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0 Queen's University, Department of Biology, Kingston, Ontario, Canada K7L 3N6
Received for publication November 16, 1999. Accepted for publication March 3, 2000.
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMETHODSRESULTSDISCUSSIONLITERATURE CITED |
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Key Words: apical dominance • branching • compensation • seed production • reserve meristem • Scrophulariaceae • Verbascum thapsus.
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONLITERATURE CITED |
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; Inouye, 1982
; Argall and Stewart, 1984
; Sheldon, 1986
; Aarssen and Turkington, 1987
; Paige and Whitham, 1987
; Benner, 1988
; Maschinski and Whitham, 1989
; Michaud, 1991
; Fox, 1995
; Hicks and Reader, 1995
) usually in the form of shoot apex removal. In this study, compensation is explicitly tested using Verbascum thapsus and its seed predator, the weevil Gynmnetron tetrum Fab. Verbascum thapsus expresses strong apical dominance with infrequent branching late in the growing season and only in the largest individuals (Naber and Aarssen, 1998
). The weevil larvae of G. tetrum dramatically decrease net seed set of the plant by consuming virtually all of the seeds within infested fruits (Reinartz, 1984a
). Hence, strong apical dominance in V. thapsus may permit a temporal escape from damage via compensatory seed production on axillary branches after the main risk of weevil infestation has subsided. This system provides an excellent opportunity to test the reserve meristem hypothesis, which proposes that the suppression of lateral meristems and branches represents the principal adaptive value of strong apical dominance (Aarssen, 1995
).
We are primarily interested in testing whether fitness can be increased through delayed branching. Similar to the reserve meristem hypothesis, previous studies suggest that dormant or "reserve" meristems may facilitate an effective temporal escape from damage resulting from herbivory (Crawley, 1987
; van der Meijiden, 1990
; Whitham et al., 1991
; Vail, 1992
; Tuomi, Nilsson, and Astrom, 1994
; Nilsson, Tuomi, and Astrom, 1996
). The conditions that most likely support this interpretation are high predictability of damage, high cost of herbivory, and a low probability of repeat damage. Under the reserve meristem hypothesis as a potential explanation for the strong apical dominance and delayed branching exhibited by V. thapus, we can make the following predictions. At the population level, (1) the proportion of branched plants within a population will increase with increasing levels of weevil infestation, and at the individual plant level, (2) main stalk damage will be greater on branched plants than on unbranched plants of the same size, and (3) branching compensates for damage in terms of higher net seed production relative to similar-sized unbranched neighbors. The latter prediction is the critical test of the fitness consequences of strong apical dominance in V. thapus. These predictions were tested with two mensurative experiments on 50 populations of V. thapsus.
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METHODS |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONLITERATURE CITED |
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). Numerous, usually quiescent axillary meristems occur along the main stalk. Flowering is indeterminate from June through September (Naber and Aarssen, 1998
). The weevil G. tetrum oviposits in the flowers, and the developing larva effectively destroys most of the seeds (Reinartz, 1984a
). Weevil activity is confined largely to the first few weeks of flowering, and weevils are found primarily on the largest plants within a population (Naber and Aarssen, 1998
).
Population level
In September 1994, 50 populations of V. thapsus were selected close to Kingston, Ontario, Canada. A group of V. thapsus plants that composed at least 25 individuals within a few metres of each other was considered a population. Total population size and number of branched plants were recorded for each population.
At each population, the ten largest plants were selected (since only large plants branch). For each plant the following characters were recorded: height, number of branches, total branch length, total number of fruits on the main stem and on branches, and proportion of fruits infested by weevils on the main stem and on branches. A vertical transect was selected along the inflorescence, and all the fruits were opened along this length to assess the percentage of fruits damaged. Three categories of damage were used: undamaged fruits with full seed set; damaged fruits with minimal seed and either weevil larvae or frass evident; and damaged fruits with minimal seed set but no evidence of weevils (only 3% of the fruits were in this category).
