Entomologia Experimentahs etApphcata 80: 365-374. 1996 365 @ 1996 Kluwer Academic Publishers. Printed in Belgium.

Insect-crop interactions in a diversified cropping system: parasitism by Aleochara bilineata and Trybliographa rapae of the cabbage root fly, Delia radicum, on cabbage in the presence of white clover

Vibeke Langer Section of Zoology, Department of Ecology and Molecular Biology, The Royal Veterinary and Agricultural Universi~. , BMowsvej 13, DK-1870 Frederiksberg C, Denmark Present address: Agroecology, Department of Agricultural Sciences, The Royal Veterinary and Agricultural Universi~, Agrovej 10, DK-2630 Taastrup, Denmark

Accepted November 21. lC~C~5

Key words: Delia radicum, Aleochara bilineata, Trybliographa rapae, parasitoid, cover crops, host plant finding

Abstract

Parasitism of the cabbage root fly, Delia radicum (L.) by the staphylinid Aleochara bilineata Gyllenhal and the cynipid Trybliographa rapae Westwood was examined in a cabbage monoculture and a mixed stand of cabbage undersown with white clover. Number of overwintering cabbage root fly pupae per plant was consistently reduced in the mixed stand, and the incidence of plants attacked by cabbage root fly was either reduced or not different in the mixed stand compared to cabbage monoculture. For both parasitoids, the probability of D. radicum attacked plants having at least one parasitized pupa increased with density of cabbage root fly pupae around the plant. For A. bitineata, this positive relation between presence of parasitism and host density was consistently stronger in cabbage monoculture than in cabbage undersown with clover. Location of a host plant by T. rapae was not consistently affected by the presence of clover. D. radicum attacked plants situated in the cabbage and clover mixture were found by T. rapae as easily as in cabbage monoculture. Overall, the 'total risk of parasitism' for a cabbage root fly pupa by A. bilineata was reduced in the mixed stand compared to the cabbage monoculture, whereas the risk of parasitism by T. rapae was not consistently affected by clover. For both parasitoids, intensity of parasitism showed a variable relationship with host density on individual plants attacked by the cabbage root fly. Overall, in spite of consistently lower total density of pupae in the mixed cabbage - clover than in cabbage monoculture, the density of unparasitized pupae was reduced by the presence of non-host plants only in two of the four experiments. The results emphasize the need to include not only herbivore and crop, but also other plant species as well as natural enemies when evaluating management methods.

Introduct ion

Crop diversification by undersowing or intercropping has been considered potentially useful to control Delia radicum (L.) (Diptera: Anthomyiidae) in cruciferous crops. Reduced numbers of D. radicum eggs, larvae or pupae have been recorded around brassica plants grown in clover or other plant species (O'Donnell & Coaker, 1975; Ryan et al., 1980; Tukahirwa & Coaker, 1982; Theunissen et al., 1992). Evaluating the potential for practical use of these systems needs to clarify how crop diversification affects the inter-

action between D. radicum and its natural enemies. In the present study, parasitism the two main para- sitoids found in diapausing D. radicum pupae, Tr3,- bliographa rapae Westwood (Hymenoptera: Cynipi- dae) and Aleochara bilineata Gyllenhal (Coleoptera: Staphylinidae) in cabbage (Brassica oleracea L. con- var. capitata (L.)) monoculture and cabbage under- sown with white clover, was investigated. Focus was on the effects of ground cover on the intensity and dis- tribution of parasitism rather than on adult parasitoid populations. Two questions were asked: in what way does the presence of undersown white clover affect the

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intensity of parasitism of the overwintering generation ofD. radicum by A. bilineata and T. rapae?, and does clover presence act directly on parasitoid host finding or indirectly via D. radicum density and spatial pattern?

Both A. bilineata and T. rapae parasitize D. radicum, one of the most serious pests of cruciferous crops in Northern Europe (Coaker & Finch, 1971). In Denmark, D. radicum and T. rapae both have two and in some years three generations, whereas A. bilineata has two generations (Bromand, 1974).

D. radicum larvae feed on roots of cruciferous plants, causing damage that ranges from insignificant growth inhibition to plant death depending on plant condition and larval density. Although D. radicum has other parasitoids, A. bilineata and T. rapae are the most important ones found in diapausing pupae (Finch & Collier, 1984; Jonasson, 1994). Parasitism by A. bilin- eata and T. rapae of D. radicum has large variations between years, sites, generations, crops and pesticide history (Abu Yaman, 1960; Read, 1962; Sundby & Taksdal, 1969; Bromand, 1974, 1980; Ryan & Ryan, 1980; Finch & Collier, 1984). In Denmark parasitism ranges from 0 to 88% by A. bilineata and from 0 to 49% by T. rapae (Bromand, 1980).

