Managing Western Flower Thrips (Thysanoptera: Thripidae) on Lettuce and Green Peach Aphid and Cabbage Aphid (Hemiptera: Aphididae) on Broccoli with Chemical Insecticides and the Entomopathogenic Fungus Beauveria bassiana (Hypocreales: Clavicipitaceae)



Surendra K. Dara*
University of California Cooperative Extension, 2156 Sierra Way, Ste. C, San Luis Obispo, CA 93401


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© 2017 Surendra K. Dara.

open-access license: This is an open access article distributed under the terms of the Creative Commons Attribution 4.0 International Public License (CC-BY 4.0), a copy of which is available at: https://creativecommons.org/licenses/by/4.0/legalcode. This license permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

* Address correspondence to this authors at the University of California Cooperative Extension, 2156 Sierra Way, Ste. C, San Luis Obispo, CA 93401, Tel: 805-720-1700, Fax: 805-781-4316; E-mail: skdara@ucdavis.edu


Abstract

Aims:

Lettuce and broccoli are high value vegetable crops in California. The western flower thrips, Frankliniella occidentalis on lettuce, and the cabbage aphid, Brevicoryne brassicae and the green peach aphid, Myzus persicae on broccoli are important insect pests that are frequently managed with chemical insecticides.

Observation:

Efficacy of various chemical insecticides and the entomopathogenic fungus Beauveria bassiana was evaluated against these pests in field studies in the Santa Maria area of California. Some insecticides varied in their efficacy against F. occidentalis from year to year and against different aphid species.

Conclusion:

A new insecticide sulfoxaflor provided good control of aphids on broccoli. Beauveria bassiana demonstrated a potential for broccoli and lettuce integrated pest management.

Keywords: Beauveria bassiana, Cabbage aphid, Green peach aphid, Western flower thrips.



1. INTRODUCTION

Lettuce and broccoli are important agricultural crops in California [1]. Lettuce is grown in 200,000 acres and is the 8th most important agricultural commodity with a crop value of $1.4 billion while broccoli, grown in 119,000, acres is ranked 17 with a value of $645 million. The western flower thrips, Frankliniella occidentalis (Pergande) on lettuce and the cabbage aphid, Brevicoryne brassicae (Linnaeus) on broccoli are important insect pests which require regular insecticidal treatments [2]. The role of F. occidentalis as a vector of tomato spotted wilt virus is more important than the scarring caused by its feeding. In broccoli, B. brassicae can stunt plant growth and even cause plant death at high infestation levels [3]. The green peach aphid, Myzus persicae (Sulzer) is also a frequent pest of broccoli, but is less important because it feeds mostly on older leaves. However, it requires insecticidal treatments as the presence of aphids on harvested broccoli reduces crop value.

Among hundreds of thousands of pounds of insecticide active ingredients applied on lettuce and broccoli in 2012, entomopathogenic fungus Beauveria bassiana accounts for a negligible 40 lb (pounds) [4]. Repeated use of chemical insecticides can lead to the development of resistance and undermines integrated pest management (IPM) efforts. Different species of aphids and F. occidentalis are known to develop resistance to various insecticides around the world and the risk is especially higher for the latter [5-9]. Successful IPM involves rotation of insecticides with different modes of action and alternating chemicals with non-chemical options to reduce the risk of pesticide resistance. Considering entomopathogenic fungi such as B. bassiana can help IPM practices. Beauveria bassiana is pathogenic to several pests and its efficacy against F. occidentalis was demonstrated under greenhouse conditions in different parts of the world [10-13]. Pathogenicity of B. bassiana against different species of aphids including M. persicae and B. brassicae has also been studied under laboratory conditions [14-16], but information on its field efficacy against vegetable pest management especially in California is lacking.

Field studies were conducted in 2011 and 2012 in the Santa Maria area to evaluate the efficacy of existing, newly registered, and experimental insecticides. In the 2012 studies, a commercial formulation of B. bassiana was also evaluated. Results of these studies are important for vegetable IPM in California.

