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Keywords:

  • Compensatory photosynthesis;
  • concentrated damage;
  • dispersed damage;
  • herbivory;
  • Solidago altissima

Abstract

  1. Top of page
  2. Abstract
  3. Introduction
  4. Materials and methods
  5. Results
  6. Discussion
  7. Acknowledgements
  8. References

1. Leaf area was removed from Solidago altissima in either a dispersed pattern (half of every leaf removed) or a concentrated pattern (every other leaf removed) and effects on leaf gas exchange, vegetative growth and flowering were examined relative to undefoliated controls. Gas exchange was measured for leaves remaining after defoliation and for regrowth leaves that developed post-damage (at 7, 16 and 26 days post-defoliation).

2. Area-based photosynthetic rates of leaves remaining after defoliation were not affected by either dispersed or concentrated damage, but damage of both types enhanced area-based photosynthesis of regrowth leaves at 16 days post-defoliation and to a lesser extent at 26 days post-defoliation.

3. Dispersed damage, but not concentrated damage, stimulated mass-based photosynthesis of undamaged leaves remaining after defoliation. Undamaged leaves remaining after defoliation and regrowth leaves on damaged plants had higher specific leaf area (leaf area/leaf mass) than comparable leaves on control plants. Mass-based photosynthesis was more strongly elevated by defoliation than area-based photosynthesis because of this increase in specific leaf area.

4. Plants with dispersed damage recovered more quickly from defoliation; they had higher relative growth rates in the first week post-defoliation than plants with concentrated damage. Both types of defoliation caused similar reductions in flower production.

5. These results add to accumulating evidence that dispersed damage is generally less detrimental to plants than concentrated damage and suggest that physiological changes in leaves may be part of the reason.


Introduction

  1. Top of page
  2. Abstract
  3. Introduction
  4. Materials and methods
  5. Results
  6. Discussion
  7. Acknowledgements
  8. References

Plant responses to defoliation depend on more than just the total amount of leaf area that is lost. The distribution of damage within the plant canopy can also affect plant recovery from herbivore feeding, even when the overall level of leaf area removed is held constant (Lowman 1982; Wit 1982; Watson & Casper 1984; Gold & Caldwell 1989; Marquis 1992, 1996; Mauricio, Bowers & Bazzaz 1993). Different patterns of damage arise because herbivores vary in their feeding behavior. Many invertebrate herbivores feed in a way that leads to dispersed damage on the host plant (Edwards & Wratten 1983; Mauricio & Bowers 1990), possibly because damage-induced changes in plant chemistry cause herbivores to move after eating a small portion of a leaf (Edwards & Wratten 1983). However, some insects feed in a manner that tends to concentrate damage on entire leaves. Some caterpillars completely consume a leaf before moving on to another leaf, while others will partially consume a leaf then excise the remainder by chewing through the petiole, causing the plant to lose the entire leaf (Heinrich 1993).

