Microcosm studies on control of aphids by generalist arthropod predators: Effects of alternative prey

BioControl 49: 483–504, 2004.© 2004 Kluwer Academic Publishers. Printed in the Netherlands.

Microcosm studies on control of aphids by generalistarthropod predators: Effects of alternative prey

Michael MADSEN, Steen TERKILDSEN and Søren TOFT∗Department of Zoology, University of Aarhus, Building 135, DK-8000 Århus C, Denmark∗Author for correspondence; e-mail: [email protected]

Received 7 October 2002; accepted in revised form 16 December 2003

Abstract. Generalist predators are potential control agents of aphids in cereal fields. Becauseaphids are low-quality prey for most generalist predators, the availability of alternativehigh-quality prey may influence the interactions between aphids and their predators byreducing the predation rate due to lowered preference for aphids. We analysed this by testingthe ability of six generalist predators (the spiders Erigone atra (Bl.), Clubiona lutescens(Westr.)/reclusa O.P.-C., Pachygnatha degeeri Sundevall, Pardosa prativaga (L.Koch), thecarabid beetle Bembidion lampros (Herbst), and the harvestman Oligolophus tridens (C.L.Koch)) to suppress Rhopalosiphum padi (Linné) populations in the presence or absence ofalternative prey types (fruit flies Drosophila melanogaster (Meigen) or the collembolan Tomo-cerus bidentatus (Folsom)). Experiments of 10 days duration were carried out in a microcosmset-up. Without alternative prey all predators except B. lampros were able to reduce aphidpopulation development significantly relative to predator-free controls. The harvest spiderO. tridens was the most efficient predator (>90% reduction). Presence of alternative prey(fruit flies) had a significant negative effect on aphid limitation by P. prativaga and a weakpositive effect in B. lampros, but did not influence the ability to reduce aphids in E. atra,Clubiona, P. degeeri and O. tridens. In addition, 24-hours’ consumption experiments withadult P. degeeri and subadult C. lutescens/reclusa, using R. padi and D. melanogaster as preytypes, showed markedly lower consumption rates of aphid than of fruit fly prey. The micro-cosm arrangement is a simple way to partly simulate the habitat complexity of an agriculturalfield under laboratory conditions and proved to be a useful tool for investigating complexpredator-prey interactions.

Key words: aphid consumption, Araneae, Carabidae, microcosm, Opiliones, pest control,polyphagous arthropod predator, prey tolerance

Introduction

Generalist arthropod predators may have a significant impact on insect pestsin agricultural crops, including aphids in cereal fields (review in Symondsonet al., 2002). This is in spite of findings demonstrating that aphids are low-quality food for a wide range of generalist insectivores (spiders: Toft, 1995;Bilde and Toft, 2001; carabid beetles: Bilde and Toft, 1994, 1999; Jørgensen

484 MICHAEL MADSEN ET AL.

and Toft, 1997a, b; partridge chicks: Borg and Toft, 2000), revealed bylow survival, low growth rate and low fecundity on a pure aphid diet. Toft(1995) and Bilde and Toft (1994) showed that lycosid spiders and carabidbeetles consumed cereal aphids, Rhopalosiphum padi (Linnaeus), at a ratefar below their overall energy demand and independently of hunger. Suchfindings indicate that many generalist predators are unable to tolerate largeamounts of aphid prey. Other species may consume larger amounts of aphids,but their reproductive benefit from aphid consumption is anyway low (Bildeand Toft, 1999). Studies of dietary mixing have revealed a positive effectof combining aphids with high-quality prey (Wallin et al., 1992; Bilde andToft, 1994, 2000; Borg and Toft, 2000), even at a low aphid consumptionrate. If aphids contribute positively to predator nutrition, the predators shouldbe ready to incorporate small amounts of aphids in their diet (Waldbauerand Friedman, 1991). This may explain why aphids have a high incidencein predator stomach contents (Sunderland, 1975; Chiverton, 1987; Sunder-land et al., 1987) and thus why generalist arthropod predators may playan important role in the population dynamics of cereal aphids (Edwardset al., 1979; Chiverton, 1986; DeBarro, 1992; Holland and Thomas, 1997;Symondson et al., 2002) in spite of the low food value of the aphids asthe main food. Chiverton (1986) showed that exclusion of predators frombarriered plots during the aphid establishment phase resulted in a two to six-fold increase in aphid (R. padi) numbers compared with those in unenclosedcontrol areas. The same experiment found a negative correlation betweenpeak numbers of R. padi and numbers of generalist predators. These relation-ships indicate a significant effect on aphid density by an abundant generalistpredator fauna. Theoretically, predation prior to the exponential growth phaseof the aphid population, when predator-prey ratios are high, should have thegreatest impact, which has been confirmed by field experiments (Edwards etal., 1979; Chiverton, 1987). However, the knowledge of individual predatorspecies in agricultural ecosystems is still limited and exact estimates offeeding capacity and predator induced prey mortality are very restricted.

