Importance of tolerance to herbivory for plant survival in a British grassland
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1 Journal of Vegetation Science 15: , 2004 IAVS; Opulus Press Uppsala. - Importance of tolerance to herbivory for plant survival in a British grassland Importance of tolerance to herbivory for plant survival in a British grassland del-val, E. 1,2 & Crawley, M.J. 1 1 Biological Science Department, Imperial College, Silwood Park, Ascot, SL5 7PY, U.K.; 2 Corresponding author and current address: CASEB, Facultad de Ciencias Biológicas, Pontificia Universidad Católica de Chile, casilla 114-D, Santiago, Chile; Fax ; ek@ekdelval.com Abstract. Question: Is plant capacity to regrow under different herbivore treatments related to herbivore increaser/decreaser plant status? Location: Grassland in Southeast England (GR 41/944691). Methods: A field experiment was established in order to understand the role of plant tolerance to herbivory in explaining the abundance of nine grassland species previously known as herbivore increasers or decreasers. Tolerance was measured as a plant s capacity to regrow after exposure to herbivores. The experiment was designed to measure the impact of rabbits, molluscs, insects and clipping (artificial damage). Plants were propagated by stolons, exposed to different treatments in the field and then allowed to recover in the greenhouse for a month Results: Previous studies have stated that plants that are able to persist in a herbivore environment could be tolerant or resistant, in agreement with the later our results showed that rabbit increaser plants were tolerant to herbivory in terms of biomass regrowth. Nonetheless, insect and mollusc increasers did not show any particular pattern related to plant compensation and some decreaser species were intolerant. Conclusions: This study shows that tolerance to herbivory could be an important mechanism for rabbit increaser species survival in grazed ecosystems. Keywords: Insect; Mollusc; Plant regrowth; Rabbit herbivory. Nomenclature: Stace (1997). Introduction Herbivores can have a major impact on the vegetation of certain ecosystems. Several studies have shown that herbivore grazing has a significant effect on the relative abundance and composition of species in plant communities (McNaughton 1979; Belsky 1987; Milchunas et al. 1988; Huntly 1991; Sinclair 1995; Latsch 1997; Holl & Nietzen 1999). The effect of herbivores in grasslands has been well studied. Some authors have found that the abundance of some plant species is favoured by grazing (increasers) whereas others become scarce (decreasers) as a consequence of herbivory (Crawley 1990; Edwards & Crawley 1999a; Bullock et al. 2001; Vesk & Westoby 2001; Frank 2003). Vertebrate herbivores are particularly influential on plant communities because of the amount they eat (McNaughton 1979; Stebbins 1981; McNaughton 1983, 1986; Milchunas et al. 1988; Sinclair 1995; Augustine & McNaughton 1998; Edwards & Crawley 1999a, b; Edwards et al. 1999; Vesk & Westoby 2001) but invertebrates can have significant effects as well (Frank 2003). In particular molluscs are known to prefer seedlings rather than mature plants and prefer dicots to monocots (Dirzo & Harper 1980, 1982; Cottam 1986; Hanley et al. 1995). Therefore the selective influence they exert on plant populations is greater than the amount of biomass they consume because they can prevent plants from establishing and becoming adults (Hanley & Fenner 1997; Rodriguez & Brown 1998). Insect herbivores have more subtle effects in grasslands than vertebrates, but they can also affect plant populations dynamics as they alter relative competitive abilities (Crawley 1989; Trumble et al. 1993; Tscharntke & Greiler 1995; Latsch 1997), particularly root feeding insects (Brown & Gange 1992). Herbivore effects on plants have been shown to be more than just a removal of biomass because they can induce the production of chemical or physical defences that can change plant s quality and future allocation patterns (Karban & Baldwin 1997; Agrawal et al. 1999). The changes in plant communities related to herbivore grazing can be generally explained by four broad mechanisms: herbivore preference (related to plant nutritive quality and plant defence mechanisms), tolerance to herbivory (plant capacity to regrow after herbivore damage), disturbance caused by herbivores in the environment or by an alteration of the nutrient cycle, and by interactions between these four mechanisms (McNaughton 1979; 1990; 1997; Augustine & McNaughton 1998; de
