Diversity and invasion within a predator community: impacts on herbivore suppression

Authors


Correspondence author. E-mail: hoggbrian@yahoo.com

Summary

1. Management strategies to enhance ecosystem services in agroecosystems often seek to increase predator biodiversity. Invaders commonly dominate predator communities in agricultural landscapes, however, and the impacts of exotic predators on native predators and ecosystem services are largely unknown. Exotic predators may complement native predator diversity and enhance herbivore suppression, or they may disrupt herbivore suppression through predator interference.

2. We examined the impacts of a dominant exotic predator within the diverse predator community of a California vineyard. Interactions between the exotic wandering spider Cheiracanthium mildei, its closest native ecological homologue (the wandering spider Anyphaena pacifica) and a native spider displaying a different hunting mode (the cobweb-weaving spider Theridion melanurum) were tested in a manipulative field experiment, with the grape leafhopper Erythroneura elegantula acting as a shared herbivore prey source.

3. We found that the exotic wandering spider suppressed both grape leafhoppers and other unmanipulated leafhopper species that were present in cages. Native spiders had little or no impacts on leafhopper suppression. Thus, C. mildei appears to drive predatory impacts in this system, although evidence also indicated that it is limited by intraspecific interactions. The superior predatory ability displayed by this spider may be shared by other invasive predators that dominate agroecosystems.

4. Despite its effects on leafhoppers, C. mildei negatively impacted a range of spider species, including A. pacifica, T. melanurum, and other unmanipulated native spiders. These impacts are likely to have been mediated through intraguild predation. The wandering hunting mode of C. mildei may have facilitated its role as an intraguild predator.

5.Synthesis and applications. Our results highlight the sometimes conflicting aims of biological control and conservation. Here, a dominant invasive predator increased ecosystem services but also caused declines in numbers of native predators. As disturbed conditions in agroecosystems are likely to put invasive predators at an adaptive advantage, efforts to conserve biodiversity in agricultural landscapes should focus on shifting the outcomes of species interactions to favour native species.

Introduction

Biodiversity is threatened by both habitat destruction (Loreau et al. 2001) and the spread of invasive species (Mack et al. 2000). These processes may work in conjunction (Didham et al. 2007). In plant communities, for example, reduced biodiversity is often characteristic of invaded habitats (Shea & Chesson 2002), and may be caused, in part, by the displacement of native species by invaders (Levine et al. 2003). Predators are particularly vulnerable to extinction through changes in habitat structure (Duffy 2003). More information is needed to predict the implications of predator losses and invasions for ecosystem functions such as herbivore suppression (Byrnes & Stachowicz 2009).

In this study, we tested the effects of a dominant exotic predator on a taxonomically and functionally diverse assemblage of native predators, and assessed the resulting impacts on herbivores. In theory, predators have a cascading effect in food webs and increase primary production by lowering herbivore abundance (Hairston, Smith & Slobodkin 1960). If predators interfere with each other, however, an increase in predator diversity may dampen trophic cascades. Generalist arthropod predators can have significant impacts on herbivore populations (Symondson, Sunderland & Greenstone 2002), but by preying on each other they can decrease the total number of predators in the system and diminish impacts on herbivores (Finke & Denno 2004).

If predator interference is absent or minimal, on the other hand, an increase in predator diversity may have no impact or even an increased impact on herbivores. Predator identity can be important: the presence of effective predator species can drive impacts on herbivores, independent of diversity (e.g. Schmitz & Sokol-Hessner 2002; Chalcraft & Resetarits 2003; Straub & Snyder 2006). Alternatively, an increase in the functional diversity of predators may result in niche partitioning, whereby predator species exhibit different hunting modes, causing the predator complex as a whole to consume more prey than each species alone (Losey & Denno 1998; Ives, Cardinale & Snyder 2005).

Predator diversity and ecosystem functions could be influenced by the addition of invasive predators to native food webs. Invasive arthropod predators can negatively impact native predators through intraguild predation or competition (Snyder & Evans 2006). Their effects may extend to a range of native predators or to only specific functional groups; invaders may interact primarily with functionally similar native species (Prieur-Richard et al. 2000). Alternatively, invasive predators may complement predator diversity (Niemelä, Spence & Carcamo 1997; Burger et al. 2001) and may enhance ecosystem services (Snyder & Evans 2006).