Because of their low food value aphids contribute little to the reproductionof generalist predators, which are therefore dependent on alternative preysources for maintaining or increasing their populations. However, alternativehigh-quality prey should be better preferred than aphids by the predators,which may therefore be detracted from aphids by a high availability of alter-native prey. Because of this potentially dual effect of alternative prey on aphidpredation by generalist predators, the combined effect of alternative prey inthe field is not easily predicted.

Our goal in the present study was to quantify the impact on R. padipopulations by several different arthropod predator species (Araneae, Cara-

MICROCOSM STUDIES ON CONTROL OF APHIDS 485

bidae, Opiliones) under controlled conditions. In particular we wanted toinvestigate if alternative high-quality prey interferes with the predation effecton the aphid. Furthermore we were interested in seeing if predator huntingstrategy may affect aphid suppression. In order to investigate these relation-ships, predators with different hunting strategies and hunting habitats werechosen for the experiments. The predators’ ability to suppress the develop-ment of R. padi populations on wheat seedlings was evaluated in a microcosmarrangement. The microcosm design is a possible way to partly simulate thecomplex habitat structure of a cereal field and at the same time keep exper-imental parameters constant. This combination is often difficult to obtain inpetri dish or field experiments. The effect of generalist predators on R. padipopulations was tested both without and with alternative high-quality preyavailable.

Tolerance to consumption of aphids (i.e., consumption capacity relative tofood demand) was known from previous studies with respect to three of thespecies (Toft, 1995; Bilde and Toft, 1997), but unknown for the other threespecies used in the microcosms. In order to examine any correlation betweenaphid consumption and hunger level and to establish an estimate of dailyfood demand, measurements of prey specific consumption capacity wereperformed with two additional spider species. The results of the toleranceexperiment can be interpreted to indicate a difference in predator preferencefor the presented prey types.

Materials and methods

The generalist predators

Predator species from two classes and three orders of arthropods wereselected to increase generality of the study. Furthermore, the individualpredator species used were chosen in relation to their different huntingstrategies. All predators were collected in cereal fields or pastures on variousdates between autumn 2000 and autumn 2001 at Stjær, Denmark.

Erigone atra (Blackwall) is a 2 mm ground-living sheet-web spider(family Linyphiidae) and one of the most abundant spider species on all soiltypes in Danish fields (Toft, 1989). Cereal aphid feeding has repeatedly beenreported in E. atra (Sunderland et al., 1986, 1987; Alderweireldt, 1994b). Itseems to have two generations per year with breeding periods in early springand summer (De Keer and Maelfait, 1988). Only adult females were used.

The Clubiona species (size: 4–8 mm; family Clubionidae) are nocturnalfoliage hunters found on low vegetation, bushes and trees. We were not ableto determine the species before the experiments because the spiders were


subadults. Following the experiments five individuals were reared to maturityand identified. Four of these belonged to C. lutescens Westring and oneto C. reclusa O.P.-Cambridge. Only females were used in the microcosmexperiment, and both sexes in the comsumption measurements.

Pachygnatha degeeri Sundevall (family Tetragnathidae) is widespread inNorthern Europe. It has a mature size of 3–3.75 mm in females and 2.5–3 mmin males. Adults make no webs but seem to climb high up in the vegetationat night. In the daytime they are found at ground level (Roberts, 1996). Itreproduces in spring with one generation per year (Alderweireldt and DeKeer, 1990). Adult females were used for the microcosm experiments, andadults of both sexes were included in the consumption measurements.

Pardosa prativaga (L. Koch) is a common ground-living wolf spider(family Lycosidae) of open habitats in Northern Europe, including agricul-tural fields and meadows. It matures in spring, reproduces throughout thesummer and reaches a size of 4–6 mm. Wolf spiders are considered diurnalsit-and-wait predators (Ford, 1978). Large female juveniles were used in themicrocosm experiments.

Bembidion lampros (Herbst) is a 3–4.5 mm spring-breeding ground beetle(family Carabidae) and an abundant predator in European agricultural fields(Ekbom and Wiktelius, 1985). High rates of aphid consumption have beenreported in this diurnal ground-hunting beetle (Chiverton, 1988). Unsexedimagines were used in the microcosm experiments.