The life cycle of A. bilineata is well synchronized with that of D. radicum, as adult beetles hatch two to three weeks later than D. radicum and oviposit around attacked plants at the time of pupation (Finch & Collier, 1984). Newly formed D. radicum puparia are located and penetrated by the first instar A. bilineata larvae. Other anthomyiid Diptera (e.g.D. floralis, D. antiqua, D.florilega, D. platura) also serve as hosts forA. bilin- eata (Fuldner, 1960; Sundby & Taksdal, 1969; Moore & Legner, 1971; Peschke & Fuldner, 1977; Jonasson, 1994). Adult A. bilineata feed on dipteran eggs and lar- vae (Fuldner, 1960; Read, 1962; Peschke & Fuldner, 1977) and on Collembola and Acari (Good & Giller, 1988).

T. rapae is more specific than A. bilineata and is synchronized to attack first and second instar larvae of D. radicum, in which early larval stages live endopar- asitically and the later ones ectoparasitically (Wishart & Monteith, 1954; Finch & Collier, 1984; Jones et al., 1993). Its only other main host is the closely related species D.floralis (Bromand, 1974; Jones et al., 1993).

In A. bilineata, the adult female and the first instar larva participate in host finding, but female behaviour when selecting an oviposition site is not well known. After hatching, the first instar A. bilineata larvae find the D. radicum puparia by random search (Fuldner, 1960; Putnam, 1957; Jones et al., 1993) and need to

locate a host puparium within a few days (Colhoun, 1953).

The adult female T. rapae responds to olfactory cues from the frass of D. radicum larvae (Jones et al., 1993) as well as to physical stimuli from larval move- ment (Vet & van Alphen, 1985).

Two main consequences of undersowing are plant diversification and increased plant cover, and it is unknown how they affect abundance and activity of adult A. bilineata and T. rapae. Several investigations indicate that staphylinid numbers are enhanced (Purvis & Curry, 1984; Powell et al., 1985) or unaffected (Tukahirwa & Coaker, 1982) by the presence of ground cover, as may also happen with Hymenoptera (Purvis & Curry, 1984). Reported effects of ground cover on par- asitism include a reduction in parasitism ofD. radicum by A. bilineata and an increase in parasitism by T. rapae in cabbage undersown with clover compared to cab- bage monoculture (Ryan & Ryan, 1980). Parasitism by A. bilineata was consistently reduced by the pres- ence of a mulch of grass clippings, whereas parasitism by T. rapae was unaffected (Hellquist, 1996).

Materials and methods

Sites and treatments. The effect of the presence of ground cover around cabbage plants on number of overwintering D. radicum pupae and on parasitism by A. bilineata and T. rapae was assessed in four field experiments. A pure stand of white cabbage was com- pared to white cabbage undersown with white clover in a randomized block design with three to nine repli- cations and a single plot size of 200-400 m 2. Two experiments were on a clay soil at the experimental farm of the Royal Veterinary and Agricultural Univer- sity, HCjbakkeg~d, in T~strup (1990, 1991). A further experiment was done on a sandy loam at SCtofteg~d, a biodynamic farm in southern Sjaelland in 1990, and a final one was placed on a loamy soil at a conventional vegetable farm in Brenderup, Fiinen (1992). Cabbage plants were either directly sown (1991) or transplanted, and white clover was established either in the preceed- ing autumn (1990, HCjbakkeghrd) or in early spring (Sctofte 1990 and 1991) or simultaneously with cab- bage planting in May (1992). In 1992 the cabbage variety 'Erdeno' and the clover variety 'Pertina' were used, whereas cabbage cv. 'Olympiade' and clover cv. 'Kent' were used in all other experiments. Cab- bage plants were planted with 60 or 70 cm between rows and 50 cm between plants. Clover was kept in

Table 1. Density of D. radtcum pupae and percent parasitism by A. bihneata and T. rapae in two habitats. Four field experiments, 1990-1992

