height and for a given layer height, then turned upside down and the whole canopy layer grass leaf blade angles were similar to those obtained in the clipped with battery powered shearers. The cut material was controlled environment study. separated into grass and clover and subsamples taken. The Tube solarimeters (measuring radiation in the grass subsample was separated into leaf lamina, sheath and 400–2500 nm waveband) were used in the field studies by dead material and clover into leaf lamina, petiole, stolon Woledge (1988) and Woledge et al. (1992), to determine and dead material. The lamina area was measured (LI-3100, daily averages of the light extinction profile. The radiative Area Meter, Li-Cor, Lincoln, Nebraska, USA). Finally transfer simulations were run by assuming 100% diffuse roots were also harvested and separated to grass and clover. radiation, since such conditions usually yield estimates of For each layer, all fractions of the subsamples and the radiative balance that are close to the daily averages (Varlet- remainder of grass and clover were dried at 80 mC for 24 h Grancher and Bonhomme, 1979; Sinoquet et al., 1990; and weighed. The amount of dead material in the total Sinoquet and Bonhomme, 1992). sward mass was always less than 10%. The simulations of the radiative balance were made, assuming a vertical light RESULTS source and 10% of diffuse radiation in the PAR waveband, the conditions in the growth cabinet. Sward productiŠity and cloŠer content in the controlled enŠironment experiment At the time of canopy closure, approximately 800 Cd Field data analysis: radiatiŠe balance simulation m cumulative temperature, the percentage clover contents of Woledge (1988) and Woledge et al. (1992) determined the the simulated swards differed markedly (Table 1). The mean canopy structure of mixed tall fescue\white clover swards or clover content, both in biomass and in leaf area, was mixed ryegrass\clover swards, using the point quadrat significantly lower at Tk (9\12) mC than at Tj (20\16) mC 38 Faurie et al.—Light Partitioning and Use in Grass–CloŠer Swards

A Ryegrass Clover B Ryegrass Clover C Ryegrass Clover 40

30

20 Height (cm)

10 N–T–RA N–T+RA N–T+C LAI=2.0 LAI=1.1 LAI=1.5 0

D Ryegrass Clover E Ryegrass Clover F Ryegrass Clover 40

30

20 Height (cm)

10 N+T–RA N+T+RA N+T+C LAI=5.4 LAI=1.1 LAI=1.4 0 60 40 20 020 40 60 60 40 20 020 40 60 60 40 20 020 40 60

G Ryegrass Clover H Ryegrass Clover I Ryegrass Clover 40

30

20 Height (cm)

10 N–T–RA N–T+RA N–T+C LAI=8.3 LAI=9.2 LAI=9.1 0

J Ryegrass Clover K Ryegrass Clover L Ryegrass Clover 40

30

20 Height (cm)

10 N+T–RA N+T+RA N+T+C LAI=12.9 LAI=11.2 LAI=10.9 0 60 40 20 020 40 60 60 40 20 020 40 60 60 40 20 020 40 60 (m2m–3) (m2m–3) (m2m–3)

F. 1. Vertical distribution of ryegrass and white clover leaf area density after 800 (A to F) and 1200 (G to L) mC d thermal time (Tk), (Tj), respectively, 12\9 mC and 20\16 mC; (Nk), (Nj), respectively, low and high N supply, (C), (RA), respectively, constant and relative addition N supply mode. The treatment (N supply, temperature, N supply mode) and the sward LAI are mentioned at the bottom of each figure. The dotted line separates the upper layers of the canopy (cumulative LAI below 3). Faurie et al.—Light Partitioning and Use in Grass–CloŠer Swards 39

40 100 A ° 35 90 60° 80 30 30°

25 0° 60

20 40

15 Calculated (%) Layer height (cm) 10 20

5

0 100 B 15 20 2530 35 40 Sward height (cm) 80 F. 2. Mean leaf lamina angle of grass within horizontal layers of a simulated ryegrass-white clover canopy as a function of sward height (x axis) and of layer height (y axis). The mean leaf lamina angle is shown 60 as the angle (in m) of a line segment. An angular scale, graduated in m, is given for comparison. The results are the means of two to five canopy layers, with 30 replicate measurements per layer. 40 Calculated (%)

