ORIGINAL ARTICLE OA
Functional
Ecology 1998
12, 270–279
000
EN
Pattern of defoliation and its effect on photosynthesis
and growth of Goldenrod
G. A. MEYER
Department of Biology, Williams College, Williamstown, MA 01267, USA
Summary
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.
Key-words: Compensatory photosynthesis, concentrated damage, dispersed damage, herbivory, Solidago
altissima
Functional Ecology (1998) 12, 270–279
Introduction
© 1998 British
Ecological Society
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
270
271
Effects of
defoliation on
Goldenrod
© 1998 British
Ecological Society,
Functional Ecology,
12, 270–279
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, KolodnyHirsch & 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 inves-
tigated 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
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
272
G. A. Meyer
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
© 1998 British
Ecological Society,
Functional Ecology,
12, 270–279
above the twist ties as the stems grew. The first and second leaves above the lower twist tie were used for gasexchange 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.
Photosynthetic rate and stomatal conductance were
measured using a Li-Cor 6200 portable photosynthesis system equipped with a quarter-litre chamber (LiCor 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
Fig. 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 gasexchange 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.
273
Effects of
defoliation on
Goldenrod
wavelength of 670 nm and because there is no infrared 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 gasexchange 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
EFFECTS OF DAMAGE ON GAS EXCHANGE
© 1998 British
Ecological Society,
Functional Ecology,
12, 270–279
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 equiv-
Fig. 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 A N O VA . U vs D, comparison of undamaged to damaged plants (whole-leaf removal
and half-leaf removal combined); † P < 0·10; ** P < 0·01.
alent to controls for both whole-leaf removal and halfleaf 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.
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 halfleaf removal plants showed photosynthetic rates per
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 wholeleaf removal plants were similar to controls (Fig. 4,
leaf 2). For regrowth leaves measured at 16 days postdefoliation, 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
274
G. A. Meyer
Fig. 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 A N O VA . U vs D, comparison of undamaged to damaged plants (whole-leaf removal
and half-leaf removal combined); † P < 0·10; ** P < 0·01.
© 1998 British
Ecological Society,
Functional Ecology,
12, 270–279
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.
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).
Fig. 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 A N O VA . 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.
275
Effects of
defoliation on
Goldenrod
Fig. 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 (wholeleaf removal and half-leaf removal combined); * P < 0·05;
** P < 0·01.
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.
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
above the controls (18% and 27% increase for wholeleaf removal and half-leaf removal, respectively).
Although half-leaf removal plants had higher massbased photosynthetic rates than whole-leaf removal
plants for both regrowth leaves, these differences
were not significant.
EFFECTS OF DAMAGE ON GROWTH AND FLOWERING
© 1998 British
Ecological Society,
Functional Ecology,
12, 270–279
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).
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
Fig. 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 A N O VA . U vs D, comparison of undamaged
to damaged plants (whole-leaf removal and half-leaf
removal combined); ** P < 0·01; *** P < 0·001.
276
G. A. Meyer
(Fig. 8). The differences between whole-leaf and halfleaf 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.
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 A N O VA ). 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.
Discussion
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
Fig. 7. Effects of defoliation on relative growth rates. Means and standard errors are
shown. Significance levels shown are for contrasts following randomized block
A N O VA . 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.
Fig. 8. Effects of defoliation on main stem heights. Means and
standard errors are shown. Significance levels shown are for
contrasts following randomized block A N O VA . 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.
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 wholeleaf 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.
277
Effects of
defoliation on
Goldenrod
Fig. 9. Effects of defoliation on inflorescence mass. Means
and standard errors are shown. Significance levels shown
are for contrasts following randomized block A N O VA . U vs
D, comparison of undamaged to damaged plants (whole-leaf
removal and half-leaf removal combined); * P < 0·05.
© 1998 British
Ecological Society,
Functional Ecology,
12, 270–279
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 gasexchange 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 photosynthe-
sis 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 areabased 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 midsection 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.