Oligolophus tridens (C.L. Koch) (family Phalangiidae) is a commonharvest spider distributed throughout the ground and field layer of grass- andwoodland habitats (Todd, 1949). It hatches in May/June and becomes matureduring the summer (Phillipson, 1959) with a size of 5–6.5 mm in the maturefemale. The general assumption is that harvestmen are both opportunisticscavengers and predators (Todd, 1949; Halaj and Cady, 2000). Phillipson(1960) indicated that phalangids are not active hunters, but remain stationarywith their legs, responsive to tactile stimulation, radiating from the body.Phalangids are considered to be mainly active at night though not strictlynocturnal (Phillipson, 1960). Only adult females were used.

When not in experiments, predators were kept isolated and refrigerated(5 ◦C) in individual plastic containers (height 7 cm, � 2 cm). The containerswere supplied with a bottom layer of moist plaster mixed with charcoal toassure a high humidity and closed with a foam rubber plug.

Aphid and alternative prey

For all experiments R. padi was obtained from a laboratory culture, rearedon wheat seedlings of mixed cultivars. Aphids are one of the most abundant


cereal pests in Europe. In years of outbreak R. padi is the major cereal aphidpest in the Scandinavian countries (Ekbom and Wiktelius, 1985).

Vestigial winged fruit flies Drosophila melanogaster (Meigen) (vg) rearedon Drosophila medium (formula 4–24� Instant Drosophila medium, Caro-lina Biological Supply Company, P.O. Box 6010, Burlington, NC 2716-6010,USA), was used as alternative prey in most of the microcosm experiments.D. melanogaster is considered a relatively high quality food for generalistpredators (Bilde and Toft, 1994; Toft, 1995; Marcussen et al., 1999). Thevg mutant was chosen in order to increase capture efficiency of the arachnidpredators while freeze-killed flies were used for the carabid beetle. The fruitflies were also chosen to be representative of other potential prey types forthe predators.

Additionally a culture of the collembolan Tomocerus bidendatus (Folsom)was raised on baker’s yeast. T. bidentatus has proved to be of extremely highfood value and sustained high rates of survival, growth and development inthe wolf spider Schizocosa, even when given as a monotypic diet (Toft andWise, 1999).

Microcosm study

We used a microcosm set-up roughly similar to the arrangement described byDinter (1998a). The microcosm consisted of a plastic flowerpot (� 14 cm,height 15 cm) with a transparent Perspex cylinder (� 13 cm, height 30 cm)on top. To confine the animals a piece of tulle covered the top of the Perspexcylinder, secured by a rubber band. Each pot was half filled with Leca�

stones, half with peat soil (sphagnum) on top. The soil was heated in anoven (100–105 ◦C) for 6 hours before use in order to eliminate moulds.Water was supplied by placing the microcosms in water filled trays (60 cm ×60 cm). Wheat seedlings (mixed cultivars) were grown in small aluminiumtrays, filled with Vermiculite� growth medium. Three days from sowing,the seedlings were picked one by one from the trays and transplanted to theflowerpots. Guidelines from The Danish Institute of Agricultural Sciencesrecommend an average of 400 wheat seedlings per m2 in cereal fields. Thisdensity is equivalent to 5 seedlings per microcosm which was the numberused. The seedlings were allowed four days of settling in the microcosm.This procedure resulted in one-week-old seedlings. Prior to experiment startall predators were standardized by being fed ad libitum for four days withD. melanogaster, followed by three days of starvation. The pre-experimentalstandardization as well as all subsequent experiments were carried out at22 ◦C and a 16 h light: 8 h dark photoperiod. Each experimental seriesconsisted of four treatments: two controls, (I) with aphids only, (II) withaphids plus alternative prey; and two experiments: (III) with predator and


aphids, (IV) with predator and aphids plus alternative prey. All treatmentsin all experimental series consisted of 10 replicate microcosms. We added10 aphids (mixed fourth instar juveniles and adults) per microcosm on thesoil at the centre of the microcosm. Aphids were allowed approximately twohours to settle on the plants. This period was enough for the aphids to settleon a plant (own observations). Next the predators and alternative prey wereadded to the microcosms. In all cases one predator individual was added permicrocosm.

The experiments were run for 10 days at various times from November2000 to March 2001 and September 2001 to December 2001. Watering andaddition of alternative prey were done as needed, always ensuring that themicrocosms experienced a minimum of disturbance. At all times there wereat least five living fruit flies or Collembola in the relevant microcosms. At theend of each experiment the wheat plants with aphids were cut at soil level andfrozen until the aphids were later counted in order to estimate the final aphidpopulation size. Live aphids away from the plants were counted at the end ofthe experiment.

