Agriculture, Ecosystems and Environment 103 (2004) 595–599

Aphid response to vegetation diversityand insecticide applications

J.E. Banksa,∗, J.D. Starkba Interdisciplinary Arts and Sciences, University of Washington, Tacoma, 1900 Commerce Street, Tacoma, WA 98402, USA

b Department of Entomology, Puyallup Research and Extension Center, Washington State University,7612 Pioneer Way E., Puyallup, WA 98371, USA

Received 12 December 2002; received in revised form 21 October 2003; accepted 4 November 2003

Abstract

A field experiment was conducted to determine the effects of vegetation diversity and pesticide disturbance on insect herbi-vore populations in a broccoli agroecosystem. Varying concentrations of the selective insecticide imidacloprid were applied topatches of broccoli surrounded by bare ground or weedy vegetation during one growing season in western Washington (USA).Aphids responded to an interaction between vegetation diversity and pesticide concentration, and their response varied as afunction of time after pesticide disturbance. These results suggest that simplistic, linear predictions of the effects of chemicaldisturbance and natural enemies on insect herbivore populations will not be forthcoming.© 2003 Elsevier B.V. All rights reserved.

Keywords:Aphids; Habitat heterogeneity; Imidacloprid; Weed intercrop

1. Introduction

Vegetation diversity has long been regarded as im-portant in insect population regulation, especially forherbivorous insects (Cromartie, 1975; Bach, 1980;Perfecto, 1992; Banks, 1998). Increased plant diver-sity in agroecosystems has been frequently touted asa means of reducing herbivore populations, either bydiminishing herbivore colonization and tenure-timeon host plants, or bolstering natural enemy popula-tions (Root, 1973; Vandermeer, 1989; Landis et al.,2000). Despite promising results in many field tri-als, surveys of hundreds of experiments testing theeffects of increased vegetation diversity on herbi-

∗ Corresponding author. Tel.:+1-253-692-5838;fax: +1-253-692-5718.E-mail address:banksj@u.washington.edu (J.E. Banks).

vore populations have revealed a modest effect atbest (Andow, 1991; Tonhasca and Byrne, 1994). Inresponse to increasing global concerns over envi-ronmental and public health risks associated withtraditional, broad spectrum pesticides, a new suite ofmore selective pesticides are being developed. Thesenew pesticides are designed to target only certaininsect taxa, leaving the remainder of biological com-munities largely intact. This facilitates combinationsof pesticide-imposed disturbances working in con-cert with biotic factors to regulate insect herbivorepopulations. Of particular interest within the realmof biological control applications is the possibilityof incorporating arthropod natural enemies into inte-grated pest management (IPM) schemes. Field stud-ies have demonstrated that combinations of two ormore natural enemies may act in an additive fashion(Chang, 1996), in a sub-additive fashion (Rosenheim

0167-8809/$ – see front matter © 2003 Elsevier B.V. All rights reserved.doi:10.1016/j.agee.2003.11.005

596 J.E. Banks, J.D. Stark / Agriculture, Ecosystems and Environment 103 (2004) 595–599

et al., 1993) or synergistically (Losey and Denno,1998).

The field experiment described here explored the ef-fects of selective pesticide disturbance combined withincreased vegetation diversity. Aphid densities wererecorded on broccoli plants that had been sprayed withdifferent concentrations of selective pesticide in plotssurrounded by either weedy vegetation or bare ground.

