Responses of the specialist biological control agent, Aleochara bilineata, to vegetational diversity in canola agroecosystems

Biological Control 52 (2010) 58–67

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Responses of the specialist biological control agent, Aleochara bilineata, to vegetational diversity in canola agroecosystems Jim S. Broatch a,*, Lloyd M. Dosdall b, John T. O’Donovan c, K. Neil Harker c, George W. Clayton d a

Alberta Agriculture and Rural Development, 6000 C and E Trail, Lacombe, Alta., Canada T4L 1W1 Department of Agricultural, Food and Nutritional Science, 4-10 Agriculture/Forestry Centre, University of Alberta, Edmonton, Alta., Canada T6G 2P5 c Agriculture and Agri-Food Canada, Lacombe Research Centre, 6000 C and E Trail, Lacombe, Alta., Canada T4L 1W1 d Agriculture and Agri-Food Canada, Lethbridge Research Centre, 5403 – 1 Avenue South, Lethbridge, Alta., Canada T1J 4B1 b

a r t i c l e

i n f o

Article history: Received 4 May 2009 Accepted 30 August 2009 Available online 2 September 2009 Keywords: Aleochara bilineata Delia radicum Brassica napus Brassica rapa Weeds Biological control Spatial heterogeneity Parasitism Predation

a b s t r a c t Plant biodiversity is known to affect insect populations, both herbivores and their natural enemies, and as a consequence, habitat management through increased plant species composition and abundance can be exploited for sustainable pest management. In agroecosystems where crop monocultures are the routine production practice, plant biodiversity can be increased by maintaining small populations of weeds, with potential beneficial effects arising from concomitant increases in the abundance of predator and parasitoid populations. We manipulated weed populations in both species of canola, Brassica rapa L. and Brassica napus L., to investigate responses of adults of Aleochara bilineata Gyllenhal (Coleoptera: Staphylinidae), an important natural enemy of root maggots (Delia spp., Diptera: Anthomyiidae). Larval root maggots feed on canola taproots, disrupting the flow of water and nutrients within the plants, causing substantial yield reductions. Aleochara bilineata is a predator–parasitoid that attacks all root maggot pre-imaginal life stages. Activity density of A. bilineata increased as monocotyledonous weed biomass declined. Significant preferences between canola species were observed, with A. bilineata associated most frequently with B. rapa compared with B. napus. Our research suggests that improved management of root maggot infestations in canola through enhancement of populations of the A. bilineata predator–parasitoid could be accomplished by reducing weed infestations; however, such recommendations should consider other predators in the system and the role of weeds in reducing root maggot oviposition and damage. Ó 2009 Elsevier Inc. All rights reserved.

1. Introduction Increasing plant biodiversity in agroecosystems has the potential to reduce the abundance and economic damage of herbivore pests through a number of different mechanisms (Altieri and Letourneau, 1984). For instance, greater plant biodiversity can increase the number of different habitat types and the variability in microclimatic conditions within crop canopies, and so increase the availability of protective refugia for predators and parasitoids of herbivore pests (Landis et al., 2005; Pavuk et al., 1997). Canola (Brassica napus L. and Brassica rapa L.) is routinely grown in several regions worldwide in systems that strive to produce weed-free monocultures (Christen et al., 1999; Stanley and Potter, 1999; Thomas, 2002), and perhaps the simplest approach for increasing biodiversity in canola agroecosystems would be to include small populations of weeds. The widespread adoption of genetically

* Corresponding author. Address: Alberta Agriculture and Rural Development, Pest Management Branch, 6000 C and E Trail, Lacombe, Alta., Canada T4L 1W1. Fax: +1 403 782 8878. E-mail address: [email protected] (J.S. Broatch). 1049-9644/$ - see front matter Ó 2009 Elsevier Inc. All rights reserved. doi:10.1016/j.biocontrol.2009.08.009