2. MATERIALS AND METHODS

2.1. F. occidentalis on Lettuce

Studies were conducted in commercial lettuce fields in the Santa Maria area. Each plot included a 10’ long and 64” wide bed with 5 rows of lettuce and arranged in a randomized complete block design with four replications. Insecticides were applied using a CO2-pressurized backpack sprayer equipped with three flat fan nozzles that covered the entire bed. A spray volume of 50 gallons/ac was used for all treatments except for B. bassiana where 100 gallons/ac were used. A non-ionic surfactant was included at 0.1% (v/v) concentration for acetamiprid, 0.125% for B. bassiana, and 0.25% for the rest of the treatments. The number of F. occidentalis was monitored before treatment and two to three times after each spray application. On each sampling date, four plants in 2011 and five plants in 2012 were randomly collected from each plot and gently beaten on a wire mesh over a plastic container with a 9X5” yellow sticky card placed inside according to the method described by Palumbo [17]. The number of F. occidentalis dislodged from the plants and stuck to the card were counted under a dissecting microscope. Data were summarized by the analysis of variance and significant means were separated using Tukey’s HSD test.

2.1.1. 2011 Study

A lettuce field was planted in cultivar Durango on June 8. Treatments included an untreated control, acetamiprid (Assail 70 WP, 1.7 oz/ac), spinetoram (Radiant SC, 7 fl oz/ac), methomyl (Lannate SP, 0.75 lb/ac), tolfenpyrad (Torac, 21 fl oz/ac), and a combination of tolfenpyrad (Torac, 21 fl oz/ac) and methomyl (Lannate SP, 0.75 lb/ac). Treatments were administered on July 16, July 22, and August 3.

2.1.2. 2012 Study

A field was planted in cultivar Vandenberg on April 6. Treatments included an untreated control, acetamiprid (Assail 30 SD, 4 oz/ac), spinetoram (Radiant SC, 8 fl oz/ac), B. bassiana strain GHA (BotaniGard 22 WP, 2 lb/ac), methomyl (Lannate SP, 0.75 lb/ac), a combination of tolfenpyrad (Torac, 21 fl oz/ac) and methomyl (Lannate SP, 0.75 lb/ac), and an experimental insecticide referred to as NNI-1171 (21 fl oz/ac). Treatments were administered on May 16, May 24, and June 6.

2.2. M. persicae and B. brassicae on Broccoli

Study was conducted in a commercial broccoli field in Santa Maria in 2012. The field was planted in cultivar Beneforté on July 31. Each plot was 20’ long and 64” wide with 5 rows of broccoli replicated four times in a randomized complete block design. Treatments included an untreated control, acetamiprid (Assail 30 SG, 4 oz/ac), B. bassiana (BotaniGard 22 WP, 2 lb/ac), tolfenpyrad (Torac, 21 fl oz/ac), an experimental insecticide, pyrifluquinazon (3.2 fl oz/ac), NNI-1171 (21 fl oz/ac), and sulfoxaflor (Sequoia), at two rates (1.5 and 2 fl oz/ac). All treatments were applied using a CO2-pressurized backpack sprayer with three flat fan nozzles. A spray volume of 50 gal/acre was used for all, but B. bassiana which used 100 gal/ac as per the label recommendations. A non-ionic surfactant was added at 0.1% (v/v) concentration for acetamiprid, 0.125% for B. bassiana, and 0.25% for the remaining treatments. Treatments were initiated on September 5 and repeated on September 25. The number of M. persicae and B. brassicae were monitored on five randomly selected plants per plot prior to the first application and 3, 7, and 12 or 13 days after each spray application. On each observation date, sample plants were pulled out and the number of aphids on each leaf was counted. Data were subjected to analysis of variance and significant means were separated using Tukey’s HSD test.