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Year and Cabbage monoculture N Cabbage wtth clover site Total no. Pupae/ % parasitism Total no. Pupae/ % parasitism

of pupae plant 1 of pupae plant I A. bd. T. rapae A. bil. T. rapae

1990 280 4.8a 33.6 15.4 58 113 1.3b 9 7 35.4 90 H~bakke 1990 338 5.7a 30 2 16 9 59 145 1.7b 18.6 22.1 87 S~tofte 1991 460 15.9a 21.1 31.7 29 293 9.8b 2.7 27.3 30 H~bakke 1992 446 5.6a 14 3 22.0 80 248 4.1b 10.9 20.6 60 Bmnderup

i Analysis is based on no. of pupae/plant transformed to In (pupae +1) Means are to be compared between treatments only (horizontally). Different letters indicate treatment effects with P<0.05

an approximately 35 cm wide strip between cabbage rows by hand and was suppressed by mowing several times during the growing season in 1990 and 1991. No pesticides were applied.

Assessment o f pupal density and parasitism. Puparia of diapausing D. radicum were collected in Nov. 1990, Nov. 1991 and Sept. 1992. Soil samples, 15 cm in diameter and 15 cm deep, were taken around 10, (20 in 1992) randomly chosen plants per plot and stored at 5 ~ until processing. Plants were harvested for fresh weight determination. Puparia were separated from the soil by flotation in water and kept at 4 ~ until exami- nation under a binocular microscope for parasitism. All puparia with a visible entrance hole or a visible A. bilin- eata larva were classified as parasitized by A. bilineata. This included puparia with decayed contents following unsuccessful parasitism by A. bilineata, e.g. caused by parasitism by T. rapae prior to the attack by A. bilin- eata (Reader & Jones, 1990). Sorting of pupae was done in late winter, when most pupae parasitized by T. rapae could be recognized by their smaller size and, in the parasitoid's ectoparasitic stages, the presence of dark, granular meconium. The number of puparia with dead contents, but with no entrance hole, never exceeded 4% of the total number, and no attempts were made to distinguish between different causes of death. In both 1990 experiments puparia were sorted accord- ing to external criteria and were allowed to hatch or were dissected if hatching failed. In the 1991 and 1992 experiments pupae were sorted on external features, only supplemented by dissection if needed. Plant fresh weight at harvest was used as an estimate of competi-

tion exerted on cabbage plants.

Data analysis. Effects of treatment and plant weight, on D. radicum pupal densities were analysed with analysis of variance and covariance (SAS Institute, 1987) after transformation (In (pupae + 1)). The spatial distribution of host and parasitoids (incidence of plants with D. radicum pupae, incidence of plants with par- asitized pupae and probability of parasitism for indi- vidual pupae) were analysed using logistic regression (CATMOD procedure) (SAS Institute, 1987). In this analysis, comparisons between treatments were car- ried out by testing the odds-ratio (pl/1-pl)/(p2/1-p2), where Pl and P2 are the probabilities of an event hap- pening in treatment 1 and 2, respectively. The events occurring were e.g. a pupa being parasitized or a plant being located by a parasitoid. The odds-ratio gives a relative measure of the difference in chance of a cer- tain event, e.g. parasitism, happening in the two treat- ments (Andersen, 1990). Density dependence of para- sitism by the two parasitoids was also tested via logistic regression, with the response function being the logit of the dependent variable, p, in this case the propor- tion of D. radicum pupae parasitized around individ- ual cabbage plants with varying host density. In the CATMOD procedure, generalized logits are analysed through maximum-likelihood estimation (SAS Insti- tute, 1987).

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Table 2. Individual D. radicum pupae's risk of being parasitized by the parasitoids A. bihneata or T. rapae. Odds ratio describes the probability of attack or discovery for pupae in cabbage-clover plots compared with pupae m pure cabbage stand. Odds ratio < 1 indicates, that the probability of parasitism is larger in a pure cabbage stand than in cabbage undersown with clover

Experiment Parasitism by A. bilineata P T. rapae Odds ratio Odds ratio

HCjbakke 1990 0 24 *** 2.94 *** Sctofte 1990 0 54 ** 1 43 ns. Hcjbakke 1991 0.09 *** 0 89 ns. Brenderup 1992 0.66 ns. 0.98 ns.