2 358 del-val, E. & Crawley, M.J. Table 1. Experimental species with herbivore category and recorded biomass from previous experiments in Nash s field. Showing mean biomass (g) ± SE in plots with and without herbivores in 1997 from cm quadrats (M.J. Crawley unpubl.). Data shown only concerns the specific herbivore that influences the particular species. All differences significant at p < Species Family Category Biomass Biomass + herbivores (g) -herbivores (g) Senecio jacobaea Asteraceae Rabbit increaser 3.48± Rumex acetosella Polygonaceae Rabbit increaser 2.76± ±0.12 Trifolium repens Fabaceae Rabbit increaser 0.02± Holcus lanatus Poaceae Rabbit increaser 6.12± ±0.5 Festuca rubra subsp. rubra Poaceae Rabbit decreaser 12.42± ±1.2 Vicia sativa subsp. nigra Fabaceae Rabbit decreaser ±0.02 Luzula campestris Juncaceae Insect increaser 0.39± ±0.02 Galium saxatile Rubiaceae Mollusc increaser 0.69± ±0.06 Achillea millefolium Asteraceae Mollusc decreaser 0.33± ±0.27 Mazancourt et al. 1999). The few investigations on the relationship between plant tolerance to herbivory and the persistence of a species in an ecosystem have found contradictory results. Anderson and Briske (1995) found that species preferred by herbivores had smaller biomass than avoided plants while Bullock et al. (2001) described that preferred species had greater biomass than non-preferred. Therefore, the role of plant tolerance to herbivory at a community level is not well established. We were interested in determining if plant tolerance to herbivory at the individual level is related to the species persistence in a community under grazing pressure. In particular we aimed to answer the following questions: Is plant capacity to regrow under different herbivore treatments related to herbivore increaser/decreaser plant status? Does herbivory have a different effect on plant regrowth capacity than simulated damage? Methods Experimental design A field experiment was set up in Nash s field, Silwood Park, Berkshire, UK (GR 41/944691), a species poor grassland on acid, sandy soil. Using data from a longterm experiment that measured the impact of herbivores on the plant community in the same field (Crawley 1990 and M.J. Crawley unpubl.), nine plant species classified as increaser or decreaser for different herbivores (rabbits (Oryctolagus cuniculus), insects and molluscs) were selected. Because rabbits are the most influential herbivore in the system, we used 6 species influenced by them. Species are considered to be increasers if their abundance is augmented by 50% or more when herbivores are present, and decreasers are species that are diminished by 50% or more in presence of herbivores (Table 1). The field experiment was designed as a split-plot with four treatments: +/ fencing (to prevent rabbit access), +/ insects, +/ molluscs, and +/ clipping (simulated herbivory plus insecticide and molluscicide) and control (where all herbivores had access). There were six experimental blocks (20 10 m) and half of each was protected from rabbit grazing since 1990 (10 10 m). Fences were constructed of 1-cm wire mesh buried 5 cm deep, with the bottom 15 cm of wire turned outwards (Fig. 1). There were two replicates per fenced block (the replicates are considered independent because they were spatially distinct) giving a total of 12 replicates. Insecticide, molluscicide and clipping treatments were nested in the fenced plots, each having an area of m. The experiment was fully randomised. The nine species were propagated by stolons (collected from plants growing in the field) in a greenhouse until they were established (~ 1 month). 200 plants per species were grown in jiffy pots (biodegradable pots made out of peat) of 8cm diameter with a soil mix of 50% sand, 20% loam and 30% peat. This particular mixture of soil was used to mimic the nutrient poor soil conditions from Nash s Field. We decided to use jiffy pots because they are permeable to water and therefore ideal for maintaining soil moisture. Once plants were established, 192 individuals of each species were transplanted to the field and exposed to different experimental treatments (n = 12). All plants are considered as mature because even though none were flowering when collected, they were obtained from adults growing in the field. Vicia sativa subsp. nigra was very difficult to cultivate, and when exposed to herbivores, the plants were not very healthy. Thus, this species was not exposed to all treatments but just to the putative main driver: rabbit herbivory (48 individuals). Experimental treatments were applied in early June 2000 (5-9 June). Rabbit grazing had been prevented by fencing since For insect exclusion, we used a
