Interspecific competition and tolerance to defoliation in four grassland species

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1 871 Interspecific competition and tolerance to defoliation in four grassland species Ek del-val and Michael J. Crawley Abstract: Herbivory and competition are known to influence plant performance. Recent investigations showed that tolerance is an important strategy for plant survival under herbivory, but few have examined its interaction with plant competition. We evaluated in a greenhouse experiment if plant tolerance to defoliation is related to species presence in a grazed habitat and how plant tolerance to herbivory changes in a competitive environment. Regrowth capacity of four grassland species, Trifolium repens L., Rumex acetosella L., Vicia sativa L. subsp. nigra (L.) Ehrh., and Senecio jacobaea L., was evaluated as the capacity to compensate for 75% of aboveground biomass removed. Target plants were also grown in competition with Festuca rubra L. subsp. rubra, and different clipping treatments were applied. Plant biomass (above- and below-ground) was measured after 5 months. Rumex acetosella, T. repens, and S. jacobaea were able to compensate fully when grown alone. In competition, only R. acetosella was still able to regrow. In no case did clipping the competitor improve target plant performance (i.e., no beneficial effect from competitor release). These results highlight the importance of considering plant competition when studying plant responses to herbivory. Key words: herbivory, regrowth, competitor release, biomass compensation. Résumé : On sait que l herbivorie et la compétition influencent la performance des plantes. Des travaux récents montrent que la tolérance est une stratégie importante pour la survie des plantes soumises à l herbivorie, mais peu de chercheurs ont examiné son interaction avec la compétition végétale. Les auteurs ont cherché à déterminer, lors d expériences conduites en serres, si la tolérance des plantes à la défoliation est reliée aux espèces présentes dans un habitat pâturé, et comment la tolérance des plantes à l herbivorie se modifie dans un environnement compétitif. Ils ont évalué la capacité de reprise de la croissance chez quatre espèces de prairie, soient les Trifolium repens L., Rumex acetosella L., Vicia sativa L. subsp. nigra (L.) Ehrh. et Senecio jacobaea, quant à leur capacité à compenser une ablation de 75 % de leur biomasse épigée. Les plantes ciblées ont également été cultivées en compétition avec le Festuca rubra subsp. rubra, en appliquant différents traitements de tonte. Ils ont mesuré la biomasse végétale (épigée et hypogée) après cinq mois. Les Rumex acetosella, T. repens et S. jacobaea se sont avérées capables de pleine compensation lorsque cultivées seules. En compétition, seul le R. acetosella a été encore capable de reprise. En aucun cas la tonte des compétiteurs n augmente la performance des plantes cibles (i.e., aucun bénéfice suite au relâchement des compétiteurs). Ces résultats soulignent l importance de considérer la compétition végétale, lorsqu on étudie les réactions des plantes à l herbivorie. Mots clés : herbivorie, reprise de croissance, relâchement des compétiteurs, compensation de biomasse. [Traduit par la Rédaction] del-val and Crawley 877 Introduction Plant population dynamics is known to be shaped by different selective pressures, herbivory and competition being two of the most important (Harper 1977; Crawley 1997). Nevertheless, the interaction between these processes is not well understood (Ritchie and Olff 1999). Whenever herbivores are present, some plants become scarce or completely disappear (herbivore decreasers), whereas others become Received 22 October Published on the NRC Research Press Web site at on 20 July E. del-val 1,2 and M.J. Crawley. Department of Biological Sciences, Imperial College, Silwood Park, Ascot, SL5 7PY UK. 1 Corresponding author ( ek@ekdelval.com). 2 Present address: CASEB, Facultad de Ciencias Biológicas, Pontificia Universidad Católica de Chile, casilla 114-D, Santiago, Chile. more abundant (herbivore increasers) (Crawley 1983, 1990; Lauda et al. 1990; Edwards and Crawley 1999; Vesk and Westoby 2001). However, factors that change a plant community s competitive interactions, such as disturbance, can alter the effect of herbivory on species abundance (Crawley 1990). An important goal in plant ecology is to understand how variation of herbivory, plant defences, and plant competition affect which species are either herbivore increasers or decreasers. Several broad mechanisms have been proposed to explain these changes in plant communities: (1) herbivore preference (related to plant quality and plant defence mechanisms), (2) plant capacity to regrow after herbivore damage (tolerance to herbivory), (3) competitor release (greater herbivore impact on competing species), (4) disturbance caused by herbivores in the environment, (5) phenological escape, or (6) by an alteration of nutrient cycle, as well as interactions between these mechanisms (McNaughton 1979; Milchunas et al. 1988; Crawley 1989, 1990, 1997; Huntly 1991; Pacala Can. J. Bot. 82: (2004) doi: /B04-066