The impacts of invasive predators may be especially pertinent to agricultural systems. Modified habitats such as agroecosystems are often dominated by invasive species (Shea & Chesson 2002) and many native species persist only at the edges of agricultural landscapes (Bianchi, Booij & Tscharntke 2006). While there is increasing awareness that conservation of natural habitat can enhance natural enemy diversity (Tscharntke et al. 2005), the impact of predator invasions on ecosystem services remains largely unexplored.

We examined predator interactions within a community of important and ubiquitous generalist arthropod predators, the spiders. Spiders are often the most abundant generalist arthropod predators (Wise 1993) and can suppress insect populations in agroecosystems (Riechert & Bishop 1990; Nyffeler & Sunderland 2003). The impact of a dominant exotic spider on native spiders and herbivore suppression was tested in a vineyard ecosystem. By including two native spider species that differed in their hunting modes and their functional similarity to the exotic spider, we assessed whether the addition of the exotic spider to the native predator community resulted in an increase in herbivore suppression through niche partitioning or predator identity, or a decrease in herbivore suppression through predator interference.

Materials and methods

Study system and focal taxa

The yellow sac spider Cheiracanthium mildei (Miturgidae) was the studied exotic predator; this nocturnal, wandering hunter is a Mediterranean native that was first reported in North America in the late 1940s (Bryant 1951). We used vineyards in Napa County, California, as a test ecosystem, where up to 95% of the arthropod predators are spiders (Costello & Daane 1999). The grape leafhopper Erythroneura elegantula Osborn (Cicadellidae) was the dominant herbivore and the primary spider prey. In previous surveys, increased dominance of C. mildei was accompanied by reduced native spider abundance and diversity (Hogg, Gillespie & Daane 2010; Hogg & Daane in press), and we suspected that C. mildei may have played a role in driving this pattern.

We used a field experiment to assess interactions between C. mildei and two native spiders: the nocturnal wandering spider Anyphaena pacifica Banks (Anyphaenidae), the most abundant native ecological homologue of C. mildei; and the cobweb weaver Theridion melanurum Hahn (Theridiidae), which is a potential leafhopper predator (Costello & Daane 2003) but is a sit-and-wait forager and functionally dissimilar to the two wandering spider species. While T. melanurum was first described in Europe, initial records in North America were also quite early (Banks 1897) and it is distributed throughout the Holarctic; therefore, we consider it a native species, although we acknowledge the possibility of an early introduction. To assess the predatory ability of C. mildei and A. pacifica under more controlled conditions, a greenhouse experiment was conducted.

Field experiment: predator identity, niche partitioning or predator interference

The field experiment took place in a Cabernet Sauvignon cv. vineyard, planted in 1998 in Napa County, California. No pesticides were applied, except sulphur dust to control fungus. Although C. mildei dominated the vineyard’s spider community, a second exotic species, Cheiracanthium inclusum Hentz, was present in low numbers. Cheiracanthium inclusum and C. mildei are similar in size and appearance, and are likely to be close ecological homologues. In addition to the grape leafhopper, the variegated leafhopper Erythroneura variabilis Beamer and a sharpnosed leafhopper, Scaphytopius sp., were present at low densities. The experiment took place from August to September 2007, when spider and prey abundances in Napa vineyards are highest (Hogg & Daane 2010).

Preliminary tests using marked spiders indicated that enclosures would be necessary to reduce spider emigration and immigration. Cages enclosed one grape vine (∼1·5 m wide × 1 m tall) and were made of nylon mesh (∼2·75 × 3 m, 1 mm gauge), which was draped over vines and sealed on all open sides with staples. Holes on either side of the enclosure, which could be opened and resealed with clips, allowed access to vines.

