Ecology, 78(6), 1997, pp. 1684–1695
q 1997 by the Ecological Society of America
POLLEN AND RESOURCE LIMITATION OF COMPENSATION TO
HERBIVORY IN SCARLET GILIA, IPOMOPSIS AGGREGATA
THOMAS JUENGER1,2
AND
JOY BERGELSON1
1
Department of Ecology and Evolutionary Biology, University of Chicago, 1101 E. 57th Street,
Chicago, Illinois 60637 USA
2Mountain Research Station, University of Colorado, 818 County Road 116, Nederland, Colorado 80466 USA
Abstract. This study was motivated by an interest in herbivore–pollinator interactions,
and in the potential of pollination ecology and the physical environment to influence levels
of tolerance to herbivore damage in scarlet gilia, Ipomopsis aggregata. To investigate these
potential interactions, we performed a factorial combination of clipping treatments, fertilizer
additions, and hand pollinations in a natural population of scarlet gilia in 1994 and 1995.
Clipping imposed the strongest treatment effect on plants and acted by delaying phenology,
altering plant architecture, and reducing plant fitness in both years. Hand pollinations
increased the production of fruits and seeds in 1995 only, suggesting that our population
was pollen limited in that year. Clipped plants could compensate for damage, but only
under a restrictive set of environmental conditions, including fertilizer and hand pollinations
in 1994, and hand pollinations in 1995. We did not detect significant overcompensation in
either year of study, even under conditions releasing plants from nutrient and pollen limitation. A phenotypic selection analysis was conducted in 1995 to investigate several traits
thought to influence fitness in the presence and absence of herbivore damage. Clipped plants
were under strong selection for early flowering and increased plant height. We did not
detect a significant association between branch production or plant size and fitness in grazed
plants, suggesting that other factors determined the ability of plants to compensate for
damage in 1995. We suggest that clipping-induced changes in plant architecture and phenology altered interactions between damaged plants and pollinators. We offer several hypotheses to explain these patterns and highlight the complexity of pollinator- and herbivoremediated selection in natural plant populations.
Key words: compensatory growth; herbivory; Ipomopsis aggregata; Polemoniaceae; pollen limitation; pollination biology; scarlet gilia; tolerance.
INTRODUCTION
Most plants experience herbivore damage during
some part of their life history (Crawley 1983), and this
damage generally causes a decrease in the fecundity of
individuals (Marquis 1992). Plants may reduce the fitness impact of herbivores by escaping them in space
or time, or by coping with the damage they impose.
Recent authors have defined these two strategies as
defense (the ability to decrease the frequency of attack)
and tolerance (the ability to maintain fitness after experiencing damage) (Rosenthal and Kotanen 1994,
Fineblum and Rausher 1995). Although numerous studies have investigated the ecology and evolution of plant
defense, particularly via chemical or morphological
mechanisms (Karban and Meyers 1989, Fritz and
Simms 1992), much less is known about the incidence,
ecology, and evolutionary dynamics of tolerance. The
purpose of this study is to experimentally investigate
the effects of the physical environment and pollination
ecology on levels of tolerance to herbivore damage in
a natural plant population.
Manuscript received 29 April 1996; revised 18 September
1996; accepted 25 November 1996.
Plant tolerance to herbivory can arise from the interaction of a variety of plant traits and external environmental factors. Several studies have documented
compensatory regrowth via the release of lateral dormant buds (Inouye 1982, Islam and Crawley 1983,
Paige and Whitham 1987a, Benner 1988, Doak 1991,
Bergelson and Crawley 1992a, b, Rosenthal and Welter
1995), through increased growth and photosynthetic
rates (Welter et al. 1989, Oesterheld and McNaughton
1991), or through postdamage resource allocation patterns (Bilbrough and Richards 1993). In most cases,
the degree of physiological or developmental compensation is also influenced by the amount of nutrient and/or
water resources available to an individual for regrowth
(Cox and McEvoy 1983, Benner 1988, Maschinski and
Whitham 1989, Mutikainen and Walls 1995). Such results have led to the development of a ‘‘compensatory
continuum hypothesis’’ (Maschinski and Whitham
1989, Whitham et al. 1991), which posits that the fitness effects of herbivore damage will vary with the
degree of resource limitation. In general, plants in nutrient-rich habitats with low competition are expected
to compensate more effectively for herbivory than
those plants growing in stressful, nutrient-limited conditions.
1684
September 1997
TOLERANCE TO GRAZING IN IPOMOPSIS
One factor not commonly considered in discussions
of tolerance to herbivory is the potential for pollinators
to limit reproduction in obligately outcrossing species,
due to decreases in pollinator visitation or effectiveness. If pollen limitation is general (Bierzychudek
1981, Zimmerman and Pyke 1988, Burd 1994), the
fitness consequences of herbivory may be determined
primarily by impacts on mating success, rather than on
leaf or flower production. For instance, the loss of small
amounts of leaf tissue via herbivore damage may have
minimal fitness effects if species naturally overproduce
reproductive structures because of pollen limitation or
fruit abortion (Stephenson 1981). Alternatively, herbivore-induced decreases in plant fitness could be large
as a result of decreases in mating success. This could
occur if, for example, phenological delays associated
with the activation and growth of axillary buds (Collins
and Aitken 1970, Harnett and Abrahamson 1979, Islam
and Crawley 1983, Marquis 1988, Marquis 1992) cause
damaged plants to miss peaks in the abundance of pollinators (English-Loeb and Karban 1992, N. M. Waser,
personal communication). Likewise, herbivore damage
may alter floral display (total number of flowers, number of flowers open at a given time, floral morphology,
or pollinator rewards) and thereby influence pollinator
effectiveness or the overall attractiveness of a damaged
plant to pollinators (Karban and Strauss 1993, Strauss
et al. 1996). Under these conditions, a key component
of tolerance to herbivory may be the ability to maintain
high levels of pollination after experiencing damage.