2 872 Can. J. Bot. Vol. 82, 2004 and Crawley 1992; Anderson and Briske 1995; Augustine and McNaughton 1998; Rodriguez and Brown 1998; de Mazancourt et al. 1999). Plant tolerance to herbivory has been defined as the capacity of a plant to endure herbivory, with little loss in growth or reproductive output, or more specifically as a fitness reaction norm of genotypes under a gradient of herbivory pressure (Tiffin and Rausher 1999; Fornoni and Nuñez-Farfán 2000). Broadly speaking, tolerance is related to, or equated with, the capacity to compensate for tissue loss (Rosenthal and Kotanen 1994; Fineblum and Rausher 1995; Rosenthal and Welter 1995; Marquis 1996; Strauss and Agrawal 1999; Stowe et al. 2000). Despite plant defence mechanisms having been studied for several decades, plant tolerance has generally been little studied, and only recently has the relevance of this strategy been recognised. The importance of competitive forces in shaping plant communities has been known for a long time, although its relative magnitude has been hotly debated for several years (Grime 1973; Smith and Huston 1989; Tilman 1990; Tilman and Wedin 1991). The number and type of species growing in a particular site are correlated with resource availability and hence with the competitive environment (Crawley 1997; Olff et al. 2002). Nevertheless the link between plant responses to herbivory and plant competition is rarely examined (but see Ellison 1987; Reader 1992; Shabel and Peart 1994; Wardle and Barker 1997). In the present study, we attempt to address the interaction between a plant species ability to tolerate defoliation and interspecific competition, using four grassland species in a greenhouse experiment. Our specific questions were as follows: Are increaser and decreaser species able to compensate after simulated herbivory (clipping)? Does competition affect the regrowth capacity of a species? Do plants experience a competitor release effect after clipping their competitor, Festuca rubra L. subsp. rubra? Materials and methods Study species Four typical grassland species native to the British Isles (BI) were chosen to investigate plant tolerance to herbivory in competitive conditions. We chose four species that are known to respond differentially to herbivore presence in South East England grasslands (Crawley 1990). Rumex acetosella L. (Polygonaceae), Trifolium repens L. (Fabaceae), and Senecio jacobaea L. (Asteraceae) are increasers under rabbit herbivory, whereas Vicia sativa L. subsp. nigra (L.) Ehrh. (Fabaceae) is a decreaser. 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% (del-val and Crawley 2004). We used F. rubra subsp. rubra (Poaceae) as the competitor, because it is one of the dominant species in Southern England grasslands where the other four species occur, and it is capable of producing a spatially uniform sward under experimental conditions. Experimental design Cuttings of R. acetosella and T. repens were collected on May 2001 from grasslands in Silwood Park, Berkshire (GR 41/944691); each cutting was planted into individual pots in the greenhouse. Senecio jacobaea seeds were collected from the same field on 7 August 2001 and sown immediately in the greenhouse. Vicia sativa subsp. nigra and F. rubra subsp. rubra seeds were purchased from Emorsgate Seeds, Kings Lyn in Norfolk, UK. Vetch seeds were scarified with sand paper before planting and sown on 16 May Each target plant was planted individually in a 20-cm plastic pot in a mixture of soil: 50% sand, 20% loam, and 30% peat. The experiment consisted of six treatments: two treatments with target species growing alone, (a) control and (b) clipped, and four grown in competition with F. rubra subsp. rubra, (c) control (both species unclipped), (d) both species clipped, (e) only target species clipped, and ( f ) only competitor clipped. The six treatments constituted a 3 2 factorial design, with three levels of competition (alone, with competitor, or with clipped competitor) and two levels of clipping on target plants (clipped or unclipped) (Fig. 1). Sample size for each treatment per species was n =5. Once the target plants were established, 15 d after sowing (30 May 2001), 30 seeds of F. rubra subsp. rubra per pot were added to the competition treatments. Twenty-three days after (22 June 2001) clipping was carried out by removing 75% of the aboveground biomass of each plant (measured in height) using a pair of scissors, this was performed only once on the assigned treatments. 