Results

Pupal density. Pupal density and overall parasitism by A. bilineata and T. rapae on overwintering D. radicum pupae is shown in Table 1. In the two experiments in 1990 pupal density was low, averaging 2.7 and 3.3 pupae/plant when both treatments were included. In 1991 and 1992, average pupal numbers were higher, 12.9 and 5.0 pupae/plant respectively. In all experi- ments, number of D. radicum pupae/plant were signif- icantly reduced by the presence of undersown clover (Table 1). In all experiments clover covered the ground at the onset of second generation oviposition. Clover growth vigour and thus competitive effect, however, differed between years, and was reflected in a signifi- cantly reduced cabbage plant weight at harvest in the cabbage - clover system (in 1990 and 1991 20 to 45% of monoculture) (Langer, unpubl, data). The reducing effect on pupal numbers due to smaller plant size could not be separated from that of presence of ground cov- er in these two years. However, in 1992, when plant size did not differ between treatments, pupal numbers on plants situated in clover were shown to be signifi- cantly reduced by the treatment (F = 5,27; df = 1,133; P = 0.02) and to increase linearly with increasing plant size at harvest (P = 0.01 in monoculture, P = 0.06 in the mixed stand), with the same slope in both treatments, i.e. the interaction between treatment and plant size was non-significant.

Overall parasitism. In all experiments, total 'risk of parasitism' of D. radicum pupae by A. bilineata was decreased when located on a plant in the clover- cabbage mixture compared to the cabbage monoculture (Table 2). The total risk is the result of the probabil- ity of two events happening: the cabbage plant being

found by the A. bilineata female (i.e. location and oviposition), and the individual pupa being located and successfully penetrated by a first instar A. bilin- eata larva. A significantly lower 'risk of parasitism' by A. bilineata was seen in the mixed stand in three experiments, ranging from 0.09 (1991) to 0.54 (S~tofte 1990) times that in monoculture (Table 2). Although the risk of parasitism was lower in mixed culture than in monoculture (0.66) also in 1992, this was not sig- nificant. Unlike A. bilineata, no consistent effect of ground cover was observed in the 'risk of parasitism' by T. rapae. Only in the Hcjbakkeghrd 1990 experi- ment was the risk of parasitism significantly lower in the pure cabbage stand (Table 2).

In spite of the significantly reduced total number of pupae/plant in the mixed stand compared to the monoculture in all four experiments, the number of healthy (unparasitized) overwintering pupae differed between treatments only in the two 1990 experiments (HCjbakke F= 5.2, df= 1,141, P = 0.02; SCtofte F= 6.8, df= 1,140, P=0.01). In 1991 and 1992 the density of pupae, which could be anticipated to give rise to healthy flies in the spring, was not affected by treat- ment.

Spatial distribution of hosts and parasitism. The pro- portion of plants, attacked by D. radicum, that was 'dis- covered' by the parasitoids, i.e. on which at least one parasitized pupa by A. bilineata or T. rapae was found, is shown in Figure 1. Plants attacked by D. radicum, represent potential oviposition sites to the searching female parasitoids, and the odds-ratios (Table 3) show that the relative probability for an individual plant being a potential oviposition site was significantly low- er in the cabbage-clover than in the cabbage monocul- ture in 1990, whereas in 1991 and 1992 it was not affected by the presence of clover.

In all experiments, the probability of a D. radicum attacked plant being discovered by A. bilineata was reduced in the cabbage-clover stand. Again, unlike A. bilineata, the D. radicum attacked cabbage plants' probability of being located by T. rapae was not affect- ed by the presence of clover (Table 3).

For both A. bilineata and T. rapae, the propor- tion of attacked plants, on which at least one para- sitized pupae was found, increased with the number of D. radicum pupae around the plant. Regressions of In(p/l-p) (p = proportion of plants discovered by the parasitoid) against host density, show that the odds of discovery of the plant were significantly dependent upon host density for both parasitoid species in all

Table 3. Indwidual cabbage plants' risk of being attacked by D. radtcum, and D. radicum attacked plants' chance of being discovered by the parasitoids A. bilineata and T. rapae. Odds ratio describes the probability of attack or discovery for plants in cabbage-clover plots compared with plants in pure cabbage stand. Odds ratio < 1 indicates, that the probability of the event occuring is larger in a pure cabbage stand than in cabbage undersown with clover

Experiment Attack by D. radtcum Discovery by

Odds ratio P A. bihneata P T. rapae P

Odds ratio Odds ratio

H~jbakke 1990 0.03 *** 0.05 *** 1.64 ns.

SCtofte 1990 0.06 *** 0.25 *** 0.78 ns. Hcjbakke 1991 1 ns. 0.02 *** 0.25 ns

Brenderup 1992 0.47 ns 0.40 * 0 64 ns.