One of the most striking examples of tolerance to
herbivory comes from field studies of ungulate grazing
on the perennial wildflower, scarlet gilia, (Ipomopsis
aggregata, Polemoniaceae). Elk and mule deer browse
the single bolting inflorescence of scarlet gilia and
stimulate the growth of additional flowering stalks from
axillary buds. In a widely debated study, Paige and
Whitham (1987a) experimentally demonstrated that
seed production and subsequent seedling survival of
naturally grazed and artificially clipped plants increased to 2.4 times that of undamaged control plants.
The authors concluded that this fitness benefit, or
‘‘overcompensation,’’ was due to grazing-induced
changes in plant architecture and flower production.
Since that time, various clipping experiments (conducted by several researchers, at many populations, and
with several subspecies of Ipomopsis aggregata) have
failed to detect significant overcompensation in this
species. Nevertheless, it is frequently the case, in these
studies, that scarlet gilia can compensate for clipping
in terms of flower or fruit production, indicating that
individuals may be highly tolerant of grazing (Maschinski and Whitham 1989, Bergelson and Crawley
1992a, b, Bergelson et al. 1996; A. K. Brody, personal
communication).
Although the issue of ‘‘overcompensation’’ in scarlet
gilia remains contentious (Belsky 1986, Bergelson and
Crawley 1992a, b, Belsky et al. 1993, Paige 1994, Ber-
1685
gelson et al. 1996), all parties agree that there is enormous variation among populations in the ability of
scarlet gilia to compensate for herbivore damage. There
is reason to believe that both nutrient levels and the
activity of pollinators can influence tolerance in Ipomopsis aggregata. First, several published studies have
shown that levels of regrowth depend on nutrient and
water availability (Maschinski and Whitham 1989) and
competition from neighboring plants (Maschinski and
Whitham 1989, Paige 1992b). Second, field experiments have demonstrated experimentally that the fruit
set and total seed production of scarlet gilia can be
pollen limited under natural conditions (Hainsworth et
al. 1985, Paige and Whitham 1987b, Campbell 1991,
Campbell and Halama 1993). Moreover, phenotypic selection studies have demonstrated that the pollinators
of scarlet gilia, hummingbirds and moths, respond to
several traits that might be affected by grazing, such
as reproductive phenology, flower number, plant
height, and the spatial patterns of flowering (Campbell
1989, 1992, Campbell et al. 1991, Wolf and Hainsworth
1991, Mitchell 1992, 1993, 1994). Despite intensive
research programs that have independently investigated
the regrowth potential and pollination biology of scarlet gilia, little is known about the interaction between
herbivores and pollinators on scarlet gilia fitness (but
see Hainsworth et al. 1984, Brody 1992, with respect
to pre-dispersal seed predation).
We utilized experimental manipulations to explore
the single and interactive effects of an artificial clipping
treatment, fertilizer additions, and hand pollinations on
fitness in scarlet gilia. The primary purpose of this
study was to determine whether levels of nutrient or
pollen availability influence the degree of tolerance to
ungulate herbivory in a natural scarlet gilia population,
and whether grazed and ungrazed individuals respond
similarly to the availability of limiting resources. To
further investigate traits influencing the compensatory
ability of damaged plants, we conducted a selection
analysis, examining the effect of natural selection on
various plant traits in the presence and absence of grazing.
METHODS
Study system
We studied a large population of scarlet gilia, Ipomopsis aggregata subssp. candida (Polemoniaceae), located on the Colorado Front Range just north of the
University of Colorado Mountain Research Station.
Scarlet gilia is a common monocarpic, perennial wildflower of western montane habitats. At this site, it
grows in large montane meadows interspersed with
small patches of ponderosa pine forest occurring at
ø2500 m elevation. After germination, scarlet gilia
grows as a hardy rosette for 2–5 years until it bolts an
indeterminate flowering stalk, reproduces, and dies (D.
H. Wilken, personal communication). Scarlet gilia has
1686
THOMAS JUENGER AND JOY BERGELSON
flowers that are hermaphroditic, protandrous, and selfsterile (D. H. Wilken, personal communication; T.
Juenger, unpublished data). The flowers in this Front
Range subspecies range in color from pure creamy
white to light shades of pink. They are pollinated by
the white-lined hawkmoth (Sphingidae: Hyles lineata)
and, to a lesser extent, by resident and migratory hummingbirds, including Broadtailed Hummingbirds ( Selaphorus platycerus), Rufous Hummingbirds (Selaphorus rufus), and Calliope Hummingbirds (Stellulla calliope) (Elam and Linhart 1988; T. Juenger, personal
observation). This montane population is frequented
by mule deer (Odocoileus hemionus), and ø44% of
bolting scarlet gilia shoots experience early-season
grazing (Bergelson et al. 1996). In addition to ungulate
herbivory, plants on the Front Range are attacked by
a seed fly (Anthomyiidae: Hylemya sp.), two lepidopteran fruit predators (Noctuidae: Heliothis phloxiphagus; Tortricidae: Olethreutes sp.), green aphids, and an
unidentified dipteran root borer. For additional details
on the natural history of scarlet gilia, see Pleasants
(1983) and Wilken and Allard (1986).
