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Ecology |
Department of Biological Sciences, University of Pittsburgh, Pittsburgh, Pennsylvania 15260 USA
Received for publication January 9, 2003. Accepted for publication March 18, 2003.
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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Key Words: eastern North America • Liliaceae • Odocoileus virginianus • reproductive success • simulated herbivory • spatial variation • timing of herbivory • tolerance • Trillium grandiflorum
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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; Stowe et al., 2000
). Plants will differ in fitness responses if they experience herbivory at different intensities (e.g., Tolvanen et al., 2001
; Hickman and Hartnett, 2002
), on different tissues (e.g., stem vs. leaf damage; Ehrlen, 1995
; Houle and Simard, 1996
; Marquis, 1996
), at different life stages (e.g., Warner and Cushman, 2002
), or at different times during the growing season (e.g., Maschinski and Whitham, 1989
; Marquis, 1992
; Garcia and Ehrlen, 2002
). Even when the same level of herbivory is imposed upon different individuals within a population, fitness may vary as a result of genetic, maternal, or environmental differences among plants (e.g., Weiner et al., 1997
; Juenger and Bergelson, 1998
; Agrawal, 1999
; Hawkes and Sullivan, 2001
; Ferraro and Oesterheld, 2002
).
Although many studies have examined the effects of herbivory on plant fitness and the variation among individuals in their responses to herbivory (see earlier citations), far fewer studies have examined the extent to which plants in different populations vary in their responses to herbivory (e.g., Dyer et al., 1991
; Huhta et al., 2000
; Loreti et al., 2001
). However, the mechanisms that create variation in fitness responses at the individual level can be expected to create variation in fitness responses to herbivory across populations.
First, many plant populations vary in the frequency and pattern of consumption by a single herbivore species as a result of variation in its local abundance or behavior (reviewed in Huntly, 1991
). If herbivores vary in their density and/or in their proportional consumption of a particular plant species across plant populations, then the overall effect of that herbivore will vary spatially. Thus, while experiments that explored the effects of herbivory by removal (e.g., caging or insecticides) have had variable results across sites (e.g., Augustine and McNaughton, 1998
; Russell et al., 2001
), this variation could either be due to differential responses of plants or differential consumption by herbivores.
Second, even if the magnitude of herbivory is the same among plant populations, variation among populations in its seasonal timing can create variation in its average effects on plant fitness. While only a few researchers have examined the effects of herbivory timing on plant response, they have often found that plants consumed early in the growing season had higher fitness than those consumed late (Maschinski and Whitham, 1989
; Gedge and Maun, 1992
; Tiffin, 2000
). In these studies, which were all on short-lived plant species (annuals, biennials), partial defoliation early in the season was less detrimental because it allowed more time for regrowth before reproduction. However, defoliation early in the season may be more detrimental to herbaceous perennials, which are often completely defoliated (Miller et al., 1992
) and unable to regrow in the same season (e.g., Augustine and Frelich, 1998
), because early herbivory causes the plant to lose a larger portion of its growing season.
Finally, even if the frequency and pattern of herbivory is identical among plant populations, the average effects of herbivory may still differ for a variety of reasons. First, many abiotic and biotic factors, which may vary among populations, can affect plant growth and survival in the face of herbivory. For example, resource availability can either positively or negatively influence the degree to which plants can tolerate herbivory (reviewed in Hawkes and Sullivan, 2001
; Ferraro and Oesterheld, 2002
). Second, the effects of herbivory may vary among populations that differ in the frequency of past herbivore attacks. The average effects of herbivory may be exacerbated in populations with previously high levels of herbivory relative to populations with previously low levels of herbivory if past herbivore attacks have physiologically weakened plants (Ehrlen, 2000
). Alternatively, the opposite response could occur if after past herbivore attacks plants have either evolved traits that confer tolerance to herbivory (reviewed in Strauss and Agrawal, 1999
; Stowe et al., 2000
) or induced defenses (reviewed in Karban et al., 1999
).
Clearly, empirical estimation of the effects of herbivory and its variation among plant populations is necessary to accurately assess the effects of an herbivore on any given plant species. In this study, I addressed the effects of herbivory by white-tailed deer on the perennial herb, Trillium grandiflorum (Liliaceae). Using both natural and experimentally manipulated herbivory, I examined the patterns of among-population variation in the average effects of herbivory and evaluated potential mechanisms that contributed to those patterns. Specifically, I studied 12 natural populations and first asked to what degree the frequency and timing of herbivore attacks naturally varied across populations. Next, I determined to what extent herbivory and the timing of herbivory affected the future stage of reproductive plants.
