Leaf expansion, photosynthesis, and water relations of sunflower plants grown on compacted soil

Plant and Soil 149: 175-184, 1993. © 1993 Kluwer Academic Publishers. Printed in the Netherlands. PLSO 9607

Leaf expansion, photosynthesis, and water relations of sunflower plants grown on compacted soil

A. ANDRADE l, D.W. WOLFE 2 and E. FERERES I lDepartmento de Agronomia, Universidad de C6rdoba, C6rdoba, Spain and 2Department of Fruit and Vegetable Science, Cornell University, Ithaca, NY 14853, USA (address for correspondence)

Received 14 May 1992. Accepted in revised form 11 December 1992

Key words: compaction, Helianthus annuus L., leaf expansion, nitrogen, osmotic potential, photosynthesis, root growth, soil strength, turgor, water potential

Abstract

Leaf expansion and growth response of sunflower (Helianthus annuus, L.) to soil compaction were investigated in relation to compaction effects on water relations, nitrogen nutrition, and photosynthesis. A series of field experiments were conducted with plants grown in 20 cm-diameter cylinders with soil bulk densities ranging from 1.2 to 1.7 g cm -3 at the 0-20 cm depth (equivalent to 0.8 to 2.4 MPa soil strength measured with a soil penetrometer). Relative leaf expansion rate (RLER) decreased linearly with increasing soil strength. Smaller plant size in compacted treatments was due not only to slower expansion rates, but also smaller maximum size of individual leaves. Sensitivity of leaf expansion to soil strength was best illustrated by a reduction in RLER and maximum size of the first leaf to emerge in a treatment with only the lower 10-20 cm of the profile compacted (bulk density of 1.7 g cm-3). Root growth was less affected than shoot growth by compaction and root:shoot ratios of compacted treatments were significantly higher than the control.

Soil compaction had no significant effect on pre-dawn or midday leaf water potential, osmotic potential or leaf turgor. Specific leaf weight was usually higher in plants grown on compacted soil, and leaf nitrogen and photosynthesis per unit leaf area were either unaffected by treatment or significantly higher in compacted treatments. The results suggest that early growth reduction of sunflower plants grown on compacted soil was more sink- than source-limited with regard to water, nitrogen, and carbon supply. Further evaluation of this hypothesis will require verification that these whole-leaf measurements provided a sufficiently accurate approximation of treatment effects on the dynamic equilibria of expanding cells.

Introduction

Soil compaction can significantly reduce yields of many agronomic species, and in addition to its natural occurrence, has become a chronic prob- lem in many areas due to heavy equipment traffic through the fields (Blackweli et al., 1985 Brereton et al, 1986; Henderson, 1991). Soil strength and resistance to root penetration increase as soils dry, and therefore even in non-

compacted soils the plant response to soil strength is important during drought. Whiteley et al. (1981) suggested that some drought effects on plant growth are associated with increased soil strength and mechanical impedance of roots. Passioura and Gardner (1990) found that the decline in growth of wheat seedlings occurred at a higher soil water content in dense soil compared to loose soil. Taylor and Ratcliff (1969), working with cotton and peanuts and Masle and

176 Andrade et al.

Passioura (1987), working with wheat, docu- mented similar leaf expansion reductions at high soil strength regardless of whether high soil strength was caused by increasing bulk density of the soil or lowering soil water content. These results suggest some similarity in plant response mechanisms to soil water deficit and soil compaction.

Shoot growth is often more reduced than root growth when plants are grown with a restricted rooting volume or on compacted soils (Carmi et al., 1983; Masle and Passioura, 1987). Masle et al. (1990) reported slower shoot growth of wheat seedlings grown on compacted soil even before the first leaf was fully expanded and plants were still in the seed reserve-dependent growth stage. At later growth stages, wheat plants grown on compacted soils were found to have a higher photosynthetic rate per unit leaf area, although leaf expansion and total photosynthetic area had been substantially reduced (Masle and Farquhar, 1988). These results suggested that carbon supply was not a major factor limiting growth in their study. They also found no evidence that nutrients or water were limiting growth since leaf phosphorous levels and bulk leaf water status were similar between soil density treatments. Treatment effects on leaf osmotic potential and leaf turgor in relation to photosynthesis and leaf expansion rates were not examined. They concluded that a hormonal signal from the roots is the primary cause of shoot growth reductions on compacted soils. Several years earlier, Goss and Russell (1980) suggested that a hormonal mechanism may play a role in controlling root growth response to mechanical impedance on compacted soils.

