Summary Basal shoots produced by Arbutus unedo L. after cutting at ground level vary in size and growth rate, and are classified accordingly as dominant or suppressed. The sup-pressed shoots eventually cease growth and die. In this study, we investigated the role of light and water in the competition among shoots of A. unedo.
Dominant and suppressed shoots of A. unedo showed simi-lar leaf water potentials and tissue water relations over the year, suggesting that water status is not responsible for the lack of flushing in suppressed shoots. Although suppressed shoots did not flush under low light, they showed many characteristics of shade-tolerant plants. Leaves of suppressed shoots had lower leaf conductance and light-saturated photosynthetic rate, and higher specific leaf area than leaves of dominant shoots. We conclude that light was the main resource determining compe-tition among shoots and the death of suppressed shoots. Keywords: competition, growth rate, irradiance, leaf conduc-tance, leaf water potential.
Introduction
Many Mediterranean species resprout after disturbance, pro-ducing new shoots from roots and stumps. Although emer-gence from dormant buds occurs almost simultaneously, there is soon much variation in the size of shoots (Hara 1984), leading to the dominance of a relatively few shoots over the majority that remain suppressed (White and Harper 1970). Dominant shoots have higher growth rates than suppressed shoots, thus differences in relative size and the hierarchical status increase over time. Eventually, competition leads to the death of most of the suppressed shoots (see Ford and Newbold 1970, Retana et al. 1992).
We tested the hypothesis that, in Arbutus unedo L., an evergreen laurophyllous tree, light and water are the resources for which shoots chiefly compete. The species is widely dis-tributed in the Mediterranean Basin and can resprout vigor-ously after fire or decapitation, producing a large number of shoots. We analyzed the ecophysiology of dominant and sup-pressed shoots of A. unedo to establish the relative roles of light and water in the competition between them. In addition, we considered both morphological and physiological acclimation to low light and water availability in terms of how these
resources affect the dynamics of resprouting and the regenera-tion process after disturbance.
Materials and methods
Study site
The study site is located at an elevation of 350 m, on a southern slope (15--20°) of the Collserola Natural Park in northeast Spain, near Barcelona (41°25′25″ N, 2°6′30″ E). The area, which was burned in the summer of 1973, has vegetation 3--4 m tall and is dominated by Arbutus unedo L., Quercus ilex L. and Pinus halepensis Mill.
During the study period (June 1990--May 1991), total rain-fall was 940 mm (mean annual rainrain-fall = 725 mm). The dry period lasted from late June to late August, with a total rainfall of only 29 mm. The soil is shallow (19 ± 1 cm, n = 18) and comprised of a loamy-clay that developed on Paleozoic schists. The soil has a low water storage capacity.
Plant material
Five A. unedo trees were felled on May 3, 1990, to induce sprouting of basal shoots. The tallest shoots, which received full sunlight, were defined as dominant, whereas the shorter shoots, which were located inside the stool and were shaded by the dominant shoots, were defined as suppressed. Only three of the five trees were used for the ecophysiological measurements, but all five trees were used for measuring growth rates. Sampling was carried out from July 1990 to May 1991.
Water potential and gas exchange
Leaf water potential (Ψ) was measured at dawn and midday with a pressure chamber (Model 3005, Soil Moisture Inc., Santa Barbara, CA), as described by Scholander et al. (1965). Photosynthetically active radiation (PAR), leaf conductance, water loss to the porometer chamber (hereafter referred to as transpiration rate), and net photosynthetic rate were measured with a field IRGA-porometer (Model LCA-2, ADC Ltd., Hod-desdon, U.K.). The quotient between net photosynthesis and transpiration was used to estimate water use efficiency. Hourly measurements began when stools were in full sunlight and finished when they became shaded. Each sampling consisted
Water relations, gas exchange and growth of dominant and suppressed
shoots of
Arbutus unedo
L.
