Myzus Persicae) (Sulz.), Citrus Mealybug (Planococcus Citri) (Risso

ARTICLE IN PRESS

Crop Protection xxx (2009) 1–14

Contents lists available at ScienceDirect

Crop Protection

journal homepage: www.elsevier.com/locate/cropro

Suppression of green peach aphid (Myzus persicae) (Sulz.), citrus mealybug (Planococcus citri) (Risso), and two spotted spider mite (Tetranychus urticae) (Koch.) attacks on tomatoes and cucumbers by aqueous extracts from vermicomposts

Clive A. Edwards a,*, Norman Q. Arancon b, Marcus Vasko-Bennett a, Ahmed Askar a, George Keeney a, Brandon Little a a Soil Ecology Laboratory, The Ohio State University, 400 Stanley Aronoff Laboratory, 318W. 12th Avenue, Columbus, OH 43210, USA b University of Hawaii at Hilo, 200W. Kawili St., Hilo, HI 97620, USA article info abstract

Article history: Vermicomposts are produced through interactions between earthworms and microorganisms in the Received 24 April 2009 breakdown of organic wastes. Aqueous extracts were prepared in commercial brewing equipment Received in revised form (Growing Solutions Inc.) from vermicomposts processed from pre-consumer food waste. The ratio of 14 August 2009 vermicompost to water was 1 to 5 v:v to produce a 20% aqueous solution. The effects of soil drenches at Accepted 21 August 2009 dilutions of 20%, 10%, and 5% vermicompost extracts, were compared with those of deionized water, in the suppression of green peach aphids, mealybugs, and two spotted spider mites attacking tomatoes and Keywords: cucumbers, in greenhouse cage experiments. Citrus mealybugs Green peach aphids Tomatoes and cucumber seedlings were germinated and grown for four weeks in 25 cm diam. pots Two spotted spider mites containing a soil-less growth medium Metro-Mix 360 and thinned to 4 plants per pot. They were then Tomatoes put under cages (40 cm 40 cm 40 cm) with a 0.2 mm mesh, with one pot containing 4 plants in each Cucumbers treatment cage. Plants were treated with soil drenches of 5%, 10%, or 20% vermicompost extracts or Vermicomposts a deionized water control to ﬁeld capacity, at germination and at weekly intervals thereafter. In each Aqueous extracts experiment, either 100 green peach aphids, mealybugs, or two spotted spider mites were released into Pest suppression each cage (25 pests per test plant), on leaves of the same plant species. Each vermicompost extract treatment and the deionized water control were replicated 4 times per pest cage experiment laid out in a randomized complete block design. Numbers of pests were counted and damage was rated (0, none to 5, total) on days 1, 3, 5, 7, 9, 11, 13 and 14 after pest release into the cages. All of the vermicompost extracts suppressed pest establishment on the plants, and their rates of reproduction for all three species of pests, signiﬁcantly. They also caused some of the pests on the plants receiving the higher extract application rates to die after 14 days of treatment. The higher the rate of extract application the greater was the suppression of the pests. We concluded that the most likely cause for the unacceptability of the plants to pests and decreased reproduction and mortality, was the uptake of soluble phenolic materials from the vermicompost extracts into the plant tissues. These compounds are known to make plants unattractive to pests and to affect pest rates of reproduction and survival. Published by Elsevier Ltd.

1. Introduction between earthworms and microorganisms in breaking down organic wastes. Solid vermicomposts increase plant germination, Vermicomposts are finely-divided, fully-stabilized organic growth, flowering and fruiting of a wide range of crops through materials supporting large microbial numbers and activity. They hormonal effects, independent of nutrients (Edwards, 2004). Low are produced in a mesophilic process through interactions vermicompost application rates in the field, or substitutions of vermicomposts into plant growth media in the greenhouse, have been shown to suppress numbers of plant parasitic nematodes (Arancon et al., 2002), plant pathogens (Chaoui et al., 2002), and * Corresponding author. Tel.: þ1 614 292 1149; fax: þ1 614 292 2180. E-mail addresses: [email protected] (C.A. Edwards), [email protected] pest arthropods (Arancon et al., 2006; Edwards et al., 2007; Yardim (N.Q. Arancon). et al., 2006).

0261-2194/$ – see front matter Published by Elsevier Ltd. doi:10.1016/j.cropro.2009.08.011

Please cite this article in press as: Edwards, C.A., et al., Suppression of green peach aphid (Myzus persicae) (Sulz.), citrus..., Crop Protection (2009), doi:10.1016/j.cropro.2009.08.011 ARTICLE IN PRESS

2 C.A. Edwards et al. / Crop Protection xxx (2009) 1–14

45 h g 40 f e Day 1 35 d e day 3 c de e bc d day 5 30 b c c ab b bc a a a d a b e day 7 25 f c g d day 9 e day 11 20 f g day 13 15 h day 14 10

5 Mean number of aphids per plant 0 Water 5% 10% 20% (control) Vermicompost tea concentration

Fig. 1. Changes in green peach aphid (Myzus persicae) numbers on tomatoes treated with a range of concentrations of food waste vermicompost aqueous extracts (means S.E.). Means followed by the same letters are not signiﬁcantly different for each treatment concentration (P 0.05).

Various forms of organic matter applied to soils, may help to aphids (Myzus persicae), citrus mealybugs (Pseudococcus citri), and decrease numbers of arthropod pests and the resultant crop damage two spotted spider mites (Tetranychus urticae) infesting tomatoes (Patriquin et al., 1995). In preliminary research in our laboratory, and cucumbers. These vermicompost aqueous extracts were solid vermicomposts suppressed numbers and damage by arthropod applied to the plants as soil drenches to ﬁeld capacity at germina- pests, such as aphids and cabbage white caterpillars (Arancon and tion and thereafter at weekly intervals. Edwards, 2004; Arancon et al., 2005a,b). Other workers have reported that vermicomposts suppressed attacks by jassids, aphids 2. Materials and methods and spider mites (Rao et al., 2001; Rao, 2002) and psyllids (Biradar et al., 1998). More recent research in our laboratory has demon- 2.1. Production of greenhouse test plants strated signiﬁcant suppression of plant parasitic nematodes, arthropod pests and plant diseases by vermicompost aqueous Cucumbers (Cucumis sativa) and tomatoes (Lycopersicon escu- extracts (Edwards et al., 2007). Vermicompost extracts are much lentum) were sown in the greenhouse and grown in a soil-less easier to handle and apply to crops than solid vermicomposts, which bedding plant medium, Metro-Mix 360 (MM360). MM360 is are bulky and heavy and need soil incorporation. a preparation from vermiculite, Canadian sphagnum peat moss, The greenhouse experiments that are reported in this paper bark, ash, sand, and has a starter nutrient fertilizer in its formula- describe the effects of aqueous extracts produced from food waste- tion (Scotts, Marysville, OH). The commercial pre-consumer food based vermicomposts, on numbers and damage by green peach waste vermicomposts, processed from supermarket food wastes