Several studies have shown that damage dispersed over many leaves is less detrimental to the plant than damage concentrated on fewer leaves (Lowman 1982; Marquis 1992; Mauricio et al. 1993; but see Wit 1982). If dispersed damage generally has less of an effect on plant growth than concentrated damage, then it is possible that one function of induced defences is to cause herbivores to feed in a way that reduces the impact on the host plant (Edwards & Wratten 1983; Marquis 1992). It is not yet fully understood why dispersed and concentrated damage affect plants differently. In woody species, movement of resources between branches is often restricted (Stephenson 1980; Watson & Casper 1984; Marquis 1988, 1992; Wisdom, Crawford & Aldon 1989). Heavily defoliated branches on trees that are otherwise undamaged may not be able to draw sufficient resources from the rest of the crown to maintain growth (Honkanen & Haukioja 1994). Localized damage can lead to the reduction or loss of reproductive output from the damaged branches and thereby have a greater impact than damage spread throughout the crown (Marquis 1992). However, restricted resource movement between branches does not explain why the pattern of damage influences the growth of herbaceous plants consisting of a single shoot (e.g. Mauricio et al. 1993). In these cases, the distribution of damage could potentially affect plant recovery from defoliation by influencing the likelihood of compensatory photosynthesis. Compensatory photosynthesis is defined as an increase in the photosynthetic rate of remaining or regrowth foliage on damaged plants above the levels seen in similar-aged leaves on undamaged plants (Nowak & Caldwell 1984) and is commonly found in defoliated plants (reviews by Welter 1989; Trumble, Kolodny-Hirsch & Ting 1993; Rosenthal & Kotanen 1994). Enhanced photosynthesis of damaged plants can result from changes in the source–sink ratio following defoliation, although reduced competition between remaining leaves for water, nutrients or hormones supplied by the roots may also play a role (McNaughton 1983; Mooney & Chiariello 1984; Trumble et al. 1993). Dispersed and concentrated damage could differentially alter the flow of photosynthate between sources and sinks within the plant and thereby influence the likelihood of compensatory photosynthesis. A direct vascular connection is generally necessary for the transport of carbohydrates from a source leaf to a developing, sink leaf (Dickson & Isebrands 1991). When damage is dispersed over the plant, source area is reduced more or less evenly across all mature leaves and all developing leaves would retain connections to functional source leaves. Compensatory photosynthesis may be more likely in this case, because demand from the sinks could enhance photosynthesis in all of the source leaves. In contrast, when damage is concentrated on fewer leaves, source leaves are either lost altogether or they could be so heavily damaged that they fail to contribute much photosynthate to developing sinks. A sink leaf that has lost its connected source leaves may not have any influence on undamaged source leaves to which it has no direct vascular connection. Concentrated damage may therefore not stimulate photosynthesis in the remaining leaves to the same degree as dispersed damage. These predictions would be modified if damage has direct effects on leaf physiology. The severing of vascular connections and wounding of leaf tissue associated with defoliation could impair leaf function. If damage to individual leaves generally reduces their photosynthetic rates, then plants with dispersed damage might do worse than plants with concentrated damage, because most or all of their leaves would experience some defoliation.

In spite of its potential for explaining plant responses to defoliation, little work to date has investigated how the pattern of damage influences photosynthetic rate (but see Hall & Ferree 1976; Morrison & Reekie 1995). In addition, these studies have not linked changes in photosynthetic rate to plant growth or reproduction (e.g. Hall & Ferree 1976; Morrison & Reekie 1995). In the experiment reported here, I examined how dispersed and concentrated damage affected gas exchange, growth and flowering of Goldenrod, Solidago altissima. My experiment addressed the following hypotheses: (1) compensatory photosynthesis is more likely following dispersed damage than concentrated damage, for the reasons outlined above, (2) compensatory photosynthesis is more likely in an undamaged leaf than a damaged leaf, because the wounding associated with damage could impair leaf function, and (3) plants should recover more readily from dispersed damage than concentrated damage, because dispersed damage should enhance photosynthesis more than concentrated damage.

Materials and methods

  1. Top of page
  2. Abstract
  3. Introduction
  4. Materials and methods
  5. Results
  6. Discussion
  7. Acknowledgements
  8. References

PLANTS

Solidago altissima L. (Compositae) is a native, perennial forb that is abundant in the north-eastern United States. Ramets emerge from overwintering rhizomes as the ground warms in spring and the unbranched shoots grow rapidly into the summer. Flowering occurs in late summer to early autumn, seeds are dispersed through the autumn and all above-ground parts die back each winter. More information on the biology of S. altissima and related species can be found in Werner, Bradbury & Gross (1980) and for a description of the insect herbivore fauna associated with S. altissima see Root & Cappuccino (1992). Field-collected seeds were sown in a greenhouse on 24 March 1995, using a peatmoss-based potting medium. Identification of S. altissima was based on the treatment in Melville & Morton (1982) and Semple & Ringius (1983). Seedlings were transplanted to 20 cm pots on 28 May. The potted Goldenrods were arranged outside on a flat roof adjacent to the greenhouse at Williams College, Williamstown, MA, USA. The plants initially grew as a single stem. Midway through the experiment, buds at the base of the main stem began developing so the plants consisted of a main, central stem surrounded by several lateral stems.