engineered herbicide-tolerant crops in several countries worldwide can enable growers to manipulate weed populations with herbicides in these systems to enhance beneficial effects of weeds without compromising yield (Dewar et al., 2003). Root flies or root maggots (Delia spp., Diptera: Anthomyiidae) are chronic and serious pests of canola in western Canada, particularly in vast areas of cropland throughout northern and central Alberta and in the Aspen Parkland Ecoregion of Saskatchewan and Manitoba (Soroka et al., 2004). Damage is caused by larvae feeding on canola taproots, and this can lead to reductions in yield and host plant vigor (McDonald and Sears, 1991; Griffiths, 1991; Soroka et al., 2004). Five root fly species occur in canola, but most damage is inflicted by the cabbage maggot, Delia radicum (L.), the turnip maggot, Delia floralis (Fallén), and the seedcorn maggot, Delia platura (Meigen) (Liu and Butts, 1982; Griffiths, 1986a,b; Broatch et al., 2006). The predator–parasitoid Aleochara bilineata Gyllenhal (Coleoptera: Staphylinidae) is the dominant natural enemy of root maggots in canola and other brassicaceous crops in western Canada (Read, 1962; Turnock et al., 1995; Hemachandra, 2004). Adults of A. bilineata are voracious predators of D. radicum eggs and larvae.

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Read (1962) concluded that under optimum conditions a single pair of A. bilineata adults could destroy approximately 1210 eggs and 128 larvae in their lifetimes. Each A. bilineata female can produce approximately 9–15 eggs per day or 700 eggs in its lifetime (Colhoun, 1953; Fournet et al., 2000). Larvae of A. bilineata hatch in 3–7 days, and first instars locate root maggot puparia. After chewing an opening in the puparial wall, the larva consumes the developing root maggot pupa within (Royer et al., 1998). Overwintering of A. bilineata occurs as a first instar within the puparium, and new generation adults emerge in the following spring (Colhoun, 1953). In canola crops in western Canada, emergence and seasonal activity patterns of A. bilineata are well synchronized with occurrence of their primary hosts, D. radicum and D. platura, with beetle emergence occurring near the time when egg laying by root maggots begins in spring (Broatch et al., 2008a). Recent studies determined that weeds in canola were associated with reduced infestations of Delia spp. (Dosdall et al., 2003; Broatch et al., 2008b), presumably because weeds interfered with the sequence of behaviors required by female flies before oviposition (Kostal and Finch, 1994; Finch and Collier, 2000). The diversity of microhabitats that weeds create has the potential to enhance biological pest control. However, the influence of weeds on populations of root maggot natural enemies, such as A. bilineata, has never been investigated previously in canola agroecosystems. The objective of our study was to vary herbicide application rates in herbicide-tolerant canola to manipulate weed populations, and so test the hypothesis that A. bilineata activity density increases with greater vegetational heterogeneity.

2. Materials and methods 2.1. The study site and experimental design The study was conducted during 2003, 2004, and 2005 at the Agriculture and Agri-Food Canada Research Station, Lacombe, AB, Canada (113°440 W; 52°280 N). Soils at the site developed on glacial lacustrine deposited material (Bowser and Peters, 1951). Plots seeded to canola were on black Chernozemic clay loam soil (43% sand, 21% silt, and 36% clay) with a pH of 5.9 and 8.2% organic matter content. The experiment was duplicated in each year of the study by seeding new canola plots that were approximately 0.5 km from those of the preceding year. The experiment was a randomized complete block design with four replications involving factorial combinations of six herbicide application rates and two canola species. Plots of B. napus (cv. InVigor 2733) and B. rapa (cv. Hysyn 110) were seeded on 2 May 2003, 17 May 2004, and 10 May 2005 and were fertilized at 100% of the soil test recommendations for canola production. Plots measured 8  15 m and were seeded into cereal stubble with a ConservaPakÒ drill specialized for operating with minimal disturbance of the soil profile. Row spacings were 30.5 cm and the seeding density was 150 seeds m2. Seed was treated with HelixÒ (containing 10.3% thiamethoxam, 1.24% difenoconazole, 0.39% metalaxyl-M, and 0.135 fludioxonil) at the manufacturer’s recommended rate to reduce herbivory to seedlings by flea beetles (Phyllotreta spp.) (Coleoptera: Chrysomelidae). To simulate natural weed populations, tame oat (Avena sativa L.) was seeded at 100 seeds m2 perpendicular to the canola seed rows. Plots were separated within the blocks by 2 m of bare soil, and between blocks by a 15-m strip seeded with winter wheat (Triticum aestivum L.). Dicotyledonous weeds were removed from the plots through applications of MusterÒ (ethametsulfuron-methyl) and LontrelÒ (clopyralid) applied in-crop at 22 and 150 g active ingredient (a.i.) ha1, respectively. Herbicide rates for monocotyledonous weeds involved sethoxydim applied at 0%, 20%, 40%, 60%,