Two identical microcosm series were performed for each of the predatorsE. atra and O. tridens. In both cases D. melanogaster was used as alterna-tive prey. In addition, with P. prativaga two separate experiments with fruitflies (D. melanogaster) and Collembola (T. bidentatus) as alternative preywere carried out to establish whether different alternative prey might differ-ently affect predation on aphids. Clubiona, P. prativaga and B. lampros wereweighed before and after experiments in order to elucidate any differences inpredator condition between the treatments.

Consumption rates in the 24 h study

The consumption of R. padi relative to food demand in C. lutescens/reclusaand P. degeeri was determined in 24-hour experiments. Prior to the measure-ments, feeding on fruit flies ad libitum for one week standardized the indi-viduals. Consumption rates of R. padi and D. melanogaster were measuredin satiated (SAT), one-week-starved (1WS) and two-weeks-starved (2WS)animals. Both male and female spiders were evaluated to determine anydifferences in consumption between the sexes. Individuals of P. degeeri (16females and 11 males) were offered 5 fruit flies for SAT and 1WS and 7 fruitflies for 2WS. The corresponding number of aphids was 10 for SAT and 1WSand 15 for 2WS. Each individual of Clubiona (12 females and 11 males) wasoffered 5 fruit flies in the SAT treatment, 7 fruit flies for 1WS and 14 fruit fliesfor 2WS. Aphid numbers for the same experiment were 10 for SAT, 15 for1WS and 20 for 2WS. Different amounts of prey were used because of differ-ences in size between species as well as different hunger levels. Amounts of


prey offered were always well above what was consumed. Each predator wasweighed before and after the experiment enabling determination of specificfood consumption (mg consumed prey d.w./mg spider).

The predators were kept in plastic containers (described above) and exper-iments were run at the same temperature and photoperiod as the microcosmexperiments. Experiments were carried out between November 2001 andJanuary 2002. Every sample of prey was weighed before being offered. Inorder to determine fresh weight/dry weight coefficients, weighed samplesof both prey types were dried in the vacuum oven at 80 ◦C for at least twodays and reweighed. At the end of the 24-h feeding experiment uneaten preywas dried and weighed as above. The 24-h dry weight consumption was thencalculated by subtracting the dry weight of uneaten prey from the calculateddry weight of food offered.

Statistical analyses

Two-way ANOVA (JMP 4.0 by SAS Institute) on aphid numbers was used toanalyse the effects of the predators, alternative prey, and their interactions inthe microcosm study. Aphid data for P. degeeri, O. tridens and P. prativaga(with T. bidentatus as alternative prey) were Box-Cox transformed in orderto meet the assumption of equal variances. For P. prativaga with fruit fliesas alternative prey, no transformation was able to homogenize the variances.Using the four groups of the experimental design as levels of a nominal factorin a one-way ANOVA, followed by paiwise Tukey-Kramer tests were there-fore used to statistically confirm the results of the initial two-way ANOVA.For species (E. atra and O. tridens) where experimental series were repli-cated, 3-way ANOVA with a replication term was applied. However, for thelatter species variance homogeneity could not be obtained for the experi-mental series combined; therefore they were analysed separately. Comparisonof differences in mean body mass gain between predators was carried outusing a t-test. For the 24-h consumption measurements three-way ANOVA onBox Cox transformed data (to obtain homogeneity of variance) were initiallyused to test the effects of hunger level, prey type, sex and their interactions.Hunger level was entered as an ordinal variable. No significant differenceswere obtained between the sexes, and sex was deleted as a factor in theanalyses reported.


Figure 1. Aphid populations after 10 days in microcosms with or without predators (a,b: E.atra (adult females), c: C. lutescens (sub-adult females), d: P. degeeri (adult females), e,f:P. prativaga (large juvenile females), g: B. lampros (adult males/females), h,i: O. tridens(adult females)) in the presence or absence of alternative prey (Drosophila melanogaster(a,b,c,d,e,g,h,i) or Tomocerus bidentatus (f)). Initially ten aphids were added to each micro-cosm. Note that a,b and h,i are replicate pairs of identical experiments performed at differenttimes, whereas e,f are experiments with the same predator but different alternative prey.


Figure 1. Continued.

Results

Rhopalosiphum padi

There were considerable differences between experimental series in the aphidpopulations of the control treatments (Figure 1). This is due to the fact thatthe nine experimental series were run at different times, and therefore allseries had their separate control treatments. However, within each series theaphid populations of the two control treatments (without predators) wereremarkably similar. In the absence of predators the average number of aphidsin control microcosms increased from 13.3-fold up to 44.6-fold. Alternativeprey had no influence on aphid population development rate in the predator-free controls (ANOVA analyses). Only a few alate specimens of aphids wereobserved indicating a well-proportioned ratio of aphids to plant numbers.