CARLES CASTELL and JAUME TERRADAS
Centre de Recerca Ecològica i Aplicacions Forestals, Facultat de Ciències, Universitat Autònoma de Barcelona, 08193 Bellaterra, Spain
Received October 19, 1993
of measurements on a leaf of one dominant and one suppressed shoot of each stool. A sample leaf was selected from among the third to seventh fully developed leaves from the branch tip. All measurements were made on leaves produced in the spring, except from October to May, when measurements for domi-nant shoots were made on leaves produced in the autumn because the autumn shoots shaded the spring leaves. Measure-ments were made weekly during the dry period, monthly in autumn, and seasonally in winter and spring.
Pressure--volume curves
Pressure--volume curves were performed on a single leaf of one dominant and one suppressed shoot of each stool on June 26, August 3 and December 12. Samples were cut and trans-ferred to test tubes containing distilled water, covered with a plastic bag, and kept overnight in darkness in a refrigerator (Kubiske and Abrams 1991). The next morning, samples were allowed to dehydrate, and water potential and leaf weight were periodically measured (Wilson et al. 1979). After a Type-II transformation (Tyree and Richter 1981, 1982), osmotic poten-tial at saturation, (Ψs(sat)), osmotic potential at the bulk tissue turgor loss point (Ψs(tlp)), relative water content at the bulk tissue turgor loss point (RWC(tlp)) and the maximum bulk modulus of elasticity (ε) were calculated according to Wilson et al. (1979). Although this technique has limitations (see Dreyer et al. 1990), the data are useful for comparative pur-poses. Cuticular transpiration (Ec) was estimated on the basis of leaf weight loss during the course of dehydration (Larsson and Svenningsson 1986).
Nutrient content and growth
Nitrogen and phosphorus contents of leaves of dominant and suppressed shoots of each stool were determined on August 14 and December 12. Nitrogen was analyzed by the Kjeldahl method, in a Kjeltec 1030 Auto Analyzer (Tecator, Höganäs, Sweden), and phosphorus was assayed by the vanado-molybdate colorimetric technique in an FIA 5020 Analyzer-Spectrophotometer 5023 (Tecator) (Allen et al. 1974). Specific leaf area (SLA) was determined from the projected leaf area, which was measured with a leaf area meter (Model LI3000, Li-Cor Inc., Lincoln, NE).
From July to December, relative growth rate (RGR) was periodically determined on the basis of height increase in one dominant and one suppressed shoot of each stool, according to Hutchings (1986).
Statistical analyses
Data were compared by repeated measures analysis of vari-ance (Potvin et al. 1990). If necessary, this test was followed by mean comparison contrasts to determine when significant differences occurred. All tests were performed with Super-ANOVA software (Abacus Concepts Inc., Berkeley, CA).
Results
Mean daily PAR was higher for dominant than for suppressed shoots throughout the year (Figure 1). Thus, PAR in dominant
shoots always exceeded 1000 µmol m−2 s−1, except on overcast days, whereas PAR in suppressed shoots never exceeded 500 µmol m−2 s−1 and decreased over time because of the growth of dominant shoots.
With one exception, there were no significant differences in predawn Ψ between dominant and suppressed shoots, but Ψ at midday was often lower in dominant shoots than in suppressed shoots (Figure 2). Values of leaf conductance and transpiration followed the same time course in dominant and suppressed shoots, but were always higher in dominant shoots than in suppressed shoots (Figure 3). The greatest difference between dominant and suppressed shoots was in net photosynthetic rate, which was six times higher in dominant shoots than in suppressed shoots. The larger difference in net photosynthetic rate than in transpiration rate meant that water use efficiency was greater in dominant shoots than in suppressed shoots. Photosynthetic response to light also differed between the dominant and suppressed shoots (Table 1). Leaves of sup-pressed shoots had lower compensation points, saturating ra-diation (PARsat) and net photosynthetic rates per unit leaf area (Amax area−1) and per unit leaf mass (Amax mass−1) than leaves of dominant shoots.
In June and September, the only differences observed in the pressure--volume curves of the dominant and suppressed shoots were higher values of Ec in suppressed shoots (Table 2). In December, Ψs(sat), Ψs(tlp), ε and RWC(tlp) were lower in sup-pressed shoots than in dominant shoots, probably because of the different ages of the sampled leaves (spring leaves of suppressed shoots versus autumn leaves of dominant shoots).