DAMAGE TREATMENTS

Undamaged control plants were compared with plants with dispersed or concentrated damage. Herbivore damage was simulated because the major focus of this experiment was to determine how the pattern of damage affected plant physiology and growth, and it is difficult to control the pattern of feeding when using insect herbivores. Leaves were damaged with a hole punch every day for 10 days (19–28 June). At the end of the damage period, plants with dispersed damage had lost the distal half of every leaf (except for a single leaf designated for gas-exchange measures), while plants with concentrated damage had lost every other whole leaf (except for one leaf that was partially damaged and used for gas-exchange measures). Total leaf area loss was thus held constant at 50% for the two types of damage. Only leaves on the main stem were damaged; lateral stems were undamaged on all plants. Plants were arranged in groups of three before damage was applied based on size and appearance, and then treatments were randomly assigned within each block. There were 15 replicates of each treatment.

GAS-EXCHANGE MEASUREMENTS

Gas exchange was measured both for leaves remaining after defoliation and for regrowth leaves produced subsequent to defoliation. To insure that leaves used for gas-exchange measures developed at the same time on control plants and damaged plants, the main stem of each plant was marked below the bud with a twist tie on 19 June, just before damage treatments were begun, and on 29 June, immediately after damage treatments ended. Leaves were added rapidly above the twist ties as the stems grew. The first and second leaves above the lower twist tie were used for gas-exchange measures of remaining leaves (Fig. 1, leaf 1 and 2) and the first two leaves above the upper twist tie were used for gas-exchange measures of regrowth leaves (Fig. 1, leaf 3 and 4). Because damage to the leaf itself may affect photosynthesis, gas-exchange measurements were taken both for damaged remaining leaves and undamaged remaining leaves (Fig. 1, leaf 1 and 2, respectively). Gas exchange of remaining leaves was measured at the end of the damage period, before much regrowth had occurred (29 June for leaf 1, 30 June for leaf 2). Gas exchange of regrowth leaves was measured at 7, 16 and 26 days post-defoliation (leaf 3 was used for the 7 and 16 day measurements and leaf 4 was used for the 26 day measurement). Days post-defoliation were counted using 29 June, the day after damage treatments ended, as day 1.

image

Figure 1. . Leaves used for gas-exchange measurements. The lower tag was placed below the bud just before damage treatments began and the upper tag was placed below the bud at the end of the damage period. Control, undamaged plants not shown, but they were tagged at the same time as damaged plants and leaves used for gas exchange were in the same position relative to the tags. Note that percentage leaf area loss on leaf 1 was 25% rather than 50% to allow sufficient remaining leaf area for gas-exchange measures. Gas exchange was measured on remaining leaves at the end of the damage period, on leaf 3 at 7 and 16 days after damage ended, and on leaf 4 at 26 days post-damage.

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Photosynthetic rate and stomatal conductance were measured using a Li-Cor 6200 portable photosynthesis system equipped with a quarter-litre chamber (Li-Cor Inc., Lincoln, NE, USA). A QBeam QB6200 LED lighting system (Quantum Devices, Barneveld, WI, USA) was used to provide a saturating light intensity (photon flux density was ≈ 1100 μmol m–2 s–1). This lamp provides monochromatic light with a peak wavelength of 670 nm and because there is no infra-red radiation the lamp remains cool. At high light intensities, photosynthetic rate and stomatal conductance may be slightly lower under a monochromatic red light compared with a white light but plant responses to the two types of light are generally similar (Tennessen, Singsaas & Sharkey 1994). All measurements were taken between 09.00 and 11.00 h, outside on the roof where the plants were growing. The portion of the leaf placed within the chamber was kept constant across treatments.

