Predation by ground beetles and wolf spiders on herbivorous insects in a maize crop

Agriculture, Ecosystems and Environment 72 (1999) 189±199

Predation by ground beetles and wolf spiders on herbivorous insects in a maize crop Andreas Langa,1,*, Juliane Filsera, Johannes R. Henschelb a

GSF-Forschungszentrum fuÈr Umwelt und Gesundheit, Institut fuÈr BodenoÈkologie, Neuherberg, Postfach 1129, D-85758, Oberschleiûheim, Germany b Desert Ecological Research Unit, P.O. Box 953, Walvis Bay, Namibia Received 25 May 1998; accepted 28 October 1998

Abstract Ground beetles (Carabidae) and wolf spiders (Lycosidae) are among the dominant epigeal arthropod predators in arable land. Their predation effect on potential insect populations was examined in a maize ®eld. The abundance and effects of ground beetles and wolf spiders were manipulated by removal or addition within ®eld enclosures during two study periods, midseason and end-season. Both Carabidae and Lycosidae depressed populations of Cicadellidae and Thysanoptera, and a reduction of Aphididae was indicated in mid-season. The results indicated a size-dependent predation effect of Carabidae on Cicadellidae, the highest predation being on Cicadellidae with a body length above 1.1 mm. There was no strong evidence that the predation changed with the season. The present study con®rmed that ground beetles and wolf spiders may play an important role in controlling herbivore populations in agricultural ®elds, and revealed their potential to limit Cicadellidae and Thysanoptera in maize ®eld. # 1999 Published by Elsevier Science B.V. All rights reserved. Keywords: Carabidae; Lycosidae; Natural enemies; Generalist predators; Herbivores; Agroecosystem

1. Introduction Understanding the population dynamics of insects is of major interest in agroecosystems for controlling pest outbreaks. Predation by natural enemies, which control pest organisms has received much attention, especially under reduced management intensity, aimed at reducing pesticide applications. Generalist predators are thought to be important, because, unlike *Corresponding author. Tel.: +49-89-5902-616; fax: +49-895902-461; e-mail: [email protected] 1 Present address: Zoologisches Institut der UniversitaÈt, LudwigMaximilians-UniversitaÈt, Karlstr. 25, D-80333 MuÈnchen, Germany.

specialized enemies, they persist in the crop during periods of low pest density and can prevent early season build-up of pest numbers (Curry, 1993). The soil surface-dwelling ground beetles (Carabidae) and wolf spiders (Lycosidae) are common and abundant predators in agroecosystems (Ekschmitt et al., 1997). These generalist predators are considered to be capable of reducing population densities of insect populations (e.g. Riechert and Lockley, 1984; Luff, 1987). Evidence provided by gut content analyses, ®eld observations, and laboratory studies show that ground beetles and wolf spiders are true generalists feeding on many insect taxa (e.g. Sunderland, 1975; Hengeveld, 1980; Nyffeler et al., 1994), and

0167-8809/99/$ ± see front matter # 1999 Published by Elsevier Science B.V. All rights reserved. PII: S0167-8809(98)00186-8

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consuming considerable amounts of prey organisms (e.g. Sopp and Wratten, 1986; Mansour and Heimbach, 1993). Manipulative ®eld experiments are a powerful tool to demonstrate that predators control prey populations (Wise, 1993), and have been used to show that spiders and beetles can limit some prey populations in agroecosystems (e.g. Edwards et al., 1979; Oraze and Grigarick, 1989; Riechert and Bishop, 1990). However, these ®eld studies often dealt either with a whole predator community (e.g. all epigeal predators), or considered a single prey taxon. Manipulative ®eld experiments conducted in arable land have concentrated on aphids as a major pest (e.g. Edwards et al., 1979; Chiverton, 1986; Winder et al., 1994; Holland and Thomas, 1997), although the outcome of other predator±prey interactions can affect the conclusions (Abrams et al., 1996). Abundance and species composition of epigeal arthropod predators are known for most European crop types (cf. Thiele, 1977; Ekschmitt et al., 1997), yet many of the experimental studies addressing predation impact have been carried out in wheat ®elds (e.g. Edwards et al., 1979; Winder et al., 1994; Dennis and Wratten, 1991; Holland and Thomas, 1997). There is a need for more data on possible predator±prey associations in the food webs of different crops. The present study investigated the predation effects of ground beetles and wolf spiders in a maize ®eld. Ground beetles and wolf spiders were studied simultaneously, because they represent a functional unit, i.e. a trophic guild. Both are generalist predators of similar body size, occupy the same habitat and stratum, and search the ground for prey. Their numbers were manipulated within ®eld cages during two study periods, mid-season and end-season, and the subsequent effects were measured upon different insect populations in an attempt to answer the following questions: (1) do ground beetles and wolf spiders reduce prey numbers in a ®eld situation? (2) which prey populations are affected? (3) does the predation impact change with season? 2. Material and methods 2.1. Study area The present study was conducted within the FAM research network (Forschungsverbund AgraroÈkosys-

