49
Plant Ecology 166: 49–61, 2003. © 2003 Kluwer Academic Publishers. Printed in the Netherlands.
Grazing tolerance of Gentianella amarella and other monocarpic herbs: why is tolerance highest at low damage levels? Ari-Pekka Huhta 1,2,*, Kalle Hellström 1, Pasi Rautio 1 and Juha Tuomi 1 1
Department of Biology, University of Oulu, P.O. Box 3000, FIN-90014, Finland; 2Current address: Botanical museum, University of Oulu, P.O. Box 3000, FIN-90014, Finland; *Author for correspondence (e-mail:
[email protected]; phone +358–8–553 1562; fax +358–8–553 1061) Received 5 September 2000; accepted in revised form 7 March 2002
Key words: Apical dominace, Branching, Clipping, Herbivory, Overcompensation, Regrowth Abstract Plants have adapted to compensate for the loss of vegetative biomass and reproductive potential caused by grazing. Shoot damage breaks down the correlative inhibition maintained by apical dominance. The consequent increased branching may lead to increased production of flowers and fruits in damaged plants, provided that enough resources, both in terms of meristems and nutrients, are available. In Gentianella amarella, the removal of the apex of the main stem (10% clipping) had no pronounced effect on branching and plant performance. In one of the two study populations, however, apically damaged plants produced more fruits than undamaged control plants. The plants also fully compensated for 50% removal of the main stem in terms of above-ground biomass, but their fruit production was reduced compared to control and apically damaged plants. After 75% clipping, fruit production was not significantly reduced compared to 50% clipping. Consequently, G. amarella showed highest tolerance in the presence of minor shoot damage. The pattern is qualitatively similar in some other monocarpic species (Gentianella campestris, Erysimum strictum and Rhinanthus minor). Multiple constraints as well as selective forces may shape these compensatory responses: (1) A lack of basal meristems may constrain tolerance of high damage levels. (2) Species with basal meristems may have a potential to tolerate major damage, but a shortage of resources or otherwise unfavourable growth conditions may constrain their compensatory ability. (3) It may be adaptive to have maximum tolerance of low and moderate damage levels if chemical defences reduce the risk of extensive shoot damage as well as the risk of repeated grazing. (4) The compensatory ability of monocarpic species may be affected by selective forces that favour fast vertical growth early in the season and unbranched architecture in undamaged conditions. Therefore, it is not the mere grazing history, but also other factors associated with growth conditions that are required to explain the variation in grazing tolerance. Introduction Herbivores have a major impact on plant growth, reproductive ability and subsequent survival (Whitham et al. 1991). Generally, consumers cause significant losses to plant biomass and fecundity (Belsky 1986; Crawley (1987, 1997)). However, some plants are tolerant of grazing (Beard 1973; McNaughton 1986) and may partially or fully compensate for the lost vegetative biomass or reproductive potential (Kemp 1937; Paige and Whitham 1987; Lennartsson et al. (1997, 1998)). The degree of compensation varies from un-
dercompensation (grazed plants perform less well) and full compensation (grazed and ungrazed plants perform equally well) to overcompensation (grazed plants perform better than ungrazed ones; McNaughton (1979, 1983) and Belsky (1986), Paige and Whitham (1987)). The degree of compensation is often sensitive to the timing and intensity of damage (Maschinski and Whitham 1989; Alward and Joern 1993; Trumble et al. 1993; Paige 1994; Lennartsson et al. 1998). Species also differ as to their compensatory capacity. Some species are easily able to compensate for their lost tissue, while other species are
50 less tolerant of shoot damage (Verkaar 1986; Prins et al. 1989). In addition, there seems to be great variation in grazing tolerance even within species (Bergelson and Crawley (1992a, 1992b); Bergelson et al. 1996; Lennartsson et al. 1997; Paige 1999). Consequently, plant responses to herbivory attack are highly variable. The effect of grazing varies from immediate death to increased growth of damaged plants (Wandera et al. 1992). Herbivores affect plant architecture directly by cutting shoots and indirectly by changing apical dominance. When the uppermost meristems are removed or injured by herbivores, the production of auxin is interrupted, which, in turn, releases previously inhibited lateral buds (Phillips 1975; Hillman 1984). Repeated herbivory on the same individual perennial woody plant may lead to a highly branched, broom-like growth form (Mopper et al. 1991). The presence of apical dominance and lateral branching is supposed to reflect the adaptation to competition for light, since in their competition to reach a light gap, unbranched individuals are likely to succeed better than individuals that share their limited resources between vertical growth and the production of secondary branches (Aarssen and Irwin 1991). According to Järemo et al. (1996), however, if the evolutionary history of a plant involves both competition for light and herbivory, the latter is bound to be decisive. Competition directs selection towards a capacity to modify architecture, which, in turn, is used and further improved to cope with herbivores. In the present study, we tested the tolerance of the biennial herb Gentianella amarella over a range of damage levels from minor apical damage to more extensive shoot damage in two populations in northern Finland. Lennartsson et al. (1997, 1998) have studied the grazing tolerance of a related species, G. campestris. In some populations, damaged plants overcompensate for shoot damage (50% of the main stem removed), whereas in other populations, such plants compensate only partially or at best fully. Similar variation has also been seen in G. amarella. T. Lennartsson (unpublished data in Järemo et al. (1996)) found evidence of overcompensation in one of his eleven study populations. In this population, the removal of 50% of shoot biomass improved fruit production, but reduced seed number per fruit and seed weight. In overcompensating populations of G. campestris, shoot damage did not affect either seed number per fruit or seed weight (Lennartsson et al. 1997). According to these common garden experiments, both species tolerate simulated grazing rela-
tively well, but overcompensation is presumably more common in G. campestris than in G. amarella. The second aim of this study is to compare the observed compensatory responses of Gentianella amarella to a few other monocarpic herbs for which similar data are available. These species are Gentianella campestris (Huhta et al. 2000b), Erysimum strictum and Rhinanthus minor (Huhta et al. 2000a). In most cases, the general shape of the compensatory responses is qualitatively similar, although deviating patterns were also found. This comparison indicates that experiments testing for tolerance at a fixed damage level may not provide firm grounds for broad generalizations. Maximum tolerance is achieved at low damage levels in some cases and at higher damage levels in others. The need to explain this variation provides a major challenge to plant-herbivore research.
