Invertebrate biodiversity affects predator fitness and hence potential to control pests in crops

Biological Control 51 (2009) 499–506

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Invertebrate biodiversity affects predator fitness and hence potential to control pests in crops James D. Harwood a,*,1, Sarah W. Phillips a,b,2, Joanne Lello a, Keith D. Sunderland b, David M. Glen c,3, Michael W. Bruford a, Georgina L. Harper a, William O.C. Symondson a a b c

Cardiff School of Biosciences, Cardiff University, Biomedical Sciences Building, Museum Avenue, Cardiff CF10 3AX, UK Warwick HRI, Wellesbourne, Warwick CV35 9EF, UK IACR-Long Ashton Research Station, Department of Agricultural Sciences, University of Bristol, Long Ashton, Bristol BS41 9AF, UK

a r t i c l e

i n f o

Article history: Received 31 March 2009 Accepted 14 September 2009 Available online 17 September 2009 Keywords: Biodiversity Carabid beetles Diverse diet Generalist predators Linyphiid spiders

a b s t r a c t Natural enemies that control pests usually allow farmers to avoid, or reduce, the use of pesticides. However, modern farming practices, that maximize yields, are resulting in loss of biodiversity, particularly prey diversity. Does this matter? Pests continue to thrive, and without alternative prey the predators should, perforce, concentrate their attentions upon the pests. We showed that a diverse diet significantly enhances predator fecundity and survival. Experiments were conducted using common generalist predators found in arable fields in Europe, the carabid beetle Pterostichus melanarius (Coleoptera: Carabidae) and the linyphiid spider Erigone atra (Araneae: Linyphiidae). We tested the hypothesis that mixed species diets were optimal, compared with restricted diets, with respect to parameters such as predator weights, egg weights, numbers of eggs laid, egg development times, egg hatching rates and predator survival. In carabids, an exclusive earthworm diet was as good as mixed diets containing earthworms for egg production and hatching, but less good than such mixed diets for increase in beetle mass and sustained egg laying. For spiders, aphids alone (Sitobion avenae) or with the Collembola Folsomia candida, drastically reduced survival. Aphids plus the Collembola Isotoma anglicana improved survival but only aphids with a mixed Collembola diet maximized numbers of hatching eggs. Predators offered only pests (slugs or aphids) had lowest growth rates and fecundity. We therefore demonstrated that conservation of a diversity of prey species within farmland, allowing predators to exploit a diverse diet, is essential if predators are to continue to thrive in crops and regulate agricultural pests. Ó 2009 Elsevier Inc. All rights reserved.

1. Introduction For centuries the ability of generalist predators to control invertebrate crop pests has been exploited by farmers and has been clearly demonstrated many times (Symondson et al., 2002a). Such background control, and the ecosystem services it provides (Altieri, 1999; Luck et al., 2003), allows reduction, or even avoidance, of pesticides (DeBach and Rosen, 1991; Gurr et al., 2000). This control is further enhanced by management practices that promote pred* Corresponding author. Fax: +1 859 323 1120. E-mail address: [email protected] (J.D. Harwood). 1 Present address: Department of Entomology, University of Kentucky, S-225 Agricultural Science Center North, Lexington, KY 40546-0091, USA. 2 Present address: Royal Botanic Gardens – Kew, Richmond, Surrey TW9 3AB, UK. 3 Present address: Honorary Professor of Cardiff University and Independent Consultant at Styloma Research and Consulting, Phoebe, The Lippiatt, Cheddar BS27 3QP, UK. 1049-9644/$ - see front matter Ó 2009 Elsevier Inc. All rights reserved. doi:10.1016/j.biocontrol.2009.09.007

ator biodiversity; communities of natural enemies can co-exist through mechanisms of niche partitioning (Finke and Snyder, 2008; Snyder et al., 2008), allowing the community as a whole to reduce prey numbers to a greater extent than is possible by individual species acting alone (Sunderland et al., 1997; Symondson et al., 2002a). However, modern arable farming has increased productivity but at the expense of invertebrate diversity (Sotherton, 1998; Krebs et al., 1999; Tilman et al., 2002; Benton et al., 2003), in particular a loss of diversity amongst the prey species available to predators. Nevertheless, pests continue to thrive, and it might be argued that predators should do well on this glut of prey. However, predators may need to balance their amino acid requirements or avoid prey toxins by eating diverse prey (Greenstone, 1979) and/ or optimize their intake of proteins and lipids (Mayntz et al., 2005). Certain spiders, for example, require a diverse diet to maintain normal growth and reproduction (Wise, 1993) and single-species diets can reduce the fecundity of both spiders and carabid