teme MuÈnchen). This project is a long-term (15 years) study aimed at the registration, prognosis and evaluation of environmental changes in agroecosystems caused by different management practices (Beese et al., 1991). The predator experiment took place during summer 1994 on the experimental farm of the project in Scheyern, Southern Bavaria, about 40 km North of Munich, Germany. The study site was a 3.83 ha maize ®eld (soil: ®ne-loamy, mixed mesic, pH 6.4, C content 1.51%) where herbicide (Starane) was applied 7 June 1994. The ®eld was harrowed and fertilized with liquid manure (30 m3 haÿ1) on 22 June 1994, and no herbicide, insecticide, or fertilizer was applied afterwards. 2.2. Predator density manipulation and assessment of arthropod densities Experiments were conducted within 0.5 m2 enclosures consisting of stainless steel rings (79 cm diameter), dug 10 cm deep into the soil and projecting 15 cm above the ground. Each enclosure was covered with a nylon net kept upright by four sticks and attached to the ring with adhesive tape and cord. The net mesh size of 0.3 mm effectively prevented arthropod predators and prey from leaving or entering. The overall height of the enclosures was about 100 cm, which gave most of the enclosed vegetation enough room to grow except for maize plants (3.96  0.13 tillers per enclosure, mean  SE) which were cut to ®t the cages. Mid-season lasted from 4 July to 11 August 1994, and end-season from 26 August to 3 October 1994 (Table 1). Twelve experimental predator enclosures were established during each study period in the ®eld. Four enclosures in total were omitted as outliers leaving 10 enclosures during each study period for analysis, the criterion for exclusion being that the total biomass of Carabidae and Lycosidae within an enclosure was more than one standard deviation below (predator enrichment) or above (predator reduction) the average of the concerned sampling distribution. During the ®rst week of each study period, as many predators as possible were removed from all enclosures (Table 2(A)), using two pitfall traps (7 cm diameter) and manual searching with as little disruption of the vegetation as possible. After removal, a speci®c number of ground beetles and wolf spiders was added

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Table 1 Experimental protocol and assessment dates

Mid-season 4 July±11 August 1994 No. of enclosures Predator removal Predator addition Sampling methods Pitfall trapping D-Vac Hand searching End-season 26 August±3 October 1994 No. of enclosures Predator removal Predator addition Sampling methods Pitfall trapping D-Vac Hand searching

Manipulated predator enclosures (MPEs)

Natural density assessments (NDAs)

P‡

Pÿ

N1

N2

5 4±10 July 11 July

5 4±10 July ±

6 ± ±

6 ± ±

3±10 August 4 August 11 August

3±10 August 4 August 11 August

4±10 July 12 July 10 July

3±10 August 4 August 11 August

5 26 August±2 September 4 September

5 26 August±2 September ±

6 ± ±

5 ± ±

26 September±3 October 24 September 3 October

26 September±3 October 24 September 3 October

29 August±8 September 8 September 8 September

20±29 September 30 September 29 September

P‡ ˆ predator-enriched enclosures, Pÿ ˆ predator-reduced enclosures, N1 ˆ natural density assessment at the start, N2 ˆ natural density assessment at the end.