Table 4. Maximum likelihood equations for the relation between D. radtcum density and 'discovery' of D radwum attacked plants by A. bthneata and T. rapae. The dependent variable is In (p/1 - p), where p is the proportion of D. radicum attacked plants found by the parasitoad. The independent variable ~s the number of D. radtcum pupae per plant. Equations for both treatments are shown together as well as separately

Experiment Treatment A. bilineata P T. rapae P

1990 Hcjbakke both -2.1 + 0.50 x < 0.001 - 0.5 + 0.15 x 0007

pure cabbage - 0.9 + 0.44 x 0005 -1 4 + 0 3 0 x 0.004

cabbage+clover -4.1 + 0 5 7 x 0.008 - 0.2 + 0.33 x 0.11 (ns.)

1990 SCtofte both -1 1 + 0.42 x < 0.001 - 0.7 + 0 14 x 0.02

pure cabbage - 0 9 + 0 . 4 4 x 0.01 - 0.3 +0.09 x 0.21 (ns.) cabbage+clover -1.0 + 0.28 x 0.08 (ns.) -1 2 + 0.35 x 0 04

1991 both -2.1 + 0.16x 0.001 -0.4 + 0.24x 0.01

pure cabbage - 0.5 + 0.16 x 0.05 - 0.3 + 0.31 x 0.12 (ns.)

cabbage+clover - 2.9 + 0.10 x 0.33 (ns.) - 0.4 + 0.21 x 0.07 (ns.)

1992 both -1 1 +0.15x 0.004 - 0.9 + 0.30 x <0001

pure cabbage -1.0+ 0 18x 0.01 - 0 . 6 + 0 2 4 x 0.008

cabbage+clover - 1.1 + 0 08 x 0.32 (ns.) -1.3 + 0.43 x 0.006

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e x p e r i m e n t s , w h e n the two t r ea tmen t s were p rocessed

t o g e t h e r (Table 4).

P r o c e s s i n g the two t r ea tmen t s separate ly , the odds

o f D. radicum a t t acked p lants b e i n g d i s cove red by

A. bil ineata i n c r e a s e d wi th inc reas ing D. radicum den-

sity in all e x p e r i m e n t s in the c a b b a g e m o n o c u l t u r e . T he

a s soc ia t ion b e t w e e n hos t dens i ty and p lan t a t t ract ive-

ness (odds o f d i scove ry ) was weake r in the cabbage -

c love r s tand, as on ly the 1990 H~jbakkegf i rd exper i -

m e n t s h o w e d any s ign i f ican t ly inc reased d i scovery of

h i g h dens i ty p lan ts by A. bil ineata (Table 4). As an

example , 1992 resu l t s are s h o w n in F igures 2 A and

2B. For T. rapae a separa te ana lys i s o f c a b b a g e m o n o -

cu l tu re and c a b b a g e - c l o v e r s h o w e d that the p r e sence of

g r o u n d c o v e r d id not cons i s t en t ly af fec t p l an t loca t ion

(Table 4).

In bo th 1991 and 1992, w h e n the i n c i d e n c e o f

D. radicum a t tacked p lants in the two t r e a t m e n t s was

similar , the m e a n n u m b e r o f pupae pe r p lan t was s ignif -

icant ly h i g h e r on a t t acked p lan t s wi th p u p a e pa ras i t i zed

by A. bilineata t han on p lan t s w i t h o u t pa ras i t i zed

pupae in the c a b b a g e m o n o c u l t u r e ( 1 9 9 1 : 1 7 . 3 and 9 .0

pupae plant , P = 0.04; 1 9 9 2 : 7 . 1 and 4 .6 pupae /p l an t ,

P = 0.005) . In the m i x e d cabbage -c love r , the n u m b e r o f

pupae did not d i f fer s igni f icant ly b e t w e e n p lan t s wi th

and wi thou t pa ras i t i sm (1991 :12 .8 and 9.7 pupae /p l an t ;

1 9 9 2 : 5 . 3 and 4.3 pupae /p lan t ) .