A number of field compaction studies have focused on yield response, but they are not easy to interpret in terms of specific environmental stress factors involved and the nature of the physiological response. The recent work by Masle and co-workers (Masle and Passioura, 1987; Masle and Farquhar, 1988; Masle et al., 1990) described above has provided some new insight, but only one crop species was examined, and experiments were not conducted under field conditions. In the field, young seedlings are exposed to extreme microenvironments affecting water relations (Seymour-Berg and Hsiao,

1986), which may result in a response to soil compaction not observed in controlled environ- ments. Also, compacted zones are not always in the upper-most layer in field soils, and we have little information on the relationship between location of the compacted layer and physiological response.

The primary objective of our study was to examine the growth response of sunflower to soil compaction under field conditions in relation to compaction effects on water relations, nitrogen, and carbon supply. A range of soil densities and compaction of upper and lower soil layers were compared. Plants were monitored for leaf expansion rate and root growth, leaf water potential components, leaf nitrogen and photosynthetic rate.

Materials and methods

Soil compaction treatments

The soil used in all experiments was a sandy- loam of alluvial origin, Typic Xerofluvents, with good internal drainage characteristics and a water content upper limit (field capacity) of 0.23cm 3 cm -3 (Villalobos and Fereres, 1990). The soil was collected from the field, dried, and passed through a 5 mm sieve. Various compaction treatments were obtained by varying the dry weight of soil per unit volume (i.e., bulk density) placed into galvanized steel cylinders of 20 cm diameter and 20 cm depth. Soil of known weight to obtain desired bulk densities was added to the cylinders in 3cm increments to help insure uniformity of bulk density throughout the profile. The cylinders had bottoms which were removed when placed into the field so that drainage and soil gas exchange would not be impeded.

Soil compaction treatments in Exp. 1 were uniform bulk densities throughout the 0-20 cm profile of 1.2, 1.4, 1.6, or 1.7g cm -3, corre- sponding to soil strengths of 0.8, 1.1, 1.7, and 2.4 MPa, respectively. This range of soil densities is typical of the range between non-compacted and compacted field soils reported in the literature (Henderson, 1991; Reeves et al., 1984). Two treatments were used in exp. 2: D1,

Growth and photosynthesis on compacted soil 177

the control, with non-compacted soil at bulk density of 1.3g cm -3 throughout the 0-20cm profile; and D2, with a lower compacted layer (10-20cm depth compacted at 1.7 g cm -3) but the upper 0-10cm at 1.3g cm -3. Exp. 3 in- cluded a third treatment, D3, with the entire

- 3 0-20 cm profile compacted at 1.7 g cm Soil penetrometer resistance was measured at

the end of each experiment with an Electronic Cone Penetrometer (Aguera and Ribes, 1991), equipped with a 1.283 cm diameter cone and a cone angle of 30 ° . The velocity of penetration was 3.0 cm s -t. The device was connected to a portable computer (Toshiba Model T1000, Mid- dlesex, UK) that recorded data for each 0.5 cm depth. Penetration resistance data reported are in MPa units and are the average for the cylinder or particular bulk density layer.

statistical contrasts were calculated as described in Steel and Torrie (1980).

After emergence, plants were irrigated at a frequency that varied from every other day to twice daily, depending on local weather conditions, pan evaporation data and plant size. The irrigation regime was designed so that water was not limiting or excessive for optimum plant growth. Measurements of bulk leaf water status (see below) suggested that this was accom- plished. There was no evidence, based on whole- leaf measurements, that nutrients were limiting during the duration of the experiments (25-30 days). However, in Exps. 2 and 3, 10 ml liter-t of a liquid nitrogen (N) fertilizer (0.65g NH4NO 3 L -l) was added to the irrigation water at 20 days after planting to ensure adequate N availability.