Table 1. Results of the statistical analyses of the microcosm experiments (data presentedin Figure 1). Drosophila melanogaster was the alternative prey, except where indicated

Species/Source F df P

Erigone atra

Whole model 5.340 4, 72 0.0008Replication 0.739 1 0.3928Predator 20.474 1 <0.0001Alternative prey 0.014 1 0.9050Predator∗Alt.prey 0.001 1 0.9768

Clubiona sp.

Whole model 4.929 3, 36 0.0057Predator 14.599 1 0.0005Alternative prey 0.172 1 0.8604Predator∗Alt.prey 0.016 1 0.8896

Pachygnatha degeeri

Whole model # 26.288 3, 36 <0.0001Predator 76.307 1 <0.0001Alternative prey 1.115 1 0.2980Predator∗Alt.prey 1.442 1 0.2376

Pardosa prativaga

Whole model $ 22.834 3, 36 <0.0001Predator 30.779 1 <0.0001Alternative prey 15.045 1 0.0004Predator∗Alt.prey 22.677 1 <0.0001

Pardosa prativaga (alt. prey T. bidentatus)


Bembidion lampros

Whole model 3.969 3,36 0.0153Predator 2.381 1 0.1316Alternative prey 5.750 1 0.0218Predator∗Alt.prey 3.776 1 0.0599

Oligolophus tridens 1


Oligolophus tridens 2


# Analysed on Box Cox transformed data.$ Variance homogeneity could not be obtained for this analysis. One-way ANOVA usingthe four groups as levels of a nominal factor, followed by pairwise Tukey-Kramer tests,confirmed that one groups (+predator, no alternative prey) was significantly different fromthe other three groups.


Predator effects on aphids

With no alternative prey, all predator species except B. lampros had asignificant impact on aphid populations (Figure 1, Table 1). The harvestmanO. tridens had the strongest effect, reducing aphid numbers by 93% and97%, respectively, in the two replicate series. In order of decreasing effi-ciency aphids were reduced 80% by P. prativaga, 66% by P. degeeri, 37% byClubiona, and 27% and 28% (two replicate experiments) by E. atra. Thesevalues should be interpreted cautiously, however, because of the differencesin aphid multiplication rate in the control microcosms (Figure 1).

Influence of alternative prey on predator effects on aphids

Alternative prey (fruit flies) did not reduce the effect of predators on aphidpopulations as regards E. atra (Figure 1a, b), Clubiona (Figure 1c), P. degeeri(Figure 1d), O. tridens (Figure 1h, i), nor P. prativaga when the collembolanT. bidentata was the alternative prey (Figure 1f). However, with Drosophilaas alternative prey no effect of P. prativaga on the aphid population wasobserved (Figure 1e). An opposite effect was seen in B. lampros. Here thepresence of alternative prey (dead fruit flies) created a marginally significantreduction of aphids (Figure 1g, Table 1).

The mean weight gain for Clubiona in the alternative prey treatment was6.39 ± 2.10 mg compared to 1.41 ± 1.24 mg spiders in the no-alternative-prey treatment (t-test; df = 16, p < 0.0001). Similarly, mean body mass gainof P. prativaga in the fruit fly treatment was significantly higher (2.45 ±1.60 mg vs. 0.44 ± 1.03 mg) than in the corresponding no-alternative-preytreatment (t-test; df = 17, p = 0.0042).

24 h consumption studies

Clubiona sp.Specific consumption of R. padi in this species revealed no differencesbetween sexes over the three treatments (F1 = 0.075, p = 0.78). However,absolute consumption rates were higher in females than in males becauseof their larger body weight. The results in Figure 2a show that hunger level(F2 = 18.3, p < 0.0001) and prey type (F1 = 99.5, p < 0.0001) both hada strong influence on consumption. However, whereas consumption of fruitflies increased markedly with starvation level, consumption of aphids did not.This is evident from Figure 2a though no such interaction can be establishedstatistically (prey type∗hunger level; F2 = 2.23, p = 0.112). Making theseanalyses separately for each sex gave a significant interaction for the females(F2 = 3.41, p = 0.039) but not for the males (F2 = 0.72, p = 0.49).


Figure 2. Spider consumption of prey (mg d.w./mg) related to hunger level and prey type(Aphid: Rhopalosiphum padi. Fruit fly: Drosophila melanogaster). a: Clubiona lutescens. b:Pachygnatha degeeri.SAT: Satiated spider. 1WS: One week starved spider. 2WS: two weeks starved spider.