Leaves were generally excised after gas-exchange measurements and area within the chamber, total area, and total dry mass were determined. The only exception to this protocol was for the regrowth leaf measured at 7 days post-defoliation, when the measured leaf was not detached. For this date, area within the chamber was estimated using a regression that related the width of the portion of the leaf in the chamber to its area (R2 for the regression = 0·97, n = 45).

PLANT GROWTH AND FLOWERING

The number of leaves added over time was monitored by using the twist ties that were placed below the bud on 19 June and 29 June to mark leaves for gas-exchange measurements. The number of leaves added over the damage period was determined by counting leaves above the 19 June twist tie on 28 June (this count included leaves in the whole-leaf removal treatment that were cut off). Leaves above the 29 June twist tie were counted on 5 July, yielding the number of leaves added in the first week post-defoliation. The height of the main stem was measured on 19 and 28 June, 5 and 17 July, and 7 August. Relative growth rates of the main stem were calculated from these heights using the following formula: (ln height1– ln height0)/(time1– time0), where height0 is the height at the start of the interval, height1 is the height at the end of the interval and time1– time0 is the time period in days. The number and height of all lateral stems greater than 5 cm tall were recorded on 28 June and 7 August. Inflorescences were harvested on 7 September, dried and weighed. The effects of defoliation on rhizomes were not measured in this experiment because flowering is more sensitive to herbivory than rhizome growth in S. altissima (Meyer & Root 1993; Root 1996).

Results

  1. Top of page
  2. Abstract
  3. Introduction
  4. Materials and methods
  5. Results
  6. Discussion
  7. Acknowledgements
  8. References

EFFECTS OF DAMAGE ON GAS EXCHANGE

Area-based photosynthetic rates of remaining leaves were not affected by either whole-leaf removal or half-leaf removal (Fig. 2). Damage to the leaf itself did not affect photosynthesis per unit area (Fig. 2, leaf 1), and undamaged remaining leaves on damaged plants also had area-based photosynthetic rates equivalent to controls for both whole-leaf removal and half-leaf removal plants (Fig. 2, leaf 2). However, stomatal conductance of remaining leaves was higher on defoliated plants, particularly for undamaged leaves (Fig. 2, leaf 2). The pattern of defoliation did not influence stomatal conductance; increases occurred both on whole-leaf removal and half-leaf removal plants.

image

Figure 2. . Effects of defoliation on area-based photosynthesis (a) and stomatal conductance (b) of remaining leaves. Means and standard errors are shown. Leaf 1 was damaged and leaf 2 was undamaged (see Fig. 1). Significance levels shown are for contrasts following randomized block ANOVA. U vs D, comparison of undamaged to damaged plants (whole-leaf removal and half-leaf removal combined); †P<0·10; **P<0·01.

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Area-based photosynthesis of regrowth leaves was enhanced by defoliation of both types (Fig. 3). Damage-induced increases in photosynthetic rates developed slowly; there were no differences between damaged and undamaged plants at 7 days after defoliation was completed. Photosynthetic rates of regrowth leaves on damaged plants (for both whole-leaf removal and half-leaf removal) increased between 7 and 16 days post-defoliation, while photosynthetic rates of comparable leaves on control plants declined over this period. By 16 days after damage had ended, regrowth leaves on both whole-leaf removal and half-leaf removal plants showed photosynthetic rates per unit area that were elevated by 24% above similar leaves on undamaged plants. The higher photosynthetic rates were accompanied by increased stomatal conductance (Fig. 3). Area-based photosynthetic rates of regrowth leaves on damaged plants were still higher than controls at 26 days post-defoliation but the difference was not as pronounced and of only marginal significance (Fig. 3). The pattern of damage did not influence area-based photosynthetic rates or stomatal conductance; there were no significant differences between whole-leaf removal and half-leaf removal.

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Figure 3. . Effects of defoliation on area-based photosynthesis (a) and stomatal conductance (b) of regrowth leaves. Means and standard errors are shown. Significance levels shown are for contrasts following randomized block ANOVA. U vs D, comparison of undamaged to damaged plants (whole-leaf removal and half-leaf removal combined); †P < 0·10; **P < 0·01.