Experimental design and plant establishment

Experimental design and cultural practices were the same for all experiments unless otherwise noted. All experiments were conducted in the field at the Agricultural Research Center at C6rdoba, Spain (37.8°N, 4.8°W) between 1990 and 1991. The region has a Mediterranean cli- mate with an average annual rainfall of 65 cm, concentrated between November and March Sunflower (Helianthus annuus, L., cv. Arlessa) seed were sown into prepared cylinders at a rate of 4 seeds per cylinder and thinned after emergence to 2 plants per cylinder in Exp. 1, and 1 plant per cylinder in Exps. 2 and 3. Seedling dates were 16 May 1990, 31 May 1991, and 23 August 1991 for Exps. 1, 2, and 3, respectively. The cylinders were placed so that the surface of the soil inside it aligned with the field surface. Cylinders were arranged 1 m apart in a com- pletely randomized design. The number of cylinders varied depending on the number of treatments and destructive measurements required, but each experiment had a minimum of 5 cylinders (replications) for each soil compaction treatment that were monitored throughout the study period for non-destructive measurements, and a minimum of 5 additional cylinders for each measurement that involved destructive leaf sam- piing. Analysis of variance and orthogonal

Plant growth measurements

Leaf area development was monitored non- destructively on a minimum of 5 replications from each treatment throughout the study period in all experiments. The length and width of each leaf greater than 0.5 cm in length was measured at 09:00 each day on selected plants. Diurnal studies in Exps. 2 and 3 involved additional measurements at 0 : 600, 14 : 00, and 20: 00 for two consecutive days. Plant leaf area was obtained by the estimation of the area of individual leaves calculated as L x W × 0.7, where L is the length of a leaf of width, W. Plants were in the exponential phase of growth during the experiment and whole-plant relative leaf expansion rate (RLER) was calculated by the linear regres- sion of the natural logarithm of plant leaf area vs. time. The RLER of individual leaves during their exponential phase of expansion was calculated in the same manner.

A minimum of five plants from each treatment was destructively harvested at the end of Exps. 2 and 3, divided into shoot (leaves and stems) and (washed) roots, and dried at 70°C until a con- stant dry weight was obtained (usually 48 h). These data were used to determine treatment effects on total biomass produced and on the root:shoot ratio. Due to the short duration of the experiments, root growth seldom extended beyond the open cylinder bottom, and minor

178 Andrade et al.

penetration into the field soil was easily recov- ered. On rare occasions when control (D1) plants showed extensive non-recoverable root growth below the cylinder, these plants were excluded from the data analysis.

Water potential

Leaves at positions 2, 3, or 4 (counting up from the cotyledon) were measured for leaf water potential (~L) at midday (13:00-15:00) on several occasions in all experiments using a pressure bomb (Soil Moisture Equipment Corp., Santa Barbara, CA USA) following the precau- tions recommended by Hsiao (1990). Data from the most recently fully expanded leaf position are reported here. In Exps. 2 and 3, diurnal studies were conducted and xlt L was measured at pre-dawn (06 : 00), 13 : 00, and 18 : 00 for two consecutive days.

Immediately after ~L measurement, the leaf was removed, sealed in a plastic bag, wrapped in aluminum foil, and put into an ice chest at <10°C. The leaves were transported to the laboratory within 30 minutes where they were frozen and stored at < -10°C for later osmotic potential (~0) measurement. Osmotic potential was measured with a thermocouple psychrometer (Decagon Devices, Model SC10, Pullman, WA USA). A protocol for obtaining reliable ~0 data was developed in preliminary experiments and involved allowing the frozen leaves to thaw at room temperature for about 30 minutes, collecting the sap from each leaf (using a hy- draulic press) onto a filter paper disk and strip, and quickly placing the filter paper sections into the psychrometer sample cup and the sample changer. Samples were allowed to equilibrate for approximately one hour, and then readings were taken. Stable nanovoltmeter readings were usually obtained within two minutes after placing the sample beneath the thermocouple. The in- strument was calibrated at least once a day with salt solutions of known osmotic potential using the same filter paper procedure described for leaves. Turgor, or pressure potential (~p), was calculated as the difference between W E and ~0 for each sample.

Photosynthesis and leaf nitrogen

Net photosynthesis (Pn) was measured on several occasions on fully expanded leaves at positions 2, 3, or 4 using a portable closed leaf gas exchange system (LI-COR 6200, LI-COR Inc., Lincoln, NE USA). All measurements were made in the field at saturating light conditions (photosynthetic photon flux density >1500/~mol m -2 s -1) near midday on leaves which were fully exposed to the sun. For any particular set of measurements, the light level did not vary by more than 5%. Leaves were held inside the leaf chamber for a very short duration (15 s), and leaf temperature increase during measurement was <I°C. The leaves measured were usually small enough so that the entire leaf was placed inside the 4-liter leaf cuvette.