In addition to exploring the natural pattern of herbivory and response to herbivory among these 12 populations, several issues necessitated experimental manipulation of herbivory. First, it is statistically difficult to assess the average effects of herbivory in populations with naturally low levels of herbivory. Second, the effects of herbivory on plant size are difficult to discern because the size of plants eaten and not eaten by deer and the timing of consumption naturally vary. Thus, I experimentally manipulated herbivory and the timing of herbivory in four populations, while controlling for plant stage and size. I compared the responses of plants that were naturally eaten by herbivores to those that were experimentally clipped to determine how well clipping simulated natural herbivory. Finally, to determine if decreases in plant size due to herbivory could have consequences for future reproductive success, I collected fruits from reproductive plants to determine whether smaller reproductive plants made fewer ovules.
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MATERIALS AND METHODS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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). Trillium grandiflorum individuals are nonclonal and persist underground in a dormant state during autumn and winter. In northwest Pennsylvania, the leaves appear above ground in late April, before the forest canopy leafs out, and senesce in late July.
Trillium grandiflorum populations consist of four easily distinguished aboveground stages: seedling, one-leaf, three-leaf, and reproductive. Reproductive plants produce a single stem, a whorl of three leaves, and a single white hermaphroditic flower that gives rise to a single fruit. Plants in the reproductive stage can remain in that stage or regress to the three-leaf (nonreproductive) stage in the next growing season. Both three-leaf and reproductive plants can transition into a dormant stage, in which no aboveground structures are made for one or more seasons (Hanzawa and Kalisz, 1993
).
The 12 populations of T. grandiflorum monitored in this study are all in deciduous forests in northwest Pennsylvania, USA (a 50-km radius, for exact locations of populations see Supplementary Data accompanying the online version of this article). The populations are separated from each other by an average of 15 km. The overstory of all populations was dominated by sugar maple (Acer saccarum), beech (Fagus sylvatica), and red oak (Quercus rubra), but the habitat quality ranged from highly fragmented (area = 0.25 km2) to near pristine (area = 25 km2). In addition, the T. grandiflorum populations themselves varied in density, spatial extent, and stage structure (Knight, 2003
).
Trillium grandiflorum is a preferred food of white-tailed deer, Odocoileus virginianus (Augustine and Frelich, 1998
), a common and increasingly abundant native herbivore (Alverson et al., 1988
; McCabe and McCabe, 1997
). When deer consume these plants, they usually removing all of its leaf and flower tissue (i.e., complete defoliation). After consumption, plants do not regrow in the same season. However, complete defoliation does not usually kill this or other forest perennial herbs, but instead reduces growth and reproduction in subsequent growing seasons (Edwards, 1985
; Whigham, 1990
; Primack et al., 1994
; Rooney and Waller, 2001
). In these T. grandiflorum populations, seedlings, one-leaf, and small three-leaf (leaf length < 5 cm) plants were never consumed by deer. These smaller stage classes were frequent in these populations, and therefore their lack of consumption likely represents deer preference for larger plants. Only large three-leaf (leaf length > 5 cm) and reproductive plants were consumed by deer, and reproductive plants were consumed at a greater frequency (Knight, 2003
). Thus, the remainder of this paper will concentrate solely on reproductive plants.
Natural herbivory
In April 1999, 5–27 1-m2 plots (sample size depended on density of population) were randomly placed along transects through each population. In each population, at least 40 reproductive plants were permanently tagged within these plots. In general, the same plants were followed in 2000 and 2001, but when necessary, additional plants were tagged to maintain adequate sample sizes.
All tagged plants were censused biweekly for evidence of deer herbivory. Deer herbivory was easily distinguished by a direct cut on the stem. Plants consumed while in bloom (3-wk flowering period in the spring) were classified as eaten early, while plants consumed after bloom but before fruit drop were classified as eaten late. Small mammal herbivory, in which all three leaves were defoliated but the stem was left intact, was rare (<1%) in these populations, and plants subjected to this type of herbivory were excluded from all analyses.
Each tagged plant was scored for stage in April of the following two years (2000 and 2001) when the plants first emerged and before any deer herbivory. Reproductive plants that did not emerge in the following years were assumed to be dormant and not dead. Of the 547 reproductive plants that were monitored in 1999, 14 did not re-emerge in 2000 and were scored as dormant. Of those 14, 11 reemerged in 2001 and the remaining three were assumed to still be dormant. I calculated the frequency in which reproductive plants remained reproductive, regressed to the three-leaf stage, or became dormant in the next year for 1999–2000 and 2000–2001.