2. Materials and methods

The field experiment was conducted during summer1999 at Washington State University’s Puyallup Re-search and Extension Center Experimental Farm Five,70 km south of Seattle, WA, USA. Plots of broccoli(Brassica oleraceaL., var. Emporer F1, Zenner Bros.,OR) were established from seed in planting flats andkept in a greenhouse until large enough to transplantinto the field in June. Broccoli were planted in groupsof 16 plants in square plots measuring 2.5 m× 2.5 m,surrounded by 1 m wide margins of either (a) weedyvegetation or (b) bare ground. All broccoli plants werespaced 0.5 m apart within plots. Species in weedymargins were mainlyAmaranthus powellii(S. Wat-son),Chenopodium album(L.), Cirsium arvense(L.),Echinochloa coluna(L.) andE. crus-galli(L.). On 23July, 13 and 27 August, broccoli in each type of mar-gin plot were subjected to either (i) no pesticide spray,(ii) 15 g ai/ha, or (iii) 30 g ai/ha imidacloprid insecti-cide. Spraying on each date occurred by hand with abackpack sprayer early in the morning with little or nobreeze. Experimental plots were set up in three differ-ent fields, with two replicates of each treatment in eachfield for a total of 36 experimental plots. Within eachfield, experimental plots were placed at least 5.5 mapart.

Analyses were performed on the density of theaphid species (Hemiptera: Aphididae) common onfield broccoli. The main aphid species at the site wereMyzus persicae(Sulzer),Brevicoryne brassicae(L.),and Aphis fabae(Scopoli). Weedy vegetation withinbroccoli plots was mechanically removed throughoutthe duration of the experiments. Plots were wateredregularly, and dead or missing plants were replacedby similar sized plants kept in the greenhouse.

Aphids on eight plants per plot were visually cen-sused 4, 7, and 10 days after each application. All

aphids on both sides of broccoli leaves and all otherplant surfaces were counted. On 3 August, mid-waythrough the experiment, length and height of eightplants per plot were measured to calculate the meancylindrical volume of plants in each plot.

Response of aphids to treatments was analyzed byapplying multivariate analysis of variance (MANOVA)to aphid densities. MANOVA was applied to the meannumber of aphids/m3 plant per treatment, with the ninecensus dates as the multiple variable (von Ende, 2001;Scheiner, 2001). Mean aphid densities 4, 7, and 10days after spraying were log transformed (log(x + 1))and analyzed separately. To accommodate possible bi-ases due to soil moisture, microclimate, etc. in differ-ent blocks in the field, a general linear model (SPSS,2000) was used with replicates included as a possiblesource of variation. A profile analysis of aphid den-sities found to have significant responses to treatmentmanipulations in the MANOVA was performed.

3. Results

Margin type had a significant effect on aphid densityacross the duration of the experiment (Table 1). Meanaphid densities over all nine census dates followedthis pattern, with more aphids (210/m3) close to bareground than to weedy margins (166/m3). There wasa strong interaction between margin type and spraydisturbance level (Table 1).

Results broken down by number of days after spray-ing revealed that aphids responded strongly to margintype 4 days after sprays, and both margin type andspray intensity 10 days after sprays, whereas at 7 daysafter sprays they responded to margin type, spray, andthe interaction between the two (Table 2).

The overall parallel trend (Fig. 1) illustrates thesignificant treatment differences. One-way MANOVArevealed no significant results (Wilk’s lambda=Table 1Effects of vegetation margin and insecticide application on numberof aphids/m3 broccoli across the entire season

Treatment factor Wilk’slambda

F d.f. P

Block 0.000 12.946 18, 4 0.013Margin type 0.002 100.946 9, 2 0.010Spray concentration 0.005 3.033 18, 4 0.146Margin× spray 0.001 8.323 18, 4 0.026

J.E. Banks, J.D. Stark / Agriculture, Ecosystems and Environment 103 (2004) 595–599 597

Table 2Effects of vegetation margin and insecticide application on numberof aphids/m3 broccoli for varying lengths of time after insecticideapplication

Wilk’slambda

F d.f. P

Four days after insecticide applicationBlock 0.250 2.671 6, 16 0.054Margin type 0.196 10.928 3, 8 0.003Spray concentration 0.256 2.607 6, 16 0.059Margin× spray 0.422 1.439 6, 16 0.261

Seven days after insecticide applicationBlock 0.031 12.502 6, 16 0.000Margin type 0.109 21.689 3, 8 0.000Spray concentration 0.094 6.012 6, 16 0.002Margin× spray 0.112 5.304 6, 16 0.003