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beetles. However, evidence for this is equivocal: diverse prey can have either beneficial or detrimental effects on predator fitness compared with single prey diets, depending on the nutritional value or toxin load of the dietary components (Toft and Wise, 1999; Oelbermann and Scheu, 2002). Loss of prey diversity arises from many causes. For example, eliminating competition from weeds also excludes the invertebrates that live on and under them (Moreby and Southway, 1999; Dewar et al., 2003). This situation may well be exacerbated by the introduction of genetically modified herbicide-tolerant crops, which may (depending on how they are used [Dewar et al., 2003]) result in a further potential loss of invertebrate diversity (Firbank et al., 2003). Many pesticides have adverse effects on populations of non-target invertebrates while long-term reliance on inorganic fertilizers can result in a loss of organic matter in the soil with its associated invertebrate faunas. A range of temporal and spatial factors are leading to a reduction in farmland heterogeneity with a concomitant loss of biodiversity, whether of birds, plants or invertebrates (Benton et al., 2003; Gibson et al., 2007; Macfadeyn et al., 2009). If loss of prey diversity in crops leads to reduced numbers of predators and consequently increased pest numbers and damage, this could seriously limit crop management options. Non-pest invertebrates form a major component of the diets of spiders (Riechert and Harp, 1987) and carabid beetles (Larochelle, 1990; Holland, 2002), the dominant predators found within crops in much of the temperate world. Such prey help to maintain generalist predator populations within crops when pest densities are low (Murdoch et al., 1985). Predators may respond to prey diversity, and hence optimize their diets, in two ways: by eating a more diverse diet or by being more selective in their prey choice. Given the fact that generalist predators often have empty guts in the field (Bilde and Toft, 1998; Krebs et al., 1999) and may normally find suboptimal quantities of food (Anderson, 1974; Bilde and Toft, 1998; Harwood et al., 2001, 2003), they are predicted to adopt non-selective predation strategies most of the time (Symondson et al., 2002a). Although there have been many previous studies of the effects of diet on predator fitness, we wished here to specifically test the effects of prey diversity on two of the dominant predators at our field sites, as part of a longer-term study of the spatial responses of predators to prey diversity in the field. We tested the hypothesis that diverse diets would confer advantages in terms of fitness over single prey (an agricultural pest) or restricted diets. We studied predators of two pests that cause major economic damage, slugs (Mollusca: Pulmonata) and aphids (Sternorrhyncha: Aphididae). The predators were ground beetles (Coleoptera: Carabidae), represented by Pterostichus melanarius (Illiger), a common species in arable crops in Europe and the USA (Thomas et al., 1997; Shah et al., 2003; Hajek et al., 2007), and sheet-web spiders (Araneae: Linyphiidae), represented by the equally widespread and numerous European species Erigone atra (Blackwall) (subfamily Erigoninae) (Downie et al., 2000; Schmidt and Tscharntke, 2005). The beetles feed on, and are capable of limiting numbers of, both slugs (Bohan et al., 2000; Symondson et al., 2002b) and aphids (Winder et al., 2001, 2005), while spiders can regulate aphids (Chiverton, 1986) and may be effective predators of these pests in the field (Harwood et al., 2004).

2. Materials and methods 2.1. Carabid collection and maintenance Carabid beetles, P. melanarius, were collected by dry pitfall trapping in agricultural fields at Long Ashton Research Station, Bristol, UK. They were maintained individually in plastic containers