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 by 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). For S. jacobaea the dates were different, but we kept the same length interval: F. rubra subsp. rubra seeds were added on 31 August 2001 and plants were clipped on 19 September The experiment was performed in a 20 C controlledtemperature greenhouse with 12 h light : 12 h dark cycle. The bench space was divided into 20 blocks (5 blocks per species), with each block containing one replicate per treatment (six pots). Pots were arranged randomly and moved every other week. Watering was done every other day. Rumex acetosella, T. repens, and V. sativa subsp. nigra pots were harvested 3 months after sowing (17 23 August 2001), and S. jacobaea was harvested on 7 November Aboveground biomass was separated from roots, and roots were washed thoroughly to eliminate soil particles. Aboveground and root biomass were dried in an oven (80 C) for 48 h and weighed. In the competition pots, aboveground biomass was separated by species, but we were unable to separate root biomass. Root/shoot ratios were only calculated for each species when they were growing alone, both in the clipped and control treatments. Statistical analysis The data were analysed with analysis of variance (ANOVA). We performed different analysis using aboveground target biomass, root biomass, aboveground F. rubra subsp. rubra biomass, total biomass, and root/shoot ratio as response variables. Each species was analysed separately.

3 del-val and Crawley 873 Fig. 1. Experimental treatments. Table 1. ANOVA F-statistics (df in parentheses) for main effects and interactions affecting the aboveground biomass of the four target species studied. Rumex acetosella (g) Senecio jacobaea (g) Trifolium repens (g) Vicia sativa subsp. nigra (g) Competition 1.17 (1, 24) 0.06 (1, 24) 1.8 (1, 24) 1.9 (1, 17) Clipping target 1.19 (1, 24) 1.51 (1, 24) 9.8 (1, 24)** 8.04 (1, 17)* Clipping competitor 0.32 (1, 24) 2.42 (1, 24) (1, 24) 0.01 (1, 17) Competition clipping target 0.03 (1, 24) 2.75 (1, 24) 1.51 (1, 24) 0.31 (1, 17) Clipping target clipping competitor 0.01 (1, 24) 2.02 (1, 24) 0.93 (1, 24) 0.13 (1, 17) Note: *, p < 0.05; **, p < For the total biomass, root/shoot ratio, and root biomass analyses, only alone treatments were taken into account. For the aboveground F. rubra subsp. rubra biomass analysis, only competition treatments were considered; aboveground target biomass was analysed in all treatments. All analyses were performed first with untransformed data, and then the response variables were transformed to comply with ANOVA assumptions. Different variables performed best under different transformations. Total biomass, target aboveground biomass, and root/shoot ratio were squared-root transformed, whereas root biomass and competitor aboveground biomass were natural-log transformed. Analyses were carried out in SPLUS 2000 (MathSoft, Inc.). In all cases a full model was fitted to the data and then reduced to a minimal adequate model by simplification; all nonsignificant terms were removed sequentially from the full model, starting from the highest order interaction terms. Results Clipping affected aboveground biomass of V. sativa subsp. nigra and T. repens, but for T. repens this was only true when it was grown in competition (Table 1 and Figs. 2a, 2b). In contrast, clipping R. acetosella and S. jacobaea had no effect on aboveground biomass (Figs. 2c, 2d). Total biomass and root biomass were not affected by clipping for any of the species in the noncompetitive treatments (p > 0.05). Root/shoot ratios from plants growing alone were not affected by clipping in any species, but species had different root/shoot ratios (F [3,33] = 27.6, p < ). In control pots, R. acetosella (1.76 ± 0.35) (mean ± SE) and S. jacobaea (1.4 ± 0.29) had the highest root/shoot ratios, followed by V. sativa subsp. nigra (0.87 ± 0.17) and then T. repens, which had the smallest ratio (0.31 ± 0.03). There was no overall effect of neighbouring F. rubra subsp. rubra on any of the target species (Table 1). When plants were grown in competition, the effects of clipping were different from the alone pots (Fig. 2). Rumex acetosella biomass was not affected either by the presence of F. rubra subsp. rubra or by clipping the competitor. In contrast, T. repens had greater biomass when unclipped (both in control treatment and when only the competitor was clipped), while S. jacobaea and V. sativa