Immediately after Pn measurement the same leaves were removed from the plants, wrapped in damp filter paper and taken to the laboratory. Leaf area was determined gravimetrically by tracing the leaves on paper of known specific weight and cutting out and weighing the traced area. The leaves were dried for 48 h at 70°C and their dry weight recorded. The dried leaves were saved for later analysis of total nitrogen (N) using a micro-Kjeldahl procedure (Bremner, 1965). Photosynthetic data were calculated on a per unit leaf area and per unit leaf N basis.

Results

Leaf expansion, growth, and leaf water status

The initial experiment, evaluating growth re- -3 sponse to bulk densities from 1.2 to 1.7 g cm

(0.8-2.4MPa soil strength) in the top 20cm, indicated that whole-plant RLER decreased linearly with increasing soil penetrometer resistance (Fig. 1). Thus, the difference in plant size between soil compaction treatments increased with time.

Evaluation of the development of individual leaves in subsequent experiments indicated that slower leaf expansion in response to compacted soil began soon after emergence of the first leaf. This is illustrated in Figure 2 where leaf area


0.2

0.15 'o N, E

#

0.1 n - u . i . . J r r

0.05

R L E R = - . ~

r2= 0.81(P<.05)

. . . . I . . . . . . . . I , , , i ] 1 ~ 1 1

0.5 1.5 2 2.5 Soil Penetrometer Resistance (MPa)

Fig. I. Relationship between whole-plant relative leaf expansion rate (RLER) during the first 35 days after planting and average soil penetrometer resistance (0-20 cm depth). Data are from Exp. 1, with soils uniformly compacted at bulk densities ranging from 1.2 to 1.7g cm 3. Each value is the mean of 5 replications plus or minus SE.

data from the third experiment are plotted as a function of time. Expansion of the first leaf was suppressed in the D2 treatment where the zone of compacted soil began at 10 cm below the soil surface, as well as D3 where the entire 0-20 cm soil profile was compacted. Final leaf size after full expansion was also affected by compaction treatment. Maximum area of leaf 1 was largest in the control (D1), followed by D2 and D3, in that order. Emergence of upper leaves was delayed by 3-6 d in compacted treatments.

Leaf area and growth results from Exps. 2 and 3, and statistical analyses, are summarized in Table 1. Calculated whole-plant RLER was reduced about 15% and 25% in the D2 and D3 compacted treatments, respectively. Final plant leaf area relative to the control was about 35- 40% and 65% lower in the D2 and D3 treatments, respectively. The results in Table 1 also confirm that the slower whole-plant leaf area development of plants grown on compacted soil was associated not only with slower expansion rates of individual leaves, but also with reductions in final maximum leaf size. Leaf 2 of compacted treatments was significantly smaller than the control in both experiments.

The root:shoot ratio was higher (p < 0.01) in compacted treatments in both experiments

120

1 0 0

E 80

~ 60 <

~ 40 _ J

20

120

D1 (control)

, , L 2 ~

10 15 20 , , I ,

25

L3

L4

30

100 D2 (compact 10-20)

E 80

60 ~ L3 <

~ 40 L4

20 _

5 10 15 20 25 30 120

100

E 8O

~ 6o L,-

~ 4o _ J

20

D3 (compact 0-20 cm)

L2

4 L3

10 15 20 25 30 Time (days after planting)

Fig. 2. Leaf area development of individual leaves (L1-L5, counting up from the cotyledon) for control (D1) and compacted (D2, D3) soil density treatments. Each value is the mean of 5 replications plus or minus SE from Exp. 3. See Table 1 for comparison with Exp. 2, and additional statistical analyses.