I used 
2 analysis to determine if (1) the frequency herbivory varied across populations and (2) the stage of reproductive plants in the next growing season varied among plants consumed and not consumed by deer. A separate 2 analysis was performed for the 1999–2000 and the 2000–2001 data. The observed frequency of reproductive plants that became dormant in the next growing season was low (e.g., only 14 out of 547 reproductive plants in 1999 became dormant). For this reason, I combined the two nonreproductive stages (dormant, three-leaf) for this analysis.
I used 2 analysis to determine if (1) the timing of herbivory varied across populations and (2) the stage of reproductive plants in the next growing season varied among plants consumed early and late in the season. In these analyses, only reproductive plants that were consumed by deer were considered. Only the 1999–2000 data were used because almost no plants were eaten late in the season in 2000. Populations with less than five plants consumed by deer were excluded from the analysis testing if the timing of herbivory varied across populations. Therefore, only five populations were included in this analysis. As described earlier, the two nonreproductive stages (dormant, three-leaf) were combined for this analysis. All 2 analyses were done using SYSTAT 9.0 (1999)
.
Experimental herbivory
I experimentally manipulated plants in four populations, two with low ambient levels of herbivory, DC and RH, and two with high ambient levels of herbivory, TW and WH. At each population in 2000, I chose 30 triplets of reproductive plants that were not a part of the previous censuses. I chose each set of three based on similarity in size (within 1 cm in leaf length) and proximity (within 1 m) to each other. Each triplet was separated from other triplets by at least 3 m. Within each triplet, I randomly assigned one of three herbivory treatments to each plant; clipped early (1 May, while the plants were in bloom), clipped late (30 June, just prior to fruit drop), or control (unmanipulated). I clipped plants with scissors 5 cm from the base of the stem, which mimics deer herbivory. In 2001, I scored the stage of each plant. I measured the leaf length of all plants on 1 May in 2000 and 2001. I calculated the relative growth rate of plants between years as: RGR = (leaf length in 2001 – leaf length in 2000)/(leaf length in 2000). Leaf length has been shown to be highly correlated with other size-related traits of T. grandiflorum, such as leaf area, plant height, and stem diameter, and should thus be a good indicator of overall plant size (Rooney and Waller, 2001
).
To determine if experimental clipping effectively simulated natural deer herbivory, I used 2 analysis to test if the stage of reproductive plants in the next year (reproductive, nonreproductive) differed between the two types of herbivory (natural, experimental). In this analysis, only plants natural eaten early and clipped early in TW and WH were included. Late herbivory was not considered because natural herbivory late in the season was rare in 2000. Further, plants in DC and RH were not included in this analysis because natural herbivory was rare in these populations.
To determine if plants in different populations responded differently to the clipping treatments (i.e., a three-way interaction between population, stage transitions, and clipping), I used hierarchical log-linear analysis (Sokal and Rohlf, 1995
). Because the observed frequency of reproductive plants that transitioned into dormancy was low (6 of 341 experimental plants), the two nonreproductive stages (dormant, three-leaf) were combined.
Differences in the average pretreatment size of plants among populations may cause differences among populations in the frequencies by which plants remain in the reproductive stage (e.g., if smaller plants are more likely to regress to nonreproductive stages). I used ANOVA followed by Tukey's HSD to test for main and pairwise differences between populations in pretreatment size. I used logistic regression to determine if smaller plants were more likely to regress to nonreproductive stages (only plants in the control treatment were included in this analysis).
I used two-way ANOVA to test for differences among populations, clipping treatments, and their interaction on the relative growth rate (RGR). Within each population, pairwise differences among clipping treatments in RGR were tested with Tukey's HSD. I only included the RGR of plants that remained reproductive throughout this experiment, and therefore changes in RGR are independent from changes in stage. I used SYSTAT 9.0 (1999)
for these statistical tests.