Nine treatments were established in a complete factorial design: (i) no spiders added, (ii) C. mildei alone, (iii) A. pacifica alone, (iv) T. melanurum alone, (v) C. mildei + A. pacifica, (vi) C. mildei + T. melanurum, (vii) A. pacifica + T. melanurum, (viii) C. mildei + A. pacificaT. melanurum (additive-series version) and (ix) C. mildei + A. pacifica + T. melanurum (replacement-series version). Five replicates were completed for all treatments except the A. pacifica + T. melanurum and the additive C. mildei + A. pacifica + T. melanurum treatments, where one cage from each of these treatments was excluded due to complications during the final collection of spiders and leafhoppers from cages. All multiple-species treatments except the replacement-series treatment followed an additive-series design, which elevates the total number of predators in the multiple-species treatments. This design is more appropriate for examining interspecific interactions among predators, as it holds intraspecific interactions constant across different levels of diversity (Schmitz 2007). Each of these replicates received nine individuals of all appropriate spiders, which is within the density range found in Napa vineyards for each species (B. Hogg & K. Daane, unpublished data). A replacement-series version of the three-species treatment was also included, a design that isolates the effects of intraspecific and interspecific predator interactions on lower trophic levels and is more appropriate for examining niche partitioning (Byrnes & Stachowicz 2009). This treatment received three individuals of each species, giving a total of nine spiders, equal to that in the single-species treatments. Unmanipulated caged and uncaged reference vines (five replicates of each) were included to assess cage effects and ensure that numbers of spiders and leafhoppers in treatment cages reflected field densities.

To control for possible edge effects, replicates were blocked by location along vineyard rows, in a complete randomized block design. Caged vines were at least five vines (∼10 m) apart along rows. All canes were pruned to a length of 3 m before applying netting to vines, and any foliage touching neighbouring vines was cut back. To provide a measure of vine size, the number of canes and average cane length per vine were measured and were not significantly different among treatments (anova, number of canes: F8,44 = 0·16, = 0·99; cane length: F8,44 = 0·59, = 0·78). Before tested spiders were added, resident spiders were cleared from vines between 13 and 20 July, by shaking and beating vine foliage for 60 s over a 1 m2 cloth funnel equipped at the bottom with a removable plastic bag, hereafter referred to as a ‘beat’ sample, as in Costello & Daane (1997).

Carapace width and body length of spiders were measured before experiments to the nearest 0·1 mm, and spiders were distributed equally among replicates and treatments according to size class (Supporting Information, Table S1). Spider sizes used in the experiment reflected ambient conditions (B. Hogg & K. Daane, unpublished data). To allow time for collection and measurement of spiders, additions of spiders to cages occurred in phases. On 3 August, six spiders per vine of all appropriate species were added for additive treatments and two spiders of each species were added for the replacement-series treatment. An additional three spiders per vine and one spider per vine (for additive and replacement treatments, respectively) were added on 10 August. Grape leafhoppers, collected on leaves from a nearby vineyard, were introduced before spiders were added at 200 nymphs per cage on 25 July, and 80 adults per cage on 27 July. Initial leafhopper numbers were visually sampled (10 leaves/cage) before introducing spiders. To ensure that spiders would not exhaust their food supply, leafhoppers were again added 13 and 28 days after the first spider addition at 100 nymphs per cage on 16 and 31 August. Total numbers of leafhoppers added to cages were far below the maximum leafhopper densities for this site.