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80%, and 100% of the label rate of 200 g a.i. ha1 in 2003 and at 0%, 5%, 10%, 20%, 40%, and 100% of the label rate in 2004 and 2005 when canola was in the two- to three-leaf stage of development. Herbicides were applied in 110 l ha1 of water at 275 kPa using a sprayer equipped with flat-fan nozzles. Weed densities were determined for each plot approximately 48 h before and 20 days after the sethoxydim applications. All weed counts were obtained from four 0.5 m2 quadrats positioned diagonally across each plot. Population counts (plants m2) of monocotyledonous and dicotyledonous weeds were conducted concurrently, with weeds identified to species and their growth stages recorded. Biomass of weeds (kg ha1) was determined approximately 28 days after spraying from within the same four quadrats where the original pre-spray counts were performed. Weeds were cut off at the root–stem interface, sorted, bagged, labeled, and dried at 60 °C for 2 days before being weighed. 2.2. Insect sampling Pitfall traps were used each year to investigate activity dynamics of field populations of A. bilineata. One pitfall trap per plot was sampled in each canola plot in 2003, but two traps per plot were used in 2004 and 2005. Pitfall traps were established on 29 April 2003, 23 April 2004, and 22 April 2005. They were placed in random locations within the plots, except that they were at least 2 m in from the plot edges. Pitfall traps consisted of two GenPakÒ plastic cups, placed one inside the other. The bottom cup was placed into a hole 15 cm deep and 11 cm in diameter so the cup was at ground level. The second cup was placed within the first and the rim cut so that only a 2.5  2.5 cm tab remained above the soil surface. A 17  17 cm rain cap was placed about 5 cm above each trap. Pitfall traps were filled to a depth of 5 cm with propylene glycol. Pitfall trap collection and replacement occurred weekly. The inner sleeve components of the traps were removed from the field and taken to the laboratory for processing. There the trap contents were labeled as to collection date, plot number, and within-plot location and placed into 70% ethanol until specimens could later be sorted, identified, and data recorded. 2.3. Species identifications and voucher specimens Identifications of A. bilineata specimens were performed using Klimaszewski (1984) with representative species identifications verified by J. Klimaszewski (personal communication). Voucher specimens from the study have been deposited in the Strickland Museum of Entomology, University of Alberta, Edmonton, AB and at the Agriculture and Agri-Food Canada Research Centre in Lacombe, AB. 2.4. Statistical analyses Because of occasional losses of pitfall trap samples from excessive rainfall and flooding, A. bilineata trap captures were standardized for trapping effort (beetles per trap per day) prior to analysis. On each sampling date the two trap catches for each plot were combined and divided by the sum of the total number of trapping days. In addition, the beetle captures for all sampling dates were combined for each plot to obtain a total catch rate for the year. Beetle capture rates and weed densities were transformed [log10(x + 1)] before analysis to reduce heterogenous variances typical of pitfall trap data. The relationship between weed dry weight (independent variable) and activity density of A. bilineata (dependent variable) was investigated using linear regression analysis (PROC GLM,

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ESTIMATE option) (SAS Institute, Inc., 2004). Data were fitted to the linear model:

Y ¼ a þ bX

ð1Þ

where Y is A. bilineata activity density, X is weed biomass, a is the Y intercept, and b is an estimated regression coefficient. Trap captures of A. bilineata were transformed [log10(x + 1)], and compared over three years between the two canola species using PROC GLM (SAS Institute, Inc., 2004). There were six treatments in each plot, replicated four times. Ordination analysis was used to assess the responses of A. bilineata to habitats with varying weed populations, as influenced by the herbicide treatments at different application rates. Input variables consisted of a matrix of trap captures (all carabids and A. bilineata) versus treatment results expressed as weed dry weights. The analysis was similar to that of Bourassa et al. (2008). Several Carabidae (Coleoptera) species were captured in the pitfall traps in addition to A. bilineata, and although their species composition and community structure are not reported in this paper, we included some carabid activity density values in the ordination analysis to provide comparative balance for responses of A. bilineata to the various weed populations relative to other species in the beetle community. Non-metric multidimensional scaling (NMDS) analysis was performed using PCOrd to compare the beetle assemblages among treatments, a method that works well with ecological data sets that may not meet the assumption of normality (McCune and Mefford, 1999). In NMDS ordination plots, the distance between data points is directly proportional to species compositional dissimilarity (McCune and Grace, 2002). Sorensen (Bray–Curtis) distances were used to measure the dissimilarity matrix between samples. Starting coordinates were selected randomly, and 40 runs with a maximum of 400 iterations were performed using real data. This process was conducted initially with six dimensions, but in each subsequent cycle it was reduced by one dimension. The number of dimensions for the final ordination was selected when stress was not lowered by >5 and was near or below 20 (McCune and Grace, 2002). In NMDS, stress measures the distortion between the positions of real data points from the data presented graphically. Low stress represents few distortions and is associated with a graphic that more accurately represents the dissimilarities in species composition than high stress. A Monte Carlo probability was then calculated to evaluate whether the final stress associated with the ordinations differed from random. Species vectors were calculated using a minimum r2 of 0.300 and overlaid on the final ordination. The length and angle of the vector are an indication of the strength and direction of the species association, respectively. The relationship of A. bilineata activity density to canola species and weed populations of plots, as determined by herbicide application rates, was tested using multi-response permutation procedure (MRPP). MRPP tests the hypothesis of no difference between two or more groups, and is nonparametric so does not require assumptions of normality and homogeneity of variances (McCune and Grace, 2002). This procedure used Sorensen (Bray–Curtis) distances to calculate the test statistic, T, to describe the separation between groups, and the A statistic representing within-group homogeneity (McCune and Grace, 2002). Indicator Species Analysis was performed using PCOrd (McCune and Mefford, 1999) to evaluate the relative frequency and relative catch rate of A. bilineata, and to compare this among the predefined treatments. A perfect indicator of a particular group would be always present in that group. The result is then compared with a randomly achieved value using a Monte Carlo probability test. An indicator measure ranging from 0 (poor indicator) to 100 (best indicator) is then calculated with an associated P value from the

Monte Carlo test. Indicator Species Analysis is a natural companion analysis to multi-response permutation procedures, supplementing the test of no multivariate difference between groups with a description of how well each species separates among groups (McCune and Grace, 2002).

