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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 • herbivory • reproductive tissue • reserve meristem • Scrophulariaceae • Verbascum thapsus.
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONLITERATURE CITED |
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). Thus, apical dominance through delayed branching may act as a "bet-hedging" strategy or escape in time (Crawley, 1987
; van der Meijden, 1990
; Whitham et al., 1991
; Vail, 1992
; Tuomi, Nilsson, and Astrom, 1994
; Nilsson, Tuomi, and Astrom, 1996
). The reserve meristem hypothesis therefore explicitly predicts that damage induces branching through the release of apical dominance. In the present study, the primary focus was to test for a branching response to explain the natural growth pattern of Verbascum thapsus L.
Typically, studies of plant responses to damage (compensation) focus almost exclusively on ungulates and either use grazing pressure as an independent variable or simulate this damage by removing the shoot apex (i.e., McNaughton, 1979, 1983
; Inouye, 1982
; Argall and Stewart, 1984
; Aarssen and Turkington, 1987
; Paige and Whitham, 1987
). Unfortunately, field experiments rarely varied either the type of damage (removal of shoot apex) or the measure used to estimate the plant response (usually biomass). In this study, we extend the compensation literature in the following three ways: (1) the herbivore is an invertebrate. (2) the damage is novel in that we prevent seed set and leave the shoot apex intact, and (3) the response variable is degree of branching. Under the reserve meristem hypothesis, branching may be an important form of compensation in itself.
Verbascum thapsus displays exceptionally strong apical dominance. Thus, most plants do not branch, however branching may infrequently occur in the largest individuals (Naber and Aarssen, 1998
). Verbascum thapsus is also subject to seed predation by the weevil Gymnetron tetrum (Reinartz, 1984
); greater damage occurs on the primary stalk than on axillary branches and mainly in larger plants (Lortie and Aarssen, personal observation). Given that the largest plants are the most damaged and the most branched (Naber and Aarssen, 1998
), the branching response should be sensitive to fruit damage of the main stalk.
We tested whether there was a branching response in the present study by preventing seed set, by experimental addition of weevils, and by damaging fruits in natural populations of V. thapsus and recording the effects of these treatments on degree of branching.
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METHODS |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONLITERATURE CITED |
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; Reinartz, 1984
). The stem is 0.3–2.0 m tall (Gross and Werner, 1978
) with axillary meristems along the main stalk and a terminal inflorescence. Flowering is indeterminate and takes place from late June through late August. Flowers open in whorls daily along the axis of the inflorescence. Each flower is open for 1 d and may self-pollinate when the corolla dehisces at dusk.
The weevil G. tetrum oviposits in the flowers daily, and the developing larvae effectively destroy most of the seeds (Reinartz, 1984
). However, weevil activity is confined largely to the first few weeks of the flowering season (Lortie and Aarssen, personal observation). Weevils are primarily found on larger plants within a population and their distribution is virtually cosmopolitan in the Kingston area, Canada (Lortie and Aarssen, personal observation).
Prevention of seed set
Eighty pairs of the largest individuals of V. thapsus were selected at two populations in Kingston, Ontario, Canada (50 and 30 pairs; 44°15' N, 76°34' W, and 44°23' N, 76°18' W, respectively). All plants were in their second year of growth and had begun to bolt. The largest plants were selected based on an index of height, caudex diameter, and rosette size. Plants were assigned to pairs based on nearest same-sized neighbor and to a treatment or control group randomly within each pair.
The treatment was applied from 5 July 1995 to 3 August 1995 and involved stigma excision and application of lanolin to the style to prevent seed set. The majority of the flowers (including those that developed on branches) were treated as they developed daily for the length of the flowering season for each plant (weather and time permitting). Plants were treated at sunrise before pollinator activity had begun and were marked with nontoxic acrylic paint to ensure identity at harvest. Total number of treated flowers was recorded daily for each plant. Control plants were not treated.
Both populations were spot sprayed once with insecticide (Dursban 4E) on 15 June 1995 to eradicate the weevil Gymnaetron tetrum. Further treatments involved hand removal of any additional weevils that were detected during the study, which could have introduced confounding effects. Populations were checked daily over the length of the growing season to ensure that no weevils were present.
On 25 August 1995 when the majority of fruits had developed, height, number of branches, and total branch lengths were recorded for all pairs of plants. Ten fruits were randomly selected from each of 12 pairs of plants (six pairs at each population) to determine mean seed number and the effectiveness of treatment. One hundred seeds from each sample were selected and grown in petri dishes (batches of 25) for 12 d. Fluorescent light benches were used with 24 h of continuous light. The number of germinated seeds was recorded for each sample. Seedlings were dried for 24 h at 70°C and then weighed to calculate growth rate as a measure of seed quality.