Ten days after insecticide applicationBlock 0.066 7.659 6, 16 0.001Margin type 0.25 7.991 3, 8 0.009Spray concentration 0.147 4.288 6, 16 0.009Margin× spray 0.441 1.348 6, 16 0.294

0.525,F8,9 = 1.019,P = 0.484), indicating that theoverall treatment differences were consistent acrosstime. Finally, measurements of plant volumes atmid-experiment revealed that plants in weedy marginplots were on average significantly larger (0.169 m3)than plants in bare ground plots (0.127 m3) (z-test,P < 0.01).

0

100

200

300

400

500

27-J

ul

30-J

ul

2-Aug

17-A

ug

20-A

ug

23-A

ug

31-A

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/m3 b

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co

li

Bare ground, no spray

Bare ground, low spray

Bare ground, high spray

Weedy, no spray

Weedy, low spray

Weedy, high spray

Fig. 1. Profile plot for different treatments across the duration of the experiment, each point being the mean of three samples.

4. Discussion

The present results are consistent with results indi-cating that plots with weedy margins harbored feweraphid pests in mid-season samples (Banks, 2000). Thetime-series data from the current study give a morecomplex portrait of aphid population response acrossthe entire growing season—in particular, there was aninteraction between margin type and pesticide strength7 days after spraying that was not present earlier orlater in the spray cycle. This may reflect the nature ofthe insecticide mode of action—at 4 days after sprays,sufficient amounts of toxins may not have been in-gested to directly affect aphid population numbers (asevidenced by their lack of a significant response tospray concentration, but a strong response to margintype). At 10 days after sprays there were significantmain effects (margin type and spray concentration)only (i.e. no interaction between the two). At 7 daysafter sprays, however, the effect of the sprays may havereached a critical threshold rendering aphids morevulnerable to predators in weedy margin plots—thusyielding a significant interaction in margin type andspray treatments. The strong interaction between mar-gin type and pesticide spray level highlights the needto analyze population data across time and in an ap-propriate landscape context to assess the effects of tox-icants on field populations. The results illustrate the

598 J.E. Banks, J.D. Stark / Agriculture, Ecosystems and Environment 103 (2004) 595–599

difficulties of developing generalizable protocols fordeploying combinations of vegetation diversity and se-lective pesticides.

There are alternatives to interpreting the results ofthis field experiment as strictly due to the synergisticeffect of pesticide applications and weedy field mar-gins. First, differences in vegetation species diversityand composition may result in differences in micro-climate (e.g. moisture, temperature) in experimentalplots (Kuemmel, 2003). Combinations of tempera-ture, moisture, and soil structure in weedy versus bareground margin plots may have contributed to differ-ences in plant sizes and palatability. Second, recentstudies have shown that “selective” pesticides suchas imidacloprid can be harmful to non-target insects,including parasitoids (Brunner et al., 2001; Smithand Krischik, 1999; Stark and Banks, 2001). In ad-dition, resistance to imidacloprid by both target andnon-target organisms has recently been documentedin various field settings (Blom et al., 2002; Nauenand Elbert, 2003) and should be considered in fieldapplications. Finally, the spatial scale of experimentalplots may affect arthropod behavior and distribution(Marino and Landis, 1996; Banks, 1998; Banks andYasenak, 2003; Bommarco and Banks, 2003). Thepresent results illustrate the difficulties in predictingthe outcome of combinations of factors governing in-sect herbivore dynamics. They also highlight the needfor further investigations, including detailed physio-logical and behavioral experiments as well as fieldexperiments conducted at different spatial scales andfrom a broader community-level perspective.

Acknowledgements

Thanks to S. Hopkins, C. Yasenak, D. Matheson andR. Schwinkendorf for assistance in the field. The au-thors also thank two anonymous reviewers for helpfulcomments on an earlier version of the manuscript. Thisproject was supported by a USDA CSREES PMAPgrant (97-04104) to J.E.B. and J.D.S.

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