20 and at Nj compared to Nk, with no significant interactions between the factors (Table 1). The clover contents which were established at the time of canopy closure did not vary 0 20 40 60 80 100 significantly during competitive growth (Table 1). For the Measured (%) same temperature sum, the total biomass of the sward was significantly (P ! 0n01) lower at Tj than at Tk, pre- F. 3. Comparison between simulated and calculated transmitted sumably due to the smaller amount of radiation accumulated radiation using: (A) ceptometer (in the PAR waveband) for controlled environment study (10% diffuse radiation); (B) tube solarimeters (in at Tj (shorter growth period) (Table 1). the 400–2500 nm waveband) in the field studies by Woledge, 1988 and Two N supply modes (either constant or according to the Woledge et al., 1992 (100% diffuse radiation). Horizontal layers from relative addition technique) were compared at Tj the top: ($)1,(#)2,( )3,(*)4,(>)5,(=)6,(X)7,(W) 8 and (4) (20\16 mC). With the constant nitrogen supply mode, the 9. The equations of the regressions plotted in (A) and (B) are, total sward biomass was greater, but the proportion of respectively, [y l (0n85p0n03)x, r l 0n91, n l 77, P ! 0n001] and [y l (0n92p0n04)xj(3n1p2n5), r l 0n92, n l 100, P ! 0n001]. The dashed clover in the sward, both in terms of total biomass and of lines show the confidence interval of the regression at P " 0n95. leaf area, was significantly smaller (Table 1).

density was enhanced (Fig. 1). As a result, the environmental Canopy structure in the controlled enŠironment experiment conditions that favoured grass growth in leaf area (Nj, The stratified clipping technique allowed us to plot the Tk) also promoted its vertical dominance relative to the vertical distribution of leaf area density for the mixed legume. swards of grass and clover, at the start (800 mC d) and at the The mean angle of ryegrass leaf blade was calculated for end of the experiment (1200 mC d) (Fig. 1). At a given horizontal layers at different depths and according to the thermal time, perennial ryegrass developed a larger total mean sward height (Fig. 2). For a given sward height, the leaf area at Tk than at Tj and with Nj than with Nk decrease in the mean leaf blade angle with height in the (Fig. 1). canopy reflects the curvature of grass leaves. This curvature At the end of the experiment, the mixtures formed dense increased with leaf length and therefore with canopy height canopies, with LAI between 8n3 and 12n9. For each species, (Fig. 2). Thus, the tall canopies formed at Nj were partly the vertical distribution of leaf area was then of over- constituted, in the upper layers, by rather horizontal grass whelming importance for PAR interception. A large N leaves (Fig. 2) with a large leaf area density (Fig. 1). supply increased the mean height of the canopy from 30 to approx. 40 cm (Fig. 1). With N , clover leaf area density in k Partial Šalidation of the radiatiŠe balance simulations the upper canopy layers was usually larger than that of the grass. However, the opposite occurred at Nj, especially as The simulation results of transmitted radiation, below ryegrass leaf area density was greatest in the first centimetres each vegetation layer, were compared with the light of the mixed canopy (Fig. 1). Low temperatures (Tk) extinction profiles measured in the controlled environment reduced clover leaf area density, both in the lower and in the study, and tube solarimeters in the field studies by Woledge upper layers of the mixed canopy, whereas ryegrass leaf area (1988) and Woledge et al. (1992) (Fig. 3). The percentage 40 Faurie et al.—Light Partitioning and Use in Grass–CloŠer Swards

% LAI grass 100 A 100 80 60 40 20 0 100 0 80 A

80 20 60

60 40 d 40

Calculated (%) c T– 40 60 b 20 a

T+ capture grass % PAR % PAR capture clover % PAR 20 80

0 100 100 B0 20 40 60 80 100 % LAI clover 80 % LAI grass 100 80 60 40 20 0 60 100 B 0