45 a 40 a a tn

a a lpr 35 a a b b b Water

epsd b 30 b (control) a b bc a a a a b b b c ihpaforebmunnaeM c 5% 25 c c c c c d 10% 20 d 20% d 15 d

0 day 1 day 3 day 5 day 7 day 9 day 11 day 13 day 14 Time (days)

Fig. 2. Changes in green peach aphid (Myzus persicae) numbers over time on tomatoes treated with a range of concentrations of food waste vermicompost aqueous extracts (means S.E.). Means followed by the same letters are not signiﬁcantly different for each treatment concentration (P 0.05).

C.A. Edwards et al. / Crop Protection xxx (2009) 1–14 3

g day 1

tnalprepgnitaregamadnaeM f 5 f day 3 e e day 5 )latot=5-enon=0( 4 e e day 7 g day 9 d 3 d f f day 11 d day 13 d d c 2 c day 14 e bc c b d 1 b c b b b a a a a 0 Water 5% 10% 20% (control) Vermicompost tea concentration

Fig. 3. Damage ratings (0–5) of green peach aphids (Myzus persicae) on tomatoes treated with a range of concentrations of food waste vermicompost aqueous extracts (mean- s S.E.). Means followed by the same letters are not significantly different for each treatment concentration (P 0.05). that we used in our experiments, were produced in a fully auto- 2.2. Treatments mated continuous-flow vermicomposting reactor system designed by Edwards and his colleagues in the U.K. (Edwards and Arancon, The treatments consisted of a range of 3 concentrations of 2004) by Oregon Soil Corporation, Portland, Oregon and contained aqueous vermicompost extracts. The food waste vermicompost 1.3% N, 2.7% P, and 9.2% K and trace elements. extract concentrations prepared from a 20% aqueous extract were For all experiments, 8 tomato or cucumber seeds were sown into diluted to 5% and 10% (v:v), and together with a 20% extract their each 25 cm diameter plant pot, containing Metro-Mix 360, and effects were compared with those of a deionized water control. The placed in a greenhouse to germinate. After plant emergence was aqueous extracts were prepared as a 20% solution using 7.5 l of food complete, all pots were thinned to 4 seedlings per pot. Plants were waste vermicompost in 30 l of water in commercial compost extract watered with Peter’s Nutrient Solution three times weekly which brewing equipment (‘Growing Solutions10TM Compost Tea Brewing supplied all needed nutrients throughout their growth period. Equipment’, WA, U.S.). They were aerated during production over Peter’s Nutrient Solution is a water-soluble fertilizer, recommended a period of 24 h. for continuous liquid feed programs of bedding plants, and contains The 3 concentrations of aqueous vermicompost extracts (5%,10% 7.77% NH4–N, 12.23% NO3–N, 10% P2O5, 20% K2O, 0.15% Mg, 0.02% B, and 20%) and a deionized water control were applied to plants as 0.01% Cu, 0.1% Fe, 0.056% Mn, 0.01% Mo, and 0.0162% Zn. The plants soil drenches to approximately field capacity moisture content at were grown in the greenhouse for 4 weeks before they were caged sowing, and at weekly intervals thereafter. From prior tests the and infested with the test arthropod pests for a test period of two amount of aqueous vermicompost extract applied on each treat- weeks. ment date was 200 ml. The tomatoes or cucumbers were exposed

a a 5 a b b Water a b 4 (control) c 5% 3 a b c c d 10% d a c 20%

(0=none-5=total) 2 b c b c a c b Mean damage rating per plant 1 c d d c a a a a d 0 day 1 day 3 day 5 day 7 day 9 day day day 11 13 14 Time (days)

Fig. 4. Damage ratings (0–5) of green peach aphids (Myzus persicae) over time on tomatoes treated with a range of concentrations of food waste vermicompost aqueous extracts (means S.E.). Means followed by the same letters are not signiﬁcantly different for each treatment concentration (P 0.05).

4 C.A. Edwards et al. / Crop Protection xxx (2009) 1–14

4 b to test infestations by 3 species of arthropod pests (green peach b aphids, citrus mealybugs, or two spotted spider mites), for 14 days 3.5 b in cages. Plants were harvested for assessment of the mean above

3 a ground and root dry weights and leaf areas per plant after 6 weeks. Shoots were oven-dried at 60 C for 24 h before weighing to 2.5 measure shoot dry weights. On the same date mean leaf areas were 2 measured using a Licor Model 3100 leaf area meter.

1.5 2.3. Pest infestations 1 Each experimental treatment, involved growing seedlings of either 0.5 tomatoes or cucumbers in pots with 4 seedling plants per pot per Mean dry shoot weight (g) per plant per (g) weight shoot dry Mean 0 treatment, confined in a single mesh cage (40 cm 40 cm 40 cm) Water (control) 5% 10% 20% covered with a 0.2 mm aperture nylon mesh. Each cage treatment was Vermicompost tea concentration replicated 4 times. Prior to infestation, the seedlings were raised in an insect-free greenhouse environment for four weeks. For experiments Fig. 5. Effects of soil applications of vermicompost aqueous extracts on tomato dry on two spotted spider mites, citrus mealybugs and green peach aphids, shoot weights when attacked by green peach aphids (Myzus persicae) (mean S.E.). Means followed by the same letters are not significantly different for each treatment plants in cages were placed on capillary mats for ease and uniformity concentration (P 0.05). of watering without removing the cage, either with Peter’s Nutrient Solution, providing all the required nutrients, or watering with only water for irrigation, according to the experimental protocol 300 designated. For all experiments, pots each containing 4 plants, were placed 250 b b in individual cages for each treatment, which was a soil drench to field capacity with either 5%, 10%, or 20% vermicompost aqueous 200 extracts or a deionized water control. Pests were released into cages

a a on leaves of the same plant species placed on the surface of the 150 growing medium in the plant pots from which they moved on to the plants within 2 h. One hundred green peach aphids (M. persicae), citrus mealybugs (Planococcus citri) or two spotted spider 100 mites (T. urticae) were released into each individual experimental cage on the ﬁrst day of the experiment when plants were four 50 weeks old. Mean leaf area (sq. cm) per plant The numbers of insects or mites on the tomatoes and cucumbers 0 were counted on days 1, 3, 5, 7, 9, 11, 13 and 14 after infestation. On Water (control) 5% 10% 20% the same days, assessments of damage to the plants, on a rating Vermicompost tea concentration scale of 0 (none) to 5 (total) were made based on areas of leaf Fig. 6. Effects of soil applications of vermicompost aqueous extracts on tomato leaf damaged. A damage rating of 3 should equate to damage to 60% of areas when attacked by green peach aphids (Myzus persicae) (mean S.E.). Means the total foliage. These ratings were very reliable and repeatable followed by the same letters are not signiﬁcantly different for each treatment after appropriate training for the technicians making the assess- concentration (P 0.05). ments. Only damage ratings could be made for the spider mite