to half of the enclosures (predator-enriched treatment), leaving the other enclosures with reduced predator densities (predator-reduced treatment). For the mid-season treatment, two Pterostichus melanarius, two Agonum muelleri, and two subadult/adult Pardosa agrestis or P. palustris, and for end-season, two P. melanarius, two Poecilus cupreus, and two juvenile/subadult P. agrestis/palustris were added (Table 2(B)). About 3 weeks later (Table 1) the population density of arthropod predators and prey was determined in the experimental enclosures. During sampling periods the abundance of the target organisms was recorded by pitfall trapping and D-Vac suction sampling. Two continuously open pitfall traps (7 cm diameter), connected by internal plastic fences, were established inside each enclosure at its wall. Placement of the traps at the wall and fences increase sampling ef®ciency, because the ground active animals are guided along these devices into the traps. The traps were ®lled with a mixture of ethylene±glycol and detergent as trapping ¯uid and had an opaque roof. For the D-Vac sampling intervals of 90 s, a suction apparatus with a 2.2 kW motor, and a

nozzle diameter of 15 cm was used. D-Vac sampling was conducted on the ®rst dry day of each assessment period. At the end of each assessment period, pitfall traps were removed and collecting of epigeal predators was carried out by hand for 15±20 min. The density of naturally occurring arthropod predators was assessed at the beginning and the end of each study period. Natural densities were estimated in enclosures adjacent to the enclosures where predator numbers were manipulated (Fig. 1). Each sampling period took 1 week commencing on 4 July, 3 August, 29 August and 20 September 1994 (Table 1). Six enclosure rings were placed on each of the four sampling occasions, giving a total of 23 samples (one sample was lost). Arthropod abundance was determined as described above. Carabid beetles were identi®ed to species after Freude et al. (1976), and adult stages of lycosid spiders after Roberts (1985) and Heimer and Nentwig (1991). Species names followed Freude et al. (1976) for Carabidae, and Platen et al. (1995) for Lycosidae. The other arthropod predators were combined into the following groups: Staphylinidae, predacious

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Table 2 Numbers of Carabidae and Lycosidae in the manipulated enclosures

(A) Numbers removed Carabidae Lycosidae (B) Numbers added Carabidae Agonum muelleri Poecilus cupreus Pterostichus melanarius Lycosidae Pardosa cf. agrestis/palustris (C) Numbers present Carabidae Agonum muelleri Bembidion quadrimaculatum Bembidion lampros Carabus granulatus Clivina fossor Poecilus cupreus Pterostichus melanarius Stomis pumicatus Stenolophus teutonus Trechus quadristriatus Lycosidae Pardosa palustris Pardosa agrestis Juveniles

Mid-season

End-season

2.10 0.40

2.30 1.20

2 2

2 2

2

2

1.4 0.4 0.2 0.4 0.6 0.6 2 0.2

0.6 0.4 2.2

0.2 0.6 1.4 3.8 0.2 0.2 0.6

Fig. 1. Design of the experimental plot (21  21 m) showing the arrangement of enclosure rings on the 1 m grid. 1 ± Predatorenriched treatment; 2 ± predator-reduced treatment; 3 ± natural assessment control at the beginning of a study period, 4 ± control at the end of a study period.

larvae, Linyphiidae and Chilopoda; Henschel et al. (1996) for all other spiders and harvestmen; and Rogers et al. (1976) for all other insect groups. 2.3. Study site arrangement

0.8 1.4

(A) Mean numbers removed from each cage (n ˆ 10) before the start of each study period; (B) numbers added per predatorenriched cage (n ˆ 5) at the start of each study period; (C) mean numbers present per predator-enriched cage (n ˆ 5) at the end of each study period.

Coleoptera larvae (Carabidae, Staphylinidae and Cantharidae), other spiders besides Lycosidae, and other predators (Chilopoda, Pseudoscorpiones, Opiliones and predacious insects such as Reduviidae, Nabidae, Chrysopidae and Coccinellidae). The following insect groups were potential prey: Aphididae, Cicadellidae, Diptera, Hymenoptera, Thysanoptera and `other insects' (other Coleoptera, other Heteroptera, Psocoptera, Saltatoria). The dry mass of the invertebrates was estimated from their body lengths using existing regression equations: Lang et al. (1997) for Carabidae, Lycosidae, Staphylinidae, beetle