(Table 1). The treatment with all of the profile at high bulk density (D3) had a significantly higher root:shoot ratio than the treatment with only the lower profile compacted (D2). It is important to note that although compaction increased the proportion of total biomass partitioned to the

180 Andrade et al.

Table 1. Whole-plant relative leaf expansion rate (RLER), final leaf area and root:shoot (R:S) ratio (dry weight basis); and for individual leaves 1 and 2 (counting up from the cotyledon), the RLER and maximum leaf area

Exp. Soil Whole plant Leaf 1 Leaf 2 No. density

treatment a RLER Final leaf R : S RLER Max. RLER Max. (cm2cm Zd-I) area (gg-l) (cm2cm Zd-') area (cm2cm-2d 1) area

(cm 2) (cm 2) (cm z)

D1 0.21 459.8 0.25 0.15 24.6 0.31 75.6 D2 0.18 297.8 0.38 0.13 21.4 0.26 56.8 D1 vs. D2 (*) (* *) (* *) (NS) (NS) (*) (* *)

D1 0.23 641.4 0.19 0.14 29.8 0.25 82.4 D2 0.20 381.0 0.36 0.13 26.8 0.19 54.4 D3 0.17 234.6 0.28 0.09 21.4 0.17 42.8 D1 vs. D2, D3 (**) (**) (**) (**) (*) (**) (**) OEvs. D3 (* *) (* *) (* *) (NS) (NS) (NS) (NS)

a D 1 = control, D2 = compact 10-20 cm depth, and D3 = compact 0-20 cm depth. Orthogonal statistical contrasts are also presented (NS is not significant; * and * * are significant at the 0.05 and 0.01 levels, respectively)

roots , root biomass on an absolute basis was always lower in compacted t reatments than in the control (data not shown). Root biomass of D2 ranged f rom 75-90% of D1, while root biomass of D3 was about 60% of D1.

Figure 3 shows the diurnal changes in mean R L E R and ltY L in the D1 and D2 treatments. The most important finding was that the larger R L E R differences between t reatments (p < 0.01 for all measurement intervals) were not associated with any difference in XIf L o r ~ p determined pre-dawn or during the day. Mean R L E R was consistently lower in plants grown on compacted soil, while the diurnal patterns of XIt L of the control and compacted t reatments were nearly identical. Leaf solute potentials at 06:00 on the first day of the diurnal were - 0 . 9 2 and - 0 . 9 8 M P a for D1 and D2, respectively, and calculated kI'tp va lues were 0.78 and 0.85 MPa for D1 and D2, respectively. At 19:00, when both t rea tments had the most negative W E, W0 was - 1 . 3 8 and - 1 . 2 7 M P a for D1 and D2, respectively, with ~p values of 0.20 and 0.18 MPa for D1 and D2, respectively. Analyses of these data indicated no statistically significant t reatment effects on leaf water potential components . A second diurnal evaluation conducted during Exp. 3, and midday measurements collected on twelve other occasions (data not shown) verified that soil compact ion significantly reduces R L E R without any concomitant effect on XI'L, ~0, o r kI'tp

measured on expanding or fully expanded leaves.

Photosynthesis and leaf nitrogen status

Specific leaf weights of plants grown on compacted soil were in general slightly higher than the control (Table 2). Leaf N per unit leaf area was also significantly higher in compacted treatments compared to the control in some cases, indicating that a port ion of the SLW increase was associated with an accumulation of N per unit area.

Soil compact ion had either no effect, or in some cases a positive effect, on Pn (Table 2). Photosynthesis expressed on a per unit leaf area basis was significantly higher in compacted treatments on two of the four measurement dates presented, and Pn per unit leaf N was significantly higher in compacted t reatments on one occasion. The reverse, significantly higher Pn in control compared to compacted t rea tments , was never observed.

Discussion

Leaf expansion and growth

Our results indicate that leaf expansion of sunflower is highly sensitive to soil strength, at least


0.007

0.006

0.005

o E 0.004 % o9. 0.003 rr W -~ 0.002 QZ

0.001

~/.z D2 (compact 10-20 cm) I)

I

08:00-20:00 June 27

20:00-08:00 08:00-20:00 June 28

Time (hour)

"~" -0.2 c,

-0.4 E "5 -0.6 {3..