40 80 20 Calculated (%) d 20 60 c 40 b 40 a 60 026810124 14 % PAR capture grass % PAR Cumulative LAI capture clover % PAR 20 80 F. 4. Calculated values of transmitted radiation as a function of cumulative leaf area from the top of the sward to the height of the 100 layer: (A) in controlled environment study (10% diffuse radiation) and 0 20 40 60 80 100 (B) in the field studies (Woledge, 1988; Woledge et al., 1992) (100% % LAI clover diffuse radiation). Horizontal layers from the top: ($)1,(#)2,( )3, (*)4,(>)5,(=)6,(X)7,(W) 8 and (4) 9. The equations of the F. 5. Species content in leaf area and contribution to the sward PAR regressions plotted in (A) and in (B) are, respectively, (y l 100 capture: (A) in the field studies ($)Nk(Woledge, 1988), (#)Nj (−! %& ! !#)x exp n p n , r l 0n99, n l 34, P ! 0n001 at Tk and y l 100 (Woledge, 1988), (>)Nk(Woledge et al., 1992); (B) in the controlled (−! '* ! !")x exp n p n , r l 0n99, n l 48, P ! 0n001 at Tj) and (y l 100 environment study. ($)NkTj,(#)NjTj,( )NkTk,(*) (−! %!* ! !!%)x exp n p n , r l 0n99, n l 112, P ! 0n001). The dashed lines show NjTk. The dashed lines show different values (a, b, c, d) of the ratio the confidence interval of the regression at P " 0n95. of clover to grass PAR capture per unit leaf area: 1n5 (a), 2n3 (b), 3n4 (c), 5n1 (d). transmitted global radiation (field data), or transmitted therefore decreased the percentage transmitted radiation at PAR (controlled environment experiment), show that the a given LAI. simulated and measured values are highly correlated (P ! 0 001) and that the model accounts for more than 80% of n Light partitioning between grass and cloŠer the total variance. The linear regression does not differ significantly from the 1:1 slope for the field study. Under field conditions. For the field data of Woledge Nevertheless, in the controlled environment study, the slope (1988) and Woledge et al. (1992), the simulation of radiative of the linear regression is significantly less than one (Fig. transfer shows that, in a mixture, clover captured a 3A). significantly (Wilcoxon sign-test, P ! 0n001) larger pro- Simulated values of the percentage transmitted radiation portion of the light than its contribution to the mixed sward are plotted in Fig. 4, as a function of the cumulative leaf LAI (Fig. 5A). Hence, clover captured relatively more PAR area from the sward surface. The simulation results in a per unit leaf area than grass. clear exponential decline in the percentage transmitted To quantify this difference, constant values of the clover radiation (Fig. 4A and B). In the controlled environment to grass ratio of PAR capture per unit leaf area are shown experiment the decline in the percentage transmitted by dashed lines in Fig. 5. In comparison with these constant radiation was faster at Tj, compared to Tk (Fig. 4A). The ratios, it appears that in mixtures with a large clover content planophile foliage of clover led to greater light extinction in (more than 45% of the total leaf area), clover laminae the upper layers, with the vertical light source of the growth usually captured two to three times more PAR per unit leaf cabinet. The higher clover content in leaf area at Tj area than grass. By contrast, in mixtures with a lower clover Faurie et al.—Light Partitioning and Use in Grass–CloŠer Swards 41 (Sinoquet et al., 1990), the legume radiation use efficiency A (RUE) was significantly smaller (Student’s t-test, P ! 0n001) 3.0 than that of ryegrass (Fig. 6). For both species, the radiation use efficiency declined exponentially (mono-exponential 2.5 plus residual model, P ! 0n01, r l 0n490) with the mean photon)

–1 2.0 PAR capture per unit leaf area (Fig. 6A). Thus, clover’s lower RUE was apparently related to the larger mean 1.5 amount of PAR captured, per unit area, by its leaf laminae. As the lower canopy layers are shaded, they contribute little 1.0 to the PAR conversion. Thus, the same correlation was tested by using the mean amount of PAR captured per unit RUE (gDW mol 0.5 leaf area in the upper canopy layers, that is in canopy layers with a cumulative LAI below 3. The same mono-exponential 0 plus residual model was highly significant (P ! 0n001, r l B 0n601) (Fig. 6B). 3.0

2.5 Growth rate

photon) In the controlled environment experiment, due to its –1 2.0 lower radiation use efficiency, the contribution of clover to the growth (estimated as the mean growth rate of whole 1.5 plants) of the mixed sward was smaller (Wilcoxon’s sign- test, P ! 0n001) than its contribution to the PAR capture by 1.0 the mixture (Fig. 7A). However, clover contributed to the