Experimental and natural-density enclosures were located in a plot 21  21 m in the middle of the maize ®eld (distance to ®eld margin 100 m). The four different types of enclosures were placed 3 m apart on a grid (Fig. 1) to distribute any heterogeneity of the environment among enclosures (Hurlbert, 1984). Enclosures for the natural density assessments at the end of a study period (No. 4 in Fig. 1) were placed in a separate row to avoid in¯uencing other experimental activities. At the end of the ®rst study period (mid-season), enclosures were removed, and newly set for the second study period (end-season), the whole grid being shifted 2 m to the right of the ®rst study period. 2.4. Statistical analyses All statistical analyses were performed using the SPSS statistical package (Version 6.01), and average values presented are means with standard errors. In

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Table 3 Numbers of specimens recorded per arthropod group in the manipulated and the natural enclosures (P‡ ˆ predator-enriched enclosures, Pÿ ˆ predator-reduced enclosures, N1 ˆ natural density assessment at the start of the study period, N2 ˆ natural density assessment at the end of the study period). Means (and standard errors) per enclosure (0.5 m2) Arthropod group

P‡

Pÿ

Mid-season Carabidae Lycosidae Staphylinidae Beetle larvae Other spiders Other predators Aphididae Cicadellidae Diptera Hymenoptera Thysanoptera Other insects

5.80 3.20 4.00 4.80 19.60 43.60 3.20 1.20 66.00 24.60 2.00 6.20

(1.11) (1.53) (1.87) (2.20) (3.32) (4.11) (1.85) (0.73) (10.94) (7.05) (0.71) (3.81)

1.80 0.20 2.00 2.60 22.60 20.20 14.20 6.80 98.20 20.80 5.00 5.40

(0.73) (0.20) (0.71) (0.87) (5.35) (6.22) (8.26) (2.65) (25.30) (2.71) (2.05) (2.56)

2.33 1.33 4.50 0.83 17.67 0.50 0.33 2.50 15.33 5.50 1.00 6.67

(0.49) (0.33) (1.91) (0.40) (3.21) (0.22) (0.21) (1.15) (3.25) (1.06) (0.63) (1.94)

1.50 0.67 2.33 1.33 19.17 18.67 1.83 1.67 5.83 24.17 7.33 4.83

(0.81) (0.42) (0.33) (0.49) (6.81) (6.92) (0.70) (0.80) (1.56) (7.42) (1.02) (0.95)

End-season Carabidae Lycosidae Staphylinidae Beetle larvae Other spiders Other predators Aphididae Cicadellidae Diptera Hymenoptera Thysanoptera Other insects

7.00 2.20 1.00 1.00 18.80 1.60 96.00 2.80 9.80 4.00 1.00 4.20

(0.55) (0.80) (0.45) (0.32) (4.22) (1.17) (46.41) (0.66) (4.07) (0.84) (0.63) (0.97)

0.60 0.60 0.60 1.80 29.60 1.40 105.40 5.60 10.00 4.00 2.20 5.20

(0.40) (0.24) (0.24) (0.86) (6.36) (0.87) (56.54) (0.40) (2.70) (1.22) (0.58) (1.83)

3.17 0.67 1.67 1.33 26.50 5.83 9.50 2.17 8.17 13.50 2.00 3.33

(0.91) (0.42) (0.42) (0.56) (6.65) (1.49) (6.25) (0.87) (1.08) (0.06) (0.63) (0.76)

4.20 1.00 2.40 3.60 26.40 5.00 37.40 2.00 9.40 7.20 4.20 8.40

(1.24) (1.00) (0.51) (1.12) (6.07) (2.05) (32.71) (0.55) (5.65) (1.32) (2.03) (1.21)

general, all tests are two-tailed except when one-way questions were asked. One-tailed probabilities were applied to test if manipulative predator treatment worked as intended, and if enhanced predator densities reduced any arthropod group or size class of Cicadellidae. In order to test for predation effects, a twoway ANOVA was used, the factors being `treatment' (predator enrichment and reduction) and `study period' (mid-season and end-season), and in terms of biomass of arthropods (numbers of individuals are recorded in Table 3). As the data from the two study periods were not completely independent, `study period' was included in the analysis of variance as a subplot treatment, i.e. a nested ANOVA was applied. The homogeneity of variances was checked with Cochran's C, and normality with Kolmogorov±Smirp nov test. Variables were either ln(x ‡ 1) or …x ‡ 1† transformed to meet the assumptions of ANOVA.