(90 mm diameter, 45 mm depth) partly filled with hydroleca (expanded clay pebbles, diameter 10 mm) at 16 °C on a 16:8 light:dark cycle. All carabids were fed ad libitum on dog food (Complete Moist MenusTM, Town & Country Petfoods Ltd., Melton Mowbray, UK) for one month. Prior to the start of the experiment, beetles were transferred to clean containers containing hydroleca, starved for one week at the above environmental conditions and weighed. 2.2. Spider collection and maintenance Spiders, E. atra, were collected by aspirator from arable fields at Horticulture Research International, Wellesbourne, Warwickshire, UK. All spiders were kept in 5 cm diameter, triple-vented Petri dishes with a moist Plaster of Paris base to maintain humidity, and provided with an ad libitum diet of Drosophila melanogaster Meigen (Diptera: Drosophilidae) for three weeks at 16 °C (18L:6D). Spiders were then transferred into clean Petri dishes with a moist Plaster of Paris base and starved for two weeks at 16 °C (18L:6D) prior to the experiment. 2.3. Experimental design Following starvation, male–female pairs of P. melanarius were randomly assigned to one of eight treatments (n = 10 pairs per treatment, 80 pairs in total) and confined in containers with a hydroleca substrate and fine mesh base. All prey were freshly killed by freezing and each treatment provided with an ad libitum supply of food for eight weeks (Table 1). Slugs, Deroceras reticulatum (Müller) (Pulmonata: Agriolimacidae), and earthworms, Lumbricus terrestris (L.) (Haplotaxida: Lumbricidae), were collected from fields at Long Ashton Research Station, Bristol, UK. Aphids, Sitobion avenae (F.) (Sternorrhyncha: Aphididae), and housefly larvae, Musca domestica L. (Diptera: Muscidae), were from laboratory colonies. Although M. domestica are not commonly found in field they were an easily obtainable species representative of the many closely and distantly related Diptera larvae found in arable soils. On each feeding date, prey items not consumed by carabids were removed and replaced by fresh material. Daily gentle shaking of the hydroleca dislodged the eggs which fell through the mesh and were collected. Rates of egg production, egg weight and hatching success were all recorded daily. All eggs were transferred into individual wells of a 24-well CostarÒ microplates (Corning B.V. Life Sciences, Koolhovenlaan, The Netherlands) and maintained at 16 °C (16L:8D) until hatching. Male–female pairs of the spider, E. atra, were randomly assigned to one of four treatments (Table 2) (n = 20 pairs per treatment, 80 pairs in total). The ‘mixed’ Collembola were collected directly from the field and comprised mainly Isotomurus palustris (Müller) (Isotomidae), Isotoma anglicana Lubbock (Isotomidae) and Lepidocyrtus cyaneus Tullberg (Entomobryidae), plus smaller numbers of Entomobrya multifasciata (Tullberg) (Entomobryidae), Isotoma tigrina (Nicolet) (Isotomidae), Tomocerus longicornis (Mül-

Table 1 Prey species provided in each of the eight diets offered to pairs of Pterostichus melanarius. All prey was provided ad libitum. Treatment

Prey species

S E D A SE SEA SEAD AD

Slugs (Deroceras reticulatum) Earthworms (Lumbricus terrestris) Diptera (larvae of Musca domestica) Aphids (Sitobion avenae) Slugs and earthworms Slugs, earthworms and aphids Slugs, earthworms, aphids and Diptera Aphids and Diptera

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J.D. Harwood et al. / Biological Control 51 (2009) 499–506 Table 2 Prey species provided in each of the four diets offered to pairs of Erigone atra. All prey were provided ad libitum. Table

Prey species

A A + Fc A + Ia A + mixed

Aphids Aphids Aphids Aphids

(Sitobion avenae) (S. avenae) + Collembola (Folsomia candida) (S. avenae) + Collembola (Isotoma anglicana) (S. avenae) + mixed Collembola (see main text)

ler) (Tomoceridae), Orchesella villosa (Geoffroy) (Entomobryidae), Orchesella cincta (L.) (Entomobryidae) and Sminthurinus spp. (Sminthuridae). These collembolans are representative of the main species of potential prey of E. atra in winter wheat fields in the UK (Harwood et al., 2001, 2003). Aphids and the collembolan I. anglicana were from laboratory colonies initially established from field populations. Eggsacs were collected daily, placed in clean 5 cm diameter triple-vented Petri dishes containing a moist Plaster of Paris base and maintained at 16 °C (16L:8D). Number of eggs produced, hatching success, number of eggsacs produced and numbers of eggs per eggsac were all recorded. After hatching, eggsacs were dissected to determine the presence of unhatched eggs.

