Herbivore-induced responses and patch heterogeneity affect abundance of arthropods on plants

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1 Ecological Entomology (2005) 30, Herbivore-induced responses and patch heterogeneity affect abundance of arthropods on plants CESAR RODRIGUEZ-SAONA 1 and JENNIFER S. THALER 2 Department of Entomology, Michigan State University, Michigan, U.S.A., 2 Department of Entomology, Cornell University, New York, U.S.A. Abstract. 1. Plants respond to herbivore damage by inducing defences that can affect the abundance of herbivores and predators. These tritrophic interactions may be influenced by heterogeneity in plant neighbourhood. 2. In the present study, the effects of induced responses on the abundance of herbivores (flea beetles and aphids), omnivores (pirate bugs and thrips), and predators (lady beetles and spiders) on individual plants and their neighbours between and within patches composed of three tomato plants was investigated. 3. Herbivore damage was manipulated to create homogeneous patches where either all or none of the plants had defences induced by herbivore damage, and heterogeneous patches where only one of the plants was induced. 4. Arthropod abundance on plants at different scales was compared by testing between patch effects (patch level), for neighbourhood effects at the plant phenotype level (neighbourhood level), and between near and far plants (within patch position). 5. At the patch level, plants in homogeneously induced patches contained fewer flea beetles and pirate bugs, but more lady beetles, compared with homogeneously non-induced patches. There was no effect of patch type on the abundance of aphids, thrips, and spiders on plants. 6. At the neighbourhood level, induced plants in heterogeneous patches contained more flea beetles and pirate bugs compared with induced plants in homogeneous patches, indicating that the abundance of some herbivores and omnivores on induced plants varied depending on the phenotype of the other plants within the patch. Within patch position, there was no evidence that the abundance of herbivores or predators on non-induced plants was affected by proximity to an induced plant. 7. Therefore, variation in plant neighbourhood generated by induced plant responses affected the abundance of three arthropods from three feeding guilds. Key words. Arthropod abundance, herbivore-induced plant responses, Lycopersicon esculentum, neighbour effects, patch heterogeneity, phenotypic plasticity. Introduction The neighbourhood is a scale where plant species diversity has been thought to influence arthropod abundance. Plants might experience a decrease in numbers of herbivores or an increase in predators when near a more resistant neighbour Correspondence: Cesar Rodriguez-Saona, Department of Entomology, Michigan State University, East Lansing, MI 48824, U.S.A. rodri337@msu.edu ( associationalresistance ; Tahvanainen & Root, 1972; Hay, 1986). Sabelis and De Jong (1988) hypothesised that plants that are attractive to predators could increase predators on their less attractive neighbours (Stiling et al., 2003). Plants may also increase the susceptibility of neighbouring plants to attack by herbivores ( associationalsusceptibility ) (Karban, 1997; Rand, 1999). As phenotypic plasticity is the norm in nature (Pigliucci, 2001; West-Eberhard, 2003), plants will often find themselves surrounded by conspecific plants expressing different phenotypes. Abundance of herbivores and predators on a single 156 # 2005 The RoyalEntomologicalSociety

2 Induced responses and arthropod abundance in plant patches 157 plant may be altered by the phenotype of neighbouring plants (van der Meijden & Klinkhamer, 2000). Although there are a number of studies that have examined the effects of heterogeneity caused by different species of plants (e.g. Root, 1973; Andow, 1991; Siemann et al., 1998; Bernays, 1999), few have examined the role of heterogeneity caused by conspecific plants expressing different phenotypes, such as resistance induced in response to herbivore attack (e.g. Dolch & Tscharntke, 2000; Dicke & Bruin, 2001). Induced plant responses to herbivore damage can affect herbivore and predator performance on, or preference for, plants (Karban & Baldwin, 1997). For instance, many plant species respond to herbivory by emitting volatile compounds (Turlings et al., 1990; Turlings & Tumlinson, 1992; Dicke & Vet, 1999). Volatile compounds emitted from herbivore-damaged plants are a very important