Southwestern Association of Naturalists
Variable Budbreak and Insect Folivory of Gambel Oak (Quercus gambelii: Fagaceae)
Author(s): Stanley H. Faeth and Robert F. Rooney, III
Source: The Southwestern Naturalist, Vol. 38, No. 1 (Mar., 1993), pp. 1-8
Published by: Southwestern Association of Naturalists
Stable URL: http://www.jstor.org/stable/3671636
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MARCH
MARCH 1993
1993
SOUTHWESTERNNATURALIST
THE
NATURALIST 38(1):1-8
38(1):1-8
THESOUTHWESTERN
VARIABLE BUDBREAK AND INSECT FOLIVORY OF GAMBEL
OAK (QUERCUS GAMBELH: FAGACEAE)
STANLEY H. FAETH AND ROBERT F. ROONEY, III
Department of Zoology, Arizona State University, Tempe, Arizona 85287-1501
ABSTRACT-Budbreak
of individualrametsof clonal Gambeloak (Quercusgambelii:Fagaceae)was
advancedexperimentallyto test the effects of altered timing of budbreakand hence, leaf age, on
patternsof folivory.Early-seasonfolivoryby leaf-chewinginsectswas significantlygreateron younger
leavesof controlrametsthan older leavesof experimentalramets.However,differencesin cumulative
folivory between control and experimentalramets disappearedby the end of the growing season.
Colonizationby three species of late-season leafminerswas also unaffectedby altered budbreak,
indicatingthe impact of altered budbreakon folivoresis concentratedearly in the growing season.
Analysesof nutritionaland allelochemicalcontentof experimentaland controlrametscorrespondto
the patternsof folivory;leavesof experimentalrametswere significantlyhigherin gallotannincontent
than leaves of controlramets,but these differencesalso waned by the middleof the growingseason.
Our resultssuggestthat variablebudbreakcan alter degreeof folivoryon Gambeloak, but only early
in the growingseason.The evolutionaryimplicationsof, and constraintson, variationin budbreakin
woody plants are discussed.
Many folivorous insect species that feed on
deciduous or semi-evergreen trees prefer and perform better on younger leaves than old ones (e.g.,
Feeny, 1970; Rockwood, 1974; Schweitzer, 1979;
Cates, 1980; Rauscher, 1981; Kraft and Denno,
1982; Coley, 1980; Niemela and Haukioja, 1982;
Niemela et al., 1982; Fowler and Lawton, 1984).
As leaves age, they change in surface area, water
content, toughness, thickness, chemical composition and nutritional quality (Feeny, 1970;
Crawley, 1983; Raupp and Denno, 1983; Coley,
1980; Faeth, 1985a). Therefore, the synchrony
between budbreak of host trees and folivore emergence from overwintering stages is critical to folivore success. Insects that emerge too early may
starve (Futuyma and Wasserman, 1980; Hunter,
1990), while insects that emerge too late may
encounter a suboptimal food source (Embree,
1965; Feeny, 1970, 1976).
Variation in timing of budbreak often occurs
within populations of trees. For example, pedunculate oak (Quercus robur) trees vary in timing
of budbreak by as much as two weeks within a
given locality (Feeny, 1970). Because timing of
budbreak is at least partly determined by genetic
factors (Kramer and Kozlowski, 1979), variation
in time of budbreak has been considered a plant
defense against folivores, similar to other variable
plant characteristics such as allelochemistry, nu-
trition, and morphology (Haukioja et al., 1985;
Tuomi et al., 1989). Despite the potential of variable budbreak in altering folivore abundances on
trees, relatively few studies of herbivore-plant interactions have focused on this plant trait. Those
studies that have, have produced conflicting results. Feeny (1976) concluded that early or late
flushing oaks harbor fewer insects than the population in general. Defoliated branches of mountain birch (Betula pubescens ssp. tortuosa) break
bud later in the following year, and Tuomi et al.
(1989) hypothesized that these branches should
have less herbivory than branches that flush leaves
earlier. Similarly, late breaking holly oaks (Quercus ilex) had less herbivory from the folivore Tortrix viridanathan early breaking trees (Du Merle,
1988). In contrast, experimentally retarded,
younger foliage of Betulapubescens had more herbivory than older, control foliage (Fowler and
Lawton, 1984). Also, tropical plants with late,
asynchronous leaf flush typically have higher rates
of herbivory (Rockwood, 1974; Lieberman and
Lieberman, 1984; Aide, 1988).