Intensity o f parasit ism. The re la t ion b e t w e e n

D. radicum pupa l dens i ty and pe r cen t pa ra s i t i sm is

s h o w n as r eg ress ion equa t ions for all roo t fly a t t acked

p lants as wel l as on ly p lan ts loca ted by a pa ras i to id

(Figures 3 A and 3B). W h e n all p lan t s a t t acked by

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cabbage plants

iO0

90

80

70

60

50

40

30

20

•

0

g . '.., .:

k~ "..y

'!,;

7Z

Nono ~ixed Nono Nixed nono Nixed Kono Kixed

No parasitism

A.bilineata only"

T, ralDae only

i Both parasitoids

No D.radicum

i 9 9 0 H i 9 9 0 5 i 9 9 i i 9 9 2 Figure 1. Incidence of cabbage plants with D. radicum pupae and with pupae parasitized by A. bilineata, T. rapae or both. (Number of plants: 1990 H0jbakke N= 148, 1990 SOtofte N= 146, 1991 N=59 and 1992 N= 140).

D. radicum are included, intensity of parasitism by T. rapae was independent of density in three experi- ments and inversely density dependent in one exper- iment. Parasitism by A. bilineata was independent of host density in two experiments and density depen- dent in two experiments, when all D. radicum attacked plants were included. When only plants with at least one parasitized pupa were included, the proportion of parasitized D. radicum pupae was inversely related to density in all four experiments for T. rapae, whereas parasitism by A. bilineata was inversely density depen- dent in two experiments, independent of density in one and density dependent in another experiment.

Discussion

Specialist enemy response to agroecosystem diversifi- cation have received less attention than given to gener- alist enemies (Sheehan, 1986). Parasitoids like T. rapae use not only the herbivore itself, but also its host plant to locate their host (Jones et al., 1983). Observations

of A. bilineata distribution in the field (Abu Yaman, 1960; Coaker & Williams, 1963) suggest that host plants play a role in parasitoid host finding. The mech- anisms suggested in the 'disruptive crop hypothesis', in which the presence of non-host plants disrupts the ability of a herbivore to attack its host plant (Vander- meer, 1989), may apply also to the interaction between parasitoid, host and host plant: disruption of host plant finding and altered patterns of movement, resulting in decreased parasitoid success in host location.

The results show that reduction in numbers of overwintering D. radicum pupae resulting from under- sowing cabbage with clover may be counteracted by a similar decrease in parasitism by A. bilineata, in some years (1991 and 1992), with the net result of the same numbers of healthy pupae overwintering. This emphasizes the need to include higher troph- ic level organisms in studies of vegetational diversi- fication. When examining the effect of vegetational texture on parasitism, host density should ideally be kept constant. In the present study no attempts have been made to control D. radicum density. However,

included in the experiments were two sites in which both density and spatial distribution of D. radicum pupae were influenced by the habitat (H~jbakke and SCtofte, 1990) and two sites, in which spatial distribu- tion of D. radicum attacked plants was largely unaffect- ed, with only density differing among habitats, either substantially (H~jbakkeg~rd, 1991) or slightly (Bren- derup, 1992).

Habitat finding and preference The observed decrease ofA. bilineata parasitism in the cabbage - clover treatments may have been because ground cover plots were less attractive to adult A. bilin- eata. As no assessments of the numbers of adult A. bilineata and T. rapae in the two habitats were made, the numbers of parasitoid females involved are unknown. However, habitat preference by A. bilineata does not exclude those with ground cover (Tukahirwa & Coaker, 1982), and staphylinids as a group have been caught in larger numbers in weedy crops (Purvis & Curry, 1984) as well as in cabbage mulched with grass clippings than on bare soil (Hellqvist, 1996). Thus, ground cover is not likely to cause the observed impedement of D. radicum parasitism by A. bilineata in the cabbage-clover habitat.

hwidence of plants with parasitism Host density. The probability of D. radicum attacked plants being 'discovered' by A. bilhzeata or T. rapae, i.e. having at least one parasitized pupa, increased with increasing pupal numbers around the plants (Fig- ures 2A and 2B). Many parasitoids discriminate not only between the absence or presence of their host on a plant, but also between plants with high or low host density (Morrison & Strong, 1980). T. rapae adults respond to the odours emitted by D. radicum larval frass and show an aggregation response, spending more time on plants with high D. radicum densities (Jones & Hassell, 1988). No direct association has been reported between the densities of D. radicum pupae and adult A. bilineata in the soil around individual plants, but adult A. bilineata aggregate around host plants (Coak- er & Williams, 1963) with a strong preference for D. radicum attacked plants (Abu Yaman, 1960; Fuld- net, 1960). It must be considered however, that the result ofA. bilineata adults ovipositing randomly, with- out preference for plants with high host densities, was likely to be similar to the one observed in the present study, as the searching larvae would be more likely to find at least one host puparium around plants with

371

many puparia than around plants with few puparia. Thus it is not possible to be conclusive about adult host finding behaviour solely on the basis of increased incidence of parasitism with increasing host density (Putnam, 1957).