The experiment ended immediately before harvest, when harvesting machinery would have destroyed the cages. All arthropods were collected at the end of the experiment using beats, which were performed from 5 to 6 September between 21 : 00 and 6 : 00 h, when lower night temperatures allowed better collection of the winged leafhopper adults. Specimens were stored in plastic bags at −4 °C until sorting. Treatment influences on final numbers of leafhoppers and non-focal spiders (C. inclusum + all other spider species) in additive treatments were analysed using 2 × 2 × 2 factorial mixed-model anova, with the addition of each of the three spider species and their interactions as fixed effects and block as a random effect. Variegated leafhoppers, sharpnosed leafhoppers and non-focal spiders were present in all treatments, and were therefore included in analyses. Numbers of all other taxa were too low to be analysed. Grape, variegated and sharpnosed leafhoppers were analysed separately. All dependent variables were (log10 + 1) transformed prior to analysis to meet assumptions of normality. The blocking factor was dropped when non-significant. Effects of spider species on each other in appropriate additive treatments (i.e. only additive treatments that initially received a particular species were included in analyses for that species) were assessed using 2 × 2 factorial anova with the addition of the other two spider species as factors. The number of grape and variegated leafhoppers remaining in the replacement-series version of the three-species treatment was compared with the best-performing single-species treatment and the mean of the single-species treatments using t-tests and the standard Bonferroni correction to compensate for Type I error. The former comparison tests for whether one predator species dominated effects on herbivores, while the latter tests for non-additive predatory effects; if the effects of predator species in combination diverges from the sum of their individual impacts, the number of herbivores remaining in the replacement-series treatment should differ from the average of the single-species treatments (Griffin et al. 2008). As cages were not entirely effective in excluding C. mildei from cages, and C. mildei was present in all treatments, the effects of C. mildei abundance on leafhoppers and focal spiders were also examined using regression analysis.

To assess effects of spider treatments on leaf damage caused by leafhoppers, five grape leaves per cage were randomly collected at the beginning and end of the experiment. Leaves were stored in plastic bags at −4 °C until they could be scanned and analysed using procedures modified from Skaloudova, Krivan & Zemek (2006). The proportion leaf damage was determined using NIH ImageJ (U.S. National Institutes of Health; http://rsb.info.nih.gov/nih-image/). Proportions were averaged across each cage and arcsine square-root transformed, prior to comparing leaf damage between treatments using a factorial anova.

To examine possible cage effects, (log10 + 1)-transformed numbers of spiders and leafhoppers and arcsine square-root transformed leaf damage proportions were compared between unmanipulated caged and uncaged reference vines using t-tests.

Greenhouse experiment: comparing predatory impacts of exotic and native spiders

In a greenhouse trial, we compared the impacts of the exotic C. mildei and the native A. pacifica on leafhoppers. Spiders were collected from vineyards and surrounding natural vegetation. Hunger levels were standardized ∼24 h before the experiment by providing two fruit flies Drosophila melanogaster Meigen to each spider. The test arenas were Chardonnay cv. grape vines (in 7·6 L pots) enclosed by ∼45 L nylon bags, with plant size (estimated by the number of leaves) and position on the greenhouse table set in a randomized block design before treatments were randomly assigned. Prior to the addition of spiders, each plant was infested with 100 leafhopper nymphs in two installments of 50 nymphs each, 5 days apart. To provide differently sized prey, first, second, third, and fourth instars were added in the ratio of 5 : 10 : 15 : 20 and 10 : 25 : 10 : 5 on the first and second inoculation, respectively. Smaller leafhoppers were deliberately overrepresented, and fifth instars were not used to minimize the number of leafhoppers developing into adults during the experiment.

Spiders were added to appropriate caged plants, 5 days after the second leafhopper installment, in three treatments: no spiders, two C. mildei added, two A. pacifica added. Spiders were allotted to treatments such that spiders within each cage and among all treatments in each block were of similar size (by weight). All spiders were immatures. After a 10-day period, all foliage was clipped (with bags still in place such that no arthropods escaped) and stored at −4 °C for 2 days to kill all arthropods. Afterwards, the numbers of leafhoppers and spiders were recorded. Twelve replicates of each treatment were initially included; if a spider was missing, that replicate was excluded from analysis, resulting in 12, 10 and 11 replicates of control, C. mildei alone and A. pacifica alone treatments, respectively. Effect of treatment on numbers of leafhoppers remaining at the end of the experiment was assessed using anova and a Tukey HSD test for multiple comparisons.

Results

Field experiment: predator identity, niche partitioning or predator interference

Of the C. mildei initially added to cages, 53·3% were recovered during the final collection in C. mildei-only cages. Both C. mildei and C. inclusum were present in cages where they were not introduced (Fig. 1a, b). Cheiracanthium mildei-addition treatments contained more C. mildei spiders than non-addition treatments (Mann–Whitney test, U = 13·65, < 0·001; Fig. 1a). Numbers of C. mildei were not affected by the addition of other spider species to additive treatments that received C. mildei (anova, A. pacifica: F1,16 = 0·05, = 0·82; T. melanurum: F1,16 = 0·15, = 0·71).