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Defoliation of both types also caused changes in specific leaf area (leaf area/leaf mass). Both whole-leaf removal and half-leaf removal increased specific leaf area of undamaged remaining leaves (Fig. 4, leaf 2) and regrowth leaves (Fig. 5), relative to comparable leaves on control plants. Specific leaf area was consistently elevated more by half-leaf removal than by whole-leaf removal, but these differences were not significant. However, the difference between half-leaf removal and whole-leaf removal was marginally significant for the damaged remaining leaf (Fig. 4, leaf 1).

image

Figure 4. . Effects of defoliation on specific leaf area (leaf area/leaf mass, a and mass-based photosynthesis (b) of remaining leaves. Means and standard errors are shown. Leaf 1 was damaged and leaf 2 was undamaged (see Fig. 1). Significance levels shown are for contrasts following randomized block ANOVA. U vs D, comparison of undamaged to damaged plants (whole-leaf removal and half-leaf removal combined); WL vs HL, comparison of whole-leaf removal to half-leaf removal; †P < 0·10; *P < 0·05.

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image

Figure 5. . Effects of defoliation on specific leaf area (leaf area/leaf mass, a) and mass-based photosynthesis (b) of regrowth leaves. Means and standard errors are shown. Data for 7 days post-defoliation are missing because leaves were not harvested after gas-exchange measures. Significance levels shown are for contrasts following randomized block ANOVA. U vs D, comparison of undamaged to damaged plants (whole-leaf removal and half-leaf removal combined); *P < 0·05; **P < 0·01.

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Because damage affected specific leaf area, photosynthesis was also calculated per unit mass. Differences between damaged and undamaged plants became stronger when mass-based photosynthesis was examined. In contrast to the lack of an effect of defoliation on area-based photosynthesis for remaining leaves (Fig. 2), undamaged remaining leaves exhibited compensatory photosynthesis when photosynthetic rate was expressed per unit mass (Fig. 4, leaf 2). However, only half-leaf removal stimulated photosynthesis; mass-based photosynthetic rates of whole-leaf removal plants were similar to controls (Fig. 4, leaf 2). For regrowth leaves measured at 16 days post-defoliation, photosynthesis per unit mass was enhanced above control levels by 27% and 33% for the whole-leaf removal and half-leaf removal treatments, respectively (Fig. 5). At 26 days post-defoliation, photosynthetic rates were still clearly elevated above the controls (18% and 27% increase for whole-leaf removal and half-leaf removal, respectively). Although half-leaf removal plants had higher mass-based photosynthetic rates than whole-leaf removal plants for both regrowth leaves, these differences were not significant.

EFFECTS OF DAMAGE ON GROWTH AND FLOWERING

Defoliation impaired the ability of the main stem to add new leaves, but the pattern of damage did not affect leaf addition rates (Fig. 6). Damaged stems (for both whole and half-leaf removal) added fewer new leaves both over the damage period and in the first week following defoliation (Fig. 6).

image

Figure 6. . Effects of defoliation on leaf addition rates of the main stem. Means and standard errors are shown. Significance levels shown are for contrasts following randomized block ANOVA. U vs D, comparison of undamaged to damaged plants (whole-leaf removal and half-leaf removal combined); **P < 0·01; ***P < 0·001.

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Defoliation had strong effects on the relative growth rate of the main stem. Stems that were losing leaf area grew at a slower rate over the damage period, and relative growth rates for whole-leaf removal and half-leaf removal stems were similar (Fig. 7, 19–28 June). Differences between whole-leaf removal and half-leaf removal emerged in the first week following defoliation. Damaged stems, with whole-leaf removal and half-leaf removal taken together, were still growing more slowly than undamaged stems (Fig. 7, 28 June–5 July). However, while relative growth rates of whole-leaf removal stems were still well below the controls, half-leaf removal stems had almost recovered to control levels, and this difference was significant. Over the following 2 weeks (5–17 July), damaged stems were growing at a faster rate than undamaged stems and there were no significant differences between whole-leaf removal and half-leaf removal (Fig. 7). Relative growth rates of damaged stems were still elevated above controls for the next 3 weeks (17 July–7 August). Whole-leaf removal stems were growing faster than half-leaf removal stems over this period, but this difference was of marginal significance.