Experimental design
We randomly selected eight young, bolting shoots of
scarlet gilia in each of 10 5 3 10 m blocks in the early
spring of 1994 and again in 1995. All blocks consisted
of homogeneous open-meadow habitat. Within each
block, plants were randomly allocated to one of eight
treatments representing a full-factorial cross of two
grazing levels (control vs. experimentally clipped), two
resource levels (control vs. fertilizer and water addition), and two pollination levels (natural pollination
only vs. hand pollination plus natural pollination).
Thus, there were 10 replicates of each treatment combination.
We collected initial measurements on the height of
bolting inflorescence shoots, rootstock diameter (measured just below the vegetative rosette), and inflorescence stem diameter (measured at the base of the flowering stalk) for all experimental plants. ANOVAs on
each of these measures confirmed that plants were randomly assigned to treatments with respect to initial size
(in all cases, P . 0.10).
Plants that were allocated to the clipping treatment
were clipped with scissors so that 1 cm of the growing
inflorescence remained. Clipping treatments were applied on 17 May 1994 and 11 June 1995, at which time
mule deer were observed browsing in the population.
At the time of the clipping treatments, plants had recently initiated bolting (shoots were, on average, 5 cm
tall in 1994 and 6 cm in 1995) and no bud or flower
formation had occurred. The large difference between
the experiments in clipping treatment dates is due to
natural differences in reproductive phenology across
years (scarlet gilia rosettes were still under snow cover
on 17 May 1995). Although our experiments entailed
an artificial clipping treatment, several previous studies
Ecology, Vol. 78, No. 6
(Paige and Whitham 1987a, Paige 1992a, b) have documented that scarlet gilia responds similarly to appropriate clipping treatments and to natural grazing by
deer and elk. In this population, both naturally grazed
plants and experimentally clipped plants exhibit the
characteristic regrowth morphology described in early
studies of scarlet gilia regrowth and compensation
(Paige and Whitham 1987a, Bergelson and Crawley
1992a, b).
We began fertilizer treatments on 31 May 1994 and
14 June 1995, shortly after rosettes initiated bolting in
both years. Plants in the fertilizer addition treatment
received 400 mL of liquid 20-20-20 NPK fertilizer (Peter’s Professional) at the manufacturer’s recommended
concentration once per week throughout the reproductive season. Thus, our fertilizer treatment increased natural levels of both water and mineral nutrient availability. Following Campbell and Halama (1993), drip
emitters attached to plastic cup reservoirs were utilized
to restrict fertilizer delivery to the root zone of treatment plants. The final fertilizer addition was applied
on 6 September 1994 and on 30 August 1995. This
regime resulted in a total of 14 and 12 fertilizer treatments in 1994 and 1995, respectively.
Hand-pollinated plants received supplemental pollen
to female-phase flowers (stigmas exerted from corolla
tube and stigmatic lobes expanded) every other day
throughout the flowering season. We used wooden
tooth picks to collect pollen from two pollen donors
located ø3–10 m away from a treatment plant. This
distance has been shown to result in maximum seed
set in experimental studies of I. aggregata subsp. aggregata (Waser and Price 1989). This experimental protocol tests for the effects of pollen supplementation on
whole-plant seed set (Zimmerman and Pyke 1988). To
investigate seasonal patterns of reproduction, we recorded the first day of flowering for each plant and
censused flower production each week throughout the
season. At the time of census, flower sepals were
marked with a different colored ink for each week of
the study.
Plants were allowed to grow until all fruits that were
produced matured, or until the plant died. Throughout
the season, we collected mature fruits that were ready
to dehisce seed and counted the total number of fully
developed seeds produced for each plant. This is the
first study of the fitness consequences of grazing on
scarlet gilia that has measured female fitness as the
total number of seeds produced. Reproductive success
via male function (seed siring) was not estimated. All
experimental plants were monocarpic; thus, data on
reproductive success collected over a single season represent lifetime maternal fitness. The number of branches and the final height of each plant were recorded at
the end of the growing season; only stout stems derived
from rootstock tissue were considered to be branches.
To examine treatment effects on seed quality, we selected a random sample of 100 seeds (or as many as
September 1997
TOLERANCE TO GRAZING IN IPOMOPSIS
available) from the pooled seeds of each experimental
plant. These seeds were collectively weighed to the
nearest 0.001 mg using a Mettler (AE 1000) scale. The
total mass was divided by the number of seeds in the
sample to estimate the mean seed mass per seed for
each plant.
The entire experimental plot was electrically fenced
and repeatedly live-trapped to deter natural deer, elk,
and ground squirrel herbivory of experimental plants.
In spite of these efforts, 17 plants had to be excluded
from the analysis due to late-season herbivory and
unexplained mortality (possibly due to a fungal pathogen), thus leaving a total experiment sample size of 73
plants in 1994 and 70 in 1995. In both years, Heliothis
and Olethreutes fruit predators were removed from experimental plants to reduce their effect on plant female
fitness.
Selection analysis
To further investigate the role of several plant traits
on tolerance to herbivory, we conducted a two-environment selection experiment in 1995 (Arnold and
Wade 1984a, b, Wade and Kalisz 1990, Dudley 1996).
We selected 110 young, bolting scarlet gilia shoots
from our study population and randomly allocated them
to an experimental clipping treatment or left them as
control plants. Plants that were allocated to the clipping
treatment were artificially clipped with scissors on 12–
13 June 1995 so that 1 cm of the growing inflorescence
remained. An ANOVA of clipping treatment on initial
rootstock diameter confirmed that experimental plants
were randomly allocated to treatments (F 5 1.796; df
5 1, 107; P . 0.15). We collected data on initial rootstock diameter, date of first flower, final plant height,
number of branches, and total fruit production for each
plant. These variables were chosen for study because
of several a priori hypotheses concerning how herbivory might influence plant growth and reproduction, particulary via interactions with pollination, as suggested
by our preliminary studies and work presented in several published studies (Campbell 1989, 1991, Campbell
et al. 1991, de Jong et al. 1992, Mitchell 1993, Mitchell
1994).