45 h g tnalprepsdihpaforebmunnaeM 40 f ef f e 35 Day 1 e d d d day 3 30 c c b b ac a b a a a ab day 5 a ac c c a bc 25 cd d day 7 e e e 20 day 9 day 11 15 day 13 10 day 14

0 Water 5% 10% 20% (control) Vermicompost tea concentration

Fig. 7. Changes in green peach aphid (Myzus persicae) numbers on cucumbers treated with a range of concentrations of food waste vermicompost aqueous extracts (means S.E.). Means followed by the same letters are not signiﬁcantly different for each treatment concentration (P 0.05).

C.A. Edwards et al. / Crop Protection xxx (2009) 1–14 5

a 45 a 40 a b b b control 35 a (water) b a a a a 30 5% a a b c b b c a a a a c c c 25 c c d d d d 10% 20

15 20%

Mean numbers of aphids per plant 5

0 day 1 day 3 day 5 day 7 day 9 day 11 day 13 day 14 Time (days)

Fig. 8. Changes in green peach aphid (Myzus persicae) numbers in time on cucumbers treated with a range of concentrations of food waste vermicompost aqueous extract (means S.E.). Means followed by the same letters are not significantly different for each treatment concentration (P 0.05). experiments since the pests were too small to count on the plant greater suppression by 20% extract than 10% extract than 5% extract foliage. (P 0.05). All of the aphids introduced into the cages settled on the The experiments were in a completed randomized layout in the tomato plants (25 per plant). In the deionized control, aphids greenhouse. GLM procedures (SAS ver. 9.1.3, 2002–2003) were used increased in numbers significantly (P 0.05) to 40 per plant over 14 to analyze results. Repeated measurements ANOVA were made for days (Figs. 1 and 2). In the treatment receiving 5% vermicompost damage and number ratings on tomatoes and cucumbers. The GLM extract they also increased in numbers, but in the 10% extract treat- procedure for between subject effects included time and treatment cages they continued to increase significantly (P 0.05) up to ments rates in the model. For the univariate analysis for within day 7, then began to decrease in numbers significantly (P 0.05). In subject effects, the GLM procedure was used with both time and the 20% extract treatment they decreased progressively in numbers time and treatment rates included in the model. Differences from day 1 to day 14. A similar pattern occurred in terms of green between means were separated using least significant differences peach aphid damage ratings where damage leveled off to a rating of (LSD) at P 0.05 and 0.01, as indicated in the captions to the figures. 2.0 in response to 20% extract applications (Figs. 3 and 4). In terms of damage ratings, the tomatoes receiving the water (control) reached 3. Results a damage rating of 5.0 (5.0 equals total damage) compared with a rating of 4.0 for plants receiving 5% vermicompost extract, 3.0 for 3.1. Green peach aphid experiments those receiving 10% extract and less than 2.0 for plants receiving 20% extract (P 0.05). When tomato shoot dry weights were measured In the experiment on suppression of green peach aphids on (Fig. 5), only the 20% vermicompost extract produced significant tomatoes, numbers of aphids were suppressed significantly (P 0.05) increases (P 0.05), although both the 10% and 20% extract applica- by all three vermicomposts aqueous solution concentrations, with tions increased tomato leaf areas (Fig. 6).

f tnalp rep gnitar egamad naeM egamad gnitar rep tnalp 5 f day 1 day 3

)latot=5- 4 e f day 5 d e day 7 3 c day 9

e d non=0( e day 11 d b b 2 day 13 c c c c c c day 14 b b b b b b b b 1

a a a a a a 0 Water (control) 5% 10% 20% Vermicompost tea concentration

Fig. 9. Damage ratings (0–5) of green peach aphids (Myzus persicae) on cucumbers treated with a range of concentrations of food waste vermicompost aqueous extracts (means S.E.). Means followed by the same letters are not signiﬁcantly different for each treatment concentration (P 0.05).

6 C.A. Edwards et al. / Crop Protection xxx (2009) 1–14

a 5 a tnalprepgnitaregamadnaeM

4 a Water b )la (control) a b t 5% o

t=5-en a 3 10% b c c o a 20% n=0 2 a b b c

( c d bc c b b b bc b c c 1

c c a a a a 0 day 1 day 3 day 5 day 7 day 9 day 11 day 13 day 14 Time (days)

Fig. 10. Damage ratings (0–5) of green peach aphids (Myzus persicae) over time on cucumbers treated with a range of concentrations of food waste vermicompost aqueous extracts (means S.E.). Means followed by the same letters are not signiﬁcantly different for each treatment concentration (P 0.05).