subsp. nigra were affected detrimentally when they were clipped and competitor plants were left intact. Competitor biomass Festuca rubra subsp. rubra biomass was lower when clipped and the target species were left intact, and it was not affected by clipping the target species (Table 2 and Fig. 3). Comparing competitor s performance growing with the different target species, aboveground biomass of F. rubra subsp. rubra was greater when growing in pots with S. jacobaea (1.67 ± 0.22 g) and V. sativa subsp. nigra (1.63 ± 0.29 g) in comparison with R. acetosella (0.87 ± 0.1 g) and T. repens (0.46 ± 0.13 g) (Table 2). Discussion Herbivore-increaser species were able to compensate fully after 75% aboveground biomass defoliation when growing on their own. Only V. sativa subsp. nigra (herbivore decreaser) was reduced by clipping in the alone pots. In contrast with other experiments, we found no stimulation of above- or below-ground biomass (McNaughton 1983; Maschinski and Whitham 1989; Lennartsson et al. 1998; Paige 1999). In general, a plant s regrowth capacity can result from reallocation of resources from roots or storage organs to shoots, by activating dormant meristems, or by increasing physiological processes such as photosynthetic enhancement in the remaining tissue to produce more carbohydrates,

4 874 Can. J. Bot. Vol. 82, 2004 Fig. 2. Aboveground biomass of target plants under different experimental treatments, showing the four species studied. Values shown are mean sqrt(aboveground biomass) ±1 SE. Bars with the same letter are not significantly different (p > 0.05). ANOVA results are reported in Table 1. Plants growing alone (white bars), plants growing in competition (striped bars). Table 2. ANOVA F-statistics (df in parentheses) for main effects and interactions affecting the aboveground biomass of Festuca rubra subsp. rubra. F. rubra subsp. rubra (g) Species 6.39 (3, 69)*** Clipping target 1.59 (1, 69) Clipping competitor 4.47 (1, 69)* Clipping target clipping 4.25 (1, 69)* competitor Note: *, p < 0.05; **, p < 0.01; ***, p < Fig. 3. Effects of different treatments on Festuca rubra subsp. rubra biomass. Values shown are means ±1 SE, with data natural-log transformed. Bars with the same letter are not significantly different (p > 0.05). ANOVA results are reported in Table 2. changes in canopy architecture, changes in leaf morphology, increases or decreases in root respiration, and increases in nutrient uptake (Chapin and Slack 1979; Whitham et al. 1991; Trumble et al. 1993; Mole 1994; Tuomi et al. 1994; Strauss and Agrawal 1999). Rumex acetosella and S. jacobaea showed compensation after defoliation. They possess rhizomes as reserve organs (Harper and Wood 1957; Lovett Doust and Lovett Doust 1987) and had the greatest root/shoot ratios. The importance of resource allocation to herbivory tolerance before damage is inflicted was shown by Hochwender et al. (2000), who found that the genotypes of Ascelpias syriaca with the highest root/shoot ratio before damage had greater compensatory ability. Trifolium repens has a limited amount of reserves and a small root/shoot ratio, therefore it must be using a different strategy for compensation. Burdon (1983) described this species as having alternative meristems, so they may account for the observed regrowth in the absence of competition. Species that possess alternative meristems have the possibility to regrow from different branches once apical dominance is removed (Aarssen 1995). Vicia sativa subsp. nigra does not appear to have storage structures or alternative dormant meristems (Clapham et al. 1987) and was unable to compensate for the effects of clipping. It is important to take into account that the increaser species used are also perennials, while the decreaser species is annual. Selective pressures on different life-history strategies may account for the different capacity of biomass compensation observed. An additional external factor related to plant performance is competition. It is normally assumed that the presence of neighbours can reduce plant fitness and plant germination (Rees and Brown 1991). Contrary to expected, the most