2.4. Statistical analyses All analyses were conducted in the R (v2.7.1) statistical package using either generalized linear models (GLM) or generalized linear mixed models (GLMM) as appropriate. GLMMs where conducted within R using the ASReml-R v2 (VSN International Ltd., Hemel Hempstead, United Kingdom) package. Model simplifications were undertaken by stepwise deletion with Log-likelihood values used to assess the random terms of the GLMMs. Validity of the models was confirmed via assessment of the normality of the standardized residuals. Table 3 shows final models along with the error distributions and link functions used in each analysis. Post-hoc withinmodel (GLM and GLMM) comparisons to compare coefficients

within each model were used to determine significant differences between treatments. 2.4.1. Beetle mass End point mass data from male and female beetles were analyzed by GLM with beetle end mass as the dependent variable and beetle diets, start mass, sex and the interaction between these three variables as independent terms. 2.4.2. Beetle fecundity The effect of the different beetle diets on four different aspects of beetle egg production were analyzed, i.e. total egg number, proportion of eggs hatching, individual egg mass and time to hatch. The effect of diet and mean egg mass (mg) per diet, on total egg number, was analyzed using a generalized linear model. The interaction between diet and egg mass was not examined as this term led to a poor residual distribution which could not be normalized by alternate link functions. The effect of diet on the proportion of eggs hatching was also analyzed by a GLM. As data for egg mass and time to hatch involved repeated measures from the same beetles, the data were analyzed by GLMM. The initial egg mass analysis produced a non-normal residual distribution and the egg mass transformed (see Table 3). The initial fixed terms of the model consisted of week, hatch time and diet and the interactions between these variables. The random model included the beetle identification code and splinic fits for week, and week in interaction with the other fixed model terms. Following simplification of this model (see results for details) week was shown to be an influence on egg mass. Therefore, for the hatch time model, egg mass was first divided by week and this new term was included in the fixed model along with diet and the interaction between the two terms. The random term in the hatch time model was beetle identity. 2.4.3. Spider fecundity Spiders were initially maintained on four different diets (Table 2), namely aphids alone, aphid plus Folsomia candida, aphid plus I. anglicana and aphid plus mixed Collembola. However, on the first

Table 3 Final models for beetle and spider mass and/or fecundity analyses. Where Chi-squared statistics are used (for models using a Poisson error distribution) the total sample size is shown (i.e. n = x). Model type

Final model

GLM error distribution: Gamma Link function: inverse

Dependent variable: Beetle end mass (g) Independent terms: Sex Diet Start mass (g) Sex: start mass (g)

GLM error distribution: Poisson Link function: identity

Dependent variable: Beetle Total Egg Production Independent terms: Diet Mean egg mass (mg) per diet

Statistic (F/v2)

16.45 12.49 41.21 4.05

df

p-Value

1,137 7,137 1,137 1,137

<0.001 <0.001 <0.001 0.046

(n = 69) 179.53 8.68

7 1

<0.001 0.003

GLMM error distribution: Gaussian Link function: identity

Dependent variable: Ln (Beetle egg mass (mg) + 1) Independent terms: week number Random terms: beetle identification code

4.89

1,2309

0.028

GLMM error distribution: Gaussian Link function: identity

Dependent variable: Ln (Beetle egg hatchtime (days)) Independent terms: diet Random terms: beetle identification code

3.28

7,2303

0.003

GLM error distribution: Gaussian Link function: identity

Dependent variable: Spider survivorship (days) Independent terms: diet

9.07

3,76

GLM error distribution: Poisson Link function: square-root

Dependent variable: Total spider egg hatching Independent terms: Diet Total egg number

GLM error distribution: Gaussian Link function: identity

Dependent variable: Proportion of spider eggs hatching Independent terms: diet

<0.001

(n = 34) 72.43 717.94 13.10

1 1

<0.001 <0.001

1,33

<0.001

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two of these diets the spiders showed very low survivorship (mean survivorship of 25.3 ± 5.0 days and 24.6 ± 1.7 days for aphid only and aphid plus F. candida diets, respectively) and eggsac production (mean number of eggsacs produced: 0.8 ± 0.2 eggsacs and 0.3 ± 0.1 eggsacs per female on aphid only and aphid plus F. candida diets, respectively). Therefore, for the egg data analysis, only the aphid plus I. anglicana and the aphid plus mixed Collembola diets were included in the statistical analysis. Four aspects of spider egg production were considered, the number of egg sacs produced, the total number of eggs produced, the total number of eggs actually hatched and the proportion hatching on either diet. All spider egg data analyses were conducted using GLM (see Table 3 for details).