278
G. A. Meyer
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
© 1998 British
Ecological Society,
Functional Ecology,
12, 270–279
I thank Matthew Bachtold for help in carrying out the
experiment and Colin Orians for comments that
improved the manuscript.
References
Coleman, J.S. & Leonard, A.S. (1995) Why it matters where
on a leaf a folivore feeds. Oecologia 101, 324–328.
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 70,
452–456.
Dickson, R.E. & Isebrands, J.G. (1991) Leaves as regulators
of stress response. Response of Plants to Multiple Stresses
(eds H. A. Mooney, W. E. Winner & E. J. Pell), pp. 3–34.
Academic Press, New York.
Edwards, P.J. & Wratten, S.D. (1983) Wound induced
defenses in plants and their consequences for patterns of
insect grazing. Oecologia 59, 88–93.
Fay, P.A., Hartnett, D.C. & Knapp, A.K. (1996) Plant tolerance of gall-insect attack and gall-insect performance.
Ecology 77, 521–534.
Gold, W.G. & Caldwell, M.M. (1989) The effects of the spatial pattern of defoliation on regrowth of a tussock grass.
1. Growth responses. Oecologia 80, 289–296.
Hall, F.R. & Ferree, D.C. (1976) Effects of insect injury simulation on photosynthesis of apple leaves. Journal of
Economic Entomology 69, 245–248.
Harper, J.L. (1989) The value of a leaf. Oecologia 80,
53–58.
Heinrich, B. (1993) How avian predators constrain caterpillar foraging. Caterpillars. Ecological and Evolutionary
Constraints on Foraging (eds N. E. Stamp & T. M.
Casey), pp. 224–247. Chapman and Hall, New York.
Hjalten, J., Danell, K. & Ericson, L. (1993) Effects of simulated herbivory and intraspecific competition on the compensatory ability of birches. Ecology 74, 1136–1142.
Honkanen, T. & Haukioja, E. (1994) Why does a branch suffer more after branch-wide than after tree-wide defoliation? Oikos 71, 441–450.
Lee, T.D. & Bazazz, F.A. (1980) Effects of defoliation and
competition on growth and reproduction in the annual plant
Abutilon theophrasti. Journal of Ecology 68, 813–821.
Lowman, M.D. (1982) Effects of different rates and methods
of leaf area removal on rain forest seedlings of coachwood (Ceratopetalum apetalum). Australian Journal of
Botany 30, 477–483.
McNaughton, S.J. (1983) Compensatory plant growth as a
response to herbivory. Oikos 40, 329–336.
Marquis, R.J. (1988) Intra-crown variation in leaf herbivory
and seed production in striped maple, Acer pensylvanicum L. (Aceraceae). Oecologia 77, 51–55.
Marquis, R.J. (1992) A bite is a bite is a bite? Constraints on
response to folivory in Piper arieianum (Piperaceae).
Ecology 73, 143–152.
Marquis, R.J. (1996) Plant architecture, sectoriality and
plant tolerance to herbivores. Vegetatio 127, 85–97.
Maschinski, J. & Whitham, T.G. (1989) The continuum of
plant responses to herbivory: the influence of plant association, nutrient availability, and timing. American
Naturalist 134, 1–19.
Mauricio, R. & Bowers, M.D. (1990) Do caterpillars disperse their damage? Larval foraging behavior of two specialist herbivores, Euphydryas phaeton (Nymphalidae)
and Pieris rapae (Pieridae). Ecological Entomology 15,
153–161.
Mauricio, R., Bowers, M.D. & Bazzaz, F.A. (1993) Pattern
of leaf damage affects fitness of the annual plant
Raphanus sativus. Ecology 74, 2066–2071.
Meidner, H. (1969) Rate limiting resistances and photosynthesis. Nature 222, 876–877.
Melville, M.R. & Morton, J.K. (1982) A biosystematic
study of the Solidago canadensis (Compositae) complex.
I. Ontario populations. Canadian Journal of Botany 60,
976–997.
279
Effects of
defoliation on
Goldenrod
© 1998 British
Ecological Society,
Functional Ecology,
12, 270–279
Meyer, G.A. & Root, R.B. (1993) Effects of herbivorous
insects and soil fertility on reproduction of goldenrod.