N1

N2

3. Results 3.1. Predators Ten carabid species and two lycosid species were found in the predator-enriched enclosures at the end of the study periods (Table 2(C)). The carabid beetles Pterostichus melanarius, Poecilus cupreus, Agonum muelleri and the lycosid spiders Pardosa agrestis and P. palustris were most abundant re¯ecting arti®cially introduced predator species. Biomass of carabids and lycosids was signi®cantly higher in the predatorenriched replicates (102.45  8.74 mg in mid-season and 144.43  25.04 mg in end-season) compared with the predator-reduced ones (15.05  5.60 mg and 1.86  0.58 mg) (two-way ANOVA, effects of: (i) season, F3,16 ˆ 0.78; p > 0.05; (ii) treatment: F3,16 ˆ 215.45, p < 0.001; (iii) season  treatment,

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Fig. 2. Biomass (mg dry weight) of Carabidae and Lycosidae in maize at different times of the season. MPEs ± manipulated predator enclosures (predators reduced and enriched); NDAs ± natural density assessment enclosures at the start and the end of each study period. Means ‡ standard errors per enclosure (0.5 m2).

F3,16 ˆ 16.78, p < 0.01; Fig. 2). Of the total biomass of carabids and lycosids, Carabidae accounted on average for 93.9% and 82.4% (periods 1 and 2) in predator-enriched enclosures, and for 71.1% and 46.3% (periods 1 and 2) in predator-reduced enclosures. In the natural density assessments, the average contribution of Carabidae to the total amount of carabids plus lycosids was 83.3%, 76.9%, 66.2% and 64.0% for the successive sampling dates. Total carabid and lycosid biomass within the enrichment treatment was always signi®cantly higher than that of the natural density assessments (one-way ANOVA, p < 0.001, Fig. 2). In general, carabid and lycosid biomass in the reduction treatment was lower compared with the natural density assessment, but this difference was not signi®cant (one-way ANOVA, p > 0.05, Fig. 2). Other predator groups rarely showed a noticeable difference between predator-enriched and predatorreduced enclosures (Table 3). Although staphylinids were more abundant in the predator-enriched treatment during mid-season, this difference was not signi®cant (one-way ANOVA, p > 0.05). The only group showing a signi®cant contrast was the `other predators' in mid-season (Table 3), because of the higher numbers of Lamyctes fulvicornis (Chilopoda) in the predator-enriched manipulation (predator-enriched: 43.40  4.18 individuals, 25.46  3.66 mg; predatorreduced: 20.20  6.22 individuals, 10.95  3.20 mg; means  SE; one-way ANOVA, p < 0.05). 3.2. Predation effect on prey populations The combined predation of carabids and lycosids showed the strongest negative effect on Cicadellidae

(Fig. 3(B)). Biomass of this group was clearly reduced by the predators (two-way ANOVA, effects of: (i) season, F3,16 ˆ 0.52, p > 0.05; (ii) treatment, F3,16 ˆ 6.98, p < 0.01; (iii) season  treatment, F3,16 ˆ 2.79, p ˆ 0.09). The difference in Cicadellidae biomass between predator-enriched and predatorreduced enclosures appeared to be greater in midseason compared with end-season (Fig. 3(B)), however, the season  treatment interaction by ANOVA did not con®rm this (p ˆ 0.09). This difference seemed partly the result of a differential effect on the different size classes of leafhoppers (Fig. 4). Cicadellidae between 1.1 and 2.0 mm decreased only at end-season (two-way ANOVA, effects of: (i) season, F3,16 ˆ 8.71, p < 0.01; (ii) treatment, F3,16 ˆ 0.37, p > 0.05; (iii) season  treatment, F3,16 ˆ 6.34, p < 0.05), and Cicadellidae above 3 mm were more numerous in predator-reduced enclosures in mid-season (two-way ANOVA, effects of: (i) season, F3,16 ˆ 0.67, p > 0.05; (ii) treatment, F3,16 ˆ 0.67, p > 0.05; (iii) season  treatment, F3,16 ˆ 3.06, p ˆ 0.05). Although the reduction of Cicadellidae between 2.1 and 3.0 mm seemed to be stronger in mid-season (Fig. 4), the interaction of season and treatment was not signi®cant (two-way ANOVA, effects of: (i) season, F3,16 ˆ 1.23, p > 0.05; (ii) treatment, F3,16 ˆ 4.29, p ˆ 0.05; (iii) season  treatment, F3,16 ˆ 0.16, p > 0.05). In the predator-enriched enclosures (mid- and end-season pooled) average body size of Carabidae was negatively correlated with mean body size of Cicadellidae (Pearson's correlation coef®cient, r ˆ ÿ0.64, p < 0.05). Possibly, the larger carabid beetles reduced numbers of the larger leafhoppers indicating a size-dependent predation. Neither average body size of Lycosidae alone nor that of Lycosidae