Pachygnatha degeeriNo difference between specific food consumption in the two sexes was found(F1 = 0.05, p = 0.82). There were significant effects of prey type (F1 = 162.2,p < 0.0001) and hunger level (F2 = 59.0, p < 0.0001) (Figure 2b). In contrastto fruit fly consumption that of aphids seemed independent of starvation level(Figure 2b), suggesting a limited tolerance to aphids by the predator. This


was confirmed by a significant prey type∗hunger level interaction (F2 = 5.04,p = 0.0076). Making these analyses separately for each sex gave a significantinteraction for the females (F2 = 5.77, p = 0.0045) but not for the males (F2 =0.25, p = 0.78).

Discussion

Microcosm experiment

The microcosm experimental design proved to be an appropriate tool toinvestigate predator-prey relationships. Despite the limitations of a labora-tory experiment we were able to simulate a habitat structure which in manyways is representative of cereal fields. One spider per microcosm equalsapproximately 75 m−2. Seasonal maxima of spider densities in Europeanfields range from 78 m−2 up to c. 600 m−2 (Dinter, 1995; Sunderland andTopping, 1995; Toft et al., 1995; Samu et al., 1996). Thus, the density usedin the microcosms may well reflect average field densities. Ground beetlesare estimated at levels of 33 m−2 (Hance, 1992). However, mean densities ofB. lampros of 61 (±10) m−2 were reported by Scheller (1984) from Denmark.Densities of harvestmen were estimated by Bachmann and Schaefer (1983)to reach 16.5 m−2 in grassland ecosystems. Thus, the microcosm densitiesof B. lampros were just above reported field densities, whereas densities ofO. tridens were somewhat higher.

The present study demonstrated that several generalist predators (exceptBembidion lampros) without alternative prey were able to reduce aphid(R. padi) population development significantly relative to predator-freecontrols. Of the examined species Oligolophus tridens turned out to be themost efficient predator with an ability to reduce aphid numbers up to 97%.When the generalist predators were offered alternative prey, no differencesin ability to suppress aphid population numbers in comparison to predatorswithout alternative prey were observed in E. atra, Clubiona, P. degeeri andO. tridens.

Dinter (1998a) simulated natural disturbance factors (wind or rain) thatare absent under laboratory conditions by shaking the microcosms daily. Inthe present experiment we did not make these daily disturbances. In this waywe reduced the influence of abiotic factors, which would only increase theimpact of predators on the aphid populations.


Erigone atra

The observed reduction in aphid population growth caused by E. atra wasexpected according to literature. Using a comparable experimental designMansour and Heimbach (1993) found that E. atra significantly reduced thedevelopment of R. padi by 58%, compared to 28% in our study. Other work(Sunderland et al., 1986; Alderweireldt, 1994a) has shown that linyphiidspiders can restrict aphid population development in cereal crops.

Because the microcosms only experienced a minimum of disturbance, thenumber of aphids falling into the small webs of E. atra must have been insig-nificant, at least at the beginning of the experiment. In addition, very fewaphids are expected to walk on the ground prior to the exponential growthphase (Wiktelius and Ekbom, 1985). No study has shown whether groundwebs of Erigoninae are capable of capturing walking aphids. Prior to theaphid exponential growth phase E. atra must have experienced a time oflow aphid encounter rates. The observed aphid reduction may in fact expressE. atra’s ability to hunt aphids outside the sheet web (Alderweireldt, 1994b).In cereal fields the aphid suppression potential of E. atra might be even higherbecause more aphids are falling into their webs caused by rain and winddisturbances (Sunderland et al., 1986; Mann et al., 1995).

Contrary to Dinter (2002) we found no effect of alternative prey on theability of E. atra to suppress aphid population growth. This difference maybe due to the fact that Dinter (2002) used both fruit flies and an entomobryidcollembolan as alternative prey. Possibly, the fruit flies were not so easilycaptured by E. atra in the microcosms as the collembolan, which is active onthe soil surface where the spider builds its web.

Clubiona and Pachygnatha degeeri

Alternative prey did not cause any difference in aphid predation between thetreatments in Clubiona and P. degeeri. Both predators were able to reducethe aphid numbers relative to controls (Figure 1c and d). Both are planthunting as evidenced by rich webbing of silk in the microcosms at the endof the experiments. Clubiona had a remarkably higher body mass increasewith alternative prey than without it. This indicates a preference for fruit fliesrelative to aphids which was confirmed in the 24-h consumption experiments.This result may lead to the expectation that the presence of high-quality foodshould lower aphid predation, but this was not confirmed.