3 - Importance of tolerance to herbivory for plant survival in a British grassland Fig. 1. Experimental layout showing one block of the split-plot design. Treatments: -I insecticide, -M molluscicide, Cl clipping + molluscicide +insecticide, +I+M control. combination of two insecticides, Danadim 40 (from Cheminova; 400g/l dimethoate) and Dursban (from DowElanco; 480g/l chlorpyrifos); 25 ml of each chemical were diluted in 10 L of water and then sprayed once on the experimental plants. For mollusc exclusion, Mifaslug (from Farmers Crop Chemicals Ltd.; 6% metaldehyde) was used at 11.1mg of molluscicide per m 2 as suggested by the provider. This particular combination of pesticides was used because we knew from previous experiments that they do not have phytotoxic effects on the chosen species (M.J. Crawley unpubl.). For the clipping treatment, 75% of the total shoot biomass of each plant was removed with scissors and then insecticide and molluscicide were applied at the same concentrations as above. We decided to use 75% defoliation because we wanted to impose a significant damage to plants. At the same time, we aimed to discover differences between species that could only be found imposing relatively high defoliation because most species are known to have regrowth ability for low levels of biomass removal (Belsky et al. 1993; Crawley 1997). In order to assess the impact of herbivores on the experimental plants, after one month in the field (time 1, third week of July) half of the plants were harvested (96 individuals per species) to measure plant biomass (both above and belowground). Plants were harvested, dried in an oven (80 C) for 48 hrs and then weighed. The remaining plants were transported back to the greenhouse, where they were allowed to recover from tissue loss for a month (time 2, end of August). At the end of the month plants were harvested, dried in an oven (80 C) for 48 hrs and then weighed. This recovery period gives an estimate of plant regrowth after defoliation. Mortality was also recorded. Results were analysed in S-PLUS 2000 (Mathsofth Inc.) using generalised linear models. First we analysed biomass at time 1 with a split-plot model incorporating different error terms for plots and subplots. The structure of the error term tells the program to consider the correct degrees of freedom for the different plot sizes (i.e. 6 df for rabbit exclusion and 82 df for the other treatments). The response variable biomass was naturallog transformed and the explanatory variables used were +/ rabbit grazing, +/ insects, +/ molluscs and +/ clipping. Regrowth biomass at time 2 was calculated as biomass at time 2 minus biomass at time 1. Regrowth biomass was also natural-log transformed and then analysed with the same explanatory variables plus a covariate of natural-log of plant biomass at time 1. For this analysis we could not use a split-plot model because there was some mortality at time 1 and the design did not remain fully factorial. Mortality data were analysed as a binary response (dead or alive) with binomial errors and the explanatory variables used were all the experimental treatments. Some species flowered during the experiment and therefore the number of plants flowering per treatment was also evaluated as a binary response (flowering or not flowering) with binomial errors and same Table 2. Split-plot analysis of variance for the different experimental treatments on biomass at time 1. Only the main effects and significant interactions are shown; rabbit*clipping and rabbit*insects were not significant for any species. For the minimal model the response variables was log-transformed. Note that molluscs, insects and clipping were nested within fenced plots. ~ These interactions were taken out from the model because they were not significant. Source of variation Rabbits Molluscs Insects Clipping Rabbits*Clipping Species df F p df F p df F p df F p df F p A. millefolium 1, , , , ~ ~ ~ F. rubra subsp. 1, , > , , ~ ~ ~ rubra G. saxatile 1, , , , ~ ~ ~ H. lanatus 1, , > , , ~ ~ ~ L. campestris 1, , , , , R. acetosella 1, ,81 2, , , ~ ~ ~ S. jacobaea 1, , , , ~ ~ ~ T. repens 1, , > , , ~ ~ ~