image

Figure 7. . Effects of defoliation on relative growth rates. Means and standard errors are shown. Significance levels shown are for contrasts following randomized block ANOVA. U vs D, comparison of undamaged to damaged plants (whole-leaf removal and half-leaf removal combined); WL vs HL, comparison of whole-leaf removal to half-leaf removal; †P < 0·10; *P < 0·05; **P < 0·01; ***P < 0·001; ****P < 0·0001.

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These differences in relative growth rate led to differences in stem heights (Fig. 8). Damaged stems, with whole-leaf removal and half-leaf removal taken together, were significantly shorter than controls at the end of the damage period (Fig. 8). Heights of damaged stems were still depressed below control levels at both 1 and 3 weeks following damage. The defoliated Goldenrods eventually caught up to the controls but it took them nearly 6 weeks to do so; stem heights of damaged stems did not reach those of undamaged stems until 7 August (Fig. 8). There was some evidence that pattern of damage influenced regrowth after defoliation. While mean heights of whole-leaf removal and half-leaf removal stems were virtually identical at the end of the damage period, half-leaf removal stems were taller than whole-leaf removal stems at both 1 and 3 weeks following defoliation (Fig. 8). The differences between whole-leaf and half-leaf removal were only marginally significant; however, this pattern is consistent with the elevated relative growth rate seen for half-leaf removal plants in the first week post-damage.

image

Figure 8. . Effects of defoliation on main stem heights. Means and standard errors are shown. Significance levels shown are for contrasts following randomized block ANOVA. Stem heights were ln-transformed prior to analysis. Note that although the treatment means are very close to each other on some dates, block effects were highly significant in these analyses, and inclusion of block removed much of the variation. U vs D, comparison of undamaged to damaged plants (whole-leaf removal and half-leaf removal combined); WL vs HL, comparison of whole-leaf removal to half-leaf removal; †P < 0·10; *P < 0·05; **P < 0·01; ***P < 0·001; ****P < 0·0001.

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In contrast to the strong effects of defoliation on growth of the main stem, lateral stems were generally unaffected by damage. Defoliation did not influence either the number of lateral stems or their mean heights (P > 0·10 for defoliation main effect and interaction in repeated measures ANOVA). Across all treatments, the Goldenrods had an average of 4·5 lateral stems on 28 June (SE = 0·19), with a mean height of 17·2 cm (SE = 0·90). By 7 August, on average the plants had 5·5 lateral stems (SE = 0·23) and their mean height had increased to 73·3 cm (SE = 1·89).

Defoliation reduced flower production of the main stem (Fig. 9). Both whole-leaf removal and half-leaf removal stems had inflorescences that were about 30% smaller than undamaged stems and the pattern of damage had no significant effect. Flowering of the lateral stems, which were undamaged on all plants, was not affected by defoliation (Fig. 9). There were no overall effects of damage or differences owing to the pattern of damage for lateral stem inflorescence mass.

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Figure 9. . Effects of defoliation on inflorescence mass. Means and standard errors are shown. Significance levels shown are for contrasts following randomized block ANOVA. U vs D, comparison of undamaged to damaged plants (whole-leaf removal and half-leaf removal combined); *P < 0·05.

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Discussion

  1. Top of page
  2. Abstract
  3. Introduction
  4. Materials and methods
  5. Results
  6. Discussion
  7. Acknowledgements
  8. References

The prediction that dispersed damage is more likely to result in compensatory photosynthesis than concentrated damage because all developing leaves retain vascular connections to functional source leaves was supported by the results of this experiment. Plants with half-leaf removal, but not whole-leaf removal, showed enhanced mass-based photosynthesis for the remaining, undamaged leaf at the end of the damage period. However, the pattern of damage only influenced photosynthesis at the end of the damage period, when defoliation was completed and regrowth was just beginning. Dispersed and concentrated damage had similar effects on photosynthesis for measurements taken on regrowth leaves, after defoliated plants had time to partially restore their leaf area. These results suggest that source–sink interactions were important in generating the difference between dispersed and concentrated damage at the end of the damage period. If defoliation acts to free the plant from internal constraints imposed by the accumulation of assimilate within the leaf, then compensatory photosynthesis would be expected when the ratio between sources and sinks was most reduced for damaged plants.