component of herbivore and predator host location. Herbivores such as spider mites and beetles can be attracted to volatiles released from damaged plants (Dicke & van Loon, 2000; reviewed by Dicke & Vet, 1999). In contrast, these volatiles can repelmany species of moths (e.g. De Moraes et al., 2001; Kessler & Baldwin, 2001; Harmon et al., 2003). Volatiles emitted from induced plants frequently attract predators and parasitoids of herbivores (Turlings et al., 1990; Vet & Dicke, 1992; De Moraes et al., 1998; Thaler, 1999; Kessler & Baldwin, 2001). However, induced responses may reduce the number of predators if reduced herbivore density affects recruitment of predators (McAuslane, 1994; Thaler, 2002), if damaged plants induce changes in the behaviour or quality of herbivores that affect the behaviour of their predators (McAuslane, 1994), or if predators are omnivores and obtain resources directly from plants (Agrawal et al., 1999). The effects of induced responses by a single plant on colonising insects may change depending on the plant neighbourhood. For example, the discrimination of herbivores and predators between plants of different phenotypes can be influenced by volatile emissions from other plants within the patch. Karban et al. (2003) showed that amount of herbivore damage on tobacco plants is reduced when grown in close proximity (within 10 cm) to clipped or herbivore-damaged sagebrush. Alternatively, plants might not affect the abundance of arthropods on their neighbouring plants. Dicke et al. (2003) tested the effects of mixing volatiles from two plant species on the foraging behaviour of the predatory mite, Phytoseiulus persimilis Athias-Henriot. They found that attraction of the predatory mites to Lima bean plants infested with spider mites (prey) was not affected by the presence of Brussels sprouts infested by caterpillars (non-prey). In the present study, tomato plants, Lycopersicon esculentum Mill., were used to investigate how herbivores and predators respond to phenotypic variation between and within patches of plants. Previous field experiments found that induction of plant responses affected the abundance of herbivores and their natural enemies on single plants (Thaler, 1999, 2002; Thaler et al., 2001). In this study, herbivore damage to tomato plants (and thus defence phenotype) was manipulated in the field to create homogeneous patches, where either all or none of the plants had defences induced, and heterogeneous patches where only one of the plants was induced. It was hypothesised that homogeneously noninduced patches may initially contain a greater abundance of herbivores, due to the occurrence of higher quality plants for food in these patches compared with homogeneously induced patches. Homogeneously induced patches are hypothesised to initially have more predators because these patches are emitting cues indicative of herbivore presence. Omnivores are predicted to behave like herbivores in low prey availability situations and like predators in high prey availability situations (Agrawal et al., 1999). Once these patterns were tested at the homogeneous patch level it was asked how predator and herbivore abundance was altered by a heterogeneous patch and on individuals of different phenotypes within a patch. Thus, a hierarchicalanalysis was conducted first testing effects of induced responses at the patch level, and then testing for neighbourhood effects on particular plant phenotypes. The following specific questions were addressed: at the patch level, does the abundance of arthropods differ between patches? At the neighbourhood level, does the abundance of arthropods on individualplants of a particular phenotype differ between homogeneous and heterogeneous patches? Within patch position, does the abundance of arthropods on a particular phenotype in a heterogeneous patch differ depending on the phenotype of the neighbouring plant? These neighbour effects were examined when plants were located near to (adjacent), or far from (two plants away), an induced or a non-induced plant. Methods Study site and plants The study was conducted at the Koffler Scientific Reserve at Jokers Hill (University of Toronto), a 350-ha area located in Southern Ontario, Canada ( N, W), in a ploughed field 30 m long and 20 m wide, previously planted with hay. On the north side of this field there was a hardwood and poplar forest, elsewhere hay fields surrounded the study site. Seeds of L. esculentum cv. Castlemart were grown in 500- mlpots containing a soilmix (Premier Horticulture Ltd, Quebec, Canada), and 5 10 pellets of Nutricote ( N-P-K; Chisso-Ashai Fertiliser Co., Ltd, Tokyo, Japan). Plants were grown in greenhouses at the University of Toronto under natural lighting supplemented with 400-W sodium halide lamps, watered daily, and fertilised weekly with N- P-K fertiliser (Plant-Products, Ontario, Canada). Patch configuration One month after seeds were planted, tomato plants were transplanted to the field. At this stage plants had four or