4 360 del-val, E. & Crawley, M.J. Fig. 2. Effects of herbivory and defoliation treatments on plant biomass when harvested from the field (time 1). Values shown are mean biomass at time 1 ± 1SE, averaged from rabbit fencing and rabbit control. Bars with the same letter do not differ (p > 0.05), n.s. = all treatments were not significantly different. Note that statistical analyses were performed with log-transformed data. explanatory variables. In all cases a full model was fitted to the data and then reduced to a minimal adequate model by simplification; all non-significant terms were removed sequentially from the full model, starting from the highest-order interaction terms. Statistical analyses are presented as the simplified models with the main factors and significant interactions. Results Herbivore impact (time 1) Rabbit grazing showed no effect on plant biomass when harvested from the field for any species (Table 2). The interactions between rabbit grazing and the rest of the treatments were also not significant. Mortality was very high (40%) for V. sativa subsp. nigra and this was not related to rabbit grazing (p = 0.9). We did not detect differences in biomass between grazed and ungrazed plants (p = 0.7). It is important to mention that all individuals of this species were dead after the recovery period. Insect exclusion significantly affected one species. Surprisingly, the only insect increaser species, Luzula campestris, showed a significant reduction in biomass in control plants (i.e., where insects grazed; p = 0.02) (Fig. 2). Mollusc exclusion was the treatment with greatest impact (5 species). Festuca rubra subsp. rubra, H. lanatus, G. saxatile, S. jacobaea and T. repens benefited from mollusc exclusion (p < 0.05, Table 2). Achillea millefolium, a mollusc decreaser, did not show any effect (Fig. 2). There was little response to clipping treatment; only two species were influenced by it. Trifolium repens was affected by the artificial removal of biomass (p = 0.001) (Fig. 2). For L. campestris there was a difference between clipped and control plants only in the grazed area
5 - Importance of tolerance to herbivory for plant survival in a British grassland Table 3. Analysis of variance for the different experimental treatments on regrowth biomass. Only the main effects and the covariate log (biomass time 1) on regrowth biomass are shown, as none of the interactions were significant for any species (p > 0.05). For the minimal model the response variables were log-transformed. Source of variation Log (biomass 1) Rabbits Molluscs Insects Clipping Species F p F p F p F p F p A. millefolium df = 1, < F. rubra subsp. rubra df = 1, G. saxatile df = 1, H. lanatus df= 1, L. campestris df = 1, > R. acetosella df = 1, S. jacobaea df = 1, T. repens df = 1, (rabbit*clipping interaction; p = 0.02), where clipped plants were bigger than control plants. Plant regrowth (time 2) The recovery period without the presence of herbivores was sufficient for plants to attain full compensation in most species (i.e., herbivorized plants were not different from controls) (Table 3). Nevertheless, in some cases the impact of herbivores was still evident and regrowth was not enough to even out plant s biomass (Fig. 3). Galium saxatile and H. lanatus showed a negative effect on biomass regrowth after mollusc grazing (p < 0.05). In all species clipped plants were able to compensate (p > 0.05), and for L. campestris clipped plants were bigger than herbivorized plants (p = 0.02). An extreme case was A. millefolium that did not show an effect at time 1 under rabbit grazing but after the recovery period plants that had been exposed to rabbits were smaller (p = 0.05). Mortality In general, plant survival at the recovery period was high (88.4%) for all species. Nonetheless, for some species there were significant differences between plant mortality due to the different treatments (Table 4). Achillea millefolium showed higher mortality in plants grazed by rabbits and molluscs at the same time (12.2% vs. 3.2% mortality) and L. campestris was also negatively affected by rabbit grazing (29% vs. 0% mortality). Galium saxatile survival was adversely affected by clipping (50% mortality) and mollusc