Material and methods Study species and populations Autumn gentian, Gentianella amarella L. (Gentianaceae), is a circumpolar species of temperate and cool regions (Hultén and Fries 1986). The seeds of this biennial herb germinate in spring. It forms a rosette in the first summer and flowers in the second summer. According to Hämet-Ahti et al. (1998), G. amarella includes two taxons, the early-flowering (June-July) var. lingulata and the late-flowering (August-September) var. amarella. In appearance, the early-flowering taxon differs from the late-flowering one by having two to three fewer internodes and less pointed leaves, though a number of intermediate forms are also reported (Kytövuori 1980). The study populations belong to the early flowering type, although notable variation in flowering time exists within both populations. The flowering peak occurs in mid-July, and the latest flowering individuals were observed in Kuusamo in late September. The plants usually grow to be 15-20 cm tall, though there is also a great deal of variation in size from a few centimeters up to 40 cm. The distribution of G. amarella in Finland is fairly scattered due to its calcicole nature and the scarcity of lime-rich habitats. It is regarded as native in most part of Finland, but traditional agriculture has favored its propagation to human-influenced habitats. Management has compensated for the lack of lime in soil
51 in a way that enables the species to occur in soils with a somewhat lower pH than its postulated physiological optimum (cf. Ekstam et al. (1988)). In fact, in many of its archaeophytic occurrences G. amarella has severely declined after the discontinuation of traditional land use, i.e. mowing and grazing (HämetAhti and Suominen 1993). Presently, the species is red-listed in Finland (Rassi et al. 1991). Melalahti village (64°20⬘ N, 27°30⬘ E) belongs to the rural community of Paltamo (NE Finland). The habitat of the Melalahti population is a pasture, which has been grazed for at least 60 years (Latvalehto 1997). In recent years, however, the grazing pressure has decreased considerably (Latvalehto 1997). The pasture was earlier grazed by sheep, nowadays by cattle. During the experiment in 1998, an area of about 3 hectares was grazed by five young cows. The grazing period lasted from July till the end of September. According to Påhlsson’s (1994) classification of meadow types, the vegetation type in Melalahti resembles the Leucanthemum type, although the species combination differs even with regard to some dominant species. Most of the G. amarella individuals concentrate around short-grass stands surrounding exposed bedrock and characterized by low-growing species, e.g. Antennaria dioica, Erigeron acer, Fragaria vesca ja Pilosella offıcinarum. The two calcicoles that indicate dolomite disclosures along with G. amarella are Carex capillaris and Selaginella selaginoides. Taller species, such as Anthriscus sylvestris, Carum carvi, Epilobium angustifolium, Geranium sylvaticum ja Ranunculus acris, colonize the immediate surroundings of the short-grass meadows. The taxonomic nomenclature is as proposed by Hämet-Ahti et al. (1998). The high calcium concentration (3640.6 mg/l) is also reflected in the soil pH value, which is about 6.7 in the short-grass stands (Latvalehto 1997). The Liikasenvaara village lies in Kuusamo (NE Finland) close to the Russian border (66°20⬘ N, 29°30⬘ E). Small isolated populations of G. amarella occur here and there along the scarcely vegetated Likasenvaara village road verge through Oulanka National Park. Our study population was the largest we found, consisting of several hundreds of plants. The number of flowering individuals varies considerably from year to year due to variation in temperature and rainfall, which is typical of annual and biennial species (Pitt and Heady 1978). Accompanying species for G. amarella in Kuusamo are Achillea millefolium, Euphrasia stricta, Melampyrum sylvaticum, Parnas-
sia palustris, Ranunculus acris, Rhinanthus minor, Trifolium repens and T. pratensis. Moreover, the same calcicoles, i.e. Carex capillaris and Selaginella selaginoides, are also present here. Unlike in Paltamo, the Kuusamo population suffers no regular disturbances. However, the road verges are irregularly mown in order to remove high vegetation and this may occasionally cause minor damages also on G. amarella. Experimental design The plants were cut at an interval of 1–1.5 weeks before flowering: on July 7th in Kuusamo and on July 16th in Paltamo. Equal-sized individuals were marked and thereafter distributed randomly between the treatment groups. Each treatment group consisted of 15 individuals at the beginning of the experiment. The cutting intervals were specified based