We tested the influence of variable budbreak
on folivory by advancing the timing of budbreak
experimentally within clones of Gambel's oak
(Quercus gambelii Nutt.). Since spring folivores
generally prefer and perform better on younger
leaves than older leaves, presumably because of
2
The Southwestern Naturalist
TABLE 1-Budbreak phenology of experimental (E)
and control (C) ramets.
Difference
Tree
Exposure
1
1
1
1
N
S
E
W
16
16
16
16
April
April
April
April
30
30
30
30
April
April
April
April
14
14
14
14
days
days
days
days
2
2
2
2
N
S
E
W
26
30
26
26
April
April
April
April
5
5
5
5
May
May
May
May
9
5
9
9
days
days
days
days
3
3
3
3
N
S
E
W
30
30
30
30
April
April
April
April
15
15
15
15
May
May
May
May
15
15
15
15
days
days
days
days
4
4
N
S
26 April
30 April
12 May
12 May
16 days
12 days
26 April
12 May
16 days
4
Eb
4
W
(E)
(C)
a Mean difference in budbreak between experiment
(E) and control (C) ramets = 12.8 ? 3.28 days.
b
Ramet 4EX was destroyed by snow on 17 April,
1988.
lower amounts of allelochemicals and degree of
toughness and higher amounts of nutrients (Feeny,
1970), we predicted that older leaves produced
by early leaf flush should have lower rates of
folivory than control (normal budbreak) leaves.
We monitored nutrition (protein) and allelochemistry (tannins) to determine phytochemical
differences between advanced and control leaves
that might explain any differences in folivory.
We also examined the distribution of late-season
leaf-mining insects to determine whether differ
ences in the advanced experimental leaves and
the younger control leaves persist for late-season
folivores.
MATERIALS AND METHODS-Experiments and observations were conducted on clones of Gambel oak
(Quercusgambelii) at Aztec Peak (2,225 m elevation),
Tonto National Forest, Gila County, Arizona, from
March 1988 to November 1988. The study site is an
open canopy mixed woodland dominated by mixed oak
(Quercusgambelii and Quercusarizonica), Arizona walnut (Juglans major), ponderosa pine (Pinus ponderosa),
Douglas fir (Pseudotsuga taxifolia), and quaking aspen
(Populus tremuloides). Clearcutting of the study area
in 1959 and subsequent regrowth of Gambel's oak has
resulted in genets with oldest ramets of approximately
uniform age, although rootstock age is unknown.
vol. 38. no. 1
Typical leaf flush of Gambel's oak at Aztec Peak
occurs in late April to early May. Most leaves remain
on trees until late September to early November. No
secondary leaf flush occurred on the study genets during the course of this study. Most leaves abscise by
mid-November, although some senesced leaves remain
on the ramet until budbreak in the following spring.
Gambel oak exists in clones (genets) composed of many
individual shoots (ramets), connected to the same root
system. By using clones, we could manipulate budbreak
of adult trees in the field, while controlling for genetic
variability between treatment and control ramets in
resistance to folivory.
To advance budbreak, four genets of Gambel's oak
were selected on the basis of similar size (approximately 10 m in height and 10 m in diameter) and
exposure (level ground in full sunlight). All genets were
apparently healthy and located within a 300-m radius.
Clonal Gambel's oak in this area grows as large, distinct genets composed of 10-50 ramets, which range
from less than 1 m to over 10 m in height. Study genets
were divided into four quadrants corresponding to the
four cardinal compass points to account for variation
in budbreak within clones due to different sun exposure. One experimental and one control ramet were
selected randomly from the pool of ramets within quadrants of approximately 1.5-3 m in height and not more
than 2 m from the outermost ramets, giving a total of
16 control and 16 experimental ramets.
On 29 March 1988, all experimental ramets were
enclosed in 1 m x 2 m bags of 2.5 mm thick polyethylene to increase temperatures sufficiently to induce
early budbreak. All enclosed and control ramets were
inspected twice weekly for time of budbreak. Bags were
removed from experimental ramets when the control
ramet from paired controls broke bud, so that exposure
time to folivores was equivalent on experimental and
control ramets. The experimental ramets broke bud an
average of 12.8 (+3.28) days earlier than the control
ramets (Table 1). Some frost damage was recorded on
the experimental ramets of Trees 1 and 2 on 12 May,
resulting in the loss of some leaves. A late snowstorm
on 17 April resulted in the loss of ramet 4EX due to
breakage caused by accumulation of snow on the bag.