The responses of the cucumbers to aphid infestations per plant on day 14 in the deionized water control (Figs. 13 and 14). followed a similar pattern, in terms of numbers of aphids, except Mealybug numbers increased significantly (P 0.05) when 5% that control plants reached a total of 43 aphids per plant after 14 extracts were applied and decreased significantly (P 0.05) in days (Figs. 7 and 8). Aphid numbers increased significantly response to 10% and 20% extract applications. However, damage (P 0.05) in response to the 5% vermicompost extract treatment ratings (Figs. 15 and 16) increased significantly (P 0.05) from 0.5 but decreased for the whole exposure period in response to the 10% to 2.5 over 14 days on the deionized water controls and much less and 20% vermicompost extract treatments. The damage ratings in the 5% extract treatment (rating of 2.0), 10% extract treatment (Figs. 9 and 10) were higher than those on tomatoes, with the (rating of 1.5) and 20% extract treatments (rating of 1.35) (P 0.05). plants in the water control suffering very severe damage to a rating There were significant (P 0.05) increases in dry shoot weights of of nearly 5.0 after 14 days. Damage ratings were 3.3 in response to tomatoes (Fig. 17) and mean leaf areas (Fig. 18) in response to all 5% extracts, 2.1 for 10% extracts, and 1.4 for 20% extract treatments concentrations of vermicompost extract treatments. (P 0.05). Shoot dry weights increased significantly (P 0.05) in The responses of cucumbers infested by mealybugs were similar response to 10% and 20% extracts (Fig. 11) and so did leaf areas but numbers increased significantly (P 0.05) from 25 to 33 per (Fig. 12). plant in the water control, rather less in the 5% extract treatment, not at all in the 10% extract treatment, and decreased significantly 3.2. Citrus mealybug experiments (P 0.05) in response to the 20% extract treatment (Figs. 19 and 20). The damage ratings decreased significantly (P 0.05) from 2.5 per In the experiments on the effects of vermicompost extracts on plant in the water control to 1.9 per plant in response to the 5% citrus mealybug (P. citri) numbers on tomatoes were quite similar to extract treatment, 1.75 per plant in the 10% extract treatment, and those of green peach aphids in response to the same vermicompost 1.5 per plant in the 20% extract treatment (Figs. 21 and 22). There extract concentrations. However, numbers of mealybugs increased were significant differences (P 0.05) in cucumber dry shoot significantly (P 0.05) from 25 per plant on day 1 to more than 29

350 b tnal tnalp rep )g( thgiew toohs yrd naeM yrd toohs thgiew )g( rep tnalp 4 300 b p r p c ep )mc . )mc ep bc 250 3 ab 200 a a qs( aera fael naeM fael aera qs( a

2 150

100 1 50

0 0 Water (control) 5% 10% 20% Water (control) 5% 10% 20% Vermicompost tea concentration Vermicompost tea concentration

Fig. 11. Effects of food waste vermicompost aqueous extracts on cucumber shoot dry Fig. 12. Effects of food waste vermicompost aqueous extracts on cucumber mean leaf weights when attacked by green peach aphids (Myzus persicae) (mean S.E.). Means areas when attacked by green peach aphids (Myzus persicae) (mean S.E.). Means fol- followed by the same letters are not signiﬁcantly different for each treatment lowed by the same letters are not signiﬁcantly different for each treatment concentration concentration (P 0.05). (P 0.05).

C.A. Edwards et al. / Crop Protection xxx (2009) 1–14 7

35 tnalp rep sgub ylaem fo rebmun rebmun fo ylaem sgub rep tnalp f 30 e e d d d d d cd c bc b ab a ab a a a a a a aab b bc c day 1 25 c c d d e day 3 f day 5 20 day 7 day 9 15 day 11 day 13 10 day 14

naeM 5

0 Water (control) 5% 10% 20% Vermicompost tea concentration

Fig. 13. Effects of food waste vermicompost aqueous extracts on citrus mealybug (Planococcus citri) numbers on tomatoes (mean S.E.). Means followed by the same letters are not significantly different for each treatment concentration (P 0.05). weights (Fig. 23) and leaf areas (Fig. 24) in response to 10% and 20% significantly (P 0.05) in response to all of the extract application extract treatments but not in response to the 5% extract treatment rates (Fig. 28). (P 0.05). For cucumbers infested by two spotted spider mites, damage ratings increased from 1.0 on day 3 to 5.0 (out of a total of 5.0) on 3.3. Two spotted spider mite experiments day 14, in the deionized water control treatment. By comparison there were significantly lower increases (P 0.05) from 0.5 to 2.9 in The two spotted spider mites were too small for their numbers response to the 5% extract treatment, from 0.5 to 2.8 in response to to be counted on the leaves, but the damage that they caused was the 10% extract treatment, and from 0.3 to 1.85 in response to the severe. Two spotted spider mite damage ratings on tomatoes 20% extract treatment, after 14 days (Figs. 29 and 30). In terms of between treatments increased from a rating of 1.0 on day 3 to dry shoot weights only the 20% extract treatment increased shoot a rating of 4.5 (out of a total of 5.0) on day 14 in the deionized water dry weights significantly (P 0.05) but all three extract treatments controls (Figs. 25 and 26). By comparison, damage ratings increased (Fig. 31) increased the leaf areas of cucumbers infested with two significantly (P 0.05) from 0.5 to 2.5 in response to 5% extract spotted spider mites significantly (P 0.05) (Fig. 32). treatments, from 0.5 to 2.0 in response to 10% extract treatments, and from 0.3 to 1.5 in response to 20% extract applications after 14 4. Discussion days. Tomato dry shoot weights increased significantly (P 0.05) in We focused on tomatoes and cucumbers in these experiments response to both the 10% and 20% extract applications but not to the because they are valuable greenhouse crops which are very 5% extract treatment (Fig. 27). Tomato leaf areas increased susceptible to a range of foliar pests that are expensive to control.

35 t

nal a 30 a a a pre b a a b a a a a a a a a a ab ab a a

ps b c b b b Water 25 c c c c gubylaemfos (control) d d 20 5%

10% 15

r 20% ebmun 10

n 5 aeM

0 day 1 day 3 day 5 day 7 day 9 day 11 day 13 day 14 Time (days)

Fig. 14. Effects of food waste vermicompost aqueous extracts on citrus mealybug (Planococcus citri) numbers on tomatoes over time (means S.E.). Means followed by the same letters are not signiﬁcantly different for each treatment concentration (P 0.05).

8 C.A. Edwards et al. / Crop Protection xxx (2009) 1–14

3 e day 1 2.5 d day 3 d

gnitar egamad naeM egamad gnitar day 5

)latot=5-enon=0( d c 2 day 7 c c e day 9 d e d day 11 1.5 bc c d day 13 d b c day 14 b c 1 b b a a a 0.5 b ab a a a a a 0 Water (control) 5% 10% 20% Vermicompost tea concentration

Fig. 15. Damage ratings (0–5) of citrus mealybugs (Planococcus citri) on tomatoes treated with a range of concentrations of food waste vermicompost aqueous extracts (means S.E.). Means followed by the same letters are not signiﬁcantly different for each treatment concentration (P 0.05).