Relationship between plant size and number of ovules
Plants that make more ovules have the potential to make more seeds and thus have greater female reproductive success. Because pollen and resource limitation may interfere with the number of ovules that actually become mature seeds, the number of ovules indicates the potential female reproductive success of plants. To determine if larger plants had more potential reproductive success, in 2000 I randomly chose approximately 25 reproductive plants that were not part of either the natural or the experimental herbivory studies from each of eight populations (DC, DH, EL, LR, RH, TW, WC, WH) (N = 180 plants total). I measured their leaf length and collected their fruits. I counted the seeds and unfertilized ovules per fruit using a dissecting microscope. I used linear regression to determine the relationship between plant size (leaf length) and the total number of ovules (total number of ovules = number of seeds + number of unfertilized ovules). The total number of ovules was log transformed. Because the linear regression did not differ among populations, populations were pooled.
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RESULTS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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2 = 0.42, df = 1, P = 0.52) and WH (N = 33 naturally eaten, N = 27 clipped, 2 = 0.021, df = 1, P = 0.89). The effect of clipping on the stage of plants in the next year did not vary among populations (a nonsignificant three-way interaction, Table 1). In all populations, early but not late clipping reduced the proportion of reproductive plants that remained reproductive (Fig. 4).
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Clipping decreased the future size of reproductive plants. Among the reproductive plants in 2000 that remained reproductive in 2001, the relative growth rates of plants differed significantly among clipping treatments (F2, 207 = 6.98, P = 0.001), populations (ANOVA: F3, 207 = 5.09, P = 0.002), and their interaction (F6, 207 = 2.87, P = 0.01). While the effect of clipping treatment on growth rate varied among populations, in general, clipped plants had reduced growth relative to unclipped plants (Fig. 5).
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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), and thus, there are many potential factors at a landscape level that could cause some populations to experience higher levels of herbivory than others. These include the proximity of the populations to busy roads; the availability of other edible forest species; the level of habitat fragmentation; and the adjacent land-use practices (e.g., agriculture, human habitation). These factors may also create variation in the timing of herbivory across these populations (Fig. 2).
Because natural and experimental herbivory affected plants similarly (in terms of the stage in the next growing season), I will discuss the observational and experimental results simultaneously. Eaten reproductive plants were three times more likely to regress to nonreproductive stages than uneaten plants (Figs. 3, 4). Herbivory also decreased the growth rate of those plants that did remain reproductive (Fig. 5) (see also Anderson, 1994
). Because smaller plants produce fewer ovules (Fig. 6), plants consumed by deer will have lower potential reproductive output in the next growing season. These results are consistent with other studies at the population level in which increases in the frequency of herbivory caused plants to decrease in size and regress in stage (Rauscher and Feeney, 1980
; Doak, 1992
; Bastrenta et al., 1995
; Ehrlen, 1995
).
Early-season herbivory was more detrimental than late-season herbivory. Because deer completely defoliate T. grandiflorum, plants eaten both early and late in the season have a complete loss of female reproductive success for that season. However, in the following growing season, more of the plants that were consumed early in the season were nonreproductive, whereas plants that were eaten late in the season were just as likely to be reproductive in the next season as those that were not consumed at all.
While several other studies have considered the effects of herbivory timing, this is the first on a perennial species that is completely defoliated. Studies on short-lived annual and biennial plants have found that plants eaten earlier had higher reproductive success than those consumed later in the season (e.g., Maschinski and Whitham, 1989
; Gedge and Maun, 1992
; Tiffin, 2000
). These plants have few stored resources and reproduce only once. Thus, early-season herbivory allowed more time for regrowth in that season prior to reproduction. Studies on these plants differ from T. grandiflorum in that complete defoliation does not occur and the response to herbivory is measured only in the same growing season in which the herbivory occurs.
In long-lived plants, late-season herbivory should generally be less detrimental than early-season herbivory, as was observed here. Two nonexclusive mechanisms contribute to this result. First, if plants cannot regrow leaves until the next season, then a plant eaten early has less potential for photosynthesis in the current growing season than a plant eaten late. Second, plants that are limited by light from a canopy may do most of their photosynthesis early in the season, prior to the leaf canopy development (e.g., Routhier and Lapointe, 2002
). In this scenario, plants eaten during this early period will lose this peak time for photosynthesis in a given season. Both of these mechanisms could occur in T. grandiflorum, because (1) defoliation by deer is complete and individuals cannot regrow following herbivory until the next growing season, and (2) plants emerge in the early spring, prior to forest canopy closure.