5 del-val and Crawley 875 striking fact in this experiment was that the presence of F. rubra subsp. rubra did not reduce the biomass of any species, and T. repens actually tended to increase in biomass in the presence of F. rubra subsp. rubra, suggesting some kind of facilitation (i.e., possible retention of water in the soil). A possible limitation for the interpretation of the present study is that even though 30 plants of F. rubra subsp. rubra were sown in each pot and were competing with only one target plant, they may not have exerted enough competitive pressure for the studied species. Another argument could be that because target plants were already established when Festuca seeds were added, they did not experience competition at the beginning of the experiment. Nevertheless, later on when clipping the plants and F. rubra subsp. rubra was established, the target plants experienced limitation of resources (competition) when needing to compensate for defoliation, and this was translated into a decrease in regrowth capacity as shown in other experiments that evaluated herbivore effects under competition (Shabel and Peart 1994; Wardle and Barker 1997). At the end of the experiment we were able to see that F. rubra subsp. rubra roots were forming a dense mat and occupying most of the pot, suggesting that target plants were experiencing some competition for nutrients and (or) water. This evidence could also suggest that a possible reason for why few studies have succeeded in finding costs for tolerance (Lowenberg 1994; Mauricio et al. 1997; Agrawal et al. 1999; Fornoni and Nuñez-Farfán 2000) is related to plants being grown without competition. Because plants normally grow in a competitive environment, we suggest that to evaluate possible costs for plant tolerance competition should be considered for further examinations and that trade-offs could be found when plants are grown in competition. Several studies have found that compensation occurs only when competition is not important (Maschinski and Whitham 1989; Alward and Joern 1993; Shabel and Peart 1994; Huhta et al. 2000), while others propose that the impact of herbivores should be greatest when environmental constraints limit plant response and compensatory growth (Lauda et al. 1990). Our experiment supports these ideas, because in the treatment where only the target species was clipped, the resultant biomass was smaller in all target species except R. acetosella. The lack of effects from the different treatments on R. acetosella may be related to its large storage organs, which are able to reallocate resources for compensation notwithstanding being in competition, but this result could be different under repeated defoliation. Festuca rubra subsp. rubra biomass was also affected when it was clipped and target species were not. We postulate that if a selective defoliation on the target species takes place and the rest of the competitors are left intact, the capacity to replace tissues after defoliation is detrimentally affected. Different authors have proposed that when herbivores preferentially consume neighbouring plants, the species in question can be positively affected because of competitor release (Milchunas et al. 1988; Crawley 1989, 1990, 1997; Huntly 1991; Pacala and Crawley 1992; Rodriguez and Brown 1998). Despite these postulations, this effect did not occur in our experiment. When F. rubra subsp. rubra was clipped (i.e., competitor preferentially grazed), none of the species benefited from it, suggesting that shading of target plants by F. rubra subsp. rubra was not important (i.e., light was not a limiting factor). In contrast, other authors have found that S. jacobaea and Aristolochia reticulata grew better when surrounding vegetation was clipped (Fowler and Rausher 1985; McEvoy et al. 1993). Therefore, competitor release was an important aspect of these systems. In our view, this aspect highlights the importance of defining which are the limiting resources that would affect the outcome of competing species (Tilman 1982) and questions the importance of competitor release when light is not the limiting factor of the system; the assumption of herbivory leading into competitor release is contingent on which resources are limiting a plant s growth. We realise that competitor release can be very important in field situations when species are involved in complex interactions and when different resources are limiting. Overall, we can say that tolerance appears to be playing a role in the persistence of a species in a community where herbivores graze frequently: the three increasers were able to compensate for defoliation whereas the one decreaser was not. When growing in competition, clipping a neighbouring species did not improve target species status, but competition reduced the ability to compensate. This experiment shows that investigating different selective pressures in conjunction (i.e., herbivory and competition) in the same system will help us to better understand the processes we observe in the field. This can help us to separate the responses related to individual reactions and those related to population community processes. Acknowledgements We thank C. de Mazancourt, R. Keane, and M. 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