Ecology 74, 1101–1116.
Meyer, G.A. & Whitlow, T.H. (1992) Effects of leaf and sap
feeding insects on photosynthetic rates of goldenrod.
Oecologia 92, 480–489.
Mooney, H.A. & Chiariello, N.R. (1984) The study of plant
function: the plant as a balanced system. Perspectives on
Plant Population Ecology (eds R. Dirzo & J. Sarukhan),
pp. 305–323. Sinauer Associates, Sunderland, MA.
Morrison, K.D. & Reekie, E.G. (1995) Pattern of defoliation
and its effect on photosynthetic capacity in Oenothera
biennis. Journal of Ecology 83, 759–767.
Nowak, R.S. & Caldwell, M.M. (1984) A test of compensatory photosynthesis in the field: implications for herbivory tolerance. Oecologia 61, 311–318.
Root, R.B. (1996) Herbivore pressure on goldenrods
(Solidago altissima): its variation and cumulative effects.
Ecology 77, 1074–1087.
Root, R.B. & Cappuccino, N. (1992) Patterns in population
change and the organization of the insect community
associated with goldenrod. Ecological Monographs 62,
393–420.
Rosenthal, J.P. & Kotanen, P.M. (1994) Terrestrial plant tolerance to herbivory. Trends in Ecology and Evolution 9,
145–148.
Salisbury, F.B. & Ross, C.W. (1985) Plant Physiology.
Wadsworth Publishing Company, Belmont, CA.
Satoh, M., Kriedemann, P.E. & Loveys, B.R. (1977)
Changes in photosynthetic activity and related processes
following decapitation in mulberry trees. Physiologia
Plantarum 41, 203–210.
Schmid, B., Puttick, G.M., Burgess, K.H. & Bazzaz, F.A.
(1988) Clonal integration and effects of simulated herbivory in old-field perennials. Oecologia 75, 465–471.
Semple, J.C. & Ringius, G.S. (1983) Goldenrods of Ontario:
Solidago and Euthamia. University of Waterloo Biology
Series no. 26, Waterloo, Ont., Canada.
Stephenson, A.G. (1980) Fruit set, herbivory, fruit reduction,
and the fruiting strategy of Catalpa speciosa. Ecology 61,
57–64.
Tennessen, D.J., Singsaas, E.L. & Sharkey, T.D. (1994)
Light-emitting diodes as a light source for photosynthesis
research. Photosynthesis Research 39, 85–92.
Trumble, J.T., Kolodny-Hirsch, D.M. & Ting, I.P. (1993)
Plant compensation for arthropod herbivory. Annual
Review of Entomology 38, 93–119.
Wareing, P.F., Khalifa, M.M. & Treharne, K.J. (1968) Ratelimiting processes in photosynthesis at saturating light
intensities. Nature 220, 453–457.
Watson, M.A. & Casper, B.B. (1984) Morphogenetic constraints on patterns of carbon distribution in plants. Annals
of Reviews of Ecology and Systematics 15, 233–258.
Welter, S.C. (1989) Arthropod impact on plant gas
exchange. Insect–Plant Interactions, vol. 1 (ed. E. A.
Bernays), pp. 135–150. CRC Press, Boca Raton, FL.
Werner, P.A., Bradbury, I.K. & Gross, R.S. (1980) The biology of Canadian weeds. 45. Solidago canadensis L.
Canadian Journal of Plant Science 60, 1393–1409.
Wisdom, C.S., Crawford, C.S. & Aldon, E.F. (1989)
Influence of insect herbivory on photosynthetic area and
reproduction in Gutierrezia species. Journal of Ecology
77, 685–692.
Wit, A.K.H. (1982) The relation between artificial defoliation and yield in Brussels sprouts as a method to assess
the quantitative damage induced by leaf-eating insects.
Zeitschrift fur Angewandte Entomologie 94, 425–431.
Received 6 January 1997; revised 29 April 1997; accepted 9
May 1997