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195

Fig. 3. Predation effect on different insect prey groups in maize, i.e. biomass (mg dry weight) in the predator-reduced (open bars) and predator-enriched (filled bars) treatment. Means ‡ standard errors per enclosure (0.5 m2). Note different range of the axes.

plus Carabidae showed a relationship to body size of Cicadellidae (Pearson's correlation, p > 0.05). Population density and biomass of Aphididae, mainly Rhopalosiphum padi, increased markedly from mid- to end-season (Fig. 3(A)), but, although average biomass values were generally lower in the predator-enriched enclosures, the predation impact was not signi®cant (two-way ANOVA, effects of: (i) season, F3,16 ˆ 7.84, p < 0.05; (ii) treatment, F3,16 ˆ 0.78, p > 0.05; (iii) season  treatment, F3,16 ˆ 0.13, p > 0.05). The seasonal effect was further explored by analysing the results of the study periods separately, and it was found that aphid biomass was decreased in the predator-enriched treatment during mid-season (p < 0.05) but not in end-season (p > 0.10, one-way ANOVA in both cases).

Population density of Thysanoptera decreased from mid- to end-season in the experimental enclosures (Fig. 3(E)), and their biomass was reduced by carabids and lycosids (two-way ANOVA, effects of: (i) season, F3,16 ˆ 1.91, p > 0.05; (ii) treatment, F3,16 ˆ 3.43, p < 0.05; (iii) season  treatment, F3,16 ˆ 0.14, p > 0.05). Although Diptera and `Other Insects' showed a reduced biomass in the predator-enriched enclosures, the effect was never signi®cant (Fig. 3). Hymenoptera also showed no signi®cant in¯uence of the predator manipulation, and were the only insect group whose average biomass was always higher in the predatorenriched treatment. Likewise, neither pooling all insect groups nor pooling a subset (Aphididae, Cicadellidae plus Thysanoptera) for analysis revealed any signi®cant predation effect (ANOVA, p > 0.10).

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Fig. 4. Predation effect on different size classes of Cicadellidae in manipulated predator enclosures (predators reduced and enriched). Size classes are 0±1.0 mm, 1.1±2.0 mm, 2.1±3.0 mm, and 3.1±4.0 mm. Values are mean numbers of Cicadellidae ‡ standard errors per enclosure (0.5 m2).

4. Discussion 4.1. Predator density manipulation The experimental manipulation was successful, and resulted in carabid and lycosid biomass being always signi®cantly higher in predator-enriched than in predator-reduced enclosures. The present study created a situation where densities of invertebrate epigeal predators increased rather than the effect of a naturally present enemy guild. Most of the effect was attributed to the arti®cially added Carabidae and Lycosidae, and some other carabids present in the ®eld also contributed to the overall effect. Other ground beetles may have moulted from pupae in the enclosure rings, may have burrowed their way into the enclosures despite the fact that these were dug 10 cm deep into soil, or may have escaped the pitfall traps (Mommertz et al., 1996; Lang, 1998). These factors randomly changed the composition of predator species among the replicate enclosures. Nevertheless, carabid and lycosid species present were characteristic of an agricultural site in mid-Europe (Luff, 1987), and biomasses were within the naturally occurring range for the ®eld under study recorded at other sampling occasions (Lang, 1998). Other generalist arthropod predators probably also contributed to predation, but their effect was overshadowed in the predator-enriched enclosures. Mid-