STATISTICAL ANALYSIS
Field experiment
We used a multivariate analysis of variance (MANOVA) to conservatively test for the effects of year,
block, clipping, fertilizer, and hand pollination on the
growth and reproduction of scarlet gilia, using the GLM
procedure of SuperAnova (Abacus Concepts 1990). In
all cases, the independent variables were considered
fixed effects. We chose to consider Block a fixed effect
in our analysis because our sampling of blocks covered
an entire scarlet gilia meadow, and, thus, blocks were
not a random sample across some larger universe about
which we wished to generalize our results. The MAN-
1687
OVA considered simultaneously the following seven
response variables: seed production, fruit production,
flower production, mean mass per seed, plant height,
number of branches, and initial date of flowering. When
necessary, response variables were transformed to ensure normality and to homogenize variances. The initial
model contained all possible interactions between year,
clipping, fertilizer, and pollination factors. Since significant interactions involving year were detected (Year
3 Nutrient and Year 3 Clipping), we subsequently
performed the analysis on each year individually. The
response variable mass per seed was excluded from the
MANOVA for 1995 data because of numerous missing
values (several experimental plants failed to set seed
in 1995).
Detection of a significant treatment effect with
MANOVA indicates that differences exist among treatments, but it does not indicate which response variables
in the analysis contribute most to the differences.
Therefore, each MANOVA was followed by univariate
ANOVAs to explore which variables contribute to significant MANOVA effects.
To determine the degree to which plant tolerance to
herbivory was influenced by pollen and nutrient availability, we made planned comparisons between the total
seed production of control plants contrasted with that
of clipped plants in each of the four nutrient and pollination treatments: control vs. clipped, control vs.
(clipped 1 fertilizer), control vs. (clipped 1 hand pollination), control vs. (clipped 1 fertilizer 1 hand pollination). These nonorthogonal planned comparisons
were performed with a adjusted to 0.0125, because of
the nonindependence of the contrasts.
Selection analysis
We performed a multiple regression analysis to estimate the strength of selection on each of the measured
response variables in both clipped and unclipped treaments (Lande and Arnold 1983, Arnold and Wade
1984a, b, Wade and Kalisz 1990, Dudley 1996). Standardized selection gradients were calculated as the partial regression coefficients of plant size (initial rootstock diameter), final plant height, date of first flowering, and number of branches produced on relative
female fitness. Lifetime female fitness was estimated
as the total number of fruits; this is a good estimate of
female fitness in scarlet gilia, because fruit set and total
seed production are tightly associated in this study population (1994: R2 5 0.826, P , 0.0001; 1995: R2 5
0.917, P , 0.0001). All independent variables were normally distributed and did not require transformation;
however, the dependent variable, female fitness, was
log-transformed to eliminate problems of heteroscedacity. All significance tests were performed using the
log-transformed relative fitness. According to the methods of Lande and Arnold (1983) and Mitchell-Olds and
Shaw (1987), linear selection gradients were calculated
using untransformed relative female fitness. In these
THOMAS JUENGER AND JOY BERGELSON
1688
FIG. 1. Results of planned comparisons contrasting seed
production in control vs. clipped scarlet gilia plants in each
of the four pollination), and nutrient treatments: control vs.
clipped, control vs. (clipped 1 hand pollination), control vs.
(clipped 1 nutrients), and control vs. (clipped 1 hand pollination 1 nutrients). These nonorthogonal planned comparisons were performed with a adjusted to 0.0125, because of
the nonindependence of the contrasts.
models, we investigated both linear and quadratic coefficients. Because none of the quadratic terms was
statistically significant, they were removed from the
model.
The results of this selection analysis are presented
as path diagrams (Li 1975, Kingsolver and Schemske
1991) in Figs. 1 and 2. The model utilized in the analysis included all possible direct and indirect paths; for
clarity, only significant path and correlation coefficients are presented in the path diagrams. Each significant path coefficient is diagrammed by a singleheaded arrow and represents the selection gradient, or
direct selection on a trait, holding all other traits constant. The double-headed arrows represent the phenotypic correlations among traits, and were calculated as
the Pearson correlation coefficient. We tested for significant differences between the path coefficients in
grazed and ungrazed environments using an analysis
of covariance (ANCOVA) to test for heterogeneity of
slopes between treatments.
RESULTS
Field experiment
Results of the MANOVA indicated a significant effect of block, clipping, hand pollination, and fertilizer
Ecology, Vol. 78, No. 6
on the growth and reproduction of scarlet gilia. No
significant interactions were detected (Table 1).
The actual mean values for each response variable
for all treatments are given in Table 2. Results from
each univariate ANOVA are given in Table 3. Control
plants in 1995 produced only half as many seeds (311
6 41 seeds, mean 6 1 SE) as those in 1994 (616 6
123 seeds). Overall, clipping significantly reduced total
seed production to 62% and 68% of the production of
control plants in 1994 and 1995, respectively. Hand
pollinations had no effect on total seed production in
1994, but led to a 52% increase in seed production in
1995, demonstrating that our study population was pollen limited in 1995. Surprisingly, fertilizer additions
did not significantly influence total seed production in
either 1994 or 1995.