3. RESULTS AND DISCUSSION

3.1. F. occidentalis On Lettuce

3.1.1. 2011 Study

Average number of F. occidentalis gradually increased towards the middle of the observation period and declined thereafter Table 1. Significant differences (P < 0.05) among treatments appeared starting from 3 days after the second spray application. When the average for seven post-treatment sampling dates was considered, spinetoram, methomyl, tolfenpyrad, and the combination of tolfenpyrad and methomyl caused a significant reduction (P = 0.0001) in F. occidentalis Fig. (1). Acetamiprid could not limit population build up.

Table 1. Mean number of F. occidentalis per plot in 2011 before and 3, 7, and 11 days after treatment (DAT).
Treatment Pre-treatment I Spray 3DAT I Spray 7DAT II Spray 3DAT II Spray 7DAT II Spray 11DAT III Spray 3DAT III Spray 7DAT
Untreated 0.50±0.50 6.75±3.83 7.75±1.88 8.00±1.87a* 17.25±3.59a 6.50±1.04ab 4.75±1.49ab 7.00±1.68ab
Acetamiprid 1.25±1.25 2.75±1.79 4.25±2.01 4.75±0.47ab 15.25±3.75ab 8.75±1.03a 7.25±2.05a 9.50±3.22a
Spinetoram 1.75±0.75 1.75±0.62 4.00±0.91 3.00±1.47b 5.75±1.03bc 3.00±0.91b 2.00±0.91b 2.00±1.08bc
Methomyl 1.25±0.62 1.25±0.25 2.50±0.86 2.50±0.86b 4.00±1.22c 3.25±0.85b 2.00±0.70b 0.75±0.25c
Tolfenpyrad 0.00 1.00±0.57 3.75±0.62 3.50±1.19b 6.00±1.08bc 2.50±1.19b 1.50±0.64b 2.25±1.03bc
Tolfenpyrad+Methomyl 1.25±0.47 1.25±0.62 3.25±0.75 3.50±0.50b 3.75±1.10c 3.50±0.64b 2.00±0.70b 1.00±0.40bc
P value 0.537 0.228 0.061 0.005 0.002 0.001 0.012 0.001
*Means followed by the same or no letter within each column are not significantly different using Tukey’s HSD.
Fig. (1). Number of F. occidentalis per plot before and after (average of seven sampling dates) treatment in 2011. Bars with no or same letters are not significantly different using Tukey’s HSD (P ≥ 0.05).

3.1.2. 2012 Study

The number of F. occidentalis was similar before the initiation of the experiment with a general decline after the second spray application and an increase thereafter Table (2). Significant differences (P < 0.05) among treatments were observed 7 and 12 days after the second spray application and 3 days after the third spray application. Post-treatment average during the seven sampling dates showed that tolfenpyrad alone and in combination with methomyl significantly reduced (P < 0.00001) F. occidentalis numbers compared to untreated control, acetamiprid, and B. bassiana Fig. (2). Plots treated with spinetoram, B. bassiana, and NNI-1171 had moderate levels of F. occidentalis during the post-treatment observation period.

Tabel 2. Mean number of F. occidentalis per plot in 2012 before and 3, 7, and 12 days after treatment (DAT).
Treatment Pre-treatment I Spray 3DAT I Spray 7DAT II Spray 3DAT II Spray 7DAT II Spray 12DAT III Spray 3DAT III Spray 7DAT
Untreated 6.25±3.27 2.50±1.04 14.50±3.40 9.75±0.47 20.00±3.74a* 17.25±2.05ab 11.75±1.88ab 9.25±3.11
Acetamiprid 3.75±0.25 3.50±1.19 14.25±2.71 9.25±2.17 11.75±2.62ab 18.75±3.42a 16.75±4.13a 13.50±3.06
Spinetoram 5.25±1.54 2.25±1.10 8.00±1.58 5.50±1.70 9.00±2.73b 15.75±1.88ab 8.50±1.19ab 7.25±0.94
B. bassiana 5.75±1.25 3.75±0.62 11.25±2.56 6.50±1.50 10.25±1.10ab 12.50±1.32ab 11.75±2.46ab 9.75±2.13
Tolfenpyrad 7.75±1.03 0.50±0.28 7.00±2.27 2.50±0.86 3.25±1.25b 8.25±0.62b 3.50±0.50b 8.75±1.43
Tolfen.+Methomyl 6.25±1.97 1.75±0.62 7.50±1.32 3.75±1.70 9.25±2.68ab 6.75±1.79 b 4.75±1.54ab 6.25±2.25
NNI-1171 5.00±1.68 1.00±0.40 13.00±4.81 6.00±2.27 4.75±2.42b 11.00±4.50ab 4.00±1.82b 3.75±1.43
P value 0.696 0.151 0.235 0.121 0.002 0.025 0.013 0.087
*Means followed by the same or no letter within each column are not significantly different using Tukey’s HSD.