3 158 Cesar Rodriguez-Saona and Jennifer S. Thaler five fully expanded true leaves. A patch consisted of three tomato plants placed in a straight line and spaced 40 cm apart, allowing plants to be close but without touching each other. Plants were transplanted into 20 rows of three patches (totalof 60 patches, 180 plants). Patches within each row and plants between rows were separated by 1.5 m. Patches were made distinct from each other by planting a grass border surrounding each patch. Grass was planted a month prior to the experiment and was cm tall. Thus, because of the greater distance between plants across patches than within patches, and the presence of grass as a physical barrier around each patch, it is likely that arthropods made decisions based on the quality of plants to remain or leave a patch. Patches were assigned randomly to one of three treatments (patch types): (1) homogeneously non-induced patches where none of the plants received herbivore damage (Control); (2) homogeneously induced patches where all plants within a patch received herbivore damage (Induced); and (3) heterogeneously induced patches where one plant within a patch was damaged (Mixed). Damage within Mixed patches was always to an end plant because one goalof this treatment was to test the effects of induced plants on non-induced plants when near (adjacent) or far (two plants away) from the induced plant. One day after the plants were transplanted, the second oldest leaf of all plants was bagged using spun polyester sleeves (35 cm wide 45 cm length). Three days after transplant, damage was initiated by placing a third-instar Spodoptera exigua (Hu bner) inside each bag of induced plants. Spodoptera exigua induces responses in tomato plants that can affect the performance of other herbivores (Stout et al., 1996, 1998) and attraction of naturalenemies of herbivores (Thaler et al., 2002). Previous studies have shown that these larvae are relatively odourless compared with volatiles induced by plants; in fact, larvae alone are not enough to stimulate a response by its parasitoid Cotesia marginiventris (Cresson) (Turlings et al., 1991), whereas herbivoredamaged tomato plants induced an easily detectable volatile response (Takabayashi & Dicke, 1993; Farag & Paré, 2002; Thaler et al., 2002). A colony of S. exigua, obtained from the USDA (Stoneville, Mississippi), were maintained on an artificial diet (Southland Products, Lake Village, Arkansas) at room temperature ( 24 C and 14:10 h L:D cycle). One day prior to the experiment, caterpillars were fed tomato foliage to acclimate them to their new diet. Caterpillars were allowed to feed on plants for 5 6 days to induce a systemic response (Stout et al., 1996). This treatment increases amounts of defensive proteins such as proteinase inhibitors and volatile emissions (C. Rodriguez-Saona, unpub. data). After this time period, caterpillars were removed from induced plants and the per cent leaf area lost was visually measured. On average, caterpillars ate (SE)% of leaf 2 (< 20% of whole plant mass). Bags were left on plants throughout the experiment to prevent visualcues from the damaging caterpillar from affecting arthropod attraction to damaged plants. The entire experiment was repeated four times with completely different plants (total number of patch types ¼ 80, 81, and 79 for Control, Induced, and Mixed, respectively) from May to August of Arthropod abundance Two methods were employed to monitor abundances of all naturally colonising arthropods in patches [as described by Thaler et al. (2001) and Thaler (2002)]. In all four trials, arthropods were counted on each individualplant 7 days after caterpillars were placed on induced plants (1 day after caterpillars were removed). In addition, in the last three trials, sticky traps were placed close to non-induced and induced plants. The sticky traps were 5 5-cm pieces of green cardboard, covered with a thin layer of Tangletrap (Grand Rapids, Michigan) and mounted on wooden