The clipping treatment significantly influenced plant
architecture by decreasing the final height of plants and
increasing the number of branches produced from lateral meristems. Clipped plants were consistently shorter in stature (45% reduction, averaged across both
years) and had a shrubby growth form in comparison
to unclipped controls (4 vs. 2.3 branches, averaged
across both years). Fertilizer additions did not influence
final plant height, but did increase branch production.
This result suggests that apical dominance in scarlet
gilia is determined not only by hormonal suppression
of lateral buds, but also by competition among meristems for limiting nutrients. In 1995, there was also a
significant interaction between the nutrient and pollination treatments on the number of branches produced,
with plants that received both pollen and nutrients initiating fewer lateral branches than those receiving only
fertilizer.
The detrimental consequences of early-season clipping on female fitness were due, at least in part, to
direct negative effects on flower and fruit production
in both years (Table 3). In both years, the clipping
treatment significantly reduced flower production to
ø49% that of control plants. Likewise, clipping reduced the production of fruits to ø62% of the production of control plants. Fertilizer additions significantly increased flower production by 37% in 1994, but
had no effect on fruit production in that year. In 1995,
fertilizer additions significantly increased fruit production, although they had no effect on flower production.
Hand pollinations had no effect on flower production
or fruit production in 1994, but led to a 41% increase
in fruit production in 1995.
Our two study years differed substantially in length
of the growing season. In particular, 1995 was an extremely short season, due to an unusually cold, wet
spring followed by an early killing frost in the fall.
This phenological difference may have had large effects on the importance of pollination biology in the
two study years, by affecting pollinator abundance and
efficacy. For example, at the Rocky Mountain Biological Research Station (RMBL), a ø75% reduction in
TOLERANCE TO GRAZING IN IPOMOPSIS
September 1997
1689
FIG. 2. Path diagram of standardized linear selection on plant height, date of first flower (phenology), plant size (initial
rootstock diameter), and number of branches in the absence of clipping. Only significant path and correlation coefficients
are presented. Dashed lines represent negative relationships. * P , 0.05, *** P , 0.001, **** P , 0.0001.
hummingbird population size was observed in 1995,
presumably due to starvation mortality from the unusually late season (W. A. Calder, personal communication). On the Front Range, plants flowered for an
TABLE 1. Results of MANOVA on growth and reproduction
in scarlet gilia: response variables include seed production,
fruit production, flower production, final plant height, number of branches produced, phenology, and mean seed mass.
Mean seed mass was excluded from the 1995 model.
Wilks’
l
F ratio
P
Source
df
1994
Block
Clipping (C)
Hand pollination (H)
Nutrient (N)
C3H
C3N
H3N
C3H3N
63, 270
7, 47
7, 47
7, 47
7, 47
7, 47
7, 47
7, 47
0.092
0.233
0.666
0.627
0.889
0.820
0.940
0.955
2.272
22.146
3.365
3.993
0.836
1.470
0.425
0.316
0.0001
0.0001
0.0054
0.0017
0.5631
0.2013
0.8816
0.9430
1995
Block
Clipping (C)
Hand pollination (H)
Nutrient (N)
C3H
C3N
H3N
C3H3N
54, 249
6, 48
6, 48
6, 48
6, 48
6, 48
6, 48
6, 48
0.297
0.172
0.713
0.835
0.880
0.889
0.835
0.814
1.243
38.601
3.225
1.586
1.094
1.004
1.580
1.834
0.1375
0.0001
0.0096
0.1719
0.3798
0.4339
0.1736
0.1124
average period of 61 d in 1994 but only 24 d in 1995.
Overall, plants were more tolerant of clipping in 1994,
when the growing season was relatively longer. Clipped
plants were significantly delayed in initial date of flowering in both years of study (9.3-d delay in 1994, 8.8-d
delay in 1995).
The ANOVA investigating the effects of treatments
on mean mass per seed revealed significant effects of
hand pollination in both years. Mean mass per seed and
mean number of seeds per fruit show a significant negative correlation (1994: r 5 20.44, P 5 0.0001, n 5
70; 1995: r 5 20.26, P 5 0.056, n 5 52). This result
suggests a trade-off in resource allocation between seed
size and number, as mediated by pollinator effectiveness, a result previously demonstrated in scarlet gilia
by Hainsworth et al. (1984) and Wolf et al. (1985), but
not detected by Campbell and Halama (1993) or A. K.
Brody and R. J. Mitchell (personal communications).
We also detected a significant positive effect of clipping
on seed mass in 1995 (control plants 0.10 6 0.04 mg,
mean 6 1 SE; clipped plants 1.15 6 0.05 mg), and a
significant interaction between hand pollination and
nutrient addition treatments. Plants that received both
hand pollination and fertilizer had significantly smaller
seeds than did control plants or plants that received
either pollen or nutrients singly. Our analysis also revealed a significant block effect on mean seed mass in
both years of study, perhaps indicating that local en-
THOMAS JUENGER AND JOY BERGELSON
1690
Ecology, Vol. 78, No. 6
TABLE 2. The effect of experimental clipping, pollen, and nutrient additions on fitness components, inflorescence architecture,
and reproductive physiology of scarlet gilia. Each value reported is a mean (6 1 SE) across 7–10 plants.
