Aphid response to vegetation diversity and insecticide applications

Aphid response to vegetation diversity and insecticide applications

Agriculture, Ecosystems and Environment 103 (2004) 595–599 Aphid response to vegetation diversity and insecticide applications J.E. Banks a,∗ , J.D. ...

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

Aphid response to vegetation diversity and insecticide applications J.E. Banks a,∗ , J.D. Stark b a

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 herbivore populations in a broccoli agroecosystem. Varying concentrations of the selective insecticide imidacloprid were applied to patches 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 a function of time after pesticide disturbance. These results suggest that simplistic, linear predictions of the effects of chemical disturbance 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 important in insect population regulation, especially for herbivorous insects (Cromartie, 1975; Bach, 1980; Perfecto, 1992; Banks, 1998). Increased plant diversity in agroecosystems has been frequently touted as a means of reducing herbivore populations, either by diminishing herbivore colonization and tenure-time on host plants, or bolstering natural enemy populations (Root, 1973; Vandermeer, 1989; Landis et al., 2000). Despite promising results in many field trials, surveys of hundreds of experiments testing the effects of increased vegetation diversity on herbi∗ Corresponding author. Tel.: +1-253-692-5838; fax: +1-253-692-5718. E-mail address: [email protected] (J.E. Banks).

vore populations have revealed a modest effect at best (Andow, 1991; Tonhasca and Byrne, 1994). In response to increasing global concerns over environmental and public health risks associated with traditional, broad spectrum pesticides, a new suite of more selective pesticides are being developed. These new pesticides are designed to target only certain insect taxa, leaving the remainder of biological communities largely intact. This facilitates combinations of pesticide-imposed disturbances working in concert with biotic factors to regulate insect herbivore populations. Of particular interest within the realm of biological control applications is the possibility of incorporating arthropod natural enemies into integrated pest management (IPM) schemes. Field studies have demonstrated that combinations of two or more 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


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 effects of selective pesticide disturbance combined with increased vegetation diversity. Aphid densities were recorded on broccoli plants that had been sprayed with different concentrations of selective pesticide in plots surrounded by either weedy vegetation or bare ground.

2. Materials and methods The field experiment was conducted during summer 1999 at Washington State University’s Puyallup Research and Extension Center Experimental Farm Five, 70 km south of Seattle, WA, USA. Plots of broccoli (Brassica oleracea L., var. Emporer F1, Zenner Bros., OR) were established from seed in planting flats and kept in a greenhouse until large enough to transplant into the field in June. Broccoli were planted in groups of 16 plants in square plots measuring 2.5 m × 2.5 m, surrounded by 1 m wide margins of either (a) weedy vegetation or (b) bare ground. All broccoli plants were spaced 0.5 m apart within plots. Species in weedy margins were mainly Amaranthus powellii (S. Watson), Chenopodium album (L.), Cirsium arvense (L.), Echinochloa coluna (L.) and E. crus-galli (L.). On 23 July, 13 and 27 August, broccoli in each type of margin plot were subjected to either (i) no pesticide spray, (ii) 15 g ai/ha, or (iii) 30 g ai/ha imidacloprid insecticide. Spraying on each date occurred by hand with a backpack sprayer early in the morning with little or no breeze. Experimental plots were set up in three different fields, with two replicates of each treatment in each field for a total of 36 experimental plots. Within each field, experimental plots were placed at least 5.5 m apart. Analyses were performed on the density of the aphid species (Hemiptera: Aphididae) common on field broccoli. The main aphid species at the site were Myzus persicae (Sulzer), Brevicoryne brassicae (L.), and Aphis fabae (Scopoli). Weedy vegetation within broccoli plots was mechanically removed throughout the duration of the experiments. Plots were watered regularly, and dead or missing plants were replaced by similar sized plants kept in the greenhouse. Aphids on eight plants per plot were visually censused 4, 7, and 10 days after each application. All

aphids on both sides of broccoli leaves and all other plant surfaces were counted. On 3 August, mid-way through the experiment, length and height of eight plants per plot were measured to calculate the mean cylindrical volume of plants in each plot. Response of aphids to treatments was analyzed by applying multivariate analysis of variance (MANOVA) to aphid densities. MANOVA was applied to the mean number of aphids/m3 plant per treatment, with the nine census dates as the multiple variable (von Ende, 2001; Scheiner, 2001). Mean aphid densities 4, 7, and 10 days after spraying were log transformed (log(x + 1)) and analyzed separately. To accommodate possible biases due to soil moisture, microclimate, etc. in different blocks in the field, a general linear model (SPSS, 2000) was used with replicates included as a possible source of variation. A profile analysis of aphid densities found to have significant responses to treatment manipulations in the MANOVA was performed. 3. Results Margin type had a significant effect on aphid density across the duration of the experiment (Table 1). Mean aphid densities over all nine census dates followed this pattern, with more aphids (210/m3 ) close to bare ground than to weedy margins (166/m3 ). There was a strong interaction between margin type and spray disturbance level (Table 1). Results broken down by number of days after spraying revealed that aphids responded strongly to margin type 4 days after sprays, and both margin type and spray intensity 10 days after sprays, whereas at 7 days after sprays they responded to margin type, spray, and the interaction between the two (Table 2). The overall parallel trend (Fig. 1) illustrates the significant treatment differences. One-way MANOVA revealed no significant results (Wilk’s lambda = Table 1 Effects of vegetation margin and insecticide application on number of aphids/m3 broccoli across the entire season Treatment factor