RUE (gDW mol mixed sward growth in proportion to its contribution to the 0.5 mixed sward leaf area index and total biomass (Fig. 7B and C). 0 40 80 120 160 200 240 (µmol photon m–2 s–1) DISCUSSION F. 6. Radiation use efficiency (RUE) as a function of the mean Model Šalidity amount of radiation absorbed per unit leaf area in the controlled environment: (A) in total leaf area; (B) in the upper layers of canopy The hypothesis of considering the mixture as a horizontally (cumulative LAI below 3). Solid symbols, ryegrass; open symbols, homogeneous, well mixed canopy is not too unrealistic: white clover. ($, #)NkTj,(X,W)NjTj,( ,*)NkTk,(>, first, clover has a stoloniferous growth habit resulting in =)NjTk. The equations of the regressions plotted in (A) and (B) (−! !!%) ! !!"%)x horizontal homogenization; second the grass, albeit sown in are, respectively, [y l (2n9p0n3) exp n p n , r l 0n490, n l 32, (−! !!(& ! !!"&)x rows, rapidly increased its leaf area, thus colonizing the P ! 0n01] and [y l (3n9p0n1) exp n p n , r l 0n601, n l 32, P ! 0n001]. The dashed lines show the confidence interval of the space between the rows. regression at P " 0n95. Discrepancies between measured and modelled values of transmitted radiation (Fig. 3) may be due to both measurement and model features. First of all, data scattering content (less than 40% of the total leaf area) clover laminae may be related to the strictness of the model-measurement were somewhat less favoured, as they captured about 50% comparison which applied to thin vegetation layers (from 2 more radiation per unit area than grass laminae (Fig. 5A). to 7 cm). Classical validation of light models is based on Under controlled enŠironment conditions. In the controlled radiation transmitted on the soil surface or vertical profiles environment experiment, the simulation of radiation in- of downward radiation only in the case of tall canopies. terception was run with a vertical light and 10% diffuse Model testing from the radiation balance of small vegetation radiation. As for the field data, clover captured a greater layers involves greater uncertainty about the description of proportion of the PAR (significant, Wilcoxon’s sign-test, canopy structure and in light measurements. Both are P ! 0n001) than its contribution to the LAI of the mixed subject to errors in identifying the layer boundaries (i.e., sward (Fig. 5B). Clover laminae captured, at Nk and Nj, stratified-clipping method, sensor location). Turning the respectively, (2n5p0n2) and (1n6p0n2) times more radiation growth cabinet sward to clip makes the stratified harvest per unit leaf area than grass (Fig. 5B). The advantage of easier but probably modifies the vertical profile of leaf area, clover in terms of radiation interception was therefore due to upside down gravity. Light measurements within the greater at the low N supply. canopy also disturb canopy structure by parting the foliage: this allows more radiation to fall on the sensor and overestimates transmittance. This phenomenon is un- Radiation use efficiency doubtedly enhanced in our study because of the dense sward In the controlled environment experiment, radiation use canopy and the vertical incident light. efficiencies of clover and grass were compared. In agreement However, model features may also explain some devia- with previous conclusions from monocultures and mixtures tions. The canopy is assumed to be horizontally homo- 42 Faurie et al.—Light Partitioning and Use in Grass–CloŠer Swards

% PAR capture grass % LAI grass 100 80 60 40 20 0 100 80 60 40 20 0 100 A 0 100 B 0

80 20 80 20

60 40 60 40

40 60 40 60 % dDW grass % dDW grass % dDW clover % dDW clover

20 80 20 80

100 100 0 20 40 60 80 100 0 20 40 60 80 100 % PAR capture clover % LAI clover

Grass content (%) 100 80 60 40 20 0 100 C 0

80 20

60 40

40 60 % dDW grass % dDW clover

20 80

100 0 20 40 60 80 100 Clover content (%) F. 7. Species contribution to the mixed sward growth (dDW) in the controlled environment as a function of clover content in (A) PAR capture, (B) leaf area and (C) total biomass. ($)NkTj,(#)NjTj,( )NkTk,(*)NjTk. geneous although it was sown in alternate rows. Even if the leads to a satisfactory simulation of the daily radiative whole canopy seems to be horizontally homogeneous after balance of the grass–legume mixture. canopy closure, effects of the row planting pattern may Such model-measurement comparison is unable to test persist: non-uniform distribution of leaf area of each species the model’s ability to partition light capture between the in the horizontal plane may occur. A simulation study made two components. This is a crucial problem because radiation from a light model devoted to row intercropping showed models for intercropping are usually aimed at estimating that such horizontal heterogeneity leads to a slight increase light competition in mixtures. In this study, the row effect in light penetration (j0n02 at total LAI l 4) when the two on associated vertical incident light in the growth cabinet species have contrasted leaf inclination (i.e. planophile Šs. could have modified significantly light partitioning by erectophile) and most radiation comes from vertical direc- counterbalancing the effect of overtoping of the dominant tions (Sinoquet and Bonhomme, 1992). This effect is not species. On the other hand, at the daily scale, simulations large enough to explain the overestimation by the whole have shown that the row structure of the canopy does not model found in the growth cabinet experiment. Moreover, significantly change light partitioning in the case of either the same simulation study showed that the row effect does clear or overcast sky (Sinoquet and Bonhomme, 1992). not modify light transmission in the case of overcast sky. This may be related to the unbiased relationship found with Light partitioning the Woledge’s data set where daily transmittances are computed by assuming an overcast sky. Ultimately these Results from the radiative transfer model show that results suggest that: (a) neglecting the row structure in the clover captured more PAR than grass per unit leaf area, growth cabinet experiment does not significantly bias the both under field and under controlled environment con- transmittance calculations; (b) the horizontally homo- ditions (Fig. 5). Yet, in the controlled environment geneous canopy associated with overcast sky conditions experiment, the growth conditions clearly favoured PAR Faurie et al.—Light Partitioning and Use in Grass–CloŠer Swards 43