The pests that we tested in our vermicompost aqueous extract The data presented in the research reported in this paper are the experiments to assess the effects of the extracts on pest suppres- first detailed reports in the scientific literature, of the suppression sion were, green peach aphids, citrus mealybugs, and two spotted of important sucking pests such as aphids, mealybugs and spider spider mites, which are all important pests of these crops, and the mites by aqueous extracts from vermicomposts. The overall effects degree of suppression of these pests by the aqueous extracts was of the aqueous vermicompost solutions on both numbers and dramatic. The availability of such innovative organic control damage by all three of these pests were dramatic, significant and measures as aqueous vermicompost extracts would be particularly consistent on two crops. Clearly, weekly applications of these welcome to organic growers who are prohibited from using inor- aqueous extracts to tomatoes and cucumbers as soil drenches had ganic pesticides on their crops. Vermicomposting is a process that three major effects. Firstly, since all three species of pests tested in can be carried out at a range of scales using relatively simple to high the experimental cages had a free choice to infest the test plants, it technologies (Edwards and Arancon, 2004) and a variety of rela- seems that the application of all application rates of the aqueous tively inexpensive equipment for vermicompost extract prepara- extracts made both tomatoes and cucumber plants much less tion is available commercially. attractive to all three species of pests. The highest application rate Yardim et al. (2006) reported suppression of the chewing pests of 20% aqueous extract stopped virtually all pest infestations and cucumber beetles and tomato hornworms by vermicomposts. the 10% extract had major impacts on the extent of infestation. In There are a few reports in the scientific literature of the suppression a number of the experiments even the 5% extracts made the plants of sucking pests by solid vermicomposts. Biradar et al. (1998) relatively unattractive to the pests. reported significant suppressive effects of vermicomposts on The weekly soil drenches of vermicompost extract to the soil in psyllid attacks, Rao et al. (2001) and Rao (2002) reported which the plants grew must also have interfered with the repro- suppression of jassids, aphids and spider mites on groundnuts by duction patterns of the green peach aphids, citrus mealybugs and vermicomposts. Arancon et al. (2006) reported suppression of two spotted spider mites, since the increased rates of application of aphids, mealybug, and spider mite attacks by solid vermicomposts. aqueous extracts decreased the rates of reproduction of the pests,

3 a

2.5 a ab

gnitaregamadnaeM ab )la a

t 2 a ab Water ot=5 bc (control) bc a bc c -en 1.5 5% b c

o b b 10% n=0 b b c 1 20%

( a b a a ab a a 0.5 ab

a a a a b 0 day 1 day 3 day 5 day 7 day 9 day 11 day 13 day 14 Time (days)

Fig. 16. Damage ratings (0–5) of citrus mealybugs (Planococcus citri) over time on tomatoes treated with a range of concentrations of food waste vermicompost aqueous extracts (means S.E.). Means followed by the same letters are not signiﬁcantly different for each treatment concentration (P 0.05).

C.A. Edwards et al. / Crop Protection xxx (2009) 1–14 9

5 because numbers of all three species leveled off or decreased b particularly in response to the higher application rates of extracts. b Finally, there was consistent evidence that the higher application 4 b rates of vermicompost extracts caused the pests to either leave the plants or die, since overall numbers of the pests on the crops 3 a decreased signiﬁcantly with time in response to these higher application rates. 2 These results raise the question of possible mechanisms of how these vermicompost extract soil drenches may affect the response of the pests when taken up into the plants. There are many reports 1 in the literature of organic nutrient sources decreasing numbers of pest arthropods (Culliney and Pimentel, 1986; Eigenbrode and 0 Pimentel, 1988; Yardim and Edwards, 2003; Patriquin et al., 1995; Mean dry shoot weight (g) per plant Water (control) 5% 10% 20% Morales et al., 2001; Phelan, 2004). There have also been sugges- Vermicompost tea concentration tions of these effects being due to the uptake into plants of phenols from organic manures (Ravi et al., 2006). However, although such Fig. 17. Effects of food waste vermicompost aqueous extracts on tomato dry shoot mechanisms may account for the suppression of pest attacks by weights attacked by citrus mealybugs (Planococcus citri) (mean S.E.). Means followed by the same letters are not signiﬁcantly different for each treatment concentration solid vermicomposts, they are unlikely to account for similar (P 0.05). suppression by liquid extracts from vermicomposts applied to the soil in which the crops grow. Materials that can pass readily from the solid vermicomposts into the aqueous extracts include soluble nutrients, free enzymes, a wide variety of microorganisms, and c 300 water-soluble phenols. Vermicomposts have much greater microbial diversity and 250 b activity than conventional thermophilic composts, because organic wastes that have been fragmented by earthworms have a much ab 200 greater surface area and can support considerably greater microbial a activity. By comparison, microbial activity tends to be suppressed 150 by the high temperatures reached during thermophilic composting. To identify the mechanism of pest suppression further, it is 100 important to discuss which of the materials passing into the extracts could be responsible for the pest suppression, since the 50 response must depend on uptake of these materials into the tomato and cucumber plants from the soil drenches. It could not be caused

Mean leaf area (sq. cm) per plant 0 by uptake of soluble nutrients since all of the experimental treat- Water (control) 5% 10% 20% ments were supplied regularly with all the nutrients that they Vermicompost tea concentration needed from Peter’s Nutrient Solution, which was applied to the experimental plants three times a week. Possibly, some free Fig. 18. Effects of food waste vermicompost aqueous extracts on tomato mean leaf areas attacked by citrus mealybugs (Planococcus citri) (mean S.E.). Means followed by enzymes in the aqueous extract could inﬂuence the pest suppres- the same letters are not signiﬁcantly different for each treatment concentration sion, but this is very unlikely on the scales and consistencies of (P 0.05). suppression demonstrated in these experiments. For instance, the

35 f ef de d 30 c d c cd d bc b b b b b ab ab b ab day 1 a a a aab ab a a ab ab b 25 day 3 bc c day 5 20 day 7 day 9 15 day 11 day 13 10 day 14

5 Mean number of mealy bugs per plant

0 Water (control) 5% 10% 20% Vermicompost tea concentration

Fig. 19. Effects of food waste vermicompost aqueous extracts on citrus mealybug (Planococcus citri) numbers on cucumbers (mean S.E.). Means followed by the same letters are not signiﬁcantly different for each treatment concentration (P 0.05).