sticks in the ground 5 10 cm away from plants, such that traps were at canopy level but not touching plants. The sticky area of all traps faced the same direction. Traps were placed outside 2 days after damaging caterpillars were placed on plants and were left in the field for three days. Most plants initiate emissions of systemically induced volatiles about 2 4 days after initialherbivore damage and stop their emissions a few days after damagers are removed (Mattiacci et al., 2001); this is also true for tomato plants where volatile emissions drop hours after herbivory is stopped (Farag & Pare, 2002). Thus, timing our sampling methods soon after (arthropod counts on plants) and during (sticky traps) herbivore damage allowed us to monitor those arthropods that may utilise plant volatiles during foraging. Two species of herbivores occurred in high abundance. Leaf-chewing flea beetles, Epitrix cucumeris (Harris) (Coleoptera: Chrysomelidae), were present throughout the field season in high numbers, and the potato aphid Macrosiphum euphorbiae (Thomas) (Homoptera: Aphididae), a phloem-sucking feeder, became abundant later in the season (trials 3 and 4). Two omnivores were present consistently throughout our experiments: western flower thrips, Frankliniella occidentalis (Pergande) (Thysanoptera: Thripidae) and minute pirate bugs, Orius sp. (Hemiptera: Anthocoridae). Besides feeding on plants, thrips prey on spider mites and their eggs (Trichilo & Leigh, 1988), while pirate bugs prey on small arthropods (Salas-Aguilar & Ehler, 1977). The two most abundant groups of predators were lady beetles (Coleoptera: Coccinellidae), predominantly convergent lady beetles, Hippodamia convergens Gue rin- Me neville, and web-building spiders (Araneae: Araneidae). Although lady beetles prefer aphids as prey, they can also feed on other small arthropods including caterpillars (Hagen, 1962). Statistical analyses At the patch level. The effects of patch type (Control, Induced, and Mixed) on arthropod abundance were tested using MANOVA (SYSTAT ver ; SPSS Science, Chicago, Illinois) (Scheiner, 1993), with treatment (patch type) and

4 Induced responses and arthropod abundance in plant patches 159 trialas main effects (independent variables). The abundances of each species (flea beetles, aphids, pirate bugs, thrips, lady beetles, or spiders) were the dependent variables. MANOVA tests were conducted for all patch types (three levels) and as a series of pairwise comparisons between patches. To determine which species were most influenced by treatment, a significant MANOVA was followed by a univariate analysis (ANOVA). Because the assumption of normality was not always met, separate Kruskal Wallis tests were conducted for each arthropod species with patch as the independent variable. Each Kruskal Wallis yielded similar results as the univariate ANOVAs, so results are only presented from the MANOVA followed by the ANO- VAs. At the neighbourhood level. To determine if arthropod abundance differed on a particular phenotype between homogeneous and heterogeneous patches MANOVA was used (as described above). Mean arthropod abundance per plant on induced plants from Mixed patches was compared with the number of arthropods on plants from Induced patches (i.e. mean arthropod abundance of three plants from Induced patches was compared with the single induced plant in Mixed patches). Similarly, MANOVA was used to compare arthropod abundance on non-induced plants from Mixed patches with the number of arthropods on plants from Control patches, such that the mean arthropod abundance of three plants from Control patches was compared with the two non-induced plants in Mixed patches. The effect of phenotypic variation within Mixed patches was determined by comparing the mean arthropod abundance from the single induced plant to the mean arthropod abundance from two non-induced plants. Within patch position. Arthropod abundance on noninduced plants near an induced plant in Mixed patches was compared using MANOVA with non-induced plants of the same spatial location within Control patches. Similarly, arthropod abundance on non-induced plants far from an induced plant in Mixed patches were compared with noninduced plants of the same spatial location within Control patches. Results The data obtained was analysed from whole-plant counts with and without the data from sticky traps. The same statisticaloutcome was achieved using the two methods, so here only the results obtained when data from these