Source–sink interactions alone, however, do not seem sufficient to explain the effects of damage on photosynthesis in this experiment. Damage-induced increases in photosynthetic rate were strongest for regrowth leaves measured at 16 days post-damage; this was true for both half-leaf removal and whole-leaf removal plants. If reduced source–sink ratios were the primary influence on photosynthetic rates, then compensatory photosynthesis should have been maximal at the end of the damage period, when source area was most reduced relative to sinks. In addition, higher photosynthetic rates of defoliated plants were accompanied by increased stomatal conductance. The enhanced photosynthesis of regrowth leaves for both half-leaf and whole-leaf removal seemed to result from delayed leaf senescence, because damaged plants did not show the same decline in photosynthesis from 7 to 16 days post-defoliation as was seen for controls. This delayed leaf senescence could have resulted from damage-induced hormonal changes. Defoliation can reduce competition between leaves for root-derived cytokinins (Wareing, Khalifa & Treharne 1968; Satoh, Kriedemann & Loveys 1977; Welter 1989); cytokinins can both delay leaf senescence (Salisbury & Ross 1985) and promote stomatal opening (Meidner 1969). While it has been suggested that defoliation may improve plant water status (McNaughton 1983), it seems unlikely that higher stomatal conductance was a result of improved water status in the experiment reported here because plants were kept well-watered, particularly prior to gas-exchange measurements.

Compensatory photosynthesis has not previously been reported for S. altissima, even though two studies have investigated gas exchange of this species following herbivore damage (Schmid et al. 1988; Meyer & Whitlow 1992). Meyer & Whitlow (1992) did not follow regrowth leaves over time; they might have detected enhanced photosynthetic rates on damaged plants if measurements had extended over a longer period. Schmid et al. (1988) had low statistical power to detect differences owing to high variability between samples. They did find that defoliated plants had higher stomatal conductance, which is consistent with the results of the present study.

The second prediction, that compensatory photosynthesis is more likely in undamaged leaves than damaged leaves, was also supported by the results of this experiment. Enhanced mass-based photosynthesis was observed in undamaged leaves remaining after defoliation and both area-based and mass-based photosynthesis were increased by damage for regrowth leaves, while damaged leaves remaining after defoliation showed no changes in either area-based or mass-based photosynthesis. There was no evidence that damage to the leaf itself inhibited photosynthesis, thus half-leaf removal plants did not suffer from having damage spread across all of their leaves. Whether or not damage to the leaf itself impairs photosynthesis appears to be related to the degree of wounding (Hall & Ferree 1976; Morrison & Reekie 1995). Compensatory photosynthesis has been observed in damaged leaves, even with 50% leaf area loss (Morrison & Reekie 1995; G.A. Meyer, unpublished data).

The third prediction, that plants should recover more readily from dispersed damage than concentrated damage, was partially supported by this experiment. Half-leaf removal plants grew faster than whole-leaf removal plants in the first week following defoliation, but differences between concentrated and dispersed damage disappeared by the end of the season. Both half-leaf removal stems and whole-leaf removal stems reached heights comparable to controls by 6 weeks post-defoliation, and flowering of the main stem was reduced by a similar amount by both types of damage. The faster growth of half-leaf removal plants immediately following defoliation is consistent with the higher mass-based photosynthetic rates of remaining leaves at the end of the damage period. However, enhanced photosynthetic rates on half-leaf removal plants were only seen for undamaged leaves. Because all leaves except for the single measurement leaf were damaged on half-leaf removal plants, it is not clear how much compensatory photosynthesis contributed to their regrowth.