Suppressed shoots had higher SLA that dominant shoots, both in August and December (Table 3), and thus a lower nutrient content per unit leaf area, despite similar nutrient contents per unit leaf weight.
Relative growth rates were higher in dominant than in sup-pressed shoots in early summer (Figure 4). During August and September, growth ceased in both dominant and suppressed shoots. In October and November, all dominant shoots flushed, whereas few suppressed shoots flushed.
Discussion
Leaf water status was similar in dominant and suppressed shoots of A. unedo (Figure 2). The only difference was that a lower leaf conductance in suppressed shoots, together with a lower vapor pressure deficit within the center of the new shoots, caused a higher transpiration rate and, sometimes, a lower leaf water potential at midday in the dominant shoots than in the suppressed shoots (Figures 2 and 3) (see Abrams 1986, Lei and Lechowicz 1990). There were no differences in predawn leaf water potential among shoots, despite higher transpiration rates in the dominant shoots (Table 1). Thus, competition among shoots for water cannot account for the differences in their growth and survival.
Sun plants growing in the shade show light acclimation, and their characteristics tend to approach those of obligate shade plants (Björkman 1981). In the same way, the characteristics of leaves of suppressed shoots of A. unedo indicated acclima-tion to low light, i.e., these leaves exhibited lower leaf conduc-tance, cuticular resisconduc-tance, light-saturated photosynthetic rate, compensation point and nutrient content per unit leaf area, and higher specific leaf area than leaves of dominant shoots (Boardman 1977, Catarino et al. 1981, Givnish 1988).
Acclimation of photosynthesis to low light may be mediated by anatomical as well as physiological changes within the leaves (Boardman 1977, Björkman 1981). In leaves of domi-nant shoots of Arbutus, area-based maximum photosynthesis increased by 360% compared to that of leaves of suppressed
Figure 2. Annual course of predawn (top) and midday (bottom) leaf water potential of dominant and suppressed shoots in the field from July 1990 to May 1991. Mean values were compared by a repeated measures analysis of variance followed by contrasts (* = P < 0.05, ** = P < 0.01, *** = P < 0.001, n = 3).
Figure 3. Annual course of daily mean (from top to bottom) leaf conductance, transpiration rate, net photosynthetic rate and water use efficiency of dominant and suppressed shoots in the field from July 1990 to May 1991. Mean values were compared by a repeated meas-ures analysis of variance followed by contrasts (* = P < 0.05, ** = P
< 0.01, *** = P < 0.001, n = 3).
Table 1. Photosynthetic characteristics of leaves of dominant and suppressed shoots (mean ± 1 SE). Data were calculated by adjusting the upper limit of the relationship between PAR and net photosynthe-sis, including all the field records, for dominant and suppressed shoots of each individual. Mean values were compared by the Student’s t-test (* = P < 0.05, ** = P < 0.01, *** = P < 0.001, n = 3).
Dominant Suppressed
Amax area−1 (µmol m−2 s−1) 10.5 ± 0.1 2.9 ± 0.1*** Amax mass−1 (nmol g−1 s−1) 72.5 ± 3.1 34.4 ± 1.6***
shoots (Table 1). Nearly 60% of this increase was due to increased mass-based maximum photosynthesis, which can be directly attributable to changes in physiological mechanisms (Björkman 1981). The remaining 40% of the increase was due to diminished specific leaf area, which can be attributed to
changes in leaf anatomy. The decrease in specific leaf area was paralleled by an increase in the quantity of photosynthetic apparatus per unit leaf area, which was also reflected in the increase in N per unit leaf area (Table 3; Ellsworth and Reich 1992, Chazdon and Kaufmann 1993).
The increase in Amax mass−1 in leaves of dominant shoots was not accompanied by an increase in N mass−1, suggesting that differences in leaf nitrogen allocation are of great impor-tance. Based on this observation, we conclude that leaves of suppressed shoots had a greater investment of nitrogen in light-harvesting machinery, whereas leaves of dominant shoots had more nitrogen invested in photosynthetic enzymes (Seeman et al. 1987, Evans 1989).