A multiple logistic regression was used to test for the variables that were most important in predicting the proportion of branched individuals in a population. The variables tested were population size, mean height, and mean proportion of fruits damaged on the main stalks. The variance inflation factors were inspected to ensure low multicollinearity between the independent variables (all values were <2), and the independent variables were also checked for linearity in relation to the logit of proportion of individuals branched in a population (no transformations were necessary) (Sokal and Rohlf, 1981
). The mean values from the ten plants measured at each population were used to estimate the population-level effects, such as plant size and proportion of fruits damaged on the main stalk. Spearman rank-order correlations were used to test for associations between all variables (partial correlation results were inspected but did not significantly differ) and only significant correlations were reported.
Individual plant level
One pair of the largest individuals of V. thapsus were selected from each of the 50 populations described above. To control for plant size and microsite effects, groups of similar-sized individual plants all within 5 m were selected at the beginning of the growing season. At the end of the season, two plants were selected: one individual of the pair was unbranched and the other branched. Other than fruit infestation by weevils, there was no other damage evident on these plants.
In September 1994 after flowering had finished, height, number of branches, length of inflorescences, and total branch length were recorded in the field for each plant. Twelve mature fruits were randomly collected from each plant. The plants were harvested immediately following measurement.
In the laboratory, the total number of fruits and proportion of fruits infested by weevils were estimated for the top, middle, and bottom thirds of the main stalk inflorescence and (where appropriate) for the branch inflorescences. The inflorescence of the main stalk was divided into equal thirds based on length. A vertical transect of the inflorescence was used to estimate the number of fruits, and along this transect, each fruit was opened to assess weevil infestation. The categories of damage were clearly discernible: undamaged fruits had set full seed, damaged fruits either had a weevil larvae or frass present and always no seeds in at least one locule. A third category was used to account for unopened fruits that did not show any signs of weevil infestation but also did not have any seeds in them (0.0009% of the fruits were in this category).
Total seed production for each plant was calculated from the average number of seeds per undamaged fruit (N = 9–12) multiplied by the total number of fruits. This value was then adjusted to reflect the degree of weevil infestation for each plant. The plants were then dried at 85°C for 48 h, and aboveground dry biomass was recorded. Seed per gram of plant biomass was also calculated.
Height, dry mass, main stalk damage, and total seed production were compared between branched and unbranched plants using paired t tests. Within the branched plants, damage on the main stalk and branches was compared using a paired t test. The degree of damage on the four inflorescence positions (branch, top main, middle main, and bottom main) were compared using a nonparametric Kruskal-Wallis ANOVA since transformations of the proportion of fruits damaged failed to improve normality (Zar, 1974
). All statistical analyses were done using JMP 3.2.1 (SAS, 1997
).
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RESULTS |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONLITERATURE CITED |
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Individual plant-level comparison
There was no significant difference in height between the branched and unbranched individuals of V. thapsus selected for the pairwise comparison (paired t test, t = 0.1229, P = 0.9027, means: branched 170.8 cm, unbranched 171.4 cm, N = 50). However, branched plants were significantly larger in terms of dry mass biomass (paired t test, t = -4.749, P = <0.0001, means: branched, 194.74 g; unbranched, 124.36 g; N = 50).
The proportion of fruits on the main stalk that were damaged by weevils was significantly greater in branched plants (paired t test, t = -2.421, P = 0.0195, N = 50); while the proportion of fruits damaged within the branched plants was significantly greater on the main stalk than on the branches (paired t test, t = 6.715, P < 0.0001, means: branches, 0.4057, main stalk, 0.7123; N = 49 pairs). Analysis of the proportion of fruits damaged in terms of position generated the following relationship: branches < top of main stalk < bottom of main stalk < middle of main stalk (Kruskal-Wallis ANOVA, H = 48.74, P < 0.0001, df = 3) (Fig. 1). Only the proportion of fruits damaged on the bottom and middle of the main stalk were not significantly different (Dunn's method, pairwise multiple comparison at P < 0.05).
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONLITERATURE CITED |
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). Evidence from the two mensurative experiments reported here supports this prediction. Branched plants, although more damaged, produced significantly more seeds and more seeds per gram of biomass than similar-sized unbranched neighbors (Fig. 2). It is therefore reasonable to suggest that delayed branching in V. thapsus overcompensates for damage.