on the increasing number of internodes removed (0%, 10%, 50% and 75%). Control plants were left intact, whereas in the 10% cutting the uppermost flower was removed. In the 50% cutting, two or three internodes were removed, leaving approximately three internodes that responded to the recovery process. In the 75% treatments, at least three internodes were always removed and one or two retained. Additionally, the immediate surroundings of each plant were mown at about 5 cm height, to prevent overtopping by competitive species and to give all replicate plants equal starting conditions. Despite the low grazing pressure in Paltamo, there were some indications of trial attempts at browsing by cattle among some of the marked (rejected from the processed data) and the nearby nonmarked individuals (down to 11 cm height, 1–2 upper internodes removed) corresponding to more than 10% but less than 50% of artificial clipping. Some of the individuals had to be rejected from the further data processing because some of them were mown in the road verge by a mowing machine in Kuusamo or eaten by cattle in Paltamo. The final number of plants in each treatment group varied between 10 and 11 in Kuusamo and between 11 and 14 in the Paltamo population. The plants were collected when the fruits had fully ripened: on September 7th in Kuusamo and on September 21st in Paltamo. Plant performance was measured by means of the final height, above- and belowground biomass, number of branches, number of fruits, number of seeds/fruit, seed weight and number of unfertilized ovules/fruit. For the biomass estimates, plants were oven-dried at 60 °C for two days. Two
52 fruits per plant, one from the upper and the other from the lower part of the plant, were used to estimate the number of seeds/capsule and the number of unfertilized ovules. Since part of the seeds had already fallen out of the capsules, the number of seed scars was used as an estimate for total seed number/capsule (Lennartsson et al. 1997). Due to a mold attack in the Kuusamo population, too few seed weight values among the control and 75%-treated plants were obtained to evaluate the impacts of cutting. The data on seed weight are therefore not presented. The 1st order branches were divided into low- and upper-node branches. The low-node branches emerge from the first node close to the ground, while the upper-node branches initiate from any node above the lowest node. A structure including at least one internode was regarded to be a branch, but a leafless pedicel growing from main stem was not. Because there was only one plant with one secondary branch in the Paltamo population, the number of secondary branches was omitted from further analysis. The proportional biomass and fruit production curves in relation to damage level were obtained by multiplying the estimated average parameter values in such a way that the control plants achieved a value of 100. The curve was drawn by connecting the treatment means. The shapes of the curves thereby obtained were compared to some other monocarpic species, Gentianella campestris (Huhta et al. 2000b), Erysimum strictum and Rhinanthus minor (Huhta et al. 2000a). Both G. campestris (Gentianaceae) and E. strictum (Brassicaceae) are biennial, while R. minor (Scrophulariaceae) is an annual species. All these studies have been carried out with the same experimental procedure and design in natural growth conditions. All other studies have been conducted in NW and NE Finland, except that on the Björnvad population of G. campestris, which is located in SE Sweden (Huhta et al. 2000b). Statistical analysis The data were analyzed by means of two-way factorial ANCOVA with origin (Kuusamo and Paltamo) and cutting intensity (0, 10, 50 and 75% of internodes removed) as factors and initial (before cutting) height as covariate. The assumption of homogeneity of variances was tested by using Levene’s test. If variances were heterogeneous, transformations (lg x+1, 冪x+0.5 or rank transformation) were applied to obtain homogeneity. The test results for transformed variables are
not reported because they did not differ from those of the original values (cf. Montgomery (1984), p. 118). Multiple comparisons of the levels of cutting intensity were performed (for original untransformed variables) using the LSD procedure (Saville 1990). In the case of a number of low-node branches in the Paltamo population, only 1-4 plants per treatment had lownode branches, and the effect of cutting intensity on the number of low-node branches was hence studied only in the Kuusamo population by means of one-way ANCOVA. Pearson’s correlation coefficient (r) was used to assess the relation between the number of branches per plant and the number of fruits per plant.