% LAI grass % LAI grass 100 80 60 40 20 0 100 80 60 40 20 0 100 A 0 100 B 0

80 20 80 20

60 40 60 40

40 60 40 60 % PAR capture grass % PAR capture grass % PAR % PAR capture clover % PAR 20 80 capture clover % PAR 20 80

100 100 0 20 40 60 80 100 0 20 40 60 80 100 % LAI clover % LAI clover

% LAI3 grass 100 80 60 40 20 0 100 C 0

80 20

60 40

40 60 % PAR capture grass % PAR % PAR capture clover % PAR 20 80

100 0 20 40 60 80 100

% LAI3 clover F. 8. Species content in leaf area and contribution to the sward PAR capture calculated with (A) the complete light model or (B) modified model, assuming the same leaf lamina angle for grass and clover (see discussion). (C) Species content in leaf area and contribution to the total PAR in the upper layers of the canopy (cumulative LAI below 3). Field studies; ($)Nk(Woledge, 1988), (#)Nj(Woledge, 1988), (>)Nk(Woledge et al., 1992). Controlled environment study, ( )Nk,(*)Nj. The equation of the regression plotted in (C) is: % clover PAR capture l (1n02p0n03) % clover LAI$j(4n4p2n6); n l 46; r l 0n96; P ! 0n001. The dashed lines show the confidence interval of the regression at P " 0n95. capture by a planophile species like white clover. However, had the same mean leaf angle, which was calculated as the the daily average of PAR interception in a natural mean of the two species leaf angles. Simulations made environment is better estimated by assuming 100% diffuse under this assumption, with the same data sets, show a clear radiation (Varlet-Grancher and Bonhomme, 1979; Sinoquet reduction in the advantage of clover PAR capture (compare et al., 1990; Sinoquet and Bonhomme, 1992). With full Fig. 8A and B). Thus, even with fully diffuse radiation, the diffuse light, simulations show that the advantage of clover planophile foliage of white clover partly explained its higher was smaller in terms of PAR capture in the controlled PAR capture per unit leaf area. environment experiment (compare Figs 5B and 8A). By suppressing leaf angle effects, simulation allowed us to Nitrogen supply reduced, or even suppressed, the ad- test the effects of species vertical dominance. The vertical vantage of clover in terms of PAR capture (Fig. 8A): in the dominance of clover was highly significant for the low N field mixtures supplied with N fertilizer (reported by treatments (P ! 0n001; Wilcoxon’s sign-test), but not for the Woledge, 1988) or the Nj treatment in the controlled high N treatments (Nj in the controlled environment environment experiment, clover had no significant ad- experiment and supplied with N fertilizer in the study by vantage, while the advantage was highly significant (P ! Woledge, 1988), which even displayed a tendency (P ! 0n06; 0n001; Wilcoxon’s sign test) for the low N treatments. Wilcoxon’s sign test) towards vertical dominance of grass The reasons for clover’s advantage in terms of PAR (Fig. 8B). This underlines that the vertical dominance of the partitioning were further investigated by comparing different legume does hold in mixed swards with little or no inorganic radiative transfer simulations. First, we assumed for each N supply, but not necessarily in mixtures grown with higher horizontal layer of the mixed canopy that grass and clover nitrogen fertility. 44 Faurie et al.—Light Partitioning and Use in Grass–CloŠer Swards Below a cumulative LAI of 3, simulations show that less rates of photosynthesis (Field and Mooney, 1986; Sinclair than 10 to 20% of the incoming PAR is transmitted (Fig. 4). and Horie, 1989; Be! langer, Gastal and Lemaire, 1992). Therefore, the contribution of clover to PAR capture by the Nevertheless, in sharp contrast with results obtained with mixture is strongly related to its share of the total leaf area grass monocultures (Be! langer et al., 1992), the mean grass in these upper (LAI$) canopy layers. The correlation between radiation use efficiency was 25% higher at Nk than at Nj −" both parameters was highly significant (Fig. 8C) and close (2n0 and 1n6 g DM mol PAR, respectively) in the controlled to the 1:1 line: environment mixtures. This discrepancy may originate from the increased shading of grass leaves by clover at the low N % clover PAR