grazing (16.7%), similar to the biomass results. Festuca rubra subsp. rubra, H. lanatus and R. acetosella showed higher mortality in plants due to insects (12.5%), clipping (16.5%), and molluscs (12.5%), respectively. The rest of the species did not show any significant mortality pattern related to the treatments. Flowering Three species flowered during the experiment: R. acetosella, A. millefolium and T. repens. Flowering increased for A. millefolium when rabbits were present (c 2 = 5.48, df = 93, p = 0.02), whereas for T. repens there were more flowering plants when rabbits and molluscs were excluded (rabbit*mollusc interaction; c 2 = 5.48, df = 93, p = 0.02). For R. acetosella flowering was not related to any treatment. Discussion Rabbit herbivory is known to have the greatest impact on grassland communities of Southeast England (Crawley 1990). However in our experiment rabbits did not have such a large effect and this is probably due to the fact that rabbit numbers at the field site have declined over the last two years (for unknown reasons). In this experiment, mollusc and insect herbivory had greater effects on plant performance. This large effect of mollusc exclusion has also been found in other grassland species (Dirzo & Harper 1980, 1982; Rees & Brown 1992). Comparing artificial defoliation with herbivore effects, six species showed similar results from both treatments, either positive or negative in both cases. In terms of mortality clipping did not accurately simulate the effects of herbivory in all cases. The flowering of studied species was not affected by clipping; however, herbivores did influence flower production for two species (A. millefolium and T. repens). These results support the idea that for some species clipping is not always a good simulator of herbivore damage (Dyer & Bokhari 1976; Paige 1999). Nevertheless, clipping treatment proved to be a good estimator of plant capacity to regrow. Species that were able to compensate for herbivore damage in terms of vegetative biomass were also able to compen-
6 362 del-val, E. & Crawley, M.J. Fig. 3. Effects of herbivory and defoliation treatments on plant regrowth biomass for different species. Values shown are mean regrowth biomass ± 1SE, averaged from rabbit fencing and rabbit control; regrowth biomass was calculated as biomass time 2 biomass time 1. Bars with the same letter do not differ (p > 0.05), n.s. = all treatments were not significantly different. Note that statistical analyses were performed with log-transformed data. sate for clipping. A possible limitation from our experiment is that herbivore exposure period might have been too short because recurrent defoliation is known to have greater effects on plant compensation capacity than only a defoliation episodes (McNaughton 1983; Oesterheld & McNaughton 1991). Increasers/decreasers Of the six species characterised as herbivore increasers at the beginning of the experiment, five showed some regrowth capacity. Regrowth capacity appears to be important for the four rabbit increasers. Surprisingly, the mollusc and insect increaser species were affected by mollusc and insect herbivory, respectively. Galium saxatile and L. campestris biomass never recovered from grazing and also suffered greater mortality. Decreaser species were assumed to be unable to regrow after herbivory. This assumption was true for V. sativa subsp. nigra and A. millefolium under rabbit grazing, but F. rubra subsp. rubra and A. millefolium compensated for clipping. Even though these results are inconclusive and more data on decreaser species are needed, regrowth incapacity does not appear to be linked with decreaser status. Anderson and Briske (1995) found that selective herbivory and not plant tolerance to herbivory was the main factor driving plant species replacement in the southern true prairie in North America whereas Bullock et al. (2001) found a positive correlation between selective grazing in spring and winter with plant biomass in British grasslands. Concurrent with Bullock et al. (2001) findings, in our experiment rabbit increasers appear to be tolerant to herbivory but we did not particularly test for herbivore preference. Another factor for consideration is that we studied perennial plants (except for V. sativa subsp. nigra) and at only one stage in their life cycle, so we did not investigate the complete scenario of plant tolerance and herbivore impact. For instance, it is known that the major impact of mollusc grazing is on seedlings (Crawley