two methods were pooled are presented, to reduce the number of zeros in the data set. At the patch level One week after caterpillars were placed on plants, the abundance of arthropods among the three patch types differed significantly (MANOVA: Wilks l ¼ 0.855; F 12,446 ¼ 3.037; P < 0.001). When arthropod abundance was compared between patches, differences were found between homogeneously induced (Induced) and homogeneously non-induced (Control) patches (MANOVA: Wilks l ¼ 0.879; F 6,148 ¼ 3.38; P ¼ 0.004). Induced patches contained 52% fewer flea beetles and 49% more lady beetles (Table 1; Fig. 1) compared with Control patches. Induced patches also contained fewer pirate bugs (Table 1; Fig. 1) in three of the four trials (significant patch-by-trial interaction; Table 1). In trials 2 4 Control patches had times more pirate bugs compared with Induced patches, whereas no differences between patches were seen in trial1. No differences were found in the number of aphids, thrips, and spiders between Induced and Control patches (univariate ANOVA, al l P-values >0.05; Table 1; Fig. 1). The total abundance of flea beetles (ANOVA: F 1,152 ¼ ; P ¼ 0.001) and pirate bugs (ANOVA: F 1,152 ¼ ; P ¼ 0.002) on plants within Mixed patches was 2.3 and 2.4 times higher, respectively, compared with Induced patches, indicating that plants in Mixed patches were preferred over plants in Induced patches (MANOVA: Wilks l ¼ 0.844; F 6,147 ¼ 4.531; P < 0.001; Fig. 1). The abundance of other arthropods was similar between Mixed and Induced patches (univariate ANOVA, al l P-values >0.05; Fig. 1). In contrast, the abundance of all arthropods on plants was similar in Mixed compared with Control patches (MANOVA: Wilks l ¼ 0.970; F 6,146 ¼ 0.757; P ¼ 0.605; Fig. 1). At the neighbourhood level Similar abundances were found of all species on noninduced plants in Mixed patches compared with Control patches (MANOVA: Wilks l ¼ 0.937; F 6,146 ¼ 1.644; P ¼ 0.139; Fig. 2a). The abundance of arthropods on induced plants, however, differed depending on whether plants were surrounded by non-induced plants in Mixed patches or surrounded by induced plants in Induced patches (MANOVA: Wilks l ¼ 0.913; F 6,147 ¼ 2.33; P ¼ 0.035). Induced plants from Induced patches had 54% fewer flea beetles than induced plants in Mixed patches (Table 1; Fig. 2b). There was also a marginally significant trend for lower abundance (50%) of pirate bugs on plants in Induced patches compared with induced plants from Mixed patches (Table 1; Fig. 2b). In contrast, the abundance of aphids, thrips, lady beetles, and spiders on induced plants was not affected by patch type (Table 1; Fig. 2b). At the plant phenotype level within Mixed patches, the abundance of lady beetles on induced plants was 40% higher than on control plants, although the difference was not statistically significant (ANOVA: F 1,150 ¼ 1.324; P ¼ 0.252). The abundance of other species of arthropods on induced plants did not differ from non-induced plants in Mixed patches (MANOVA: Wilks l ¼ 0.964; F 6,145 ¼ 0.902; P ¼ 0.495; Fig. 3).

5 160 Cesar Rodriguez-Saona and Jennifer S. Thaler Table 1. Two-way ANOVA (following MANOVA) for effects of patch type and trialon the abundance of arthropods. Induced vs. non-induced plants in homogeneous patchesyz Induced plants in homogeneous vs. heterogeneous patchesy Patch TrialPatch TrialPatch Trial Patch Trial Flea beetles ** ** NS 5.592* 6.265** NS Aphids NS ** NS NS ** NS Pirate bugs 6.439* ** 2.777* 3.299{ ** 6.428** Thrips NS 5.408** NS NS 2.772** 2.741* Lady beetles 4.252* ** NS NS ** NS Spiders NS 7.430** NS NS 5.695** NS ynumbers are F-values. Asterisks indicate significant differences: **P < 0.01; *0.01 < P < 0.05; NS, P > zd.f. ¼ 1,153 for Patch effect; 3,153 for Trialeffect; and 3,153 for Patch Trialeffect. d.f. ¼ 1,152 for Patch effect; 3,152 for Trialeffect; and 3,152 for Patch Trialeffect. {P ¼ Within patch position The abundance of arthropods on non-induced plants was similar when near to, or far from, an induced plant in Mixed patches compared with non-induced plants near to, or far from, non-induced plant in Control patches (MANOVA for plants near induced compared with non-induced plants: Wilks l ¼ 0.989; F 6,146 ¼ 0.263; P ¼ 0.953; MANOVA for plants far from induced compared with non-induced plants: Wilks l ¼ 0.949; F 6,146 ¼ 1.301; P ¼ 0.26). Discussion Mean/plant/patch ± SE a a b a a Patch type Control Mixed Induced Flea beetles Aphids Pirate bugs Thrips Lady beetles b a ab b Spiders Fig. 1. Abundance