The population-level prediction is that the proportion of branched individuals within a natural population will increase with increasing levels of weevil infestation at that site. The mean proportion of fruits damaged on ten plants was used as the population parameter estimate and did not significantly predict the proportion of individuals branched within the populations sampled (Table 1). A simple explanation is plausible. Population size was negatively associated with the proportion of fruits damaged on the main stalk, and population size acted as a significant predictor variable for the proportion of individuals branched (Table 1). Given the cosmopolitan distribution of weevils in this area, smaller populations were subject to greater infestation by weevils. This suggests that the predictability of damage increases in smaller populations as the ratio of weevil abundance to plant abundance increases. This supports a limited body of evidence, which also found that low-density host populations have greater damage (i.e., Cromartie, 1975
; Segarra-Carmona and Barbosa, 1990
; Kunin, 1999
). Clearly, at a population level other processes interact, which do not allow the reserve meristem hypothesis to accurately predict population-level trends. The predictions associated with this hypothesis should therefore be used with individual-level response with relation to branching and fitness and not extended to population-level effects.
According to the reserve meristem hypothesis, the degree of damage should be severe, predictable, and decrease in time. In V. thapsus, there was severe damage early in the growing season with the lower and middle thirds of the inflorescences on the main stalks having 88 and 90% of the fruits damaged by weevils, respectively, while the proportion of fruits damaged at the top of the main stalk and on branches was significantly lower (Fig. 1). This suggests that there was a high predictability of risk initially, but that fruits developed later in the season were likely subject to lower risk.
The reserve meristem hypothesis predicts that branched plants should be more damaged than unbranched plants. In V. thapsus, the proportion of fruits damaged on the main stalk was significantly greater in the branched plants. Main stalk damage may even act as a proximate cue that elicits the branching response. The second prediction is that branching should increase net seed production. This prediction was also supported in that branched plants produced significantly more seeds than unbranched plants (Fig. 2). An alternative strategy that may also act as an escape in time is the indeterminate growth of the main stalk. Later developed fruits may simply escape damage regardless of position. However, branches were significantly less damaged than the fruits at the top of the main inflorescence (Fig. 1). Thus, later developed fruits are less damaged in either position, but branches are more effective in this compensatory effect. This is comparable to a compensatory effect through added branches following damage as found in other species (Argall and Stewart, 1984
; Aarssen and Turkington, 1987
; Benner, 1988
; Maschinski and Whitham, 1989
; Hicks and Reader, 1995
).
Overcompensation through branching seems plausible in V. thapsus. Coupled with decreased damage of branches, greater net seed production, greater seed per gram of plant biomass, and increased biomass of branched plants all suggest that fitness is dramatically increased relative to unbranched individuals. This is supported in the overcompensation literature (Binnie and Clifford, 1980
; Inouye, 1982
; Sheldon, 1986
; Paige and Whitham, 1987
; Maschinski and Whitham, 1989
; Michaud, 1991
; Fox, 1995
), but in this study apical dominance was not disrupted by damage to the shoot apex. Hendrix (1979)
also detected a compensatory effect without shoot apex removal in Pastinaca sativa using flower and fruit destruction by the parsnip webworm larvae Depressaria pastinacella. This suggests that more subtle mechanisms of delayed release may respond to herbivore-induced disruption from which the plant may compensate.
In summary, the reserve meristem hypothesis was supported as one explanation for strong apical dominance and delayed branching in Verbascum thapsus. It was not possible to predict population-level processes under this hypothesis as other factors such as density-dependence may come into play. Nonetheless, branched individuals sustained higher levels of main stalk damage and still produced more seeds.
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FOOTNOTES |
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2 Author for correspondence, current address: Department of Botany, University of British Columbia, Vancouver, British Columbia, Canada V6T 1Z4 (Tel: 604-822-270; FAX: 604-822-6089; e-mail: lortiec{at}interchange.ubc.ca,
www.interchange.ubc.ca/lortiec/chris.htm).
3 Tel: 613-545-6133; FAX: 613-545-6617; e-mail: aarssenl{at}biology.queensu.ca
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONLITERATURE CITED |
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