Ramet 4EX was therefore treated as a missing value
in all statistical analyses. The frost damage to Trees 1
and 2 was ignored since loss of leaves was minimal.
Leaves were scored for leaf-chewing insect damage
on 29 May, 7 July, and 5 August 1988. All damage
estimates were cumulative. For ramets with fewer than
400 leaves, all leaves were examined for presence or
absence of damage. Leaves on ramets with >400 leaves
were sampled haphazardly until approximately 5075% of the leaves had been examined. Sucking insect
damage was not included; we recognize that sucking
insects may be important herbivores, but estimation of
the impact of sucking insects was beyond the scope of
this study.
March 1993
Faeth and Rooney-Budbreakand insectfolivory
Beginning on 26 September 1988, leaves about ready
to abscise were collected from each ramet. Any leaf
exhibiting a change in color was pulled lightly and
collected only if it broke at the abscission zone. If the
leaf could not be detached by light pressure then the
leaf was left on the tree until the next biweekly sample.
This process was repeated until all leaves were collected from each ramet. After each collection, leaves
were taken to the lab, pressed and air dried. Leaves
were then examined to determine total amounts of leafchewing insect damage. We estimated the percent leaf
area removed (LAR) by leaf chewers, with leaves assigned to the following damage level categories: <10%
LAR, 10-25% LAR, 25-50% LAR and 50+% LAR.
A length measurement taken from leaf base to distal
end was used to estimate total leaf area. Simple regression of leaf length on leaf area (n = 200) accounted
for 96.5% of the variability in leaf area (regression
equation; AreaI'2= 0.05(length) + 0.23 where area is
measured in square centimeters and length is measured
in millimeters).
The leaf-chewing insects that we observed feeding
on Gambel's oak were primarily Lepidoptera (Arctiidae, Noctuiidae, Geometridae, Stenomidae and Tortricidae), and Coleoptera (Chrysomelidae and Curculionidae). Leaf damage by these folivores occurs
mainly early in the growing season although lesser
amounts of leaf-chewing insect damage occur throughout the growing season.
Leaves collected from experimental and control ramets were also examined for the presence of four leafmining species that occur on Gambel's oak, Coptodisca
sp. (Lepidoptera: Heliozelidae), Stigmella sp. (Lepidoptera: Nepticulidae), Cameraria sp. (Lepidoptera:
Gracillariidae), and Phyllonorycter sp. (Lepidoptera:
Gracillariidae). All of these miners are primarily late
season feeders (Rooney, 1989), appearing in July, although a few individuals of Stigmella were observed
earlier in the season. Individuals of Coptodiscasp. appeared on only one of 16 ramets and therefore were
excluded from analyses.
Leaves for phytochemical analyses were collected
from control and experimental ramets when the control
ramets broke bud. Leaves from experimental and control ramets were then sampled at mid-season and late
season. At each interval, a haphazard sample of undamaged leaves was removed from each ramet and
placed immediately on dry ice for transportation back
to the lab. Wet weights were taken, and leaves were
then lyophilized and re-weighed to obtain dry weights.
Leaves were then ground in a Wiley mill in preparation
for phytochemical analyses. Ground leaf samples were
stored in tightly capped bottles in a 5?C cold room until
phytochemical analyses could be performed. All analyses were performed in triplicate and the readings averaged to minimize experimental error.
Total protein content of ground lyophilized leaf samples was analyzed using the BioRad Method (Rich-
3
mond, California) to determine whether there were
significant differences between treatments and among
trees. Condensed tannins were determined by using a
modified acidified vanillin method (Broadhurst and
Jones, 1978). Hydrolyzable tannin concentrations were
determined using a modified iodate technique (BateSmith, 1977) and are expressed as percent dry mass
tannic acid equivalents (TAE) as compared to a tannic
acid standard curve prepared for each run. See Faeth
(1986, 1990) for a more detailed description of all
phytochemical analyses.
We used a repeated measures ANOVA (SAS GLM
facility, SAS Institute, Cary, North Carolina) with
treatments nested within trees and ramets nested within
treatments to analyze cumulative damage (arcsine
squareroot transformed) by leaf-chewing and leaf mining insects. Quadrant was not used as a factor in the
statistical analyses because budbreak within clones was
almost invariant with respect to sun exposure (Table
1). A missing value generated by the loss of ramet 4EX
resulted in an unbalanced experimental design.