Ground cover. The presence of clover reduced the prob- ability that D. radicum attacked plants were found by A. bilineata to less than half compared with cab- bage monoculture (Table 3). In 1991 and 1992, where incidence of D. radicum attacked plants did not dif- fer between the two habitats (Figure 1), more of the attacked plants were located by A. bilineata in the cabbage monoculture than in the cabbage-clover mix- ture. The higher mean host density in the pure cab- bage in 1991 and 1992 accounted for some of the increased success through a positive host density effect on parasitoid plant location. However, the linear rela- tion between host density and odds of 'discovery' by A. bilineata was stronger in the cabbage monoculture than in cabbage-clover, suggesting that attacked plants with the same number ofD. radicum pupae were easier to locate in the absence of clover.

The ability of the female T. rapae to locate D. radicum attacked plants was not affected by the presence of ground cover, as root fly attacked plants in both treatments had the same probability of being located by T. rapae (Table 3), and the linear relation between D. radicum density and success of plant loca- tion was not consistently weaker on plants in cabbage- clover plots (Table 4).

Adult A. bilineata live mainly on the soil surface, and, lacking detailed information about their host find- ing behaviour, it can be suggested that this makes them sensitive to the physical impedement imposed by a dense plant cover (Ryan & Ryan, 1980). T. rapae, on the contrary, probably flies between plants and thus may be less affected by the presence of ground cover.

Host densit3, and intensity of parasitism Jones & Hassell (1988) found positive density depen- dence in parasitism by T. rapae on Brassica plants supported by increased searching time at patches with high host densities in the laboratory. Later work, how- ever, showed that the presence of density dependent spatial patterns was not consistent over different years (Jones et ai., 1993). The present data shows a similar inconsistency: parasitism by T. rapae was not density dependent in three experiments and was inversely den- sity dependent in one year, when all plants attacked

372

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i i �9

1

0.0! . . . . . , ' , . . . . . . o o o

0 5 10 15 20 B

D. re4~:c~t~ p ~c:et'piant

Figure 2. Plants 'discovered' by A, bilineata against D. radicum pupae in the two habitats for 1992. Data points are the proportion of plants (p) found against denmty (x). Maximum likelihood equation for the probability of discovery is In ( p / l - p ) = - 1.0 + 0.18x (P = 0.01) in the cabbage monoculture (A) and In (p/l-p) = - 1.06 + 0.08x (P = 0.32, ns.) in the cabbage with undersown clover (B). Similar equations for the three other experiments as well as for T. rapae are listed in Table 4.

parasfflzed

1~176 1 go

80

70

6o2

5o~

4oi

30.

2(1

10-

parasitized �9 loo t �9

7{?

6O

502 |

e

e e

e

�9 e o �9

�9 �9 �9 I �9 e �9 �9 �9 �9 �9 �9 �9

5 10 15 20 D. ~'cLd~c~m pupae

Figure 3A. Percentage ofD. radicum pupae, parasitized by A. bilin- eata, against number of pupae per plant zn 1992. Maximum like- lihood equations describing the relation between density and par- asiusm of indivtdual D. radicum pupae are shown below for all attacked plants (I) and for plants with parasitism by A. bilin- eata (I) for all four experiments: 1990 Hcjbakke (1), 1990 Sctofte (2),1991 (3) and 1992 (4). The dependent variable (y) m the equations is In (p/l-p), where p is proportion of pupae parasitized on the individual plant. N is the number of plants.

�9 e

1o i,

4u- �9 �9 �9

30. * oo : o

20: �9 ,~ �9 i I l l I

10i e e, a

0 ~ �9 e o o o �9 , , i . . . . . . . . . i . . . . . . . . . n . . . . . . . . . i . . . . . . . . . , . . . . . . . . . i . . . . . . . . . i

5 10 15 20 25 3Q 35 40

D. ~'CL~7;etL~ pupae

Figure 3B. Percentage of D. radicum pupae, parasitized by T. rapae, against number of pupae per plant in 1991. Maxi- mum likelihood equations describing the relation between den- slty and parasitism of D. radtcum pupae are shown below for all attacked plants (I) and for plants with parasitism by T. rapae (I) for all four experiments: 1990 HCjbakke (i), 1990 Sctofte (2), 1991 (3) and 1992 (4). The dependent variable (y) in the equatnons is In (p/I-p), where p is proportion of pupae par- asitized on the mdividual plant. N is the number of plants.