It was surprising that the two predators with distinctly different huntingstrategies, E. atra and Clubiona showed almost the same ability to reduceaphid numbers in the microcosms. One might expect a higher ability tosuppress the aphid population in Clubiona due to its tendency to actively


search for prey in the vegetation in contrast to the ground-living, web-building E. atra. Their relative sizes would also be an argument for a higheraphid predation in Clubiona. However, Wiktelius (1986) found that more than75% of R. padi populations occur on cereal plant bases at or immediatelybelow the soil surface during the earliest stages of crop growth and aphidinfestation. Thus predators like Clubiona living up in the vegetation (personalobservation) may experience a lower encounter rate with R. padi than ground-living predators like E. atra. P. degeeri is of intermediate size. It probablyhunts both on the ground and on the plants, which may explain its good abilityto reduce the aphid population.

Pardosa prativaga

Individuals of this species showed a significantly lower impact on aphidnumbers when offered fruit flies in comparison to individuals without alter-native food (Figure 1e). Also a higher mean gain in body weight in predatorswith alternative prey relative to those without was established. Thus, it wasshown that a preference for high-quality food (D. melanogaster) divertsP. prativaga from feeding on R. padi. This finding is in accordance withoptimal foraging theory (Charnov, 1976) which predicts that a lower-rankingprey may be excluded from the optimal diet if an alternative higher-rankingprey becomes abundant.

The hunger level of a predator is expected to play an important role inprey choice, i.e., whether a predator should accept a less preferred prey or not(Stephens and Krebs, 1986). Theoretically a hungry predator should morewillingly accept lower-ranking prey than a satiated predator. However, Toft(1995) showed that in spite of a higher hunger level (14 days’ starvation)average consumption of R. padi by P. prativaga was only one aphid per spiderin 24 hours, the same as that of satiated spiders. The limited consumption ofaphids in P. prativaga can be ascribed to the development of an acquiredaversion to aphids (Toft, 1997). Furthermore, studies have shown that R. padiis a low-quality prey for P. prativaga (Toft, 2000). It was therefore unexpectedthat P. prativaga without alternative prey was able to reduce R. padi numbersup to 81% relative to controls. The reason may be that initial encounter rateswere too low, so that no acquired aversion to the aphids was developed at thebeginning of the experiment.

The difference in mean body weight gain in P. prativaga demonstrates thatspiders with R. padi as the only food were starving. This result confirms thatR. padi is a low value food for P. prativaga.

The second experiment with T. bidentatus as alternative prey showed nosignificant difference between treatments (Figure 1f). This may be becauseP. prativaga was unable to locate the Collembola, due to the motionless


behaviour of T. bidentatus (personal observation). In addition, the Collembolawere often found to hide immediately below the soil surface.

Bembidion lampros

B. lampros had no significant effect on aphid population growth in theabsence of alternative prey and an only marginal effect in its presence(Figure 1g). The exclusion of abiotic disturbances may possibly explain thislow effect. In the field a larger proportion of the aphids may be active onthe ground, especially early in the season (Sopp et al., 1987). It can also behypothesized that consumption of aphids supplementary to high-quality preyis associated with a nutritional gain to the predator, which is not obtainedwhen only aphid prey is available, and therefore the beetle may eat moreaphids in the presence of alternative prey. Bilde and Toft (1994) foundincreased fecundity in the carabid beetle Agonum dorsale on a mixed dietof fruit flies, R. padi and earthworm compared to the three monotypic diets.Furthermore, Wallin et al. (1992) found B. lampros to produce both fewerand smaller eggs when fed a pure R. padi diet compared to a mixed cat-food/R. padi diet. These findings are in accordance with the present study and thatof Sørensen (1996), which suggests that B. lampros has a low preference forR. padi. In contrast, Chiverton (1988) found that B. lampros had a mean dailyconsumption of 16 1st-3rd-instar nymphs and 9 apterous adults of R. padi at25 ◦C.

An alternative explanation may be that alternative prey induces a differentsearch pattern in the beetle or make it search a slightly different microhabitat,which accidentally brings it in closer contact with aphids. Monsrud and Toft(1998) indicated a mechanism by which such an effect might come into playin the field: because Diptera are attracted to honeydew secreted by aphids,carabid beetles also aggregate around aphid colonies. This mechanism couldnot have been working in the microcosms, however. The evidence so far hasshown that a relatively large proportion of B. lampros feed on aphids (Sunder-land, 1975; Sunderland et al., 1987) and R. padi in particular (Chiverton,1986, 1987) in cereals during the aphid’s establishment phase in early springthough its main food is Collembola and Diptera (Sunderland, 1975). Thepresent work suggests that aphid predation in B. lampros is associated withthe presence of high-quality alternative prey. However, further work is neededto evaluate the proposed mechanisms for this effect.