Results Tolerance of autumn gentian: regrowth, shoot architecture, and reproduction The covariate (initial height before clipping) had a significant effect on all the performance measures studied (Table 1). Origin had a significant interaction effect with treatment (clipping) on the number of seed scars (Table 1). No other significant interaction effects were found, although there was a statistically significant difference in branching intensity between the study populations (Table 1). Clipping had statistically significant effects on all the performance measures presented in Table 1. Clipping tended to decrease both final height and above-ground biomass. Apical damage (10% clipping) of the main stem had no profound effect on final height in Paltamo (Figure 1A), and in Kuusamo the apically damaged plants tended to be slightly taller than the control plants (Figure 2A). However, higher damage levels (50–75% clipping) significantly reduced plant height both in Paltamo (Figure 1A) and in Kuusamo (Figure 2A). The overall pattern in above-ground biomass was similar, except that the clipped plants were able to fully compensate for their biomass losses up to 50% removal of the main stem (Figure 1B) and even to 75% clipping (Figure 2B). In both populations, the above-ground biomass of 75% clipped plants was significantly lower compared to 10% clipping. Consequently, clipping decreased final height more than above-ground biomass, and apical damage as such had no significant effect on these performance measures. There was no indication of re-allocation of resources into shoot growth at the cost of root growth (Figures 1C and 2C)), as there
53 Table 1. Effects of origin (Paltamo vs. Kuusamo) and treatment (clipping) on three vegetative and two reproductive characters. Measured parameter ANCOVA Initial height (cov) Origin Treatment Interaction
Height (cm)
Above ground biomass (g)
Number of branches
Number of fruits
Number of seed scars
F 1,81 47.35 P < 0.001 F 1.81 1.44 P = 0.234 F 3,81 81.57 P > 0.001 F 3,81 1.03 P = 0.383
F 1,79 18.64 P < 0.001 F 1,79 3.24 P = 0.076 F 3,79 7.37 P > 0.001 F 3,79 1.05 P = 0.38
F 1,80 9.46 P = 0.003 F 1,80 4.69 P = 0.033 F 3,80 7.50 P > 0.001 F 3,80 1.29 P = 0.283
F 1,79 12.61 P = 0.001 F 1,79 0.024 P = 0.877 F 3,79 11.37 P > 0.001 F 3,79 1.42 P = 0.242
F 1,65 9.21 P = 0.003 F 1,65 0.68 P = 0.414 F 3,65 11.44 P > 0.001 F 3,65 3.28 P = 0.026
was no statistically significant effect of clipping on below-ground biomass (ANCOVA, clipping: F 3, 71 = 1.840, P = 0.148; origin × clipping: F 3,71 = 1.77, P = 0.160). Clipping increased branching intensity in both populations. This was most pronounced in Paltamo, where apical damage as such did not increase branching, but 50% and 75% clippings induced vigorous branching (Figure 1D). The number of branches more than doubled in the 50% and tripled in the 75% clipping treatments as compared to the control group. In Kuusamo, branching intensity increased more gradually along with the increasing damage level, but due to the high variance, there were no statistically significant differences between the treatment groups (Figure 2D). A schematic representation of the cutting responses seen in the Kuusamo population is presented in Figure 3. The 10% cut plants did not differ in appearance from the control plants because apical damage did not induce branching from basal meristems. In contrast, 50% removal of the main stem induced vigorous branching from the lower nodes. The pattern was similar in the 75% cut plants, but they remained smaller compared to the other treatment groups. Branching patterns also differed between the two locations (Figure 4). In Kuusamo, the proportion of low-node branches, i.e. branches emerging from the first node close to the ground, increased along with the degree of damage (ANCOVA, clipping: F 3,36 = 4.20, P = 0.012). The number of low-node branches was higher in the 75% clipped plants than in the control plants or 10% clipped plants (black part of the column in Figure 4). The number of low-node branches in the Paltamo population was not tested statistically because very few plants in that population had low-node branches. Hence, the proportion of low-node branches tended to be lower in
that population than in the Kuusamo population (Figure 4). Fruit production responded similarly to increasing clipping in the two populations. In Paltamo, the 10% cut plants showed equal fruit production compared to the control plants (Figure 1E). In Kuusamo, the apically damaged plants produced slightly more fruits than the control plants (Figure 2E). Higher damage levels reduced fruit production. The decrease was about 40% in Paltamo and 23% in Kuusamo after 50% clipping. The difference was not significant in Kuusamo. The removal of 75% of the main stem did not further decrease fruit production (Figures 1E and 2E). Thus, mere apical damage induced full compensation or slight overcompensation, whereas higher damage levels tended to affect fruit production adversely. Interestingly, the removal of 50–75% of the main stalk strongly increased branching, but the increased branching intensity did not lead to increased fruit production at these damage levels. In spite of this, there were positive correlations between fruit production and branching intensity within each treatment group, except in the control plants in the Kuusamo population (Table 2). An estimate of seed production was obtained by counting the number of seed scars. In the Paltamo population, the seed number of the 10% clipped plants did not differ from that of the controls, but 50% clipping resulted in a slightly lower number of seeds and 75% clipping in only one third of the number produced by the controls (Figure 1F). The number of seed scars in the Kuusamo population seemed to be higher in the 10% clipped plants than in the controls and decreased in the 50% and 75% clippings, but none of these treatments differed from the controls in pairwise comparisons due to the high variances (Figure 2F). These differences in seed
54
Figure 1. Tolerance of the Paltamo population of Gentianella amarella as indicated by A. final height (cm), B. final above-ground biomass (dry wt, g), C. final below-ground biomass (dry wt, g), D. number of branches, E. number of fruits and F. number of seed scars (mean ± standard error). Treatment groups (unclipped control plants and plants with 10–75% of the main stem removed) indicated by the same letter do not differ statistically significantly from each other (P > 0.05, LSD procedure).