Low growth rates of suppressed shoots (Figure 5) cannot be attributed to a lack of turgor needed for cell elongation, be-cause there were no differences in water status between domi-nant and suppressed shoots. A more likely explanation is that low net photosynthesis in suppressed shoots led to a lack of carbohydrates in the apex of the sprout and, as a consequence, to low growth rates (see Radosevich and Conard 1980). Sup-pressed shoots did not grow in the autumn or the following spring, except for the few that received lateral illumination (data not shown). As a result, height and hierarchical status
Table 2. Tissue water relations of dominant and suppressed shoots in June, September and December 1990. Mean values were compared by a repeated measures analysis of variance followed by contrasts (* = P < 0.05, ** = P < 0.01, *** = P < 0.001. Values in brackets are ± 1 SE, n = 3).
June September December
Dominant Suppressed Dominant Suppressed Dominant Suppressed
Ψs(sat) (MPa) −0.74 −0.59 −1.80 −1.83 −1.34 −1.71*
(0.02) (0.09) (0.07) (0.03) (0.05) (0.19)
Ψs(tlp) (MPa) −0.98 −0.79 −2.19 −2.30 −1.88 −2.25
(0.03) (0.13) (0.04) (0.05) (0.06) (0.23)
ε (MPa) 7.0 4.7 14.6 14.3 16.2 13.5*
(0.5) (0.7) (1.0) (1.0) (1.1) (0.4)
RWC(tlp) (%) 92.3 91.6 89.8 89.2 92.8 89.2*
(0.9) (1.3) (0.2) (0.9) (0.2) (1.6)
Ec (mg g−1 min−1) 4.12 4.88* 1.52 2.62** 0.63 0.74
(0.43) (0.14) (0.20) (0.22) (0.04) (0.03)
Table 3. Specific leaf area, and nitrogen and phosphorous leaf contents of dominant and suppressed shoots in August and December 1990. Mean values were compared by a repeated measures analysis of variance followed by contrasts (* = P < 0.05, ** = P < 0.01, *** = P < 0.001. Values in brackets are ± 1 SE, n = 3).
August December
Dominant Suppressed Dominant Suppressed
SLA (cm2 g−1) 76.9 140.8*** 62.9 104.2***
(3.9) (9.3) (2.1) (2.8)
N mass−1 (%) 1.50 1.40 1.27 1.35
(0.18) (0.06) (0.08) (0.04)
N area−1 (g m−2) 1.95 0.99** 2.01 1.30**
(0.15) (0.06) (0.08) (0.05)
P mass−1 (mg g−1) 1.20 1.36 0.98 0.98
(0.17) (0.07) (0.06) (0.07)
P area−1 (mg dm−2) 1.56 0.97** 1.56 0.94**
(0.14) (0.07) (0.05) (0.04)
among shoots diverged. During the second summer after cut-ting, almost all of the suppressed shoots died, probably as a result of the shedding of existing leaves (12--14 months old) and the lack of carbohydrate reserves to support the production of new leaves.
We conclude that light, rather than water, is the main re-source determining competition among coppiced shoots of A. unedo, at least during the early stages of shoot regrowth. Because of their morphological and physiological plasticity, suppressed shoots became acclimated to low light and exhib-ited shade leaf characteristics; this allowed them to remain alive for some time. However, in the absence of shoot elonga-tion and producelonga-tion of new leaves, the suppressed shoots eventually died.
References
Abrams, M.D. 1986. Physiological plasticity in water relations and leaf structure of understory versus open-grown Cercis canadiensis
in northeastern Kansas. Can. J. For. Res. 16:1170--1174.
Allen, S.E., H. Grimshaw and J.A. Parkinson. 1974. Chemical analy-sis of ecological materials. Blackwell Scientific, Oxford, 565 p. Björkman, O. 1981. Responses to different quantum flux densities. In
Encyclopedia of Plant Physiology, Vol. 12A. Eds. O.L. Lange, P.S. Nobel, C.B. Osmond and H. Ziegler. Springer-Verlag, Berlin, pp 57--107.