~ -0.8

_ J

-1.2 t i I I t 06:00 13:00 18:00 06:00 13:00 18:00

June 27 June 28 Time (hour)

Fig. 3. Diurnal changes in relative leaf expansion rate ( R L E R ) and leaf water potential of the control (D1) and compacted (D2) t rea tment in Exp. 2 on 27 and 28 June (27 and 28 days after planting). Midday air temperature was 32°C and relative humidity was 35%. Each value is the mean of 5 replications plus or minus SE. Leaf solute and calculated pressure potentials measured from samples collected at 06 : 00 and 19:00 on 27 June showed no significant t reatment effect (see text for discussion).

during the early vegetative growth phase measured in this study (Figs. 1, 2; Table 1). The fact that the RLER of the first leaf to emerge was reduced in the treatment with the compacted layer 10 cm below the surface (D2), as well as in the D3 treatment, suggests a very rapid detection of the compacted layer that did not require the development of high root density. Masle and Passioura (1987) also reported an early response

in wheat, with slower expansion of the first leaf of seedlings grown on soils with bulk densities of

- 3 1.5g cm Our data clarify that the reduction in whole-

plant leaf area development on compacted soils is due not only to slower expansion rates, but also smaller maximum size of individual leaves. Preliminary anatomical observations indicated that leaves from compacted treatments were thinner with shorter palisade cells, despite the fact that they tended to have a higher specific leaf weight. This observation warrants further study to determine how soil compaction affects patterns of cell differentiation in relation to photosynthetic capacity, N and water use efficiency.

Root growth was also inhibited by compaction, but to a lesser extent than leaf growth, and root:shoot ratios were significantly higher in compacted treatments. (Table 1). Similar results have been reported for wheat (Masle and Pas- sioura, 1987) and bean (Carmi et al. 1983). As shoot growth is checked by compaction, more assimilates may become available for root growth. Osmotically active substances can ac- cumulate in root apices contacting compacted soil, coinciding with radial swelling and lateral proliferation of roots (Atwell, 1988; Goss and Russell, 1980). An increase in root:shoot ratio has been frequently observed in response to drought, and may be due to differing sensitivity of roots and the hypocotyl zone to ABA (Creel- man et al., 1990). However, Lachno et al. (1982) found that IAA, and not ABA, accumulated in maize roots when plants were subjected to mechanical stress. A study with Vicia faba (Kays et al., 1974) reported a 6-fold increase in ethylene when a physical barrier prevented axial root extension. Masle and Passioura (1987) proposed that reduced leaf expansion of compacted wheat plants is primarily a response to a hormonal message induced in the roots when they ex- perience high soil strength. Clearly, more research on hormonal and source/sink mechanisms involved in controlling root and shoot growth of plants grown on compacted soils is needed.

From an agronomic standpoint, the RLER response to soil compaction during the early exponential phase of growth will have a dramatic effect on whole-plant leaf area and canopy

182 Andrade et al.

Table 2. Specific leaf weight, leaf nitrogen (N) per unit leaf area and net photosynthesis N basis

expressed on a per unit leaf area and leaf

Exp. Leaf Date Soil density Specific Leaf no. treatment a leaf weight nitrogen

(mgcm -2 ) (/xgN cm -2 )

Photosynthesis per unit

Leaf area (p.mol m -2 s -1)

Leaf N (/zmol gN -1 s -1 )

2 2 Jul 1

3 Jul 4

3 2 Sep 10

3 Sep 16

D1 7.40 244.3 43.5 17.9 D2 7.54 291.0 51.5 17.7 D1 vs. D2 (NS) (*) (.) (NS) D1 7.78 273.1 44.8 16.4 D2 8.30 268.1 41.5 15.5 D1 vs. D2 (NS) (NS) (NS) (NS)

D1 5.30 280.4 44.5 15.9 D2 5.42 229.8 42.0 18.3 D3 5.23 273.0 44.6 16.3 D1 vs. D2, D3 (NS) (NS) (NS) (*) D2 vs. D3 (NS) ( * ) (NS) ( * ) D 1 6.05 274.1 40.2 14.7 D2 6.41 301.9 47.2 15.6 D3 6.71 332.8 43.2 13.0 D1 vs. D2, 9 3 (* ) (* ) (* *) (NS) D2 vs, D3 (NS) (NS) (* ) (NS)

"D1 = control, D2 = compact 10-20 cm depth, and D3 = compact 0-20 cm depth. Orthogonal statistical contrasts are also presented (NS is not significant; * , * * are respectively).

significant at the 0.05 and 0.01 levels,

development. For example, using the RLER data from Fi~. 1, and assuming a plant spacing of 8 plants m- , 46 days would be required for a crop grown on a soil with a penetrometer resistance of 0.7 MPa to reach an LA1 of 3.0, while a crop grown on a soil compacted at 2.4MPa would require 76 days to reach the same stage. Such a delay must have a direct effect on cumulative light interception and on yield. How- ever, experiments with peas (Dann et al., 1987) and sorghum (Ludlow et al., 1989) found reductions in early growth and biomass but no reduction in yield on compacted soils. The effect of compaction on the time to reach physiological maturity was not reported in these studies, but the likely delay caused by compaction could be of economic importance.