Weevil addition
One hundred and fifty pairs of mating G. tetrum weevils were collected from V. thapsus plants between 15 and 20 June 1995. Another 75 single adult weevils were also collected. All weevils were stored in flasks at room temperature for a few days until placed on plants. Each pair collected was stored separately. Pieces of V. thapsus leaves and sand were placed at the bottom of each flask, and water was supplied daily. The flasks were sealed with cloth mesh to allow air circulation.
From a single population of V. thapsus that was naturally weevil free (very isolated and only recently disturbed) in Kingston, Ontario (44°22' N, 76°27' W), 50 pairs of the largest unbranched plants that had not begun flowering were selected. Plants in a pair were always within 5 m of each other and were approximately the same size. A pairwise design was used in an attempt to control for size, microsite conditions, and relatedness given that 75% of V. thapsus seeds fall within 1 m of the parent plant and 93% fall within 5 m (Gross and Werner, 1978
).
Treatment was initiated on 22 June 1995, when two pairs of weevils and at least one additional weevil were placed on randomly selected plants from each pair. Mating pairs of weevils were used to ensure that at least two fertilized females were present to oviposit in the developing flowers. Cloth mesh enclosures covered the entire plant, and extra material was left at the top to permit plant growth. Control plants were left to develop naturally without weevils, but they were also enclosed with cloth mesh to prevent contact by weevils from other sources and to account for the cloth mesh treatment.
Plants were checked twice a week to ensure that weevils had not escaped from the enclosures. No damage to the plant stalk or branches was evident over the duration of the study period. Weevil behavior was also monitored. On 16 August 1995 after the last of the plants had finished flowering and had initiated fruit development, final height, number of branches, total branch lengths, presence of weevils, and fruit damage were recorded for each plant.
Fruit destruction
Seventy pairs of the largest unbranched plants of V. thapsus were selected from two populations—50 pairs at the first and 20 at the second (population A—44°28' N, 76°58' W; population B—44°23' N, 76°16' W) just after the initiation of fruit set on all plants (8 August 1995). Treated plants were selected randomly within each pair, and all fruits on the treated plants were sliced in half lengthwise twice. Thus, the fruits were damaged but not removed from the plants. Control plants were left to develop naturally. On 4 September 1995, final height and number of branches were recorded for all plants. Seed set in the damaged fruits was also assessed.
Data analyses
Preliminary analysis revealed no population effect for any of the characters examined in all three experiments (ANOVA: P > 0.05). Hence, the data from the populations were pooled within each experimental analysis. To test for differences between the control and treated plants, paired t tests were performed on the appropriate response variables. All statistics were performed using Jmp Version 3.2.1 (SAS, 1997
).
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RESULTS |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONLITERATURE CITED |
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The number of branches and total branch length on treated plants were significantly greater than on control plants (paired t tests, number of branches: t =-2.726, P = 0.0079, means: treated, 1.1; control, 0.6; and branch length: t =-2.996, P = 0.0037, means: treated, 14.96 cm; control, 5.94 cm; N = 80). Therefore, branching significantly increased with treatment (Fig. 1A, B).
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Fruit destruction
The treatment was effective in that damaged fruits did not continue to set seed but remained intact on the plants; however, none of the plants (treated or control) in this experiment branched (N = 140).
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONLITERATURE CITED |
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The prevention of seed set and weevil addition experiments significantly increased branching. The comparison of seed quality in terms of germination and seedling growth rate was not significantly different between control and treated plants in the prevention of seed set experiment, which is consistent with the reserve meristem hypothesis. Fitness differences are therefore most likely manifested in branched plants through seed number but not seed quality. There were also no significant differences in final height between control and treated plants for either experiment (seed set and weevil addition); hence, branched plants change architecture but not necessarily size. These two experiments clearly explain why larger plants are more branched.
The fruit destruction experiment effectively halted seed production in natural populations of V. thapsus, which are typically infected with weevils. The complete lack of branching by any plants in this experiment suggests that the timing of damage is integral to the branching response, i.e., the treatment was too late in this case. Damage could also be imposed at an even earlier point in time developmentally than any of the three experiments in this study. Under the primigenic dominance hypothesis, early-developing sinks inhibit later developing sinks through correlative inhibition (Bangerth, 1989
). It is the sequence of meristem development that is important and not necessarily the position on the plant. This hypothesis makes predictions similar to the reserve meristem hypothesis as removal of earlier sinks (or prevention of their development) should release later developing organs such as branches. While the primigenic dominance hypothesis is not supported here, it does suggest an alternative treatment to investigate the interaction between reproduction and apical dominance. The removal of floral buds may be a more effective means for determining the role of reproduction and timing of damage on apical dominance in some species.