A similar repeated measures nested ANOVA (Winer, 1971) was used to test for differences among trees
and between treatments in concentrations of hydrolyzable tannins and protein (arcsine squareroot transformed) in leaves collected on three dates during the
season. Analyses of condensed tannins showed concentrations near zero for the three sample dates and these
data were therefore not statistically analyzed.
RESULTS-Experimental
(older) leaves had less
damage early in the season than did control
(younger) leaves (Fig. 1, significant treatment effect, F = 47.13, d.f. = 1,24, P < 0.0001). Leafchewing damage also varied significantly among
trees (F= 115.13, d.f. = 3,24, P < 0.0001). Most
leaves of both experimental and control ramets
were damaged early in the season (significant
effect of time, F= 301.93, df. = 3,72, P < 0.0001),
with the rate of damage to leaves previously undamaged decreasing as the season progressed (Fig.
1). However, as the season progressed, cumulative differences in leaf-chewing insect damage levels between experimental and control leaves diminished. The cumulative amount of LAR at the
end of the growing season was not significantly
different between experimental and control ramets (X2 for means = 0.55, df. = 3, P > 0.90).
In both treatments, approximately 90% of leaves
damaged by leaf-chewing insects had less than
10% of their leaf area removed (Fig. 2).
Proportions of leaves mined by Stigmella sp.,
Cameraria sp., Phyllonorycter sp. leafminers did
not vary significantly between treatments (Stigmella sp., F= 2.02, d.f. = 1,7, P= 0.17, Cameraria
4
The Southwestern Naturalist
100
C1
Qw
LJ
90 -so
60
* CONTROL
* EXPERIMENTAL
z
z
z
80I
70 -
U,
CtD
60-
LI-J
m
50 -
s
vol. 38, no. 1
N
40 -
0
z
30-
I
0
20 -
m
0I
10 -
0
* CONTROL
* EXPERIMENTAL
50403020 -
10 0
JUN
JUL
AUG
SEP
OCT
i
JUNE
SAMPLEDATE
i
JULY
i
i
AUGUST
SAMPLEDATE
FIG. 1-Percentage of experimental and control leaves
damaged as a function of time. Each point is the mean
for all ramets in each treatment, weighted by the number of leaves on each ramet, ?SE.
sp., F = 0.32, d.f. = 1,7, P = 0.58; Phyllonorycter
sp., F = 3.34, d.f. = 1,7; P = 0.08). Proportion
of leaves mined by Cameraria sp. varied significantly among trees (F = 9.80, d.f. = 3,7, P <
0.001) but proportion of leaves mined by Stig-
mella sp. and Phyllonorycter sp. did not (Stigmella
sp., F = 2.45, d.f. = 3,7, P = 0.08; Phyllonorycter
sp., F = 1.40, d.f. = 3,7, P = 0.26).
Gallotannin concentrations varied significantly
with time (F = 219.76, d.f. = 2,48, P < 0.0001),
between treatments (Fig. 3, F = 16.05, d.f. = 1,24,
P < 0.001), and among clones (F = 6.04, d.f.
3,24, P < 0.01). Most of the differences occurred
on the first sampling date (Fig. 3).
Protein content varied significantly with time
?)
i
FIG. 3-Foliar
gallotannin concentrations (expressed as mean tannic acid equivalents + SE) of experimental and control ramets as a function of time.
(F = 304.11, d.f. = 2,48, P < 0.0001) but did not
=
vary between treatments (Fig. 4, F = 0.10, d.f.
1,24, P > 0.75) or among clones (F = 0.66, d.f.
= 3,24, P > 0.50). Protein content was highest
early in the season, and then declined (Fig. 4).
in the season, younger
DISCUSSION-Early
control leaves of Gambel oak suffered more folivory by leaf-chewing insects than older experimental leaves did. Past studies also show that
many (e.g., Feeny, 1970; Ayres and MacLean,
1987) but not all (e.g., Fowler and Lawton, 1984)
insect species prefer and perform better on younthe
ger foliage. Early-season Macrolepidoptera,
dominant early-season chewing folivores in this
study, typically
prefer young
foliage
(Niemela
loo
7
80
z
w
CL
0
<
60
0
I
40
z
LJ
OU
Y
I.