Oligolophus tridens

The microcosm experiments showed that O. tridens was an efficient predatorindependent of availability of alternative prey. In both treatments the predator


had a remarkable ability to reduce aphid population growth (Figure 1h andi). The observed high reduction rates may be explained by the fact thatharvestmen have metabolic rates roughly two to four times higher than otherarachnids (Anderson, 1970). The observed impact on aphid numbers in thepresent study with O. tridens needs to be further evaluated with respectto predator performance and tolerance to aphids. However, it seems thatO. tridens and other harvestmen could be an important aspect of aphid pestsuppression. Only few studies have addressed the ability of aphid suppressionin harvestmen (Bristowe, 1949; Dixon and Mckinlay, 1989; Halaj and Cady,2000; Bradbury and Cady, 2001). However, all these experiments have shownthat harvestmen are potential bio-control agents of aphid pests. Opilionidsmay have been neglected as predators of pests because they are largelyabsent from fields that are strongly mechanically disturbed. Further researchis warranted in order to investigate their potential in grassland and other cropsof higher permanence.

24 h consumption studies

According to results of the 24-h consumption experiments it seems thatprey type is among the factors determining predator performance, as alreadyestablished by Bilde and Toft (1997). The daily food demand, estimatedby D. melanogaster intake, is far above the consumption capacity forR. padi indicating physiological starvation on a strict aphid diet. The 24-hexperiments showed no difference between the two species, Clubiona andP. degeeri. We found that female food intake was equal to male intake whenaccounting for the differences in size, i.e., specific consumption. Per indi-vidual the female predators ate more than the males. The results indicate thatR. padi is deterrent to the two species and thus add two spider families to thelist of generalist predators with a low preference for aphids. This corroboratesthe opinion that the aphids are low value food for many generalist arthropodpredators.

Generalist predators as natural enemies of insect pests

In recent years agricultural management has been confronted with a risingsocio-ecological demand for reducing the intense use of artificial pesticidesin cereal fields. Focus has been directed towards a more ecological prac-tice in which the utilization of natural enemies is an important issue in thecontrol of insect pests. In accordance with earlier works the present study hasindicated that spiders, carabid beetles and harvestmen as generalist predatorsare able to make a significant contribution to aphid control. This is accom-plished in spite of low individual capture rates in the early spring prior to the


aphids’ exponential phase (Sunderland et al., 1986, 1987; Chiverton, 1987;De Barro, 1992). In early spring when aphids migrate into the fields andaphid numbers are low, each predator will encounter only a few aphids. Anincrease in predator densities within crops by changing agricultural manage-ment will create a more favourable predator to pest ratio, which may result inan improved pest control.

Recent work has focused on agricultural diversification by modification ofthe habitat or new cultural practices in order to promote a build-up (numericalor biomass) of potential aphid predator populations (review in Sunderland andSamu, 2000). The studies have shown that habitat diversification can improvethe abundance and diversification of food for spiders and thereby provide anelevated spider density. Chen and Wise (1999) were able to increase bothalternative prey and predator populations by an enhanced input of organicmaterial. J. Axelsen and S. Toft (unpublished) showed in a simulation studythat a high level of alternative prey increased the aphid predation up to acertain stage due to the increased reproductive output of spring breeders.These results may have consequences for the prospects of managing gener-alist predator communities. Thus it has been argued (Toft, 1995; Sunderlandet al., 1996) and empirically confirmed in the present study with P. prati-vaga, that with a low predator preference for aphids increased availability ofalternative prey may reduce predation on aphids. If alternative prey specieschange the suppressive impact of generalist predators on aphid developmentrate in cereal fields, it could be hypothesized, as by Bilde et al. (2000) thatimproving the availability of high-quality prey during the growth phase ofpredator population would lead to a higher predator density. Removing thealternative prey when aphid populations migrate into the fields in early spring,forcing the predators to switch prey items, would increase predator impact onaphid population development. However, this may not be the solution for allgeneralist predators as shown in the present study with B. lampros.

Further information is required to identify the bio-control potential ofindividual predator species regarding aphid predation in order to assess theecological effect of natural enemies. In addition, further knowledge regardingthe mechanisms of predator-prey interactions in single- and multi-speciespredator systems is necessary to elucidate the role of inter- and intraspecificrelations between pest antagonists of prey populations (cf. Dinter, 1998a, b,2002). The set-up of the present microcosm study may further be used toanalyse other naturally occurring alternative prey types and predators whichcan contribute to the understanding of predator-pest interactions in complexenvironments. For example, it would be of interest to investigate how alter-native prey types of different nutritional value and/or behavioural differencesinterfere with the predators’ ability to prey on aphids in different ways.


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Microcosm studies on control of aphids by generalist arthropod predators: Effects of alternative prey