There were minor variations in the efficacy of various insecticides from 2011 to 2012, but acetamiprid could not control F. occidentalis in both years. Acetamiprid, which was used as a grower standard in the current studies, effectively controlled F. occidentalis in laboratory and greenhouse studies on lettuce, pepper, and tomato in an earlier study by Broughton and Herron [18]. Results indicate possible resistance to acetamiprid and suggest a need for rotating insecticides from different modes of action groups both as a means of resistance management and to achieve effective control. Efficacy of B. bassiana was similar to spinetoram and NNI-1171 among the remaining treatments. Significant reduction in the numbers of F. occidentalis larvae, adult or soil-dwelling stages was seen in different laboratory or greenhouse studies using commercial or local isolates of B. bassiana [13, 19, 10, 20, 21]. However, data on the field efficacy of B. bassiana in lettuce, especially in California is lacking and the current studies provide useful insights into the understanding of field efficacy of a commonly available entomopathogenic fungus.

3.2. Aphids on Broccoli

M. persicae - All treatments reduced the number of M. persicae by the end of the observation period except for acetamiprid Table (3). Significant differences among treatments were seen only on 3 (P = 0.01) and 12 (P = 0.02) days after treatment. When the average for six post-treatment sampling dates was considered, sulfoxaflor at the low rate was the only treatment that had significantly (P = 0.03) lower number of M. persicae than untreated control Fig. (3). When the pre- and post-treatment averages were compared, there was a slight increase in M. persicae in acetamiprid and pyrifluquinazon treatments whereas sulfoxaflor high rate caused a 73% reduction followed by sulfoxaflor low rate (47%), NNI-1171 (44%) and B. bassiana (40%).

Table 3. Mean number of M. persicae per plot in 2012 before and 3, 7, 12 or 13 days after treatment (DAT).
Treatment Pre-treatment I Spray 3DAT I Spray 7DAT I Spray 13DAT II Spray 3DAT II Spray 7DAT II Spray 12DAT
Untreated 9.75±2.86 6.75±4.09 9.75±2.52 6.50±3.47 13.25±2.01a* 7.50±3.30 9.50±4.21a
Acetamiprid 3.75±2.25 6.75±2.78 4.50±2.59 1.75±1.03 0.75±0.47b 6.50±3.84 6.25±3.11ab
B. bassiana 11.00±6.39 9.25±2.92 10.25±3.37 5.50±2.25 5.00±1.77ab 8.50±4.64 1.00±0.40ab
Tolfenpyrad 7.50±4.17 6.00±2.79 4.25±3.27 8.00±2.08 4.50±3.06ab 3.50±2.17 2.75±1.25ab
Pyrifluquinazon 3.00±2.04 0.50±0.50 6.25±3.56 6.50±4.01 3.25±2.92b 2.00±1.22 0.75±0.47ab
NNI-1171 5.75±2.42 1.50±1.50 2.00±2.00 4.25±2.65 2.25±1.31b 8.75±8.09 0.50±0.50ab
Sulfoxaflor 1.5 2.75±1.25 3.25±1.43 0.75±0.47 4.25±3.59 0.50±0.50b 0 0b
Sulfoxaflor 2.0 9.00±6.12 0.75±0.47 2.75±2.42 2.25±2.25 3.50±3.17b 3.00±2.67 2.50±0.86ab
P value 0.694 0.095 0.075 0.771 0.005 0.703 0.023
*Means followed by the same or no letter within each column are not significantly different using Tukey’s HSD.
Fig. (2). Number of F. occidentalis per plot before and after (average of seven sampling dates) treatment in 2012. Bars with no or same letters are not significantly different using Tukey’s HSD (P ≥ 0.05).