Wilk’s lambda




Block Margin type Spray concentration Margin × spray

0.000 0.002 0.005 0.001

12.946 100.946 3.033 8.323

18, 4 9, 2 18, 4 18, 4

0.013 0.010 0.146 0.026

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

4. Discussion

Table 2 Effects of vegetation margin and insecticide application on number of aphids/m3 broccoli for varying lengths of time after insecticide application Wilk’s lambda




Four days after insecticide application Block 0.250 2.671 Margin type 0.196 10.928 Spray concentration 0.256 2.607 Margin × spray 0.422 1.439

6, 3, 6, 6,

16 8 16 16

0.054 0.003 0.059 0.261

Seven days after insecticide application Block 0.031 12.502 Margin type 0.109 21.689 Spray concentration 0.094 6.012 Margin × spray 0.112 5.304

6, 3, 6, 6,

16 8 16 16

0.000 0.000 0.002 0.003

Ten days after insecticide Block Margin type Spray concentration Margin × spray

6, 3, 6, 6,

16 8 16 16

0.001 0.009 0.009 0.294

application 0.066 0.25 0.147 0.441

7.659 7.991 4.288 1.348

The present results are consistent with results indicating that plots with weedy margins harbored fewer aphid pests in mid-season samples (Banks, 2000). The time-series data from the current study give a more complex portrait of aphid population response across the entire growing season—in particular, there was an interaction between margin type and pesticide strength 7 days after spraying that was not present earlier or later in the spray cycle. This may reflect the nature of the insecticide mode of action—at 4 days after sprays, sufficient amounts of toxins may not have been ingested to directly affect aphid population numbers (as evidenced by their lack of a significant response to spray concentration, but a strong response to margin type). At 10 days after sprays there were significant main effects (margin type and spray concentration) only (i.e. no interaction between the two). At 7 days after sprays, however, the effect of the sprays may have reached a critical threshold rendering aphids more vulnerable to predators in weedy margin plots—thus yielding a significant interaction in margin type and spray treatments. The strong interaction between margin type and pesticide spray level highlights the need to analyze population data across time and in an appropriate landscape context to assess the effects of toxicants on field populations. The results illustrate the

0.525, F8,9 = 1.019, P = 0.484), indicating that the overall treatment differences were consistent across time. Finally, measurements of plant volumes at mid-experiment revealed that plants in weedy margin plots were on average significantly larger (0.169 m3 ) than plants in bare ground plots (0.127 m3 ) (z-test, P < 0.01).

Mean no. aphids/m 3 broccoli


400 Bare ground, no spray Bare ground, low spray Bare ground, high spray Weedy, no spray Weedy, low spray Weedy, high spray




7Se p

3Se p

Au g 31 -

Au g 23 -

Au g 20 -

Au g 17 -

2Au g

Ju l 30 -

Ju l

0 27 -


Census date

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


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

difficulties of developing generalizable protocols for deploying combinations of vegetation diversity and selective pesticides. There are alternatives to interpreting the results of this field experiment as strictly due to the synergistic effect of pesticide applications and weedy field margins. First, differences in vegetation species diversity and composition may result in differences in microclimate (e.g. moisture, temperature) in experimental plots (Kuemmel, 2003). Combinations of temperature, moisture, and soil structure in weedy versus bare ground margin plots may have contributed to differences in plant sizes and palatability. Second, recent studies have shown that “selective” pesticides such as imidacloprid can be harmful to non-target insects, including parasitoids (Brunner et al., 2001; Smith and Krischik, 1999; Stark and Banks, 2001). In addition, resistance to imidacloprid by both target and non-target organisms has recently been documented in various field settings (Blom et al., 2002; Nauen and Elbert, 2003) and should be considered in field applications. Finally, the spatial scale of experimental plots may affect arthropod behavior and distribution (Marino and Landis, 1996; Banks, 1998; Banks and Yasenak, 2003; Bommarco and Banks, 2003). The present results illustrate the difficulties in predicting the outcome of combinations of factors governing insect herbivore dynamics. They also highlight the need for further investigations, including detailed physiological and behavioral experiments as well as field experiments conducted at different spatial scales and from a broader community-level perspective.

Acknowledgements Thanks to S. Hopkins, C. Yasenak, D. Matheson and R. Schwinkendorf for assistance in the field. The authors also thank two anonymous reviewers for helpful comments on an earlier version of the manuscript. This project was supported by a USDA CSREES PMAP grant (97-04104) to J.E.B. and J.D.S.

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