Figure 1.

 Numbers of (a) Cheiracanthium mildei, (b) Anyphaena pacifica, and (c) Theridion melanurum remaining at the end of the field experiment. Treatments were: C. mildei only (C); A. pacifica only (A); T. melanurum (T); C. mildei + A. pacifica (C + A); C. mildei + T. melanurum (C + T); A. pacifica + T. melanurum (A + T); C. mildei + A. pacifica + T. melanurum, additive version [C + A + T (add)]; C. mildei + A. pacifica + T. melanurum, replacement version [C + A + T (rep)]. Data are means + SE.

Only 26·6% of the A. pacifica initially added to the cages were recovered in the final collection in the A. pacifica-only treatment. Anyphaena pacifica numbers were higher, however, in A. pacifica-addition treatments than non-addition treatments (Mann–Whitney test, U = 19·70, < 0·001; Fig. 1c). The addition of other spiders to additive treatments that received A. pacifica did not impact A. pacifica (anova, C. mildei: F1,17 = 1·01, = 0·33; T. melanurum: F1,17 = 0·00, = 0·96), although regression analysis uncovered a negative relationship between A. pacifica and C. mildei numbers per cage (Fig. 2a).

Figure 2.

 Relationship between numbers of Cheiracanthium mildei per cage and (a) the spider Anyphaena pacifica, (b) the spider Theridion melanurum (c) the grape leafhopper Erythroneura elangantula and (d) the variegated leafhopper Erythroneura variabilis in the field experiment. All variables except A. pacifica are log10-transformed.

Numbers of T. melanurum recovered at the end of the experiment amounted to 53·3% of those initially added to the T. melanurum-only treatment. More T. melanurum were in T. melanurum-addition treatments (Mann–Whitney test, U = 31·96, < 0·001; Fig. 1d). The addition of C. mildei negatively impacted T. melanurum (anova, F1,16 = 7·00, = 0·02) while A. pacifica had no effect (F1,16 = 0·00, = 0·96). A significant negative relationship emerged between numbers of T. melanurum per cage and C. mildei across additive treatments that received T. melanurum (Fig. 2b).

Before treatments were imposed, leafhoppers abundance was not different between additive treatments (anova, F7,32 = 1·67, = 0·15), although there was a marginally significant effect when the replacement-series treatment was included in analysis (F8,36 = 2·00, = 0·08). Final densities of adult grape leafhoppers tended to be lower in treatments that received C. mildei (Fig. 3a). Grape leafhopper numbers were significantly affected by the blocking factor and the addition of both C. mildei and A. pacifica to treatments, while T. melanurum and spider interactions had no detectable effects (Table 1). Adult variegated leafhoppers were also different across treatments (Fig. 3b), and were impacted by the addition of C. mildei (Table 1). No other factors affected variegated leafhopper numbers. Numbers of both leafhopper species were also significantly affected by C. mildei in regression analysis. Quadratic functions provided the best fit (Fig. 2c, d), although their biological relevance may be limited, as the quadratic term failed to improve model fit when the few cages that contained no C. mildei (= 5) were removed from the analysis. Final numbers of leafhoppers in the replacement-series treatment did not differ from the average of the single-species treatments (grape leafhopper: = 0·58, = 0·58; variegated leafhopper: = 0·30, = 0·77) or the best-performing single-species treatment, the C. mildei-only treatment (grape leafhopper: = 1·38, = 0·21; variegated leafhopper: = 1·38, = 0·20). The replacement-series treatment and the C. mildei-only treatment did not differ in total spider numbers (= 0·59, = 0·21) or C. mildei numbers (= 2·22, = 0·06).

Figure 3.