season number of centipedes (Chilopoda) was higher in predator-enriched enclosures than in predatorreduced ones and could have contributed to the predation effects during the ®rst study period. The higher number of centipedes possibly re¯ected a higher activity rather than a higher population density of the centipedes, especially because pitfall traps are known to record activity densities rather than actual densities (e.g. Mommertz et al., 1996; Lang, 1998). Such changes in behaviour are also known from wolf spiders which try to emigrate out of places where other generalist predators are abundant (e.g. Moran and Hurd, 1994). 4.2. Predation effect on prey populations Ground beetles and wolf spiders were important predators in the maize ®eld and were able to limit herbivore abundance. Cicadellidae and Thysanoptera were clearly reduced by the two predator groups, Aphididae also being affected. Most European carabid beetles and wolf spiders are predominantly epigeal, while the herbivorous Cicadellidae, Thysanoptera and Aphididae live on plants. Gut dissections and ®eld observations, however, have shown that Carabidae and Lycosidae prey upon all these insect taxa in the ®eld (Pollet and Desender, 1987, 1989; Nyffeler and Benz, 1988). Some carabids and lycosids climb up the plants (Grif®ths et al., 1985; Henschel and Lang, personal

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observation, 1994), whereas herbivorous insects fall to the ground when disturbed, when migrating or when digging into the soil for the ®nal moult (Thysanoptera) (Schliephake, 1979; Winder et al., 1994). Predation by ground beetles could not be separated from that of wolf spiders, both were manipulated simultaneously. Results from the maize ®eld coincided with those of ®eld experiments conducted in other crop types where Carabidae and Lycosidae reduced densities of herbivorous insect groups (e.g. Kiritani et al., 1972; Edwards et al., 1979; Chiverton, 1986; Oraze and Grigarick, 1989; Clark et al., 1994; Holland and Thomas, 1997). The effect of polyphagous arthropod enemies on Thysanoptera is poorly documented (e.g. Frescata and Mexia, 1996), but the present study indicated that Carabidae and Lycosidae may have a negative effect on that. There was no strong evidence that the predation effect of ground beetles and wolf spiders changed with time of the season, although it has been suggested that generalist epigeal predators had a stronger effect on populations of Aphididae developing early in the season (Edwards et al., 1979; Chiverton, 1986; Dennis and Wratten, 1991). There was only a signi®cant interaction term between season and predator treatment with respect to the `1.1±2.0 mm' and `3.1±4.0 mm' size classes of Cicadellidae, and one-way ANOVA indicated that Aphididae were reduced in mid-season but not in end-season. Considering the high number of Carabidae and Lycosidae in the predator-enriched enclosures, a stronger predation effect was expected. Polyphagous predators, however, catch prey based on their relative encounter rate (Dennis et al., 1991). The predation effect of generalist predators may therefore be spread over several prey groups resulting in only a small reduction of each of them. Almost every insect group in the present study was reduced to some extent even if the difference was not statistically signi®cant. A similar scenario would arise if it is assumed that sizedependent predation operates. Some generalist predators prey within a narrow size range irrespective of taxonomic classi®cation (Diehl, 1993) as larger carabids in the present study seemed to have preyed preferentially on larger Cicadellidae. Also, preferences for Cicadellidae may have mitigated the effect on other prey groups such as aphids (Bilde and Toft, 1994).