Another simple explanation could be used to interpret the findings of this study. Larger plants have more resources and are therefore capable of compensation via increased branching following damage (as compared to smaller individuals). However, the addition of water and nutrients failed to increase branching in the absence of shoot apex damage (Lortie and Aarssen, 1997
). Thus, without a major disruption to the shoot apex, the strength of apical dominance in V. thapsus is not affected by resource status. Some form of damage is required to elicit the branching response observed in this study. Interestingly, we were able to change the strength of apical dominance here without manipulating the shoot apex itself.
The experimental design we used successfully simulated natural granivory under field conditions. To the best of our knowledge, no other studies have sought to directly manipulate seed production and damage thereof in situ to test related hypotheses. Prevention of seed set in V. thapsus was the most direct test of the proposed hypothesis. Stigma removal and lanolin application affected a dramatic reduction in seed set. The direct addition of weevils and the destruction of fruits shortly after initiation were also highly effective at reducing the seed production of the plants.
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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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LITERATURE CITED |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONLITERATURE CITED |
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———, and R. Turkington. 1987 Responses to defoliation in Holcus lanatus, Lolium perenne, and Trifolium repens from three different aged pastures. Canadian Journal of Botany 65: 1364–1370
Argall, J. F., and K. A. Stewart. 1984 Effects of decapitation and benzyladenine on growth and yield of cowpea (Vigna unguiculata (L.) Walp.). Annals of Botany 54: 439–444
Bangerth, F. 1989 Dominance among fruits/sinks and the search for a correlative signal. Physiologia Planta 76: 608–614[CrossRef]
Crawley, M. J. 1987 Benevolent herbivores? Trends in Ecology and Evolution 2: 167–168
Gross, K. L., and P. A. Werner. 1978 The Biology of Canadian weeds. 28. Verbascum thapsus L. and V. blattaria L. Canadian Journal of Plant Sciences 58: 401–413
Inouye, D. W. 1982 The consequences of herbivory: a mixed blessing for Jurinea mollis (Asteraceae). Oikos 39: 269–272
Lortie, C. J., and L. W. Aarssen. 1997 Apical dominance as an adaptation in Verbascum thapsus: effects of water and nutrients on branching. International Journal of Plant Sciences 158: 461–464[CrossRef][ISI]
McNaughton, S. J. 1979 Grazing as an optimization process: grass-ungulate relationship in the Serengeti. American Naturalist 113: 691–703[CrossRef][ISI]
———. 1983 Compensatory plant growth as a response to herbivory. Oikos 40: 329–336[CrossRef][ISI]
Naber, A. C., and L. W. Aarssen. 1998 Effect of shoot apex removal and fruit herbivory on branching and reproduction in Verbascum thapsus (Scrophulariaceae). American Midland Naturalist 140: 42–54[CrossRef][ISI]
Nilsson, P., J. Tuomi, and M. Astrom. 1996 Bud dormancy as a bet-hedging strategy. American Naturalist 147: 269–281[CrossRef][ISI]
Paige, K. N., and T. G. Whitham. 1987 Overcompensation in response to mammalian herbivory: the advantage of being eaten. American Naturalist 129: 407–416[CrossRef][ISI]
Reinartz, J. A. 1984 Life history variation of common mullein (Verbascum thapsus). I. Latitudinal differences in population dynamics and timing of reproduction. Journal of Ecology 72: 897–912[CrossRef][ISI]
SAS. 1997 Jmp 3.2.1. SAS Institute, Cary, North Carolina, USA
Tuomi, J., P. Nilsson, and M. Astrom. 1994 Plant compensatory response: bud dormancy as an adaptation to herbivory. Ecology 75: 1429–1436[CrossRef][ISI]
Vail, S. G. 1992 Selection for overcompensatory plant responses to herbivory: a mechanism for the evolution of plant-herbivore mutualism. American Naturalist 139: 1–8
van der Meijden, E. 1990 Herbivory as a trigger for growth. Functional Ecology 4: 597–598
Whitham, T. G., J. Maschinski, K. C. Larson, and K. N. Paige. 1991 Plant responses to herbivory: the continuum from negative to positive and underlying physiological mechanisms. In P. W. Price, T. M. Lewinsohn, G. Wilson Fernandes, and W. W. Benson [eds.], Plant-animal interactions: evolutionary ecology in tropical and temperate regions, 227–256. Wiley, New York, New York, USA
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