production resulted in a significant interaction between origin and treatment (Table 1). Tolerance of monocarpic herbs in relation to increasing damage level When the above results are compared to other studies conducted on monocarpic plants with the same experimental design (Figure 5), it appears that the studied species are able to fully compensate or slightly overcompensate for minor apical damage (10% clipping). The pattern is similar in above-ground biomass (Fig-
ure 5A) and fruit production (Figure 5B). In most cases, the plants are also able to compensate more or less fully for the removal of 50% of the main stem (Figure 5). However, Rhinanthus minor performed less well after 50% clipping. In contrast, this damage level induced marked overcompensation in the Björnvad population (SE Sweden) of Gentianella campestris: the 50% clipped plants produced an average of 2.8 times more above-ground biomass and 2.3 times more fruits than the unclipped control plants (Figure 5). G. campestris plants in the Keminmaa population (N Finland) were only able to fully compensate
55
Figure 2. Tolerance of the Kuusamo population of Gentianella amarella. For explanations, see Figure 1.
for 50% clipping (Figures 5A and 5B). Finally, there is a consistent trend of plant performance to decrease toward 75% clipping as compared to lower damage levels, although full or close to full compensation is achieved in some cases (Figure 5).
Discussion Patterns of plant performance in relation to damage intensity According to McNaughton (1983) and Crawley (1997), there is a certain break-point in plant tolerance in relation to damage intensity. Beyond this point, compensatory mechanisms are no longer able to alleviate the negative effects of tissue damage. This general pattern appears in G. amarella, which is able to compensate fully for low and moderate damage
56
Figure 3. Schematic presentation of shoot architecture in different treatment groups. The plants were from the Kuusamo population. The level of clipping height is indicated with an arrow.
levels, while more extensive damage (75%) tends to affect plant performance negatively. The only indication of overcompensation was a slight increase in fruit yield in the Kuusamo population after 10% clipping. In spite of minor differences, G. amarella seems to behave similarly to E. strictum and G. campestris (Keminmaa population) and also to R. minor, although the latter species is more sensitive to damage levels above 50%. The only distinct exception to this pattern is the Björnvad population of G. campestris (Figure 5). The Björnvad population is one of the five populations where overcompensation has so far been documented in G. campestris (Lennartsson et al. (1997, 1998)). Because overcompensation in this species has only been found in late-flowering populations with a long history of management in terms of grazing and/or mowing, Lennartsson et al. (1997) concluded that overcompensation in the G. campestris may well represent an adaptation to a high and predictable risk of being damaged (Crawley 1987; Paige and Whitham 1987; van der Meijden 1990; Vail 1992; Tuomi et al. 1994). According to Paige (1994), Ipomopsis aggregata (Polemoniaceae) requires very high damage levels (above 80% removal of the main stem) before full-intensity overcompensation is induced.
The populations he studied are grazed by deer, and the potential for overcompensation in this species may thus also present an adaptation to predictable damage (Paige and Whitham 1987; Paige 1992). Bergelson and Crawley (1992a, 1992b), however, found no association between the compensatory capacity of I. aggregata and the grazing history of their study populations. On the basis of the present data, no far-reaching generalizations can be made concerning the behaviour of any single species because the regrowth capacity may vary notably between populations (e.g. Bergelson and Crawley (1992a, 1992b) and Lennartsson et al. (1997)), between years (Lennartsson et al. 1998) and relative to the timing of clipping in relation to flowering phenology (Maschinski and Whitham 1989; Paige 1994; Lennartsson et al. 1998). Furthermore, fruit production may not always be a sufficient performance measure in evolutionary contexts if grazing reduces seed production or seed weight and viability (e.g. Belsky (1986) and Belsky et al. (1993)). In spite of these caveats, it seems obvious that the position of maximum tolerance in relation to damage intensity varies considerably. In some cases, as in the Kuusamo population of G. amarella,
57 Why is maximum tolerance obtained at low or moderate damage levels?
Figure 4. The percentage of different types of 1st-order branches in the Paltamo and Kuusamo study populations. Low-node branches grow at the first node close to the ground, while uppernode branches grow higher up along the main stem. Treatment groups indicated by the same letter in the Kuusamo population do not differ statistically significantly from each other (P > 0.05, LSD procedure). Table 2. Pearson’s correlation coefficients (r) between the number of fruits and the number of branches in the two studied populations. Origin Clipping 0% 10% 50% 75%
Paltamo **
0.818 0.674 * 0.818 ** 0.902 **
Kuusamo 0.163ns 0.866 ** 0.892 ** 0.924 **
Significance of r is indicated as: ns for P > 0.05, * for P < 0.05 and ** for P < 0.01.
maximum tolerance is obtained at low or moderate levels of damage, while in other cases, as in the Björnvad population of G. campestris, maximum tolerance is obtained at higher levels of damage.