10 C.A. Edwards et al. / Crop Protection xxx (2009) 1–14

35 a a a b 30 a b b a ab a c c ab a ab a aa a bcc b b c c a a a a b 25 d d Water (control) 20 5%

10% 15 20%

5 Mean numbers of mealy bugs per plant

0 day 1 day 3 day 5 day 7 day 9 day 11 day 13 day 14 Time (days)

Fig. 20. Effects of food waste vermicompost aqueous extracts on citrus mealybug (Planococcus citri) numbers over time on cucumbers (mean S.E.). Means followed by the same letters are not significantly different for each treatment concentration (P 0.05). enzyme chitinase has been reported to be present in some vermi- oxidase enzyme has been extracted from an earthworm, Lumbricus composts (Hahn, 2001) and it is feasible that this could affect rubellus, that is sometimes used in vermicomposting, and this arthropod pest molting, but there seem to be no reports in the compound can bioactivate organic compounds to form phenols, literature of this enzyme having any effects on pests, although there such as p-nitrophenol (Park et al., 1996). Polychlorinated phenols is evidence it may have some influences on plant pathogens. We and their metabolites have been reported from a range of soils reviewed possible mechanisms by which microorganisms could be containing earthworms (Knuutinen et al., 1990). Vinken et al. taken up into the tissues of plants and influence arthropod pest (2005) reported that monomeric phenols could be absorbed by feeding but could not find any relevant reports. humic acids in the gut of earthworms. The other possible mechanism by which vermicomposts and Phenolics have been identified as common insect antifeedants similar organic materials may suppress attacks by arthropod pests (Koul, 2008). Stevenson et al. (1993) reported inhibition of the on the foliage and fruits of crop plants, could be to change the pests’ development of Spodoptera litura caterpillars by a phenolic feeding responses, due to soluble phenolic substances in the soil compound present in wild groundnuts. Summers and Felton (1994) drenches that were taken up into plants from vermicomposts. It is proposed that lepidoptera larval feeding was decreased by oxida- well known that soluble phenolic substances are distasteful to tive stress caused by phenolic compounds in plants. Haukioja et al. secondary invertebrate decomposers in soil systems and can inhibit (2002) reported that phenolics in plant tissues decreased the rates the breakdown of dead and decaying plant materials (Edwards and of consumption of tissues by a geometrid caterpillar Epirrita Heath, 1963; Heath and Edwards, 1964). An endogenous phenol autumnata. Phenols deterred feeding by southern armyworms,

3 e

2.5 d

day 1 e e d 2 d day 3 d e c d day 5 d day 7 1.5 c cd d c day 9 b c day 11 d (0=none-5=total) 1 c day 13 b b c bc day 14

Mean damage rating per plant 0.5 a b ab ab a a a a 0 Water (control) 5% 10% 20% Vermicompost tea concentration

Fig. 21. Damage ratings (0–5) of citrus mealybugs (Planococcus citri) on cucumbers treated with a range of concentrations of food waste vermicompost aqueous extracts (means S.E.). Means followed by the same letters are not signiﬁcantly different for each treatment concentration (P 0.05).

C.A. Edwards et al. / Crop Protection xxx (2009) 1–14 11

3 a

2.5 a

b b b 2 Water a a bc (control) a b a 5% a c 1.5 a 10% a a a b 20% b

(0=none-5=total) 1 ab b a b

Mean damage rating per plant b b 0.5 ab ab a a a a b 0 day 1 day 3 day 5 day 7 day 9 day 11 day 13 day 14 Time (days)

Fig. 22. Damage ratings (0–5) of citrus mealybugs (Planococcus citri) over time on cucumbers treated with a range of concentrations of food waste vermicompost aqueous extracts (means S.E.). Means followed by the same letters are not signiﬁcantly different for each treatment concentration (P 0.05).

Spodoptera eridania (Lindroth and Peterson, 1988). Kurowska et al. by solid vermicomposts (Arancon and Edwards, 2004; Arancon (1990) reviewed the effects of 46 phenols as insect repellents and et al., 2005a,b). feeding deterrents and concluded that many can have signiﬁcant Chrzanowski (2008) reported that phenolic acids in blackcurrant effects in this way on pest attacks. Bhonwong et al. (2009) reported and sour cherry leaves slowed the reproduction and general fecun- that polyphenol oxidases in tomatoes could produce resistance to dity of grain aphids (Sitobian avenae). Eleftherianos et al. (2006) cotton bollworm (Helicoverpa armigera) and beet armyworm reported that changes in the levels of total phenols in maize and (Spodoptera exigua). They concluded that there was a clear feeding barley plants decreased the fecundity of the cereal aphids Rophalo- deterrent effect of these chemicals to the pests. Tomato phenol siphum padi and S. avenae. Galls induced by Pemphigus populi aphids oxidase in tomato plants slowed down feeding and rates of growth on Populus nigra were suppressed by high levels of phenols in the of the common cutworm, S. litura F. (Mahanil et al., 2008). Plant plant tissues (El-Akkad and Zalat, 2000). phenolics affected the rates of development and survival of the We hypothesize that the decreases in insect pest numbers and autumn moth, E. autumnata (Hawida et al., 2007). These diverse damage to plants grown with aqueous vermicompost extracts in results all point to the probability that water-soluble phenols, our greenhouse experiments, could be attributed to the presence of extracted from the vermicompost during aquatic extraction, taken water-soluble phenolic compounds in plants grown with vermi- up into plants from soil receiving drenches of vermicompost composts and vermicompost aqueous extracts which make the aqueous extracts, could be the most likely mechanisms by which plants less attractive to pests and interfere with their reproduction. vermicompost aqueous extracts can suppress pest attacks. A similar Although these conclusions are based on circumstantial evidence mechanism could account for the suppression of arthropod pests the breadth and weight of evidence makes it extremely likely that

3.5 c 350 c bc 3 300 bc ab 2.5 250 ab 2 a 200 a 1.5 150

1 100

0.5 50 Mean leaf area (sq. cm) per plant Mean dry shoot weight (g) per plant 0 0 Water (control) 5% 10% 20% Water (control) 5% 10% 20% Vermicompost tea concentration Vermicompost tea concentration

Fig. 23. Effects of food waste vermicompost aqueous extracts on mean dry shoot weights Fig. 24. Effects of food waste vermicompost aqueous extracts on mean leaf areas of of cucumber plants attacked by citrus mealybugs (Planococcus citri) (mean S.E.). Means cucumber plants attacked by citrus mealybugs (Planococcus citri) (mean S.E.). Means followed by the same letters are not signiﬁcantly different for each treatment concen- followed by the same letters are not signiﬁcantly different for each treatment tration (P 0.05). concentration (P 0.05).

12 C.A. Edwards et al. / Crop Protection xxx (2009) 1–14

5 f f

f day 1 4 day 3 day 5

3 e g g day 7 day 9 de fg day 11 ef e e e c c 2 cd day 13 de (0=none-5=total) de day 14 cd b cd c b b 1 b a

Mean damage rating per plant bc a a a a a a 0 Water (control) 0.05 0.1 0.2 Vermicompost tea concentration

Fig. 25. Damage ratings (0–5) of two spotted spider mites (Tetranychus urticae) on tomatoes treated with a range of soil-applied vermicompost aqueous extracts (means S.E.). Means followed by the same letters are not signiﬁcantly different for each treatment concentration (P 0.05).