The proportion of beetle eggs (n = 2477 total eggs produced by all treatments) hatching was not significantly influenced by diet (overall hatching success = 93.4%). Similarly, the egg mass (g) was not significantly influenced by diet or hatch time but was significantly associated with the week in which the eggs were laid (Table 3), such that the mass of the eggs were lower in later weeks. Beetle egg hatch time was also significantly associated with the diet upon which the beetles were fed (Table 3). Eggs from beetles fed on diets containing earthworms had shorter mean development times (14.05 days) than eggs from beetles fed on other diets (14.34 days). Additionally, egg production by female carabid beetles subjected to treatments of mixed diets containing earthworms continued producing eggs without decline over time, compared to all single-species diets where egg production was significantly reduced at the end of the experiment (Fig. 3).

3. Results

3.2. Effects of dietary diversity on spiders

The overall results of the analyses reveal that for both beetles and for spiders diet is an influential factor in both growth and/or fecundity. All final models are shown in Table 3.

3.2.1. Spider survivorship Spider survivorship showed a substantial and significant difference between the four diets (Table 3). Spiders fed on aphids alone (S. avenae) or on aphids together with F. candida, a collembolan known to be toxic to spiders (Toft and Wise, 1999; Oelbermann and Scheu, 2002; Fisker and Toft, 2004), have considerably lower survivorship than spiders fed on aphids with I. anglicana or spiders fed on aphids with a mixed collembolan diet (Fig. 4).

3.1. Effects of dietary diversity on carabid beetles 3.1.1. Beetle mass The final mass of both male and female beetles differed significantly between diets and the end mass of the beetles was also significantly influenced by the sex of the beetle in interaction with their start mass (Table 3). In both males and females there was a positive association between the start and end mass of the beetles but a disproportionate increase between males and females such that female P. melanarius increased in mass more substantially than males. Mixed species diets (slug and earthworm; slug, earthworm and aphid; slug, earthworm, aphid and Diptera) resulted in significantly heavier beetle end mass compared to single-species diets and the aphid plus Diptera diet (Fig. 1).

3.2.2. Spider fecundity Interestingly, the number of egg sacs produced was not significantly influenced by diet but the total spider egg production was significantly influenced by diet in interaction with the proportion of eggs hatching (v2 = 48.10, df = 1, P < 0.001). Surprisingly, although the raw data indicated the mean egg hatch rates of eggs from spiders on an aphid plus I. anglicana diet (44% hatching success) was lower than aphids plus mixed Collembola (71% hatching success), there was considerably lower egg production on the aphid plus mixed collembolan diet compared to the aphid plus single (I. anglicana) treatment (Fig. 5a). However, analysis of the proportion of eggs hatching (Fig. 5b) confirmed this difference in proportion hatching between treatments was significant (Table

3.1.2. Beetle fecundity The total number of eggs produced by the beetles was strongly and significantly influenced by diet (Table 3). All diets containing earthworms resulted in significantly higher egg production than diets without earthworms (Fig. 2).

0.29

a

b

b

b

A

AD

D

E

b

c

c

c

S

SE

SEA

SEAD

0.27

Beetle mass (g)

0.25

0.23

0.21

0.19

0.17

0.15

Diet Fig. 1. Predicted final mass (±SE) of male (open circles) and female (filled circles) beetles kept on different diets (females predicted at their mean start mass of 0.21 g and males at their mean start mass of 0.16 g). Diet codes: S, slugs; E, earthworms; D, Diptera and A, aphids. Different letters above points designate significant differences between treatments at P < 0.05.

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50

a

a

a

b

A

AD

D

E

a

b

b

b

S

SE

SEA

SEAD

Total egg production

45

40

35

30

25

20

Diet Fig. 2. Predicted total egg production (±SE) by beetles maintained on different diets with egg mass (mg) set at the mean. Diet codes are S, Slugs; E, earthworms; D, Diptera, and A, aphids. Post-hoc comparisons of contrasted levels from within GLM indicated that treatments A, AD, D and S were significantly lower (P < 0.001) than treatments E, SE, SEA and SEAD. Different letters above points designate significant differences between treatments at P < 0.05.