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It is acknowledged that the use of enclosed cages may have altered the abiotic environment experienced by the animals. Such changes may include radiation, air and ground temperature, wind speed or relative humidity. Chase (1996) demonstrated that by altering the abiotic environment (i.e. temperature and radiation) the predation effect of spiders on grasshoppers was moderated. Such changes in microclimate may either obstruct or favour the occurrence of a predation effect. For instance, a possible rise in temperature may increase the activity of animals, and in consequence increase the predator±prey encounter rates and predator consumption rates, thus increasing predation pressure. Con®nement of predators and prey in cages may also increase encounter rates or suppress hide and seek mosaic dynamics between predator and prey populations. This study has shown that carabids and lycosids have potential to in¯uence herbivorous insects in maize crop, but it still needs to be demonstrated that this is actually occurring in the natural unmanipulated ®eld situation. As generalist predators only take a limited share of different prey populations, predator densities must be high enough to show any effect on pest populations. Although lying within the natural range, manipulated densities of predators were higher than usually found at the study site (Lang, 1998). The support of populations of natural enemies (carabids, lycosids and other predators) is therefore of crucial importance in order to exploit fully their effect on crop pests, and various methods have been suggested to achieve this purpose (cf. review of Ekschmitt et al., 1997). Moreover, in the present study predator±prey relations were investigated only in 1 year. However, year to year variation in climatic conditions, or in species composition and population densities of predator and prey species can in¯uence the pattern of predator±prey relationships (e.g. Holland and Thomas, 1997). There is, therefore, still a clear need for more long-term studies in order to appreciate fully which predators and at what densities are able to substantially depress certain pest populations. Acknowledgements The authors thank Sebastian Diehl, Martin Nyffeler, and two anonymous referees for their helpful com-

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ments on earlier drafts of the manuscript, and Wilfried Gabriel as well as numerous people at the Institute of Soil Ecology for fruitful discussions, especially the members of the soil zoology group. The authors thank Marc Bielenberg, Michael BoÈckl, Sebastian Gigglinger, Ralf Hoffmann, Volker Kuhle, Birgit PoÈckl, and Heike Schmidt-Eisenlohr for laboratory and ®eld assistance. The scienti®c activities of the research network `Forschungsverbund AgraroÈkosysteme MuÈnchen' (FAM) are ®nancially supported by the Federal Ministry of Culture and Science, Research and Technology (BMBF 0339370). Rent and operating expenses of the experimental farm in Scheyern were paid by the Bavarian State Ministry for Education and Culture, Science and Art. References Abrams, P., Menge, B.A., Mittelbach, G.G., Spiller, D., Yodzis, P., 1996. The role of indirect effects in food webs. In: Polis, G.A., Winemiller, K.O. (Eds.), Food Webs. Integration of Patterns and Dynamics. Chapman and Hall, New York, pp. 371±395. Beese, F., Hantschel, R., Kainz, M., Pfadenhauer, J., 1991. Forschungsvebund AgraroÈkosysteme MuÈnchen (FAM) ± Erfassung, Prognose und Bewertung nutzungsbedingter VeraÈnderunÈ kol. gen in AgraroÈkosystemen und deren Umwelt. Verh. Ges. O 20, 77±80. Bilde, T., Toft, S., 1994. Prey preference and egg production of the carabid beetle Agonum dorsale. Entomol. Exp. Applic. 73, 151±156. Chase, J.M., 1996. Abiotic controls of trophic cascades in a simple grassland food chain. Oikos 77, 495±506. Chiverton, P.A., 1986. Predator density manipulation and its effect on populations of Rhopalosiphum padi (Hom.: Aphididae) in spring barley. Ann. Appl. Biol. 109, 49±60. Clark, M.S., Luna, J.M., Stone, N.D., Youngman, R.R., 1994. Generalist predator consumption of armyworm (Lepidoptera: Noctuidae) and effect of predator-removal on damage in no-till corn. Environ. Entomol. 23, 617±622. Curry, J.P., 1993. Grassland Invertebrates. Ecology, Influence on Soil Fertility and Effects on Plant Growth. Chapman and Hall, London, p. 424. Dennis, P., Wratten, S.D., 1991. Field manipulation of populations of individual staphylinid species in cereals and their impact on aphid populations. Ecol. Entomol. 16, 17±24. Dennis, P., Wratten, S.D., Sotherton, N.W., 1991. Mycophagy as a factor limiting predation of aphids (Hemiptera: Aphididae) by staphylinid beetles (Coleoptera: Staphylinidae) in cereals. Bull. Entomol. Res. 81, 25±31. Diehl, S., 1993. Relative consumer sizes and the strengths of direct and indirect interactions in omnivorous feeding relationships. Oikos 68, 151±157.

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