One possibility to achieve maximum tolerance at low damage levels is that tolerance at high damage levels is constrained by a lack of basal meristems close to the ground (A in Figure 6). This may explain the poor performance of R. minor in the 75% clipping treatment (Huhta et al. 2000a). Another possibility is that a deficiency of resources constrains more strongly regrowth at high damage levels (B in Figure 6). In general, increased resource availability and decreased competition tend to improve tolerance (Maschinski and Whitham 1989), but it is not known whether this may also alter the position of maximum tolerance in relation to damage intensity. In Erysimum strictum, maximum tolerance has been observed at a 10% clipping level both in natural growth conditions (Huhta et al. 2000a) and in experimental growth conditions with supplemental fertilization (Huhta et al. 2000c). Consequently, in some plants the maximum tolerance is restricted to low damage levels irrespective of resource availability. On the other hand, in plants with a capacity for regrowth from basal meristems, as in Gentianellas (Figure 3), variation in resource availability and growth conditions may cause a shift in maximum tolerance. Thus, due to vigorous branching from basal meristems following 50% clipping, G. amarella may also have a capacity to tolerate better high damage levels when the growth conditions are favourable (C and D, Figure 6). For instance, summer drought during regrowth and flowering may result in poor performance of 50% clipped plants in such populations of G. campestris that show overcompensation in favourable years (Lennartsson et al. 1998). The fact that 50–75% damage increased branching intensity in G. amarella, but still decreased fruit production, may indicate resource limitation at higher damage levels. A third possibility is that the plants have adapted to low or moderate levels of damage, and that they only rarely experience damage exceeding 50% tissue removal. In the present case of G. amarella, although the examined two populations had different management histories, their compensatory responses were quite similar. Despite the continuous grazing in the Paltamo population the incidental herbivory on G. amarella may not play a very prominent role compared to the ungrazed population of Kuusamo. It is therefore probable that northern populations of early flowering G. amarella face no strong selection pres-
58
Figure 5. Performance of four different monocarpic species in six populations along a gradient of increasing cutting intensity: A. aboveground biomass and B. fruit production. The average values of the unclipped control plants were set to 100. The data on G. campestris are from Huhta et al. (2000b) and that on Erysimum and Rhinanthus from Huhta et al. (2000a).
sure toward developing tolerance against high damage levels. Instead, the plant may use other strategies for coping with herbivory, including escape in time, i.e. flowering as early as possible, so that the majority of individuals are already setting seed by the time
the grazers have consumed the more preferred neighbouring plants (Lennartsson et al. 1997). More extensive injuries are thereafter hindered by unsavory taste and even toxicity, after which few further grazing attempts may occur. Over ten different phenolic com-
59
Figure 6. Multiple constraints may hierarchically explain the variation in compensatory responses in relation to damage level. The vertical axis indicates plant performance with the value of undamaged control plants being set at 100. A. Plants with no or few basal meristems, B. basal meristems are available, but growth conditions are unfavourable, C. basal meristems are available, growth conditions are favourable, and minor damage is sufficient to cause a release of meristems from correlative inhibition, and D. as in C, but a higher damage level is required to break down apical dominance.
pounds have been recognized in Gentianellas, including xanthones and cyanogenic glucosides (Hostettmann-Kaldas and Jacot-Guillarmod 1978). The main function of regrowth in both G. amarella and G. campestris may thus be to repair the minor and moderate damage that occasionally occurs in grazed habitats. Defence and tolerance of herbivory attack are not necessarily always exclusive alternatives for coping with herbivory (cf. Mauricio et al. (1997) and Rosenthal and Kotanen (1994)), but may instead synergistically alleviate the negative effects of browsing on plant performance. Chemical defences may both reduce the degree of damage on the attacked plant and decrease the risk of repeated grazing if, after trial attempts, the plants are avoided by livestock. If grazing occurs in this trial-and-error way, minor injuries may result in full compensation or even slight overcompensation. The few observed grazing attempts in Paltamo corresponded to 10-50% clipping. G. amarella is tolerant of damage of this magnitude and may fully compensate for such losses in above-ground biomass. A fourth possibility is that the shape of the compensatory response along with the increasing level of damage does not actually indicate any special adaptation to herbivory, but may, instead, indicate that the plants are selected for fast vertical growth and unbranched architecture in undamaged conditions. Consequently, regrowth and occasional overcompensation would be a mere by-product of growth conditions which favour apical dominance (Aarssen and Irwin 1991; Aarssen 1995). Because the general shape of
the compensatory responses, excluding the Björnvad population of G. campestris, is quite similar in the different species, populations and growth conditions (Figure 5), these monocarpic species may share a growth form that involves maximum tolerance at low and moderate damage levels. Selection favouring fast vertical growth and unbranched shoot architecture early in the season might well be such a common factor. Huhta et al. (2000a) suggested that this might be the case in E. strictum and R. minor, but might apply to G. amarella as well. Apical damage as such did not decrease the final plant height in either of the study populations. Thus, apically damaged plants in the 10% clipping treatment did not abandon vertical growth, as they did when damage intensity increased (Figure 3). The reason for the more abundant fruits in the 10% cut plants compared to the controls is the more effective utilization of uninitialized meristems for reproductive purposes in the upper parts of the stem. Note especially that the proportion of low-node branches was higher in Kuusamo than in Paltamo, although the former population experienced less disturbance than the latter. This indicates that it is not the mere grazing history that shapes the compensatory responses, but other factors associated with growth conditions may have a key role in explaining the variation in tolerance. In the present study, we could not judge the relative importance of these four possibilities. In spite of this, the present results provide sufficient grounds to conclude that, although the possibility of overcompensation is a most intriguing evolutionary question, the variation in tolerance over a range of damage levels may well be a more fundamental question for both theoretical and empirical studies of compensation. In the case of monocarpic herbs, it may be useful to differentiate between the response types that achieve maximum tolerance at relatively low damage levels and those that have maximum plant performance at higher damage levels (Figure 6). In the case of environmental factors, we should separately study their effects on the average plant performance over a range of damage levels and, on the other hand, whether they also affect the position of maximum performance in relation to damage intensity.