12

S

E

D

A

SE

SEA

SEAD

AD

8

Mean number of eggs laid per beetle per week

4

0 12

8

4

0 12

8

4

0 0

2

4

6

8 0

2

4

6

8

Week Fig. 3. Mean number (±SE) of eggs laid per female Pterostichus melanarius beetle per week on eight feeding regimes (n = 10 beetles per treatment). Diet codes: S, slugs; E, earthworms; D, Diptera and A, aphids.

3), giving a predicted mean proportion hatch of 0.56 on the aphids with I. anglicana diet and a mean of 0.79 on the aphids with mixed Collembola diet. Finally, the analysis of the number of eggs actually hatching reveals the overall consequence of this combination of high egg production with low hatch rate versus low egg production but high hatch rate (Fig. 5c). Overall more offspring are produced from spiders fed on the aphids with mixed Collembola diet (Table 3) compared to those on an aphid plus single collembolan diet.

4. Discussion These data provide unequivocal evidence on the profound effects of pest and non-pest prey, plus single versus mixed diets, on a range of fitness parameters relating to two of the most important groups of predators found in arable fields throughout the world. They also relate to the two most economically important groups of pests in arable farming in the UK, slugs and aphids (Glen,

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Fig. 4. Mean survival time (±SE) of female Erigone atra on different feeding regimes. Letter on the x-axis corresponds to one of the four diets which comprised combinations of Sa, aphids (Sitobion avenae) plus: Fc, Collembola (Folsomia candida), Ia, Collembola (Isotoma anglicana) and mixed, a mixture of Collembola species. Post-hoc comparisons of contrasted levels from within GLM indicated that Sa and Sa + Fc were significantly lower than Sa + Ia (P < 0.001) and Sa + mixed (P < 0.01) treatments. Different letters above points designate significant differences between treatments at P < 0.05.

1989). They demonstrate that diet has a profound effect upon predator weight, numbers of eggs laid, sustainability of egg laying, the period to egg hatching, egg hatching rates and predator survival. In every case the predators did poorly when fed on the pests only (slugs or aphids). The pests chosen were not species that have been found to be seriously toxic. Some other species of slugs (Symondson et al., 1997; Schroeder et al., 1999) and aphids (Oelbermann and Scheu, 2002) have been shown to be toxic or at least support very poor rates of growth and reproduction, although even these may be readily eaten when combined with other non-pest prey (Bilde and Toft, 2001). Only the mixed diets came out well for all parameters measured. It is energetically impracticable for a generalist predator to seek out only the highest quality prey species and indeed there is little evidence that they possess the physiological and behavioral mechanisms to do so. When prey is scarce, therefore, simply seeking a mixed diet is normally their optimal strategy and there is evidence that when predators are hungry they become less selective (e.g. Riechert and Harp, 1987; Ernsting and van der Werf, 1988). Where prey is abundant they may have the luxury of exercising greater prey choice. Modelling (Chang and Kareiva, 1999), field studies (Chiverton, 1986; Landis and van der Werf, 1997) and molecular techniques (Harwood et al., 2004, 2007) have all shown that generalist predators (e.g. of aphids) are at their most effective early in the year, when they can subsist on alternative prey and limit or delay the establishment of pests invading a crop. Luck et al. (2003) emphasize the importance of linking populations of species to the ecosystem services they provide. Previous work has already identified these carabids and spiders as potentially significant slug (Symondson et al., 1996, 2002b; Bohan et al., 2000) and/or aphid (Chiverton, 1986; Sunderland et al., 1987; Harwood et al., 2004; Winder et al., 2005) predators and control agents, both on their own and as part of a community of predators and parasitoids (Sunderland et al., 1997). We show that predator survival and fecundity are linked to a diverse diet. Earthworms were clearly a significant element in the diet of carabid beetles supporting evidence gathered in the field indicating that these prey constitute a major part of the diet of P. melanarius (Symondson et al., 2000). Interestingly, an exclusive diet of earthworms had no beneficial effect on beetle mass (Fig. 1), but did strongly affect egg production to levels only otherwise achieved by mixed