of arthropods in homogeneously non-induced (Control), heterogeneous (Mixed), and homogeneously induced (Induced) patches. Data are means of three plants within each patch. Means within arthropod groups with different letters are significantly different (P 0.05), otherwise P > Overall, it was found that a subset of the arthropod community was influenced by induced plant responses and patch heterogeneity. Although not all species in a trophic position responded to the treatments, for the subset of species affected by induced responses, the effects were consistent with the prediction that herbivores and predators should be of different abundance in homogeneously induced and non-induced patches. The effect of induction on arthropod abundance was, however, influenced by the spatialpattern of plant arrangement and the trophic position of the arthropod species. Therefore, for some Mean/plant/patch ± SE (a) Non-induced plants (b) Induced plants a b P = 0.07 Flea beetles Aphids Pirate bugs Thrips Lady beetles Patch type Control Mixed Patch type Mixed Induced Spiders Fig. 2. Abundance of arthropods on non-induced plants from homogeneously non-induced (Control) and heterogeneous (Mixed) patches (a) and on induced plants from heterogeneous (Mixed) and homogeneously induced (Induced) patches (b). Data are means of three plants from Induced patches and the single induced plant in Mixed patches. Means within arthropod groups with different letters are significantly different (P 0.05), otherwise P > 0.05.

6 Induced responses and arthropod abundance in plant patches 161 Mean/plant/patch ± SE Mixed patches 0 Flea beetles Aphids Pirate bugs Thrips Plant phenotype Non-induced plants Induced plants Lady beetles Spiders Fig. 3. Abundance of arthropods on non-induced and induced plants in heterogeneous (Mixed) patches. Data are means of two non-induced plants and a single induced plant. No significant differences were found between treatments (MANOVA). interactions, plants can be seen as independent entities, whereas for others, neighbouring plants must be considered. At the patch level, the abundance of herbivorous flea beetles was lower in homogeneously induced (Induced) patches compared with homogeneously non-induced (Control) patches, while aphid abundance did not differ. In contrast, predaceous lady beetles were more abundant in Induced patches compared with Controlpatches, while the abundance of web-spinning spiders was not influenced by patch type. As with the flea beetles, the abundance of omnivorous pirate bugs was lower in Induced patches compared with Controlpatches while the abundance of thrips was not affected by patch type. Patch heterogeneity more strongly affected the abundance of some species of herbivores and omnivores compared with the abundance of predators. For example, the abundance of flea beetles on induced plants in Mixed patches was higher compared with plants in Induced patches and not different from the abundance of flea beetles on plants in Control patches (Fig. 2). Therefore, induced responses only reduced the number of flea beetles on plants surrounded by other induced plants, but not those surrounded by non-induced plants. A similar trend was found for the omnivorous pirate bugs. Unlike flea beetles and pirate bugs, the abundance of lady beetles on induced plants did not differ between Induced and Mixed patches, suggesting that lady beetles discriminated between induced and non-induced individualplants. Within Mixed patches, the abundance of lady beetles on induced plants was 40% higher, but not significantly so, than the number of lady beetles on non-induced plants. Although not conclusive, these findings suggest that lady beetles might be foraging primarily at the plant level. As indicated above, non-induced plants in Mixed patches may influence the number of flea beetles and pirate bugs on induced plants compared with homogeneously induced patches; induced plants, however, did not influence the abundance of arthropods on their neighbouring noninduced plants in Mixed patches. No effects were found on the abundance of arthropods on non-induced plants when near to, or far from, an induced plant. Thus, the heterogeneity within a plant patch influenced the number of some herbivores in that patch as a whole, but not their distribution across plants with different phenotypes within that patch. The effects of plants on predaceous and omnivorous arthropods may be due to the abundance of prey, the attractiveness of the plant, and