20
6
H
5
4
z
3
CLi
w
0,
<10%
10-25%
26-50X
2
51-100X
% LEAF AREA REMOVED
FIG. 2-Amount of leaf area removed from experimental and control leaves. Bars are the mean for all
ramets in each treatment, weighted by the number of
leaves on each ramet, +SE.
JUNE
JULY
AUGUST
SAMPLEDATE
FIG. 4-Foliar protein concentration (mean + SE)
of experimental and control ramets as a function of
time.
March 1993
Faeth and Rooney-Budbreakand insectfolivory
and Haukioja, 1982; Fowler and Lawton, 1984).
Variation in folivory between treatments corresponds to foliar quality in terms of tannin content.
Gallotannin content of older, advanced experimental leaves was higher than that of younger
control leaves, at least early in the season.
Folivory by leaf chewers increased on experimental ramets late in the season, so that folivory
differences between treatments eventually disappeared (Fig. 1). Older leaves with less earlyseason damage thus appear more susceptible to
late-season damage than the more heavily-damaged control leaves. Late-season, leaf-chewing insects apparently prefer to feed on previously undamaged leaves. There are several possibilities
for this preference. First, wound-induced changes
in palatability or attractiveness caused by previous insect damage (Edwards and Wratten, 1983,
1985; Gibberd et al., 1988) may explain the preference for previously undamaged leaves. Damage
of individual leaves (Fig. 2) also corroborates this
hypothesis since the amount of leaf area removed
from most damaged leaves was less than 10%,
suggesting that leaf-chewing folivores remove only
small fractions of individual leaves. We did not
examine chemical or physical changes associated
with folivory (only undamaged leaves were analyzed phytochemically), but other studies with
oaks have shown induction of purported allelochemicals with folivory (Schultz and Baldwin,
1982; Faeth, 1986). Second, folivores may avoid
or suffer greater mortality on damaged leaves due
to increased attack by natural enemies that use
visual or chemical cues associated with leaf damage (Heinrich and Collins, 1983; Faeth, 1986;
Faeth and Bultman, 1986). Third, late-season
insects may be specialists on mature, older foliage
(Rhoades and Cates, 1976; Cates 1980) and
therefore prefer older, experimental leaves. This
explanation seems doubtful since, by mid-season,
experimental leaves did not differ from control
leaves phytochemically (Fig. 3) and new foliage
on Gambel's "hardens" within two weeks, long
before late-season folivores begin to feed. Finally,
the apparent preference for undamaged leaves
may simply be an artifact of categorizing leaves
by amount of damage. More than 70% of all
leaves suffer some damage (Fig. 1), and -90%
of these leaves have <10% of area removed (Fig.
2). A previously undamaged leaf slightly chewed
by folivores late in the growing season (e.g., 5%
of leaf area removed) was placed in the same
category (<10% of area removed) as a previously,
but slightly, damaged control leaf (e.g., 4% of
area removed) with the same amount of lateseason damage (4% + 5% = 9%). To determine
whether previously damaged leaves truly escape
additional folivory late in the season, future studies will need to refine damage categories, particularly the <10% category of leaf area consumed.
Colonization by three species of leaf miners in
this study was unaffected by leaves of different
ages. Leaf miners on Gambel oak are predominantly late-season feeders, and most adults oviposit after differences in chemistry and leaf-chewing insect damage between treatments had
disappeared (adult females determine feeding sites
of sedentary larval offspring). Thus, any leaf selection differences between treatments based on
chemistry or previous damage (Faeth, 1985b,
1986) would not be apparent. These results, coupled with those above involving the leaf chewers,
suggest that any impacts of variable budbreak on
folivory are most likely concentrated very early
in the growing season and are not maintained late
into the growing season.
Feeny (1976) proposed that deciduous trees,
such as oaks, in temperate climates may escape
herbivory in time by flushing leaves either earlier
or later than average budbreak of the population.
For example, Du Merle (1988) found that latebreaking trees of two species of oak (Quercuspubescens and Q. ilex) were more resistant to defoliation by the green oak leafroller, Tortrix viridana, than early-breaking trees. Tuomi et al. (1989)
suggested that leaves produced asynchronously
within individual trees also are protected from
early season folivores.
We examined experimentally the relationship
between this latter type of variation in budbreak
(i.e., variation of ramet budbreak within genets)
and folivory. Ramets with advanced leaf flush
had reduced leaf-chewing insect damage early in
the growing season, but cumulative levels of folivory did not differ among treatments. However,
reduction of early-season folivory could still increase plant fitness despite similarities in cumulative folivory between experimental and control ramets because younger foliage is generally
considered to be of greater photosynthetic value
to plants than mature foliage (Feeny, 1970; Levin, 1971).