capture (1 02 0 03) % clover l n p n supply, resulting in a 27% decline in the mean PAR capture LAI (4 4 2 6) $j n p n per unit leaf area of the grass in the upper canopy layer # " Grass\clover differences in daily light interception are (from 119 to 88 µmol PAR m− s− ). thus accounted for mostly by the proportion of clover leaf Such trade-offs between PAR capture and PAR use could area in the upper (cumulative LAI below 3) canopy layers, help stabilize the botanical composition of mixed stands in good agreement with previous conclusions by Woledge during competitive growth periods. In good agreement with (1988) and Woledge et al. (1992). This means that the a previous report by Davidson and Robson (1986), the interception efficiency of either component is strongly clover contents which were established at the time of canopy determined by its ability to place its foliage at the top of the closure did not vary significantly during the competitive mixed canopy. growth phase in the controlled environment experiment (Table 1). Thus, under controlled environment conditions, competition for light had only minor effects on the balance Radiation use efficiency and growth between grass and clover. Leaves that are photosynthetically light saturated are less This rather unexpected result can be better understood by efficient than those in the shade. Therefore, in a monoculture, considering how light quality and quantity affect extension as the fraction of shade leaf area increases, RUE also of clover petioles (Solangaarachchi and Harper, 1987; increases slightly (Sinclair and Horie, 1989). By contrast to Thompson and Harper, 1988; Varlet-Grancher, Moulia and the monoculture, the fraction of leaf in the shade can reach Jacques, 1989). Clover avoids shade and reacts quickly to one for a shaded species grown in mixture. In this case, due shading by increasing its petiole length. Therefore, the ratio to the avoidance of light saturated photosynthesis, the of the extended length of clover petioles and grass leaves is radiation use efficiency tends to increase (Willey, 1990). This approximately constant (Davies and Evans, 1990). The would explain the negative correlation between radiation large plasticity of the legume tends, therefore, to buffer use efficiency and PAR capture per unit leaf area observed competition for light in most situations. This plasticity has for mixed grass and clover in our study (Fig. 6). According hidden costs, however, like branching suppression (Simon, to this hypothesis, the lower radiation use efficiency of the Gastal and Lemaire, 1989) and the mortality of small shoot legume would be due to its higher PAR capture per unit leaf growing points in dense canopies (Soussana, Verte' s and area. Interestingly, this would lead to a compensation Arregui, 1995). between the efficiencies of PAR capture by the components Schwank et al. (1986) concluded that the growth potential and PAR use in a mixture. Such trade-offs can be illustrated of clover in natural grasslands was determined by the PAR by the nitrogen supply effects in the controlled environment intercepted by fully developed leaves in partly sunlit experiment. At Nj, the advantage of clover in PAR positions. The present study supports this conclusion, but capture per unit leaf area decreased by 28% (from 153 to also stresses that the balance between clover and grass # " 110 µmol m− s− ) but RUE increased by 20% (from 0n98 to depends upon trade-offs between PAR capture and PAR " 1n2 g DM mol− PAR). Therefore, under conditions of high use and upon the morphogenetic costs of increased leaf size. N supply, mixed clover used radiation more efficiently. However, several other factors could influence the ACKNOWLEDGEMENTS radiation use efficiency of mixed species in a natural environment. First, crop radiation use efficiency has been We thank P. Pichon for expert technical assistance. shown to increase with increased diffuse radiation (Sinclair, Shiraiwa and Hammer, 1992). Moreover, as grass\clover LITERATURE CITED differences in PAR capture per unit leaf area were smaller ! Belanger G, Gastal F, Lemaire G. 1992. 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