diets (Fig. 2) although this egg production was declined over time after reaching a peak after six weeks (Fig. 3). Those treatments containing earthworms also had a shorter hatch time. Although the proportion hatching and egg weight was unaffected by diet, shorter egg development time may have a significant effect on the population dynamics of these beetles given the vulnerability of carabid eggs to predation. However, though clearly significant the effect of earthworms on hatching times was approximately a third of a day, and given that records were taken daily (not more frequently) these results should be treated some with caution. Interestingly, egg production by carabid beetles was sustained for longer in mixed diets containing earthworms than any single-species diet (or a mixed diet of aphid plus Diptera) where declines in egg production were evident. Therefore in the context of predator recruitment and population enhancement, the provision of mixed (i.e. diverse) diets containing earthworms is likely to enhance growth and development of predator populations in agricultural systems, and thus the ecosystem services provided by the community. In spiders, although aphids and mixed Collembola did not convey nutritional benefits for all fecundity parameters measured, the overall recruitment to the population (total eggs hatching, Fig. 5c) point to biodiversity of Collembola as the primary factor promoting spider numbers and hence biocontrol potential. Prey biodiversity may lead to greater predator fitness and hence larger numbers of predators; this is a basic requirement for enhancing control by natural enemies. However, it is clearly necessary that, for example, predators and prey should be active at the same time of year and that the prey should be accessible to the predators. Even then the predators need to be at high density during the early growth phase of the prey population in order to have a significant beneficial effect (Chang and Kareiva, 1999). Linyphiid spiders are in the field during the early growth phase of the aphid population in the spring and we have shown previously that they will feed disproportionately on aphids (Harwood et al., 2004). A similar phenomenon has also been observed in other generalist predators: Orius insidiosus (Say) (Hemiptera: Anthocoridae) feeding at disproportionate rates on soybean aphids, Aphis glycines Matsumura (Sternorrhyncha: Aphididae) (Harwood et al., 2007). Both theory and practice show that such predation can limit growth in aphid numbers (Chiverton, 1986; Chang and Kareiva, 1999). Without alternative prey to foster good popula-

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The effects of prey diversity on predators demonstrated here provides a concrete mechanism by which loss of biodiversity in farmland ecosystems may be leading to a breakdown of ecosystem functions and the provision of ecosystem services, such as pest control (Altieri, 1999; Luck et al., 2003). In crops where there are plenty of pests to eat, but little in the way of alternative prey as a result of declining invertebrate diversity, these generalist predators are predicted to decline rapidly in number and are, therefore, likely to contribute little to pest control. Conservation of prey diversity is therefore at least as important as conservation of predator diversity if natural regulation of pests is to be exploited in sustainable agriculture. Acknowledgments This work was funded by the UK Biotechnology and Biological Sciences Research Council (grants held by WOCS/MWB/DMG and KDS/WOCS). K.D.S. is grateful for support from the UK Department for Environment, Food & Rural Affairs. J.D.H., S.W.P. and G.L.H. were postdoctoral associates on the grants. References

Fig. 5. Predicted egg production (±SE) at average percentage hatch per group (a), proportion of spider eggs hatching on each diet, on the original, backtransformed, p scale (i.e. ( prediction)) (b), and the actual number of eggs hatching (c). Diet codes: Sa, Sitobion avenae (aphids); Ia, Isotoma anglicana (Collembola) and mixed, mixed Collembola diet.

tions of these spider such control would be inhibited. Similarly, slug numbers build up in the autumn, coinciding with the sowing of winter wheat. This is the period when the crop is at its most susceptible to attack by these pests. This also coincides with peak populations of P. melanarius, the main predator of slugs in cereal crops in the UK (Symondson et al., 2006). Pterostichus melanarius has been shown to drive change in slug populations in the field (Symondson et al., 2002b). These are univoltine predators, breeding in later summer, however, fitness of adults, and its effect on the next adult generation, is not the only factor. The larvae too are predators of slugs, capable of affecting slug populations Thomas et al., 2009). Therefore, fitness of adults will affect egg and larval numbers, and hence potential over the short term to affect growth in slug numbers. There is also the interesting but unresolved question of whether predators aggregate to biodiversity; if biodiversity is so good for fitness then you might expect them to do so. Such an aggregative response might provide a direct mechanism whereby pests in patches of high diversity might come under greater predation pressure.

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