3. Results In total, 4100 specimens of A. bilineata were collected in the pitfall traps from 2003 to 2005 inclusive. Aleochara bilineata was the most abundant staphylinid species in the samples, but other relatively common species collected from this family included Aleochara verna Say, Dinaraea angustula (Gyllenhal), Philhygra subpolaris (Fenyes), Philonthus occidentalis Horn, Oxypoda robusticornis Bernhauer, Mocyta fungi (Gravenhorst), Mycetoporus lucidulus LeConte, Philhygra sp., and Lathrobium sp. In total 10,502 Staphylinidae were captured over the three years of trapping. A total of 14,025 carabid beetles were collected during 2003–2005. The 10 most abundant species captured over the three seasons represented 94.5% of total captures (Broatch, 2008). Those species were Pterostichus melanarius (Illiger) (56.7%), Agonum placidum (Say) (8.9%), Amara torrida (Panzer) (5.1%), Clivina fosser L. (5.4%), Amara quenseli (Schönherr) (4.7%), Amara littoralis Mannerheim (4.2%), Carabus granulatus L. (2.9%), Agonum cupreum Dejean (2.1%), Bembidion rupicola Kirby (1.5%), and Pterostichus adstrictus Eschscholtz (1.9%). Thirty species were represented by 10 or fewer specimens. Considerable variation was observed in weed populations in different sites and years. For instance, the monocot weed dry weights in untreated plots of B. rapa at Lacombe in 2004 were only 1.0% of those observed in 2003. In addition to populations of tame oat, monocotyledonous weed populations were comprised principally of wild oat (Avena fatua L.), foxtail barley (Hordeum jubatum L.), and green foxtail (Setaria viridis (L.) Beauv.). Herbicide application rate affected monocotyledonous plant populations, as represented by their dry weights with a decline in weed biomass as herbicide rate increased (Broatch et al., 2008b). Herbicide rate was responsible for most of the variation in weed biomass, with the median effective dose that eliminated 50% of the weed population lowest in 2003 and approximately three times greater in 2005 (Broatch et al., 2008b). However, reductions in weed biomass were not always proportional to the herbicide rate applied; for example, in 2003 weed biomass levels were similar with few weeds present in plots treated with herbicide at rates ranging from 20% to 100% of the label rate. As a consequence, herbicide application rates were altered during the 2004 and 2005 field seasons (from 20%, 40%, 60%, 80%, and 100% of the label rate in 2003 to 5%, 10%, 20%, 40%, and 100% of the label rate in 2004 and 2005), to achieve a broader range of background weed densities. Pitfall trap captures of A. bilineata were significantly greater in plots of B. rapa than in B. napus in all three years (F = 10.41, df = 5, 15, P < 0.01). A negative linear relationship was observed between monocotyledonous weed dry weight and A. bilineata activity density in 2003 and 2004 (Table 1). The relationship was highly significant when individual canola species data were combined for the three years of study, and when data for both canola species were grouped for all years of study (P < 0.001) (Table 1 and Fig. 1). Regression analysis found no significant relationship between dicotyledonous weed dry weight and A. bilineata activity density in any individual crop species or year (P > 0.05). In 2003, the best fit in the NMDS analysis was a two-dimensional plot (stress = 20.304; Monte Carlo Randomization Test P = 0.048). The r2 values for axes 1 and 2 were 0.384 and 0.406, respectively, explaining 79% of the variance in the data. Two dimensions provided the best reduction in stress in the Scree Plot analysis. Vectors representing A. bilineata (r2 = 0.600) were

J.S. Broatch et al. / Biological Control 52 (2010) 58–67 Table 1 Linear regression estimates for Aleochara bilineata activity density as a function of monocotyledonous weed dry weights recorded after herbicide application to Brassica napus and Brassica rapa at Lacombe, AB in 2003–2005. Year

Canola species

Regression estimatesa

P value

a

b

r2

2003 2003

B. rapa B. napus

1.21 —

0.14 —

0.30 —

0.006 Ns

2004 2004

B. rapa B. napus

1.99 1.91

0.18 0.34

0.25 0.35

0.010 0.002

2005 2005

B. rapa B. napus

— —

— —

— —

Ns Ns

Combined 2003–2005 Combined 2003–2005 Combined 2003–2005

B. rapa B. napus B. rapa and B. napus

1.80 1.61 1.70

0.36 0.37 0.35

0.33 0.28 0.28

<0.001 <0.001 <0.001

a Data were fitted to Eq. (1) (see text). Regression estimates are not presented where results were not significant (Ns) statistically (P > 0.05).

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generally directed toward treatments where herbicide was applied at 20–80% of the registered rate (Fig. 2). For comparative purposes, vectors representing the carabid beetle, C. granulatus L., are also included. MRPP analysis to determine the importance of canola species for governing beetle species assemblages was significant (T = 4.324, A = 0.050, P < 0.001) (Table 2). Herbicide treatment did not have a significant effect on overall beetle species composition. In 2004, the best fit in the NMDS analysis was a two-dimensional plot (stress = 16.383, Monte Carlo Randomization Test P = 0.039). The coefficients of determination (r2) of axes 1 and 2 were 0.355 and 0.501, respectively, explaining nearly 86% of the variation in the data. Species vectors, calculated with a minimum r2 of 0.300 and overlaid on the final ordination, indicated that A. bilineata communities were most often directed toward plots subjected to herbicide treatments at 40–100% of the label rate (Fig. 3). For comparative purposes, vectors representing the carabid beetle, P. melanarius (Illiger), are also included. The MRPP analysis found

Fig. 1. Activity density responses of Aleochara bilineata to monocotyledonous weed dry weights in Brassica rapa, Brassica napus, and both B. rapa and B. napus at Lacombe during 2003–2005. Data were fitted to Eq. (1) (see text), and curves are based on regression estimates presented in Table 1.