60 Acknowledgements The work was financially supported by the Academy of Finland (project # 40951). We thank the anonymous referee for the valuable comments on the manuscript. Sirkka-Liisa Leinonen kindly checked the English and Tommy Lennartsson gave some data of his studies on G. amarella.
References Aarssen L.W. 1995. Hypotheses for the evolution of apical dominance in plants: implications for the interpretation of overcompensation. Oikos 74: 149–156. Aarssen L.W. and Irwin D.L. 1991. What selection: herbivory or competition? Oikos 60: 261–262. Alward R.D. and Joern A. 1993. Plasticity and overcompensation in grass responses to herbivory. Oecologia 95: 358–364. Beard J.B. 1973. Turfgrass: Science and culture. Prentice-Hall. Belsky A.J. 1986. Does herbivory benefit plants? A review of the evidence. Am. Nat. 129: 870–892. Belsky A.J., Carson W.P., Jensen C.L. and Fox G.A. 1993. Overcompensation by plants: herbivore optimization or red herring? Evol. Ecol. 7: 109–121. Bergelson J. and Crawley M.J. 1992a. The effects of grazers on the performance of individuals and populations of scarlet gilia, Ipomopsis aggregata. Oecologia 90: 435–444. Bergelson J. and Crawley M.J. 1992b. Herbivory and Ipomopsis aggregata: the disadvantages of being eaten. Am. Nat. 139: 870–882. Bergelson J., Juenger T. and Crawley M.J. 1996. Regrowth following herbivory in Ipomopsis aggregata: compensation but not overcompensation. Am. Nat. 148: 744–755. Crawley M.J. 1987. Benevolent herbivores? Trends Ecol. Evol. 2: 167–168. Crawley M.J. 1997. Plant ecology. Blackwell Science. University Press, Cambridge. Ekstam U., Aronsson M. and Forshed N. 1988. Ängar. Om naturliga slåttermarker i odlingslandskapet. LTs Förlag, Stockholm. Hämet-Ahti L. and Suominen J. 1993. Kasvistomme muinaistulokkaat: tulkintaa ja perusteluja. (Archaeophytes in the flora of Finland). Norrlinia 4: 1–90. Hämet-Ahti L., Suominen J., Ulvinen T. and Uotila P. (eds) 1998. Retkeilykasvio (Field flora of Finland), Finnish Museum of Natural History. Botanical Museum, Helsinki. Hillman J.R. 1984. Apical dominance. In: Wilkings M.B. (ed.), Advanced plant physiology. Pitman Publishing Ltd, London, pp. 127–148. Hostettmann-Kaldas M. and Jacot-Guillarmod A. 1978. Xanthones et C-glucosides falvoniques du genre Gentiana (sous-genre Gentianella). Phytochemistry 17: 2083–2086. Huhta A.-P., Tuomi J. and Rautio P. 2000a. Cost of apical dominance in two monocarpic herbs, Erysimum strictum and Rhinanthus minor. Can. J. Bot. 78: 591–599.