Boardman, N.K. 1977. Comparative photosynthesis of sun and shade plants. Annu. Rev. Plant Physiol. 28:355--377.
Catarino, F.M., O.A. Correia, E. Webb and M. David. 1981. Morpho-logical and physioMorpho-logical responses of the Mediterranean evergreen sclerophyll, Ceratonia siliqua, to different light intensities. In Com-ponents of Productivity of Mediterranean-climate Region. Eds. N.S. Margaris and H.A. Mooney. Dr. W. Junk Publishers, The Hague, pp 5--15.
Chazdon, R.L. and S. Kaufmann. 1993. Plasticity of leaf anatomy of two rain forest shrubs in relation to photosynthetic light acclima-tion. Funct. Ecol. 7:385--394.
Dreyer, E., F. Bousquet and M. Ducrey. 1990. Use of pressure volume curves in water relation analysis on woody shoots: influence of rehydration and comparison of four European oak species. Ann. Sci. For. 47:285--297.
Ellsworth, D.S. and P.B. Reich. 1992. Leaf mass per area, nitrogen content and photosynthetic carbon gain in Acer saccharum seed-lings in contrasting light environments. Funct. Ecol. 6:423--435. Evans, J.R. 1989. Photosynthesis and nitrogen relationships in leaves
of C3 plants. Oecologia 78:9--19.
Ford, E.D. and P.J. Newbould. 1970. Stand structure and dry weight production through the sweet chestnut (Castanea sativa) coppice cycle. J. Ecol. 58:275--296.
Givnish, T.J. 1988. Adaptation to sun and shade: a whole-plant per-spective. Aust. J. Plant Physiol. 15:63--92.
Hara, T. 1984. A stochastic model and the moment dynamics of the growth and size distribution in plant populations. J. Theor. Biol. 109:173--190.
Hutchings, M.J. 1986. The structure of plant populations. In Plant Ecology. Ed. M.J. Crawley. Blackwell Scientific, Oxford, pp 97--136.
Kubiske, M.E. and M.D. Abrams. 1991. Rehydration effects on pres-sure--volume relationships in four temperate woody species: vari-ability with site, time of season and drought conditions. Oecologia 85:537--542.
Larsson, S. and M. Svenningsson. 1986. Cuticular transpiration and epicuticular lipids of primary leaves of barley (Hordeum vulgare). Physiol. Plant. 68:13--19.
Lei, T.T. and M.J. Lechowicz. 1990. Shade adaptation and shade tolerance in saplings of three Acer species from eastern North America. Oecologia 84:224--228.
Potvin, C., M.J. Lechowicz and S. Tardif. 1990. The statistical analysis of ecophysiological response curves obtained from experiments involving repeated measures. Ecology 71:1389--1400.
Radosevich, S.R. and S.G. Conard. 1980. Physiological control of chamise shoot growth after fire. Am. J. Bot. 67:1442--1447. Retana, J., M. Riba, C. Castell and J.M. Espelta. 1992. Regeneration
by sprouting of holm-oak (Quercus ilex) stands exploited by selec-tion thinning. Vegetatio 99/100:355--364.
Scholander, P.F., H.T. Hammel, E.D. Bradstreet and E.A. Hemming-sen. 1965. Sap pressure in vascular plants. Science 148:339--346. Seemann, J.R., T.D. Sharkey, J. Wang and C.B. Osmond. 1987.
Envi-ronmental effects on photosynthesis, nitrogen-use efficiency, and metabolite pools in leaves of sun and shade plants. Plant Physiol. 84:796--802.
Tyree, M.T. and H. Richter. 1981. Alternative methods of analysing water potential isotherms: some cautions and clarifications. I. The impact of non-ideality and of some experimental errors. J. Exp. Bot. 32:643--653.
Tyree, M.T. and H. Richter. 1982. Alternative methods of analysing water potential isotherms: some cautions and clarifications. II. Curvilinearity in water potential isotherms. Can J. Bot. 60:911--916.
White, J. and J.L. Harper. 1970. Correlated changes in plant size and number in plant populations. J. Ecol. 58:467--485.