7 - Importance of tolerance to herbivory for plant survival in a British grassland Table 4. Survival analysis showing all main effects (treatments applied) and significant interactions after the recovery period. Data were analysed as a binary response (dead or alive) with binomial error. ~ These interactions were taken out from the model because they were not significant. Source of variation Rabbits Molluscs Insects Clipping Rabbits*Molluscs df=94 df=93 df=92 df=91 df=90 Species c 2 p c 2 p c 2 p c 2 p c 2 p A. millefolium F. rubra subsp. rubra ~ ~ G. saxatile >0.001 ~ ~ H. lanatus >0.001 ~ ~ L. campestris ~ ~ R. acetosella ~ ~ S. jacobaea ~ ~ T. repens ~ ~ 1997); therefore our results for increaser/decreaser species for mollusc grazing could be underestimated. Nevertheless, our experiment does show that effects of molluscs are large in the ontogenic stages studied. This study also illustrates the importance of focusing not only on plant mortality but also on plant performance when studying herbivore impact on plant populations. The results from these two measurements are very different; as Pacala and Crawley (1992) mentioned, herbivores rarely kill the entire plant and formulations of plant-herbivore dynamics need to concentrate on the amount of herbivory per plant and how this affects competitive ability, rather than just plant mortality. Regrowth strategies of perennials can have a major impact on plant population dynamics, especially if seedling recruitment is negligible (Bond & Midgley 2001). Because tolerance is closely related to environmental factors (Whitham et al. 1991; Hochwender et al. 2000), and the summer of 2000 was particularly wet, our results could have been influenced by the unusual weather. It has been reported that not all the species are consistently increasers or decreasers (Crawley 1990; Hulme 1996; Vesk & Westoby 2001); therefore it might be possible that the plant species react differently depending on the environmental conditions and herbivore abundance. Nevertheless, all plants are evolving in a dynamic environment, so if tolerance is a character subject to natural selection it must cope with environmental fluctuations and climatic factors should not be so important. Further studies on the impact of herbivores on different ontogenetic stages including more decreaser species will help to clarify the exact role of herbivore tolerance for the persistence of a plant species in the community. Acknowledgments. We thank C. de Mazancourt, R. Keane and M. Rees for many contributions to this study. We thank K. Boege, M. Bonsall and H. Bruelheide and two anonymous reviewers for comments on earlier drafts. Funding resources for E. del-val were provided by Conacyt, Mexico and CASEB, Pontificia Universidad Católica de Chile. References Agrawal, A.A., Strauss, S.Y. & Sout, M.J Costs of induced responses and tolerance to herbivory in male and female fitness components of wild radish. Evolution 53: Anderson, V.J. & Briske, D.D Herbivore-induced species replacement in grasslands: is it driven by herbivory tolerance or avoidance. Ecol. Appl. 5: Augustine, D.J. & McNaughton, S.J Ungulate effects in the functional species composition of plant communities: herbivore selectivity and plant tolerance. J.Wildlife Manage. 62: Belsky, A.J The effects of grazing: confounding of ecosystem, community, and organism scale. Am. Nat. 129: Belsky, A.J., Carson W.P., Jensen, C.L. & Fox, G.A Overcompensation by plants: herbivore optimization or red herring? Evol. Ecol. 7: Bond, W.J. & Midgley, J.J Ecology of sprouting in woody plants: the persistence niche. Trends Ecol. Evol. 16: Brown, V.K. & Gange, A.C Secondary plant succession: how is it modified by insect herbivory? Vegetatio 101: Bullock, J.M., Franklin, J., Stevenson, M.J., Silvertown, J., Coulson, S.J., Gregory, S.J. & Tofts, R A plant trait analysis of responses to grazing in a long-term experiment. J. Appl. Ecol. 38: Cottam D.A The effects of slug-grazing on Trifolium repens and Dactylis glomerata in monoculture and mixed sward. Oikos 47: Crawley, M.J Insect herbivores and plant population dynamics. Annual Review of Entomology 34: Crawley, M.J Rabbit grazing, plant competition and seedling recruitment in acid grassland. J. Appl. Ecol. 27:
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