Treatment
Clipping
Other response variables
Fitness response variables
Pol- Nutrilen† ents‡
No. seeds
No. flowers
No. fruits
Mass/seed
(mg)
No. branches
Height
(cm)
Date of
first flower
1994
Control
Control
Control
Control
Clipped
Clipped
Clipped
Clipped
C
H
C
H
C
H
C
H
C
C
N
N
C
C
N
N
616
630
545
986
158
286
158
444
6
6
6
6
6
6
6
6
123
122
116
261
44
87
37
110
259
224
445
394
158
118
206
195
6
6
6
6
6
6
6
6
34
29
131
112
29
25
33
38
80
68
81
99
24
31
32
54
6
6
6
6
6
6
6
6
12
8
19
25
6
9
7
14
1.56
1.40
1.49
1.37
1.51
1.35
1.43
1.23
6
6
6
6
6
6
6
6
0.10
0.08
0.12
0.05
0.07
0.05
0.11
0.07
2.5
2.1
3.9
4.0
4.1
3.9
3.8
4.3
6
6
6
6
6
6
6
6
1.20
0.90
1.50
1.10
0.54
0.42
0.36
0.52
80
72
74
71
51
48
49
49
6
6
6
6
6
6
6
6
4
4
4
5
4
2
3
4
5.6
3.6
7.0
5.7
14.8
13.1
16.1
14.6
6
6
6
6
6
6
6
6
1.2
0.6
1.1
1.2
1.0
1.9
2.2
0.91
1995
Control
Control
Control
Control
Clipped
Clipped
Clipped
Clipped
C
H
C
H
C
H
C
H
C
C
N
N
C
C
N
N
311
405
425
797
81
181
98
328
6
6
6
6
6
6
6
6
41
108
76
104
113
144
132
294
140
146
208
179
51
85
103
94
6
6
6
6
6
6
6
6
25
35
26
30
11
21
29
22
45
52
62
85
9
25
15
39
6
6
6
6
6
6
6
6
6
11
11
11
5
11
7
12
1.10
0.92
1.14
0.86
1.06
1.16
1.37
1.08
6
6
6
6
6
6
6
6
0.10
0.07
0.09
0.05
0.11
0.12
0.06
0.09
1.1
1.6
2.9
1.3
3.0
3.4
4.7
4.4
6
6
6
6
6
6
6
6
0.12
0.49
0.75
0.19
0.33
0.57
0.58
0.46
78
74
78
77
40
50
41
47
6
6
6
6
6
6
6
6
4
5
5
3
3
3
2
5
8.4
8.0
8.3
8.3
18.5
17.0
18.0
13.9
6
6
6
6
6
6
6
6
1.5
1.4
1.2
0.79
1.5
2.0
1.8
1.8
† Pollination treatments were natural control (C) vs. hand pollination (H).
‡ Nutrient treatments were control (C) and nutrient (fertilizer) addition (N).
§ Date of first flower is the number of days after 28 June and 17 July (the day of initial flowering in experimental populations
in 1994 and 1995, respectively) before a plant first came into bloom.
vironmental conditions influence resource allocation to
seeds.
The degree to which clipped plants could compensate
for herbivore damage depended greatly on the environment in which plants experienced damage (Fig. 1,
Table 4). Planned contrasts revealed that additions of
either pollen or fertilizer alone could not ameliorate
the negative effects of clipping in 1994. For instance,
clipped plants that received supplemental pollination
produced significantly fewer seeds than did unclipped
control plants. Likewise, clipped plants that received
supplemental fertilizer still produced fewer seeds when
compared to unclipped controls. However, plants that
received both pollen and nutrient supplementation
TABLE 3. Results (F ratios) of univariate ANOVAs for seed production, flower production, fruit production, branch production, final plant height, and mean seed mass in scarlet gilia. Type III sums of squares were used.
Source
Flowers†
Fruits†
Mass/seed
Seeds†
1994
Block
Clipping (C)
Hand pollination (H)
Nutrients (N)
C3H
C3N
H3N
C3H3N
Residual
9
1
1
1
1
1
1
1
56
1.194
21.921***
1.697
0.965
0.629
1.114
1.531
0.610
0.863
18.765***
1.405
8.290**
0.131
0.036
0.350
0.142
1.131
17.217***
1.614
0.196
2.337
0.765
0.011
0.131
2.627*
1.590
8.542**
1.743
0.378
0.087
0.016
0.009
7.040***
3.866*
0.007
4.067*
0.051
2.459
0.415
0.025
1.391
85.554***
1.636
0.278
0.449
0.413
0.499
0.030
1.912
88.784***
3.822
3.331
0.058
0.202
0.059
0.024
1995
Block
Clipping (C)
Hand pollination (H)
Nutrients (N)
C3H
C3N
H3N
C3H3N
Residual
9
1
1
1
1
1
1
1
53
1.664
33.206***
9.849**
2.657
2.712
0.139
0.019
1.289
1.260
26.386***
0.054
3.363
0.137
0.184
0.999
0.353
1.480
44.277***
9.684**
4.033*
3.131
0.020
0.008
0.392
2.178*
8.805**
6.681*
0.222
0.433
0.773
4.977*
0.756
1.226
40.043***
0.248
8.551**
0.976
0.806
4.277*
1.022
1.536
147.814***
0.501
0.035
1.587
0.236
0.070
0.132
0.558
63.219***
1.851
0.633
1.091
1.107
0.101
0.728
* P , 0.05; ** P , 0.01; *** P , 0.001.
† Total numbers of flowers, fruits, and seeds were log(y 1 1)-transformed.
Branches
Height
Date of
first flower
df
TOLERANCE TO GRAZING IN IPOMOPSIS
September 1997
TABLE 4. ANOVA statistics accompanying the nonorthogonal planned comparisons presented in Fig. 1. Seed production in control vs. clipped scarlet gilias is compared
under four pollination and nutrient treatments. Abbreviations are: C, clipped, H, hand pollination, and N, nutrients
added.