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significant effects of canola species (T = 4.95, A = 0.067, P < 0.001) and herbicide treatment (T = 1.83, A = 0.058, P = 0.046) on beetle composition (Table 2). Indicator Species Analysis determined that A. bilineata was strongly associated with the herbicide treatment applied at 100% of the label rate (indicator value = 23.8, P = 0.006) (Table 3). Preference was shown by A. bilineata for B. rapa (indicator value = 58.1, P = 0.01).

In 2005 the best fit in the NMDS analysis was a two-dimensional plot with a stress of 8.265 (Monte Carlo Randomization Test, P = 0.0196). The coefficients of determination (r2) for the axes were 0.427 and 0.536, respectively, which together explained 96.4% of the variation in the data. Vectors representing A. bilineata were generally directed away from quadrats with higher weed biomass (no herbicide applied or a low rate applied), indicating a preferred

Fig. 2. Non-metric multidimensional scaling ordination for assemblages of Carabidae and the staphylinid Aleochara bilineata captured in plots of Brassica rapa and Brassica napus subjected to herbicide at different application rates in 2003. Vectors (minimum r2 = 0.3) represent the non-metric multidimensional scaling values for the species identified in the figure.

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J.S. Broatch et al. / Biological Control 52 (2010) 58–67 Table 2 Multi-response permutation procedure (MRPP) estimates for comparisons between canola species and herbicide application rate for each year of the study. Year

Treatment

MRPP estimates T

A

P

2003

Canola species Herbicide rate

4.324 —

0.050 —

<0.001 Ns

2004

Canola species Herbicide rate

4.95 1.83

0.067 0.058

<0.001 0.046

2005

Canola species Herbicide rate

5.038 —

0.048 —

<0.01 Ns

Table 3 Results of Indicator Species Analysis performed to identify associations of the staphylinid, Aleochara bilineata and canola species and herbicide (sethoxydim) treatment for each year of the study. Only those associations are presented where P 6 0.05. Year

Canola species or herbicide rate

Indicator species value

P value

2004 2005 2004

B. rapa B. rapa 100% rate

58.1 65.2 23.8

0.010 0.013 0.006

association for habitats with lower weed densities (Fig. 4). MRPP analysis did not show any beetle species responses to the herbicide treatment in 2005. However, canola species responses were significant (T = 5.038, A = 0.048, P < 0.01) (Table 2). Indicator Species Analysis determined that A. bilineata responded to B. rapa (indicator value = 65.2, P = 0.013) (Table 3). 4. Discussion

Fig. 3. Non-metric multidimensional scaling ordination for assemblages of Carabidae and the staphylinid Aleochara bilineata captured in plots of Brassica rapa and Brassica napus subjected to herbicide at different application rates in 2004. Vectors (minimum r2 = 0.3) represent the non-metric multidimensional scaling values for the species identified in the figure.