plant quality. Even though lady beetles are generalist predators, they have a preference for aphids (Hagen, 1962), which were abundant prey in this study. However, no effect of induced plant responses on aphid abundance was found. Thus, aphid prey availability is not a likely explanation for the higher abundance of lady beetles on induced patches compared with control patches. While pirate bugs have been shown to respond positively to volatiles from herbivore-damaged plants (Drukker et al., 1995; Venzon et al., 1999), in this study more pirate bugs were found on undamaged plants. It is possible that because of low prey availability, pirate bugs were behaving primarily as herbivores. As a consequence they were more abundant in Controlpatches where hostplant quality was higher. Agrawal et al. (1999) found that, in the absence of prey, feeding by omnivorous thrips was higher on non-induced plants compared with herbivoreinduced plants. van der Meijden and Klinkhamer (2000) argued that if the production of herbivore-induced volatiles is expensive, individual plants might cheat by not producing volatiles themselves and profiting from the volatile production of neighbours. So far, however, there is no empiricalevidence suggesting that plants that invest in volatile production can unintentionally benefit their non-volatile producing neighbours. In this study, tomato plants investing more in induced defences did not benefit their less defended neighbours by an increase in predator abundance. In addition, non-induced plants near to, or far from, an induced plant did not experience a decrease in the number of herbivores compared with those near to, or far from, a non-induced plant. Thus, in this study phenotypic heterogeneity increased abundance of some consumers on induced plants (associationalsusceptibility), but no evidence was found that heterogeneity may provide associationalresistance against herbivores by reducing the abundance of plant consumers on non-induced plants. In fact, undamaged plants in heterogeneous patches (Mixed) had the same number of flea beetles as undamaged plants in Control patches. Induced plant resistance in a tritrophic context has largely been viewed as interactions between single species of plants, their herbivores, and the natural enemies of these herbivores (Vet & Dicke, 1992). Only recently have studies considered more complex interactions (e.g. Dicke & Vet, 1999; Shiojiri et al., 2001; Vos et al., 2001; Shiojiri & Takabayashi, 2003). It has been shown here that heterogeneity in plant neighbourhood caused by phenotypic plasticity can influence the abundance of some plant consumers.

7 162 Cesar Rodriguez-Saona and Jennifer S. Thaler The data supports the notion that plants have only partial influence over their arthropod community because neighbouring plants influence the abundances of some arthropods on plants. The data also provides some support for the idea that an individual plant might influence the abundance of some organisms independently of neighbouring plants. The extent to which the biology of the herbivore, or predator, determines this pattern and whether plants can modify their defences when in different neighbourhoods remain open questions. Acknowledgements We thank Lisa Plane and Jennifer Chalmers for providing assistance in colony maintenance and for their help in conducting field experiments. We thank the staff of the Koffler Scientific Reserve, in particular John Jensen, for help maintaining field plots. Thanks to Anurag Agrawal, Richard Karban, Danush Viswanathan, Marc Johnson, Marc Lajeunesse, and three anonymous reviewers for helpful comments on the manuscript. We also wish to thank the Hybrid Vigour group for discussion of experimentaldesign and analysis. This research was supported by The Canadian Innovation Foundation, a Premier s Research Excellence Award and a Natural Science and Engineering Research Council(NSERC) Discovery grant to J.S.T. References Agrawal, A.A., Kobayashi, C. & Thaler, J.S. (1999) Influence of prey availability and induced host-plant resistance on omnivory by western flower thrips. Ecology, 80, Andow, D.A. (1991) Vegetationaldiversity and arthropod population response. Annual Review of Entomology, 36, Bernays, E.A. (1999) When host choice is a problem for a generalist herbivore: experiments with the whitefly, Bemisia tabaci. Ecological Entomology, 24, De Moraes, C.M., Lewis, W.J., Paré, P.W., Alborn, H.T. & Tumlinson, J.H. 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