Treatment
df
F
P
1994
Control
Control
Control
Control
vs.
vs.
vs.
vs.
C
C1H
C1N
C1H1N
1, 56
1, 56
1, 56
1, 56
7.774
7.572
8.178
0.695
0.0072
0.0080
0.0059
0.4081
1995
Control
Control
Control
Control
vs.
vs.
vs.
vs.
C
C1H
C1N
C1H1N
1, 53
1, 53
1, 53
1, 53
22.428
0.989
12.567
1.093
0.0001
0.3246
0.0008
0.3005
could counteract the detrimental effects of early-season
clipping.
In 1995, clipped plants that received supplemental
fertilizer produced significantly fewer seeds than did
unclipped control plants. In contrast, there was no significant difference in seed production between unclipped control plants and clipped plants that received supplemental hand pollinations. Likewise, there was no
1691
significant difference in seed production between unclipped control plants and clipped plants that received
both hand pollinations and fertilizer additions. Under
conditions of population-wide pollen limitation, hand
pollinations alone were sufficient to ameliorate the detrimental effects of early-season clipping in this year.
Selection analysis
The results of the 1995 selection analysis are presented as path diagrams in Figs. 2 and 3. In the clipped
treatment, there was a strong selection gradient on plant
height and on initial date of flowering, with plants that
reproduced earlier and that were taller having increased
female fitness. There was no significant association between female fitness and either initial plant size or
branch production. This suggests that factors other than
regrowth capability or resource reserves dominated the
ability of plants to tolerate clipping in 1995. Initial
plant size and the number of branches produced influenced female fitness indirectly via phenotypic correlations with plant height and phenology. In particular,
plant size and branch production were negatively associated with reproductive phenology. Large, bushy
plants reproduced earlier than did small, single-stalked
plants. Branch production significantly influenced rel-
FIG. 3. Path diagram of standardized linear selection on plant height, date of first flower (phenology), plant size (initial
rootstock diameter), and branch production in clipped plants. Path coefficients were estimated using relative fitness as the
dependent variable. Significance of the path coefficients in the model was tested using log(1 1 relative fitness) as the
dependent variable. Only significant paths and correlation coefficients are presented. Dashed lines represent negative relationships. * P , 0.05, ** P , 0.01, *** P , 0.001.
THOMAS JUENGER AND JOY BERGELSON
1692
ative female fitness via an indirect positive relationship
between branch production and final plant height.
In the absence of grazing, there was a strong directional selection gradient on plant height and a weak
selection gradient on initial plant size and branch production, with plants that were taller, initially larger, and
that reproduced earlier having greater female fitness.
Date of first flower was negatively correlated with both
measures of plant size, with tall and large plants reproducing earlier in the season. There was a significant
positive relationship between plant size and plant
height.
Although our estimates of selection gradients on the
same trait in different environments were often quite
different (e.g., final plant height, b grazed 5 0.482 vs.
b undamaged 5 0.130), our power to detect statistically
significant differences was low because of the relatively small sample size in our selection experiment.
However, a negative selection gradient for plant size
on female fitness in the grazed environment was significantly larger and in the opposite direction to the
gradient in the absence of herbivore damage (F 5
4.003; df 5 1,99; P , 0.0481).
DISCUSSION
Clipping had an overall greater effect on female fitness than did either nutrient or pollen limitation in both
years of study. In all cases, the fitness reduction associated with clipping outweighed that of the effects
of natural levels of nutrient or pollen limitation, suggesting that early-season browsing is one of the dominant selective pressures on this scarlet gilia population. Our results support the compensatory continuum
hypothesis (Maschinski and Whitham 1989) by demonstrating that the female fitness consequences of clipping were dependent on the pattern of nutrient and
pollen availibility in our study population. Clipped
plants were able to compensate for damage under only
a very restrictive set of environmental conditions, involving hand pollinations and nutrient additions in
1994, and hand pollinations in 1995. In contrast to the
results of Paige and Whitham (1987a) and Maschinski
and Whitham (1989), we did not find evidence of
‘‘overcompensation,’’ even under conditions releasing
clipped plants from both pollen and nutrient limitation.
This result rejects the notion that damaged plants with
multiple active meristems can more efficiently utilize
limiting resources in comparison to apically dominant,
undamaged plants in our Front Range population.
The negative effect of clipping on female fitness was
primarily due to a lower production of flowers and
lower pollination. Clipped plants produced fewer flowers, turned fewer of their flowers into fruits, and set
fewer seeds. Our experimental results suggest that the
reduced flower production associated with clipping was
due to increased nutrient limitation. Clipped plants that
received fertilizer produced as many flowers as did
control plants. Likewise, the decreased fruit and seed
Ecology, Vol. 78, No. 6
production in clipped plants was due, at least in part,
to increased pollen limitation. Clipped plants that received hand pollinations set nearly the same proportional amount of fruit and seed as did control plants,
irrespective of natural or supplemented nutrient levels.
The strongest and most consistent pattern we observed was an interplay between pollination and tolerance to herbivory. In both study years, clipped plants
were only able to compensate for damage when receiving supplemental hand pollinations, suggesting that
pollinator visitation and effectiveness can be critical
factors in determining the female fitness consequences
of damage. One plausible hypothesis explaining this
effect is that the clipping-induced delays in date of first
flowering caused clipped plants to miss the natural peak
in pollinator or pollen donor abundance at our study
population. This idea is supported by the significant
negative selection gradient on date of first flowering in
our 1995 selection analysis, and by recent phenotypic
selection analysis of flowering date in Ipomopsis aggregata subssp. aggregata (Campbell 1991). This hypothesis would gain further support from observational
data confirming a discordance between the timing of
flower production in damaged individuals and the seasonal abundances of hawkmoth and hummingbird pollinators.