5 a a

4 Water (control)

b b 5% 3 a b a 10% b b bc bc 2 a c c 20% ab bc (0=none-5=total) ab c b a ab bc c b 1 ab Mean damage rating per plant b c a a a a 0 day 1 day 3 day 5 day 7 day 9 day 11 day 13 day 14 Time (days)

Fig. 26. Damage ratings (0–5) of two spotted spider mites (Tetranychus urticae) over time on tomatoes treated with a range of soil-applied vermicompost aqueous extracts (means S.E.). Means followed by the same letters are not signiﬁcantly different for each treatment concentration (P 0.05).

b d 4 b 500

a 400 c 3 b a a 300 2 200

1 100 Mean leaf area per plant (sq. cm)

Mean dry shoot weight per plant (g) 0 0 Water 5% 10% 20% Water (control) 5% 10% 20% (control) Vermicompost tea concentration Vermicompost tea concentration

Fig. 27. Effects of a range of soil-applied vermicompost aqueous extracts on mean Fig. 28. Effects of a range of soil-applied vermicompost aqueous extracts on leaf areas of shoot dry weights of tomato plants attacked by two spotted spider mites (Tetranychus tomato plants attacked by two spotted spider mites (Tetranychus urticae) (means S.E.). urticae) (means S.E.). Means followed by the same letters are not signiﬁcantly Means followed by the same letters are not signiﬁcantly different for each treatment different for each treatment concentration (P 0.05). concentration (P 0.05).

C.A. Edwards et al. / Crop Protection xxx (2009) 1–14 13

f f 5 day 1 day 3 e 4 day 5 day 7 f f e e day 9 3 d ef day 11 cd d d day 13 de d 2 bc (0=none-5=total) day 14 c cd c bcc b bc c bc Mean damage rating per plant 1 b b b b

a a a a 0 Water (control) 5% 10% 20% Vermicompost tea concentration

Fig. 29. Damage ratings (0–5) of two spotted spider mites (Tetranychus urticae) on cucumbers treated with a range of soil-applied vermicompost aqueous extracts (means S.E.). Means followed by the same letters are not signiﬁcantly different for each treatment concentration (P 0.05).

a a 5

a Water 4 (control) 5% b a b 10% 3 b b b a ab b 20% a c 2

(0=none, 5=total) bc c ab ab c b a ab b c b Mean damage rating per plant 1 ab b b a a a a 0 day 1 day 3 day 5 day 7 day 9 day 11 day 13 day 14 Time (days)

Fig. 30. Damage ratings (0–5) of two spotted spider mites (Tetranychus urticae) over time on cucumbers treated with a range of soil-applied vermicompost aqueous extracts (means S.E.). Means followed by the same letters are not signiﬁcantly different for each treatment concentration (P 0.05).

c 300 3 bc d b 250 c a 200 2 150 b

1 100 a 50

0 0 Mean leaf area per plant (sq. cm)

Mean dry shoot weight per plant (g) Water (control) 5% 10% 20% Water (control) 5% 10% 20% Vermicompost tea concentration Vermicompost tea concentration

Fig. 31. Effects of a range of soil-applied vermicompost aqueous extracts on mean dry Fig. 32. Effects of a range of soil-applied vermicompost aqueous extracts on mean leaf shoot weights of cucumber plants attacked by two spotted spider mites (Tetranychus areas of cucumber plants attacked by two spotted spider mites (Tetranychus urticae) urticae) (means S.E.). Means followed by the same letters are not signiﬁcantly (means S.E.). Means followed by the same letters are not signiﬁcantly different for different for each treatment concentration (P 0.05). each treatment concentration (P 0.05).