 Effect of treatment on (a) grape leafhopper and (b) variegated leafhopper in the field experiment. Treatments were: Cheiracanthium mildei only (C); Anyphaena pacifica only (A); Theridion melanurum (T); C. mildei + A. pacifica (C + A); C. mildei + T. melanurum (C + T); A. pacifica + T. melanurum (A + T); C. mildei + A. pacifica + T. melanurum, additive version [C + A + T (add)]; C. mildei + A. pacifica + T. melanurum, replacement version [C + A + T (rep)]. Data are means + SE.

Table 1.   Results of factorial analysis of variance testing the effects of spider additions on grape leafhoppers, variegated leafhoppers, sharpnosed leafhoppers, non-focal spider species and percentage leaf damage
Dependent variableSource of variationd.f.FP
Grape leafhoppersCheiracanthium mildei1, 3671·51<0·001
Anyphaena pacifica1, 364·540·04
Theridion melanurum1, 360·340·56
C. mildei × A. pacifica1, 360·280·60
C. mildei × T. melanurum1, 360·000·95
A. pacifica × T. melanurum1, 362·830·10
C. mildei × A. pacifica × T. melanurum1, 360·180·67
Block4, 3310·89<0·001
Variegated leafhoppersC. mildei1, 3631·52<0·001
A. pacifica1, 362·910·10
T. melanurum1, 360·040·84
C. mildei × A. pacifica1, 360·100·75
C. mildei × T. melanurum1, 360·270·61
A. pacifica × T. melanurum1, 363·470·07
C. mildei × A. pacifica × T. melanurum1, 361·510·23
Block4, 339·57<0·001
Sharpnosed leafhoppersC. mildei1, 363·980·06
A. pacifica1, 363·720·06
T. melanurum1, 360·970·33
C. mildei × A. pacifica1, 365·800·02
C. mildei × T. melanurum1, 363·520·07
A. pacifica × T. melanurum1, 360·760·39
C. mildei × A. pacifica × T. melanurum1, 360·020·89
Non-focal spidersC. mildei1, 3614·44<0·001
A. pacifica1, 362·210·15
T. melanurum1, 361·190·28
C. mildei × A. pacifica1, 361·410·24
C. mildei × T. melanurum1, 360·030·88
A. pacifica × T. melanurum1, 360·020·88
C. mildei × A. pacifica × T. melanurum1, 363·420·07
Leaf damage (%)C. mildei1, 382·840·10
A. pacifica1, 381·910·18
T. melanurum1, 380·320·57
C. mildei × A. pacifica1, 380·560·46
C. mildei × T. melanurum1, 380·170·69
A. pacifica × T. melanurum1, 380·830·37
C. mildei × A. pacifica × T. melanurum1, 380·050·83

A total of 131 non-focal spiders were collected in beat samples, an average of 3·1 spiders per cage (Supporting Information, Table S2). These consisted primarily of Theridion dilutum Levi (Theridiidae, 24·4%), Oxyopes salticus Hentz (Oxyopidae, 31·3%) and C. inclusum (21·4%). The addition of C. mildei strongly affected numbers of non-focal spiders, while no other factors had any impact (Table 1). Besides grape and variegated leafhoppers, a total of 271 insects were collected in final beat samples. The majority (70·0%) were sharpnosed leafhoppers, Scaphytopius sp. The addition of C. mildei and A. pacifica had marginally significant effects, while the interaction between these spiders significantly affected sharpnosed leafhoppers (Table 1).

Effects on leafhoppers were not reflected in proportions of leaf damage (Table 1), which did not differ between treatments (Table S2), and there was no correlation between leafhopper densities and leaf damage (R2 = 0·009, = 0·54).

Cages had no effect on spiders, leafhoppers or leaf damage. Unmanipulated caged and uncaged vines did not differ in spider numbers (= 0·50, = 0·63), grape leafhoppers (= 1·14, = 0·29), variegated leafhoppers (= 0·16, = 0·88), or leaf damage (= 0·18, = 0·86). Total leafhopper numbers on unmanipulated vines (range: 122–833) were similar to those recovered from vines in the control treatment, indicating that leafhopper densities in cages reflected field conditions. The additive three-species treatment elevated total spider numbers beyond ambient levels, although spider numbers added to all other treatments were within the range of spider densities on unmanipulated vines (4–18).