(1)I: y = -1.86 + 0.12x (P<0.001) (N = 99)

I1' y = - 0.49 + 0.0Ix (ns.) (N = 44)

(2)I: y = -1 .04 + 0 003x (ns.) (N -- 111)

II: y = - 0.07 - 0.09x (P = 0.007) (N = 67)

(3)I: y = - 3.20 + 0.0Ix (P<0.001) (N = 58)

II: y = - L . 8 2 + 0 0 3 x (P=0.04) (N = 2 8 )

(4)1' y = -1.86 + 0.003x (ns.) (N = 130)

II: y = - 0.43 - 0.08 x (P = 0.005) (N = 57)

(1)I: y = ~0 .45-0 .14x (P<0.001) (N=99)

II: y = 1 .04-0 .29 x (P<0.001) (N = 57)

(2)I: y = -1.20 - 0.04 x (ns.) (N = 111)

II: y = 0 .03-0 .11 x (P=0.001) (N=54)

(3)I. y = - 0.73 - 0.01 x (ns.) (N =58)

II: y = - 0 . 0 3 - 0 . 0 1 x (P=0.02) (N=50)

(4)I: y = -1.14 - 0.02 x (ns.) (N = 130)

II: y = - 0 3 5 - 0 . 0 7 x (P=0.003) (N= 82)

by D. radicum were included. Parasitism by A. bilin-

eata was density independent in two experiments and density dependent in two experiments (Figures 3A and 3B).

If only plants with parasitized D. radicum pupae were analysed, intensity of parasitism was inversely dependent on host density in all four experiments for T. rapae and in two of four experiments by A. bilin-

eata (Figures 3A and 3B). Inverse density dependence is seen e.g. when the parasitoid has increasing diffi- culty in locating a suitable host with increasing host density. T. rapae host finding is performed by adults, who are able to identify and respond directly to the sta- tus of parasitism of the host larvae encountered (Jones et al., 1993) and who are capable of moving to oth- er patches if the rate of encounter with unparasitized hosts decrease (Morrison et al., 1980). Possibly con- tributing to the lower rate of parasitism by T. rapae

with increasing host density may be that parasitism by T. rapae decreases with soil depth (Bromand, 1974), indicating that vertical distribution of host pupae influ- ences exploitation.

For A. bilineata the relation between rate of para- sitism and host density is variable, as inverse density dependence is only seen in two of the four experi- ments, the other two showing no and positive density dependence. Once the female has located the cabbage plant and oviposited, the parasitoid larvae are confined in their host finding to this plant with little chance of movement to other patches, indicating that underex- ploitation of dense patches is not caused by parasitoids leaving the plant. A restriction on search ability similar to the one reported in T. rapae is also seen in A. bilin-

eata, whose first instar larvae rarely find D. radicum

puparia located directly beneath other puparia (Bro- mand, 1980). This mechanism has been suggested to explain reduced parasitism by A. bilineata on organ- ic soils, in which D. radicum pupate at lower depths than in most other soils (Finch & Collier, 1984). How- ever, as it is unknown whether D. radicum density influences vertical distribution of host pupae different- ly under varying soil conditions, the suggestion that different soil condition may account for some of the variation in parasitism can only be tentative. In the two experiments in which parasitism was inversely densi- ty dependent, soils were more sandy than in the two experiments with no or positive density dependence, which were both situated on a heavy clay soil.

The results show that host and parasitoid species react differently and unpredictably in response to veg- etational diversification. Analysis on different spatial

373

scales (host plants and individual hosts) are valuable in understanding observed parasitism in the field. In this case, the reduction in total number of overwintering D. radicum pupae in a cabbage - clover mixture is, to some extent, nullified by the decrease in parasitism by A. bilineata, resulting in no change in density of healthy flies hatching the following spring. Therefore, from a pest management point of view, it is essential when evaluating management methods utilizing ground cov- er, that not only the crop and its pest species, but also other plants present and higher trophic level organisms and their interactions are taken into consideration.

Acknowledgments

Funding for this study was provided by The Royal Veterinary and Agricultural University, Copenhagen, by the Danish Veterinary and Agricultural Research Council and by Stiftelsen Hofmansgave. I wish to thank my colleagues at Section for Zoology as well as Kees Booij and Monika Ahlstr6m-Olsson for criti- cal comments, Henrik Stryhn for statistical advice and Gunhild Michelsen for technical assistance.

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