14 C.A. Edwards et al. / Crop Protection xxx (2009) 1–14 water-soluble phenols, passing from vermicomposts into aqueous Eleftherianos, I., Vamvatsikos, P., Wards, D., Gravanis, F., 2006. Changes in the levels extracts and thence into plants, may be the main mechanism by of plant total phenols and free amino acids induced by two cereal aphids and effects on aphid fecundity. J. Appl. Entomol. 130, 15–19. which vermicompost aqueous extracts influence the suppressions of Eigenbrode, S.D., Pimentel, D., 1988. Effects of manure and chemical fertilizers on pest feeding, reproduction and mortality by aphids, mealybugs and insect pest populations on collards. Agric. Ecosys. Environ. 20, 109–125. spider mites reported in this paper. Hahn, G.E., 2001. Methods of using worm castings for insect repellency. U.S. Patent 6475503, 2 pp. Hawida, S., Kapari, L., Ossipov, V., Ramtala, M.J., Ruuhola, T., Haukioja, E., 2007. Foliar phenolics are differently associated with Epirrita autumnata growth and Acknowledgements immunocompetence. J. Chem. Ecol. 33, 1013–1023. Haukioja, E., Ossipov, V., Lempa, K., 2002. The interactive effects of leaf maturation and phenolics on consumption and growth of a geanetrid moth. Futrand. Exp. This research was funded by a Sub-Contract to a Phase II USDA Appl. 104, 125–136. Small Business Innovative Research grant awarded to the Oregon Heath, G.W., Edwards, C.A., 1964. Some methods for assessing the activity of soil Soil Corporation, Philomath, Oregon. animals in the breakdown of leaves. Pedobiologia 4, 80–87. Knuutinen, J., Palm, H., Hakala, H., Haimi, J., Huhta, V., Salminen, J., 1990. Poly- chlorinated phenols and their metabolites in soil and earthworms of a sawmill environment. Chemosphere 20, 609–623. References Koul, O., 2008. Phytochemicals and insect control: an antifeedant approach. Crit. Rev. Plant Sci. 27, 1–24. Arancon, N.Q., Edwards, C.A., March 2004. Vermicomposts can suppress plant pest Kurowska, A., Gora, J., Kalemba, D., 1990. Effects of plant phenols on insects. Pol. and disease attacks. BioCycle, 51–53. Wiadomosci Chemiczne 44, 399–409. Arancon, N., Edwards, C.A., Yardim, F., Lee, S., 2002. Management of plant parasitic Lindroth, R.L., Peterson, S.S., 1988. Effects of plant phenols on performance of nematodes by use of vermicomposts. In: Proceedings of Brighton Crop southern armyworm larvae. Oecologia 75, 185–189. Protection Conference d Pests and Diseases, 18–21 November 2002, Brighton, Mahanil, S., Attajarusit, J., Stout, M.J., Thipayong, P., 2008. Overexpression of tomato U.K., vol. II, 8B-2, 705–710. phenol oxidase increases resistance to the common cutworm. Plant Sci. 174, Arancon, N.Q., Galvis, P.A., Edwards, C.A., 2005a. Suppression of insect pest pop- 456–466. ulations and damage to plants by vermicomposts. Bioresour. Technol. 96, Morales, H., Perfecto, I., Ferguson, B., 2001. Traditional fertilization and its effect on 1137–1142. corn insect populations in Guatemalan Highlands. Agric. Ecosys. Environ. 84, Arancon, N.Q., Edwards, C.A., Bierman, P., Metzger, J.D., Lucht, C., 2005b. Effects of 145–155. vermicomposts produced from cattle manure, food waste and paper waste on Park, S.R., Cho, E.J., Yu, K.H., Kim, Y.S., Suh, J.J., Chang, C.S., 1996. Endogenous the growth and yields of peppers in the field. Pedobiologia 49, 297–306. phenoloxidase from an earthworm Lumbricus rubellus. Tongmul Hakoehi 39, Arancon, N.Q., Edwards, C.A., Yardim, E.N., Oliver, T.J., Byrne, R.J., Keeney, G., 2006. 36–46. Suppression of two-spotted spider mite (Tetranychus urticae), mealy bug Patriquin, D.G., Baines, D., Abboud, A., 1995. Diseases, pests and soil fertility. In: (Pseudococcus sp.), and aphids (Myzus persicae) populations and damage by Cook, H.F., Lee, H.C. (Eds.), Soil Management in Sustainable Agriculture. Wye vermicomposts. Crop Prot. 26, 29–39. College Press, Wye, U.K, pp. 161–174. Bhonwong, A., Stout, M.J., Attajarusit, J., Tantasawat, P., 2009. Defensive role of Phelan, P.L., 2004. Connecting below-ground and above-ground food webs: the role tomato polyphenol oxidases against collar bollworm (Helicoverpa armigera) and of organic matter in biological buffering. In: Magdoff, F., Well, R.R. (Eds.), Soil beet armyworm (Spodoptera exigua). J. Chem. Ecol. 35, 28–38. Organic Matter in Sustainable Agriculture. C.R.C. Press, Boca Raton, London, Biradar, A.P., Sunita, N.D., Teggel, R.G., Devarandavadgi, S.B., 1998. Effect of vermi- New York, Washington, D.C, pp. 199–226. compost on the incidence of subadult psyllid. Ins. Environ. 4, 55–56. Rao, K.R., 2002. Induced host plant resistance in the management of sucking pests Chaoui, H., Edwards, C.A., Brickner, M., Lee, S., Arancon, N., 2002. Suppression of the of groundnut. Ann. Plant Prot. Sci. 10, 45–50. plant diseases, Pythium (damping off), Rhizoctonia (root rot) and Verticillum (wilt) Rao, K.R., Rao, P.A., Rao, K.T., 2001. Influence of fertilizers and manures on the by vermicomposts. In:Proceedings of Brighton Crop Protection Conference d Pests population of coccinellid beetles and spiders in a groundnut ecosystem. Ann. and Diseases, 18–21 November 2002, Brighton, U.K., vol. II, 8B-3, 711–716. Plant Prot. Sci. 9, 43–46. Chrzanowski, G., 2008. Influence of phenolic acids isolated from blackcurrant and Ravi, M., Dhandapani, N., Sathiah, N., Murugan, M., 2006. Influence of organic sour cherry leaves on grain aphids (Sitobion avenae F.). Pol. Pestycydy 1–2, manures and fertilizers on the incidence of sucking pests of sunflower, Helianthus 127–133. annuus L. Ann. Plant Prot. Sci. 14, 41–44. Culliney, T.W., Pimentel, D., 1986. Ecological effects of organic agricultural practices Stevenson, P.C., Anderson, J.C., Blaney, W.M., Simmonds, M.S.J., 1993. Developmental on insect populations. Agric. Ecosys. Environ. 15, 253–256. inhibition of Spodoptera litura (Fab.) larvae by a novel caffeoylquinic acid from Edwards, C.A., 2004. The use of earthworms in processing organic waste into the wild ground, Arachis paraguariensis (Chhod et Hassl. J. Chem. Ecol. 19, plant-growth media and animal feed protein. In: Edwards, C.A. (Ed.), 2917–2933. Earthworm Ecology, second ed. CRC Press/Lewis Publ. Boca Raton, FL, pp. Summers, G., Felton, G.W., 1994. Prooxidation effects of phenolic acids on the 327–354. generalist herbivore Helicoverpa zea: potential mode of action of phenolic Edwards, C.A., Heath, G.W., 1963. The role of soil animals in breakdown of leaf compounds on plant anti-herbivory chemistry. Ins. Biochem. Mol. Biol. 24, material. In: Doekson, J., Van der Drift, J. (Eds.), Soil Organisms. North Holland 943–953. Pub. Co., Amsterdam, pp. 76–87. Vinken, R., Schaeffer, A., Ji, R., 2005. Abiotic association of soil-borne monomeric Edwards, C.A., Arancon, N.Q., 2004. The use of earthworms in the breakdown of phenols with humic acids. Org. Geochem. 36, 583–593. organic wastes to produce vermicomposts and animal feed protein. In: Yardim, E.N., Edwards, C.A., 2003. Effects of organic and synthetic fertilizer sources Edwards, C.A. (Ed.), Earthworm Ecology, second ed. CRC Press, Boca Raton, FL, on pest and predatory insects associated with tomatoes. Phytoparasitica 31, London, New York, Washington, pp. 345–438. 324–329. Edwards,C.A.,Arancon,N.Q.,Emerson,E.,Pulliam,R.,December2007.Suppressionofplant Yardim, E.N., Arancon, N.Q., Edwards, C.A., Oliver, T.J., Byrne, R.J., 2006. Suppression parasiticnematodeandarthropodpestsbyvermicompost‘teas’.BioCycle,61–63. by vermicomposts of tomato hornworm (Manduca quinquemaculata) and El-Akkad, S., Zalat, S., 2000. Populus galls induced by Pemphigus aphids in Sinai. cucumber beetle (Acalymma vittatum) populations and damage. Pedobiologia Egypt. J. Biol. 2, 15–19. 50, 23–29.

Please cite this article in press as: Edwards, C.A., et al., Suppression of green peach aphid (Myzus persicae) (Sulz.), citrus..., Crop Protection (2009), doi:10.1016/j.cropro.2009.08.011