Huhta A.-P., Lennartsson T., Tuomi J., Rautio P. and Laine K. 2000b. Tolerance of Gentianella campestris in relation to damage intensity: an interplay between apical dominance and herbivory. Evol. Ecol. 14: 373–392. Huhta A.-P., Hellström K., Rautio P. and Tuomi J. 2000c. A test of the compensatory continuum: fertilization increases and belowground competition decreases the grazing tolerance of tall wormseed mustard (Erysimum strictum). Evol. Ecol. 14: 353– 372. Hultén E. and Fries M. 1986. Atlas of North European vascular plants, North of the Trophic of Cancer. Koeltz Scientific Books, Königstein. Järemo J., Nilsson P. and Tuomi J. 1996. Plant compensatory growth: herbivory or competition? Oikos 77: 238–247. Kemp W.B. 1937. Natural selection within plant species as exemplified in a permanent pasture. J. Heredity 28: 329–333. Kytövuori I. 1980. Gentianella amarella (L.) Börner Horkkakatkero. In: Jalas J. (ed.), Suuri kasvikirja Part III. Otava, Keuruu, pp. 356–358. Latvalehto P. 1997. Melalahden perinnemaisemien ketokasvillisuus. MSc Dissertation, University of Oulu. Lennartsson T., Tuomi J. and Nilsson P. 1997. Evidence for the evolutionary history of overcompensation in the grassland biennial Gentianella campestris (Gentianaceae). Am. Nat. 149: 1147–1155. Lennartsson T., Nilsson P. and Tuomi J. 1998. Induction of overcompensation in the field gentian, Gentianella campestris. Ecology 79: 1061–1072. Maschinski J. and Whitham G.T. 1989. The continuum of plant responses to herbivory: the influence of plant association, nutrient availability and timing. Am. Nat. 134: 1–19. Mauricio R., Rausher M.D. and Burdick D.S. 1997. Variation in the defence strategies of plants: are resistance and tolerance mutually exclusive? Ecology 78: 1301–1311. McNaughton S.J. 1979. Grazing as an optimization process: grassungulate relationships in the Serengeti. Am. Nat. 113: 691–703. McNaughton S.J. 1983. Compensatory plant growth as a response to herbivory. Oikos 40: 329–336. McNaughton S.J. 1986. Grazing lawns: On domesticated and wild grazers. Am. Nat. 128: 937–939. Montgomery D.C. 1984. Design and analysis of experiments. 2nd edn. John Wiley and Sons, New York. Mopper S.J., Maschinski J., Cobb N. and Whitham T.G. 1991. A new look at habitat strcuture: consequences of herbivore-modified plant architecture. In: Bell S.S., McCoy E.D. and Mushinsky H.R. (eds), Habitat structure: the physical arrangement of objectes in space. Chapman & Hall, London, pp. 260–280. Påhlsson’s L. (ed.) 1994. Öppen brukningsbetingad vegetation. In: Vegetationstyper i Norden. Nordiska ministerrådet. Aka-print APS,, pp. 381–457. Paige K.N. 1992. Overcompensation in response to mammalian herbivory: from mutualistic to antagonistic interactions. Ecology 73: 2076–2085. Paige K.N. 1994. Herbivory and Ipomopsis aggregata: Differences in response, differences in experimental protocol: a reply to Bergelson and Crawley. Am. Nat. 143: 739–749. Paige K.N. 1999. Regrowth following ungulate herbivory in Ipomopsis aggregata: geographic evidence for overcompensation. Oecologia 118: 316–323.
61 Paige K.N. and Whitham T.G. 1987. Overcompensation in response to mammalian herbivory: the advantage of being eaten. Am. Nat. 129: 407–416. Phillips I.D.J. 1975. Apical dominance. Annu. Rev. Plant Physiol. 26: 341–367. Pitt M.D. and Heady H.F. 1978. Responses of annual vegetation to temperature and rainfall patterns in northern California. Ecology 59: 336–350. Prins A.H., Verkaar H.J. and van den Herik M. 1989. Responses of Cynoglossum offıcinale L. and Senecio jacobaea L. to various degrees of defoliation. New Phytologist 111: 725–731. Rassi P., Kaipiainen H., Mannerkoski I. and Ståhls G. 1991. Uhanalaisten kasvien ja eläinten seurantakomitean mietintö. (Abstract: Report on the monitoring of Threatened Animals and Plants in Finland). Committee report 1991:30. Ministry of the Environment, Helsinki. Rosenthal J.P. and Kotanen P.M. 1994. Terrestrial plant tolerance to herbivory. Trends Ecol. Evol. 9: 145–148. Saville D.J. 1990. Multiple comparison procedures: the practical solution. The American Statistician 44: 174–180. Trumble J.T., Kolodny-Hirsch D.M. and Ting I.P. 1993. Plant compensation for arthropod herbivory. Annu. Rev. Entomol. 38: 93–119.
Tuomi J., Nilsson P. and Åström M. 1994. Plant compensatory responses: bud dormancy as an adaptation to herbivory. Ecology 75: 1429–1436. Wandera J.L., Richards J.H. and Mueller R.J. 1992. The relationships between relative growth rate, meristematic potential and compensatory growth of semiarid-land shrubs. Oecologia 90: 391–398. Whitham T.G., Maschinski J., Larson K.C. and Paige K.N. 1991. Plant responses to herbivory: The continuum from negative to positive and underlying physiological mechanisms. In: Price P.W., Lewinsohn T.M., Fernandes G.W. and Benson W.W. (eds), Plant-animal interactions: Evolutionary ecology in tropical and temperate regions. Vail S.P. 1992. Selection for overcompensatory plant responses to herbivory: a mechanism for the evolution of plant-herbivore mutualism. Am. Nat. 139: 1–8. van der Meijden E. 1990. Herbivory as a trigger for growth. Ecology 4: 597–598. Verkaar H.J. 1986. When does grazing benefit plants? Trends Ecol. Evol. 1: 168–169.