Water relations, leaf N, and Pn

The slower leaf expansion of plants grown on compacted soils was not related to bulk leaf water status or leaf turgor (Fig. 3). Values of XI/L, ~0, and ~p of compaction treatments were nearly identical to control treatments regardless

of leaf maturity, plant growth stage, or time of day that measurements were taken. Masle and Passioura (1987) found similar results for wheat and concluded that the decrease in leaf expansion rates were not due to any effect of compaction on internal water relations. Ludlow et al. (1989) observed significant reductions in early leaf growth of sorghum, without a concomitant decline in ~L or ~p. Corroboration of these whole-leaf measurements will require more detailed evaluation of soil compaction effects on the water supply/demand equilibria within expanding cells of the leaf.

Nitrogen uptake and metabolism were not directly measured in our study, but N per unit leaf area was either unaffected or higher in compaction treatments compared to the control (Table 2). Masle and Passioura (1987) found that concentrations of both phosphorus and N in wheat plants were not affected by soil strength. They also reported that the phosphorus content of the soil and addition of macro- and micro- nutrients had no interactive effect on growth response to compaction. Nutrient deficiency is therefore an unlikely explanation for slower


growth on compacted soils, although, as dis- cussed with regard to water limitations, more detailed studies will be required to determine whether these whole-leaf measurements accu- rately reflect the status of rapidly expanding cells. Also, compaction constraints on root development may become more pronounced with time and lead to nutrient deficiencies at later growth stages if shoot growth demand exceeds supply.

The higher Pn per unit leaf area sometimes observed in plants grown on compacted soil was associated with the higher N per unit leaf area (Table 2). Nitrogen is a major component of key photosynthetic enzymes, and N level can affect mesophyll conductance to CO 2 (Longstreth and Nobel, 1980). Masle and Farquhar (1988) measured higher Pn per unit leaf area in wheat plants grown on compacted soils, and this was corre- lated with greater ribulose 1,5-bisphosphate car- boxylase/oxygenase (Rubisco) activity. Carmi et al. (1983) reported similar results for bean plants (Phaseolus vulgaris) grown with an artificially restricted rooting volume.

The increase in SLW and leaf N in plants grown on compacted soil may represent an acclimation to stress or simply be a passive response to excess assimilates. Maintenance of Pn per unit leaf area under prolonged stress may not be of adaptive advantage if it requires an accumulation of N at the expense of new leaf expansion. However, plants recovering from a short-term compaction period in the field (e.g., as roots grow beyond a compacted layer) may benefit from a higher root/shoot ratio and increased Pn per unit leaf area.

Concluding remarks

Growth of sunflower was very sensitive to soil strength under field conditions, and leaf expansion was more suppressed than root growth on compacted soil. Smaller maximum leaf size as well as reductions in RLER of individual leaves contributed to the reductions in plant leaf area and growth. Slower leaf expansion in compacted treatments was not associated with lower leaf turgor or with a decline in leaf water potential. Furthermore, we could not attribute the effects

to lower leaf N content or lower Pn. On the contrary, a higher Pn per unit leaf area, and higher N and SLW were sometimes observed in plants grown on compacted soil. Future investi- gations of the leaf expansion response to soil compaction should examine in more detail the dynamic equilibria of expanding cells with regard to carbon, water, and N supply. Our whole-leaf measurements support the hypothesis that growth of sunflower plants on compacted soil in the field is primarily sink-limited and modulated by hormonal signals from the roots.

Acknowledgements

The authors thank Dr. C Gimenez for help with field photosynthesis measurements, and Dr. H F Rapoport for help with preliminary leaf anatomical observations. DWW gratefully ac- knowledges a sabbatical leave fellowship from the DGICYT, Ministry of Education and Science of Spain.

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Leaf expansion, photosynthesis, and water relations of sunflower plants grown on compacted soil