Activity density of A. bilineata declined with an increase in monocotyledonous weed biomass in both B. rapa and B. napus (Table 1 and Fig. 1). Somewhat similar observations were reported by Dixon et al. (2004) with A. bilineata captured in higher numbers in bare plots of rutabaga (B. napus var. napobrassica) than in plots with rutabaga undersown to clover (Trifolium repens L.). Dixon et al. (2004) recorded analogous results from pitfall trap captures of A. bilineata and from rearing D. radicum puparia to determine levels of parasitism, and both methods indicated that the predator–parasitoid was more prevalent in rutabaga monocultures. Such observations of habitat preferences may result from the chemical signals emitted by canola plants and the root maggot hosts of A. bilineata. Royer and Boivin (1999) found that A. bilineata adults are attracted to volatiles associated with D. radicum and to volatiles produced by its brassicaceous host plants. In plots with low densities of monocotyledonous weeds, volatile signals emitted by canola or root maggot larvae may be stronger because of reduced interference with weed volatiles, and this could result in greater trap captures of A. bilineata in those plots. Neveu et al. (2002) found that when the roots of brassicaceous plants are attacked by D. radicum, the plants emit volatile compounds that attract Trybliographa rapae (Westwood), a hymenopteran parasitoid of D. radicum. If such volatile compounds exert a similar attraction to A. bilineata, it could also help explain higher A. bilineata populations in plots with low weed densities. Canola grown in association with low densities of weeds is subjected to greater infestations by Delia spp. (Dosdall et al., 2003; Broatch et al., 2008b). By aggregating where prey and mates are available, A. bilineata may minimize energy costs associated with resource foraging. The mechanism responsible for lowered populations of A. bilineata in canola plots with higher populations of weeds is not clear, but it could reflect stronger attraction of the staphylinid to pure stands of canola, or it could be an indirect effect of competitive interspecific or intraguild interactions. Marshall et al. (2003) suggested that staphylinid beetles tended to be reduced in activity density captures in weedy situations as a response to competition from Carabidae. Prasad and Snyder (2006a,b) found that the large carabid beetle, P. melanarius, could lower the activity density of A. bilineata and other small Carabidae, not by reducing actual numbers of individuals, but by decreasing their activity. Pterostichus melanarius was the most populous contributor to the carabid beetle community in this study (Broatch, 2008), so the possibility exists that some reductions in A. bilineata activity density are attributable to activities of this carabid. However, no evidence was found for greater abundances of P. melanarius in plots with higher weed populations (Broatch, 2008), so it is likely that the

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Fig. 4. Non-metric multidimensional scaling ordination for assemblages of Carabidae and the staphylinid Aleochara bilineata captured in plots of Brassica rapa and Brassica napus subjected to herbicide at different application rates in 2005. Vectors (minimum r2 = 0.3) represent the non-metric multidimensional scaling values for the species identified in the figure.

salient results reported here are not simply a response to P. melanarius activity density. Competitive interspecific or intraguild interactions could not be measured with the pitfall trapping regime employed here; however, such interactions must be considered as important ecological variables in future community ecosystem studies.

In each year of our study, canola species had a significant effect on A. bilineata populations, as determined in the Indicator Species Analysis (Table 2). Significantly higher numbers of A. bilineata were captured in B. rapa in two of the three years of this study, and A. bilineata was an indicator species for B. rapa in 2004 and 2005 (Table 3). When grown under analogous conditions, Delia spp. females

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deposit more eggs on plants of B. rapa than on B. napus, and larval populations and root damage by Delia spp. are greater to plants of B. rapa than B. napus (Dosdall et al., 1994, 1998). Higher trap captures of A. bilineata in B. rapa plots are therefore associated with greater prey availability, but it is unclear whether this response represents an attraction to the host plant itself or to indirect characteristics associated with this host plant like microhabitat alteration affecting prey availability, shelter, microclimate, or combinations of these (Landis et al., 2000, 2005). In ecologically simple landscapes, like crop monocultures, parasitoids may encounter less challenge in locating and attacking hosts than in more complex, dynamic communities and landscapes (Gols et al., 2005). As a consequence, parasitoids can overexploit populations of their hosts in simple landscapes, leading to unstable boom-and-bust cycles of both host and parasitoid populations (Hawkins, 1994). Reduced foraging efficiency with increased habitat complexity has been reported for predators and parasitoids in other systems (e.g., Huffaker et al., 1963; Ellner et al., 2001; Gols et al., 2005), but it is unknown whether A. bilineata forages less efficiently when plant biodiversity is increased, or whether the species simply tends to aggregate in brassicaceous monocultures. Further studies should be conducted in this system to determine predation and parasitism rates by A. bilineata in monocultures versus more vegetationally diverse habitats. This study utilized pitfall trapping for comparing A. bilineata responses to the different weed density plots, a sampling approach selected because it is inexpensive, labor-efficient, and convenient. Pitfall trap data can be less than optimal because collections can be influenced by various environmental factors and the number and arrangement of the traps (Ericson, 1979; Greenslade, 1964; Honêk, 1988; Niemalä et al., 1986; Raworth and Choi, 2001; Spence and Niemalä, 1994). Nevertheless, the samples reflect activity and density of the beetles (Thiele, 1977; Luff, 1982), and the technique does allow collections of beetles in numbers suitable for rigorous statistical analyses (Spence and Niemalä, 1994), which are important considerations because there are no reasonable sampling alternatives for most studies (Kowalski, 1975). Moreover, pitfall traps have proven quite useful as population indices for comparisons of epigaeic beetle activity between years and across similar habitats (Mitchell, 1963; Niemalä et al., 1990), which were important objectives of this study. We found that activity density of the specialist predator–parasitoid, A. bilineata, declined with increases in vegetational diversity, but it is not clear from our study whether overall predation of root maggots was affected by plant biodiversity. Approximately 60 species of Carabidae have been found associated with canola from this study site (Broatch, 2008), and several of these carabids, like Bembidion spp., are known to prey on Delia spp., especially the eggs (Wishart et al., 1956; Coaker, 1966; Ryan and Ryan, 1980). It is possible, therefore, that low root maggot predation and parasitism by A. bilineata in situations with high weed biomass could be balanced by greater carabid predation. Our results suggest directions for future research to better understand interactions among the different members of the root maggot natural enemy community in canola agroecosystems. Herbicide applications are sometimes known to directly affect insect populations, and therefore the possibility exists that activity density of A. bilineata may have been affected by the herbicides used in this study. For instance, Laster et al. (1984) reported that field applications of the herbicide dinoseb had insecticidal activity against thrips (Frankliniella spp.) and tarnished plant bug nymphs (Lygus lineolaris (Palisot de Beauvois)) in cotton. An increase in the reproductive rate of pea aphid (Acyrthosiphon pisum Harris) occurred on broad beans following application of 2,4-D (Maxwell and Harwood, 1960). Further laboratory study is needed to evaluate the