A competing explanation for the reduction in female
fitness evident in grazed plants is that clipping altered
the floral display of damaged individuals. For example,
Maschinski (1990 unpublished abstract) has observed
that many of the flowers on damaged Ipomopsis arizonica plants face inward and, subsequently, have a
lower probability of receiving pollen (lower pollinator
visitiation) than outward-facing flowers. It is possible
that such herbivore-induced changes in floral display
(e.g., reduction in final height, increased inflorescence
production, reductions in the number or orientation of
flowers presented to pollinators) influence pollinator
effectiveness or behavior, and thus have resultant effects on plant female fitness. In particular, we observe
that clipped Ipomopsis aggregata are often overgrown
by competing grasses, potentially reducing the ability
of pollinators to visit all of their open flowers. This
notion is supported by the strong selection gradient on
plant height in the presence and absence of grazing
damage, and by recent observational studies that have
documented a strong influence of plant height on hummingbird visitation in Ipomopsis aggregata subssp. aggregata (Wolf and Hainsworth 1991, Mitchell 1992,
1993, 1994). Again, these mechanistic hypotheses
would gain support from behavioral observation documenting pollinator preference for particular floral display characteristics at our study population, or by conducting experimental manipulations of these traits for
damaged and undamaged plants.
A third hypothesis explaining reduced seed production in clipped plants is that they experience an increase
in within-plant pollinator movement and associated
September 1997
TOLERANCE TO GRAZING IN IPOMOPSIS
geitonogamous (within-plant) pollen transfer. Waser
and Price (1991) have experimentally demonstrated
that scarlet gilia can experience up to a 43% reduction
in female fitness from self-pollen movement within an
individual, purportedly due to a late-acting self-incompatibility system that usurps ovules. Similarly, de Jong
et al. (1992) experimentally observed reductions in
seed set due to self-pollen movement in scarlet gilia,
with plant height influencing the degree of geitonogamous pollen transfer. Hummingbird and hawkmoth
pollinators tend to forage in inflorescence clumps (Wolf
and Hainsworth 1991; T. Juenger, personal observation) and may, therefore, make more frequent movements between branches of the same damaged individual in comparison to movement within a single-stalked
plant. This effect might be particularly important in
scarlet gilia, because grazing also causes a decrease in
ovule production (data not presented here), presumably
increasing the cost of ovule loss due to self-pollination.
This hypothesis is currently being tested using emasculation and clipping manipulations in the field.
Our observation that Front Range populations of
Ipomopsis aggregata subssp. candida were primarily
limited by pollen and grazing over the two years of our
study contrasts with Campbell and Halama’s (1993)
observation that Western Slope populations of Ipomopsis aggregata subssp. aggregata can be jointly limited by pollen and nutrients. Under natural levels of
pollination, our fertilizer addition did not lead to an
increase in total seed production, despite its positive
effect on number of flowers. Regardless, we agree with
the conclusions of Campbell and Halama (1993) that
it is overly simplistic to categorize a plant species as
‘‘pollen’’ or ‘‘resource’’ limited. It is clear from several
field experiments that both processes can act within a
population (de Jong and Klinkhamer 1989, Campbell
and Halama 1993), across space or time (Campbell
1987, Johnston 1991, Campbell and Halama 1993), and
at different stages of reproduction (Campbell and Halama 1993).
Our selection analysis suggests that differences may
exist between standardized selection gradients in the
presence and absence of grazing. Plants that were damaged by early-season clipping were under strong phenotypic selection for early flowering and increased
plant height in 1995. Unexpectedly, we did not detect
a female fitness benefit of branch production or large
initial size in clipped plants. We hypothesize that, although branch production is crucial for compensatory
regrowth of reproductive structures (e.g., inflorescence
and flower production) in scarlet gilia, its efficacy can
be limited by pollinator availability in pollen-limited
years. One of the more interesting outcomes of this
study is that considerable spatial and temporal variation
may exist for factors influencing plant reproduction.
This highlights the potential complexity of selection,
acting through pollinators and herbivores, on traits influencing compensatory regrowth and pollinator at-
1693
traction within plant populations (see also Campbell
1991, Waser et al. 1996).
In conclusion, scarlet gilia is largely herbivore and
pollen limited on the Front Range. Plants that experience early-season clipping have delayed reproduction, altered plant architecture, and reduced fecundity.
The reduced female fitness of damaged plants comes
not only from decreases in the resources available to
damaged plants for reproduction, but also through effects on the interaction between plants and pollinators.
Scarlet gilia can compensate for herbivory, but only
under favorable environmental conditions that allow
damaged plants to maintain adequate pollination. A full
understanding of this effect will only come with additional natural history information and simultaneous
behavioral observation of plant–pollinator and plant–
herbivore interactions.
ACKNOWLEDGMENTS
We thank Diane Campbell, Martin Kelly, Peter Kotanen,
Colin Purrington, Irene Shonle, Nick Waser, and Juliete Winterer for helpful comments on the manuscript. We thank dancing Sammy Machula, Jon Juenger, Jackie Juenger, and staff
and researchers at the Mountain Research Station for help
with field work and fun times in the mountains. The U.S.
Forest Service and Dick and Marjorie Morroni kindly provided access to our field population. This work was supported
by a Packard Fellowship and NSF grant DEB 9496331 to J.
Bergelson and a Sigma Xi Grants-in-Aid of Research to T.
Juenger.
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