Greenhouse experiment: comparing predatory impacts of exotic and native spiders

Cheiracanthium mildei strongly impacted leafhoppers while the effects of A. pacifica were weaker but still significant (Fig. 4). Proportions of adult leafhoppers remaining were similar across treatments, representing 92·0%, 93·0% and 92·2% of the surviving leafhoppers in the control, C. mildei and A. pacifica treatments, respectively. Numbers of surviving grape leafhoppers were affected by treatment (anova, F = 20·86, P < 0·001), with the highest and lowest numbers in the control and the C. mildei treatments, respectively (Tukey’s HSD, < 0·05).

Figure 4.

 Effect of treatment on numbers of grape leafhoppers surviving in the greenhouse experiment. Treatments were: no spiders (control), Cheiracanthium mildei (C), Anyphaena pacifica (A). Data are means + SE. Different letters above means denote significant differences (Tukey’s HSD, < 0·05).

Discussion

Our results implicated C. mildei as a dominant exotic predator that negatively impacted a range of native spider species. Costello & Daane (2003) similarly reported negative relationships between C. inclusum and several native spider species, including T. melanurum and the related T. dilutum. Intraguild predation was the most likely outcome after the addition of C. mildei to the vineyard food web in the current study. Spiders commonly prey upon each other (Wise 2006). Anyphaena pacifica and T. melanurum were small compared to C. mildei, and smaller predators are more likely to be the victims of intraguild predation (Polis & Holt 1992). Cheiracanthium mildei readily preys upon A. pacifica in the laboratory (B. Hogg & K. Daane, unpublished data). Competition is less likely, as spiders can survive long periods of starvation (Wise 1993), and final leafhopper numbers were still quite high. The larger body size of C. mildei is likely to be linked to its role as an invader. Superior consumption abilities often allow invasive arthropod predators to reach higher biomass levels than their native counterparts, particularly in managed ecosystems (Snyder & Evans 2006). Nonetheless, the large body size of C. mildei relative to native species may have influenced its impacts in this system. Interactions between spiders may be primarily influenced by relative body size (Eichenberger, Siegenthaler & Schmidt-Entling 2009; Bednarski, Ginsberg & Jakob 2010). The wandering hunting mode of C. mildei may also have facilitated its role as an intraguild predator by putting it in contact with a broad range of potential intraguild prey. Intraguild predation is more likely to occur between predators if they overlap in their hunting domains (Schmitz 2007). Assessments of C. mildei’s impacts on native spiders may, in fact, have been overly conservative due to the occurrence of C. mildei in cages where it was not introduced. Initial beats do not appear to have been entirely effective in removing all spiders from vines.

Despite its likely role as an intraguild predator, C. mildei emerged as a superior predator of leafhoppers in greenhouse and field experiments, although A. pacifica also had detectable effects. Eubanks (2001) similarly reported that invasive fire ants suppressed biological control agents and pests. Superior resource consumption ability may be common among many invasive predators (Shea & Chesson 2002; Snyder & Evans 2006). Evans (2004), for example, uncovered differences in predatory ability between native and invasive ladybirds.

The native T. melanurum had no effects on leafhoppers. Although Costello & Daane (2003) reported that numbers of Theridion spp. were correlated with leafhopper numbers in vineyards, they arrived too late in the season to be effective in leafhopper control. The minimal predatory impact of this species compared to the wandering spiders may have been due to differences in body size and mobility. Smaller predators may become satiated for longer periods after eating small numbers of prey (Rosenheim & Corbett 2003). As a sit-and-wait predator, T. melanurum can survive longer periods of starvation in the laboratory than either C. mildei or A. pacifica (B. Hogg, personal observation).