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herbicides used in this study for potential direct effects on A. bilineata; however, it is unlikely that the herbicides negatively affected their populations because activity density of the staphylinid was highest in plots subjected to applications of the greatest quantities of herbicide. Our study was designed to investigate responses of A. bilineata to canola associated with monocotyledonous weeds, and we simulated infestations of wild oat (A. fatua), the most common weed species in western Canada. Further study is needed to address effects of dicotyledonous weeds on A. bilineata activity density because responses of the predator–parasitoid may have varied depending on the dicotyledonous weed complex involved. For instance, many brassicaceous weed species serve as suitable host plants for Delia spp. (Finch and Ackley, 1977), so large infestations of such species may actually increase populations of A. bilineata. The widespread adoption of genetically engineered herbicidetolerant canola varieties by several countries worldwide can enable producers to manipulate weed populations in these crops. A simplistic interpretation of our results suggests that root maggot control in this crop would benefit if farmers minimized weed populations thereby increasing activity density levels of A. bilineata. However, previous research has shown that maintaining small weed populations in canola results in less root maggot oviposition and damage (Dosdall et al., 2003; Broatch et al., 2008b). Monocotyledonous weed populations appear to minimize opportunities for females of D. radicum to complete the behavioral sequence required for oviposition in canola, leading to reduced infestation levels in weedy systems. Considering the interactions among the A. bilineata predator–parasitoid, its root maggot prey, weeds, and agronomic variables that also influence root maggot infestations like crop species and variety, tillage regime, plant density, row spacing, and fertility regime (Dosdall et al. 1996, 1998, 2004), it is evident that such relationships are much more complex than they may appear initially. Developing recommendations that can be adopted by producers should therefore most appropriately involve an integrated approach that considers and ranks all such factors in the ecoregion under consideration. The trade-off in the benefit derived from small weed infestations from disruption of oviposition by D. radicum in canola crops versus the benefits from predation and parasitism by A. bilineata on root maggots in weedreduced systems should be investigated to enable growers to implement optimal integrated crop management in regions where infestations of root maggots are the most significant limiting factor in canola production.

Acknowledgments We are grateful to B. Pocock, L. Michielsen, P. Reid, J. Zuidhof, and E. Hartman of Agriculture and Agri-Food Canada for technical assistance in the field and laboratory. We thank S. Bourassa and J. Hummel for assistance with performing ordination analysis. This study was funded by the Western Grains Research Foundation, the Alberta Canola Producers Commission, Agriculture and AgriFood Canada, Alberta Agriculture and Rural Development, and the University of Alberta.

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