Variability in timing of budbreak also occurs
among clones of Gambel oak (Table 1, budbreak
of controls). If early budbreak can reduce folivory
by insects, then why don't trees of Gambel oak
6
vol. 38, no. 1
The SouthwesternNaturalist
advance budbreak to that of experimental ramets? In addition to escaping early season folivory, early budbreak also lengthens the growing
season. Advancing budbreak in temperate deciduous forests is, however, constrained by environmental factors such as photoperiod, temperature
and moisture availability (Feeny, 1976; Kramer
and Kozlowski, 1979; Fitter and Hay, 1987).
Buds that break too early are susceptible to late
frosts and snows. For example, the loss of the
enclosed ramet 4EX was due to late snow at Aztec
Peak and some experimental leaves were lost to
frost damage on enclosed, experimental ramets of
clones 1 and 2. Young leaves exposed to frost or
snow are usually damaged severely or abscised
(Kramer and Kozlowski, 1979). Thus, early budbreak would increase plant fitness only if the
increased risk of frost damage is outweighed by
benefits of reduced folivory and longer growing
season. Stochastic abiotic factors such as late frosts
may select for later budbreak while escape from
early-season folivores and increasing length of the
growing season may select for early budbreak
(Feeny, 1976). The mean time of budbreak in
populations of Gambel's oak may be therefore a
result of stabilizing selection from these opposing
selective forces.
Our results suggest that young, expanding
leaves are most susceptible to folivory, probably
due to their allelochemical, nutritional, and physical differences from mature leaves. Fowler and
Lawton (1984) also showed that young, and presumably high quality, leaves of birch, Betula pendula, are usually preferred by folivorous species
regardless of when they appear in the growing
season. Faeth (1987) found that late-season leaf
miners prefer and perform better on newly-flushed
leaves that were produced atypically by defoliation late in the growing season. These results
suggest most insect species prefer new foliage, if
available. The susceptibility of this young, expanding foliage appears to be a common theme
among woody plants, and may be a common underlying cause of various patterns of budbreak
found among woody plants, at least within constraints imposed by other factors. In temperate
climates, trees with delayed budbreak relative to
the population suffer less folivory because leaves
are out of synchrony with insect emergence. Insect
species specialized to feed only on new buds (Du
Merle, 1988; Hunter, 1990) or those species that
emerge from overwintering stages within narrow
windows of time (Varley and Gradwell, 1968;
Feeny, 1976; Hunter, 1990) starve if buds and
young leaves are not available. Trees breaking
bud early relative to the population escape in time
as early-season folivores are confronted with older, and hence, supposedly poorer quality, leaf
resources (Feeny, 1976; Fowler and Lawton,
1984; Haukioja et al., 1985). The latter seems to
apply to our study; advanced leaves of experimental ramets were higher in gallotannin content
than younger control leaves at the beginning of
the growing season.
In tropical plant-herbivore systems, susceptibility of young, expanding leaves also appears to
influence patterns of budbreak. Production of
leaves after the peak of budbreak of trees results
in increased herbivory (Rockwood, 1974; Lieberman and Lieberman, 1984; Aide, 1988) unlike
most temperate trees, perhaps because the seasonal nature of insect species in the tropics is less
pronounced than in temperate zones (Aide, 1988).
However, woody tropical plants can escape folivory by advancing budbreak into the dry season
when insect abundances are lower (Aide, 1988),
similar to reduction of folivory of experimentally
advanced ramets of Gambel oak in this study.
Our results and those from other studies suggests that protection of vulnerable, young foliage
may influence patterns of variable budbreak observed among many woody plants. Other factors,
however, such as frost damage and length of
growing season probably constrain the influences
of folivores on variation in budbreak.
We thank B. Axelrod,C. Febus and M. Tabbarah
forassistancein the fieldandthe laboratory.W. Boecklen, W. D. Clark, S. W. Rissing, R. Spellenberg,and
an anonymousreviewer provided constructivecommentson the manuscript.This researchwas supported
by NSF grantsBSR 8717543 and 9107296 to SHF.
LITERATURE
CITED
AIDE,T. M. 1988. Herbivoryas a selectiveagent on
the timing of leaf productionin a tropicalunderstory community.Nature (London),336:574-575.
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