Other studies on perennial plants have shown that early-season herbivory was more detrimental than late (e.g., Marquis, 1992
; Ehrlen, 1995
; Garcia and Ehrlen, 2002
). For example, although Ehrlen (1995)
did not explicitly consider the timing of herbivory on Lathyrus vernus, differences in timing of plant consumption by vertebrate and mollusk herbivores may have contributed to differences in their effects. Vertebrate grazers removed much more biomass than mollusks, but surprisingly, mollusks had more severe effects on survival, growth, and reproduction. One explanation for this result is that mollusks removed meristematic tissue early in the season, which greatly inhibited plant growth for the remainder of the season. Vertebrate grazers removed both vegetative and meristematic tissue much later in the season, after the plants had a longer opportunity to grow and acquire resources. Similarly, in an experimental study manipulating the timing of leaf removal in Primula veris, Garcia and Ehrlen (2002)
found that early-season removal diminished current-year reproduction and future growth while late-season removal did not influence any fitness components. They suggested that P. veris acquires much of its resources for reproduction and storage early in the growing season, and thus herbivory at this time is most detrimental.
Although all populations responded similarly to natural and experimental herbivory, reproductive plants in populations with high ambient levels of herbivory were smaller in size and more likely to regress to nonreproductive stages than reproductive plants in populations with low ambient levels of herbivory (Fig. 4). The legacy of past herbivory attacks may be responsible for the smaller size of these plants. In this scenario, I would suggest that there is nothing fundamentally different about the traits of the individuals across populations, or their environments, aside from past herbivory, that causes them to respond differentially to herbivory. Alternatively, I cannot rule out the slightly more complex scenario that unseen environmental or genetic differences among these populations caused the initial differences in size of reproductive plants and thus their future stage.
Herbivory and the timing of herbivory affect both current and future reproduction of T. grandiflorum. Defoliation of T. grandiflorum removes all vegetative and reproductive structures and as a result, consumed plants lose all of their female reproductive success for the current growing season, regardless of when they are eaten. However, because plants eaten early in the season are more likely to regress to nonreproductive stages than plants eaten late in the season, early-season herbivory diminishes future reproduction more than late-season herbivory. In addition, even if plants are able to remain reproductive following a bout of herbivory, they suffer a reduction in size. Such decreases in the size of the reproductive plants results in a decrease in the number of ovules those plants will produce, because plant size is positively correlated with the number of ovules (Fig. 6). Thus, herbivory affects the future reproduction of a plant either by causing it to regress to a nonreproductive stage (thereby having no reproduction in the following season) or by reducing its number of ovules.
This documented herbivory-driven reduction in female reproductive output may be accompanied by a change in the sex structure of the population. Recently, in another study on T. grandiflorum, Wright and Barrett (1999)
demonstrated that smaller plants allocated significantly more resources to male function, while larger plants allocated significantly more resources to female function. In the current study, herbivory reduced the overall size of reproductive plants and may cause the overall population to become "more male."
By increasing the probability that reproductive plants regress to nonreproductive stages, herbivory reduces the number of reproductive plants in a population. If white-tailed deer are less likely to forage on T. grandiflorum when its density is low, then herbivory will be density dependent. However, pollinators may also be less likely to forage on T. grandiflorum when its density is low. Trillium grandiflorum is an obligate outcrossing species that relies on its insect pollinators (Kalisz et al., 1999
; Irwin, 2000
). In a concurrent study, I found that low-density populations are more pollen limited (Knight, 2003
). Thus, deer herbivory may cause Trillium grandiflorum populations to be inverse-density dependent (i.e., have Allee effects).
To determine how important biotic factors, such as herbivory, will affect the persistence of a species, studies must consider how the magnitude and pattern of herbivory, as well as the plant response to herbivory, vary across populations. My study indicates that both the magnitude and timing of herbivory vary across populations of T. grandiflorum and that both significantly affect the future stage and size of reproductive plants. Plants in all populations responded similarly to herbivory. This suggests that the frequency and timing of herbivory alone should indicate how plants in a population will be affected by herbivory and that more detailed knowledge of environmental characteristics and plant traits may not be necessary for T. grandiflorum. Alternatively, environmental characteristics at larger spatial and temporal scales than those considered in this study may influence the plant response to herbivory. Understanding the mechanisms that create differences across T. grandiflorum populations in the average frequency by which reproductive plants remain reproductive and regress to a nonreproductive stage is more complex. One potential mechanism is that populations that have experienced herbivory in the past may contain plants that are of smaller size and consequently more likely to regress to nonreproductive stages.
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FOOTNOTES |
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2 Current address: Department of Zoology, University of Florida, 111 Bartram Hall, P.O. Box 118525, Gainesville, Florida 32611-8525 USA (e-mail: tknight{at}zoo.ufl.edu
)
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LITERATURE CITED |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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