We uncovered no effects of spider diversity on herbivores. Overall, predator identity was far more important than species diversity in suppressing herbivores in this system, which is in accordance with other studies (Schmitz & Sokol-Hessner 2002; Chalcraft & Resetarits 2003; Straub & Snyder 2006). Niche partitioning would not have been possible, and predator interference would not have played a role, as the intraguild prey must be the more efficient consumer for herbivore suppression to be disrupted (e.g. Rosenheim, Wilhoit & Armer 1993; Schmidt-Entling & Siegenthaler 2009). The replacement-series treatment did not differ from the C. mildei-only treatment, however, which can be explained by the similar C. mildei densities in these treatments, probably the result of cannibalism, a common occurrence among spiders (Wise 2006). Other studies have reported that strong intraspecific interactions can limit predator impacts (Wilby et al. 2005; Griffin et al. 2008). Here, the only interspecific predator interaction that impacted herbivores was between C. mildei and A. pacifica on sharpnosed leafhoppers. This result is puzzling, as intraguild predation appears to have occurred between these species and both are wandering hunters. However, interactions between predators occupying broad, overlapping microhabitats are expected to enhance herbivore suppression when the herbivore occupies a narrow microhabitat (Schmitz 2007) and sharpnosed leafhoppers may be limited to specific microhabitats within the grape vine.

Theory dictates that the intraguild predator must be the inferior consumer if it is to coexist with its intraguild prey (Polis & Holt 1992). Models based on assumptions of long-term equilibrium may not apply to this system, however. In non-equilibrium settings such as agroecosystems, predators may act as both intraguild predators and superior predators of herbivores (Rosenheim & Harmon 2006). It is also possible that our field experiment was too short in time to observe ecological interactions over the long-term. Time lags between the responses of different trophic levels may buffer trophic cascades over short periods (Polis 1994), which may explain why treatments had no effect on leaf damage. Damage levels on leaves were also high at the start of the experiment, and may have obscured any treatment effects. The use of cages did not influence plant damage results, since there were no differences in leafhopper numbers or leaf damage between caged and uncaged reference vines.

Cheiracanthium mildei appears to be a ‘driver’ of ecological change in the vineyard, supporting the idea that invaders are better suited than native species to exploiting resources in modified ecosystems (e.g. Shea & Chesson 2002). Superior adaptations to exploiting available resources may allow many invasive predators to increase ecosystem services in agricultural landscapes. However, the reduced spider abundance and diversity that often accompanies C. mildei dominance in vineyards (Hogg, Gillespie & Daane 2010) is likely to be at least partly the result of C. mildeis impacts. Similarly, MacDougall & Turkington (2005) reported that dominant invasive grasses suppressed native plants while increasing ecosystem function.

Our results highlight the sometimes conflicting aims of conservation and biological control. To increase pest control, promotion of one or a few highly effective predators could be achieved through targeted management practices (Landis, Wratten & Gurr 2000). We are unable to recommend this approach for C. mildei, however, since this species often dominates vineyard monocultures where habitat and spider species diversity is low (Hogg & Daane in press). Furthermore, any benefits that exotic predators confer in controlling pests must be weighed against their ecological impacts. Promoting the abundance of effective native predators seems a more preferable alternative. Although we uncovered only weak effects of native spiders on leafhoppers, we suspect that their impacts could be strengthened through effective habitat management. To promote native predator numbers, habitat diversity can be enhanced through the provision of non-crop habitats within agricultural fields (Landis, Wratten & Gurr 2000) or across the agricultural landscape (Tscharntke et al. 2005). Increased habitat diversity may also mitigate the spread of invasive species by shifting species interactions in favour of native species (Didham et al. 2007). Cheiracanthium mildei, for example, is less successful in vineyards near natural vegetation where A. pacifica is most abundant (B. Hogg & K. Daane, unpublished data). Most of the research on invasive arthropod predators has occurred in managed ecosystems (Snyder & Evans 2006), however, and more information is needed on the impacts of invasive predators in natural ecosystems and across different spatial scales.

Acknowledgements

This work was supported with grants from the National Science Foundation Dissertation Improvement Grant DEB 0710434, the van den Bosch Memorial Scholarship, and the California Table Grape Commission and American Vineyard Foundation. We thank vineyard managers for use of their farms, Tom Ingersoll for statistics advice, and Tian Hu, Clay Miller and Marian Sandoval for help in the field.

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