The section of the leaf from which leaf area was removed could have influenced plant recovery from defoliation. Half-leaf removal plants lost leaf area only from the distal half of the leaf, while damaged leaves on whole-leaf removal plants lost leaf area throughout the leaf. The rate of development varies within a leaf; for plants with simple leaves, the tip often matures and ceases leaf expansion before the base (Dickson & Isebrands 1991). Loss of leaf area from the base of an expanding leaf can have a greater impact on plant growth than the removal of an equivalent amount from the tip (Coleman & Leonard 1995). When leaves have matured, leaf area removal from the base and the tip of leaves have similar effects on plants (Coleman & Leonard 1995). Photosynthetic rates may also vary within leaves; Morrison & Reekie (1995) showed that the leaf mid-section had a higher photosynthetic rate than the base or tip. Intraleaf variation in photosynthetic rate could explain the faster growth rates of half-leaf removal stems if the basal portions of leaves had higher photosynthetic rates than the tips.

Differences between concentrated and dispersed damage may be more pronounced if the plants are grown in the field, where they would be subject to competition from other plants (Lee & Bazazz 1980; Cottam, Whittaker & Malloch 1986; Maschinski & Whitham 1989; Hjalten, Danell & Ericson 1993; Fay, Hartnett & Knapp 1996). The slower relative growth rates of defoliated shoots both during and immediately following the damage period could have translated into much greater reductions in height and flowering than were seen in this experiment if there had been competing plants nearby. Half-leaf removal stems might have outperformed whole-leaf removal stems in terms of end-of-season height and flowering in a field situation, because their higher relative growth rates in the first week post-damage could have given them a much greater advantage in the field than was the case here.

The results of the present study add to accumulating evidence that leaf area loss dispersed across many leaves is less harmful to plants than the same level of defoliation applied to fewer leaves. This has been found both for damage distributed over the crown compared with damage concentrated on a single branch in woody species (Marquis 1992) and for damage spread over all leaves compared with damage on fewer leaves for tree seedlings (Lowman 1982) and herbaceous species (Mauricio et al. 1993). The opposite result, that concentrated damage is less detrimental than dispersed damage, was reported by Wit (1982) in a study on Brussels Sprouts. However, in Wit’s experiment, leaf area was removed only from the top leaves of the plants for concentrated damage, while all leaves lost leaf area for dispersed damage. The dispersion of damage is thus confounded with the age of the leaf tissue that was lost. The effects of defoliation on plants can depend strongly on whether old leaves or young leaves are removed (e.g. Gold & Caldwell 1989; Harper 1989). Why the pattern of damage should matter to plants is still not fully understood, especially for herbaceous plants. Factors believed to be important include how leaf area loss is distributed across orthostichies and the degree of carbon movement between orthostichies (review by Marquis 1996). The differences seen between concentrated and dispersed damage in photosynthetic rate at the end of the damage period in the present study suggest that physiological responses of leaves may also play a role, and this area deserves further investigation. While more work with a greater variety of plants is needed, it is clear that the pattern of damage must be considered when assessing herbivore impacts on plants.

Acknowledgements

  1. Top of page
  2. Abstract
  3. Introduction
  4. Materials and methods
  5. Results
  6. Discussion
  7. Acknowledgements
  8. References

I thank Matthew Bachtold for help in carrying out the experiment and Colin Orians for comments that improved the manuscript.

References

  1. Top of page
  2. Abstract
  3. Introduction
  4. Materials and methods
  5. Results
  6. Discussion
  7. Acknowledgements
  8. References
  • 1
    Coleman, J.S. & Leonard, A.S. (1995) Why it matters where on a leaf a folivore feeds. Oecologia 12, 324328.
  • 2
    Cottam, D.A., Whittaker, J.B., Malloch, A.J.C. (1986) The effects of chrysomelid beetle grazing and plant competition on the growth of Rumex obtusifolius. Oecologia 12, 452456.
  • 3
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