B. brassicae - There was a general reduction in B. brassicae numbers in all plots Table (4). Significant differences among treatments were seen only on 3 and 7 days after the first spray application (P = 0.01). When the post-treatment average was considered, sulfoxaflor and acetamiprid had significantly lower (P = 0.003) numbers of B. brassicae compared to untreated control Fig. (4). When the pre- and post-treatment averages were compared, acetamiprid and sulfoxaflor treatments caused about 90% reduction in B. brassicae followed by pyrifluquinazon, which caused about 80% reduction.

Table 4. Mean number of B. brassicae per plot in 2012 before and 3, 7, 12 or 13 days after treatment (DAT).
Treatment Pre-treatment I Spray 3DAT I Spray 7DAT I Spray 13DAT II Spray 3DAT II Spray 7DAT II Spray 12DAT
Untreated 10.00±1.08 5.75±5.10ab* 8.75±2.35a 10.00±4.91 9.50±4.03 4.25±3.61 7.75±3.92
Acetamiprid 14.50±10.71 0.50±0.28b 0.75±0.75b 2.25±1.93 0 3.50±2.36 0
B. bassiana 9.00±1.87 19.50±5.89a 5.75±2.25ab 14.00±3.48 1.50±0.95 1.00±0.57 1.75±1.18
Tolfenpyrad 8.00±4.88 3.50±2.59b 4.75±1.79ab 5.00±2.79 4.00±3.36 0 7.75±4.32
Pyrifluquinazon 9.75±3.75 0b 1.50±0.86ab 2.25±0.75 1.00±1.00 7.25±5.99 0
NNI-1171 2.50±1.65 4.25±3.61ab 0.25±0.25b 2.50±1.32 1.75±1.43 12.25±10.34 0.75±0.75
Sulfoxaflor 1.5 9.75±5.10 0.75±0.47b 2.00±0.81ab 2.25±1.31 1.25±1.25 0 0
Sulfoxaflor 2.0 15.50±3.86 0.50±0.50b 2.25±2.25ab 3.25±3.25 2.75±1.60 0 0.50±0.28
P value 0.579 0.006 0.010 0.048 0.129 0.494 0.050
*Means followed by the same or no letter within each column are not significantly different using Tukey’s HSD.

Efficacy of some insecticides varied between species of aphids. In general, sulfoxaflor provided a good control of both species. Acetamiprid and pyrifluquinazon could not limit the increase in M. persicae, but caused a significant reduction in B. brassicae. On the other hand, NNI-1171 reduced M. persicae numbers, but could not control B. brassicae. Both B. bassiana and tolfenpyrad reduced both species of aphids, but B. bassiana was more effective against M. persicae with a 40% reduction post-treatment compared to B. brassicae with only 19% reduction. Efficacy of B. bassiana could vary depending on the isolate and insect species [14]. For example, Ying, Feng, Xu, and Ma [22] reported effective control of M. persicae in field cabbage with a Chinese isolate, while Butt, Ibrahim, Ball, and Clark [23] found that European isolates of B. bassiana were less effective against M. persicae and other pests of Chinese cabbage compared to the Brazilian or European isolates of another entomopathogenic fungus Metarhizium anisopliae. Laboratory assays also showed that B. bassiana isolates varied in their pathogenicity to M. persicae [24] and B. brassicae [25].

Fig. (3). Number of M. persicae per plot before and after (average of six sampling dates) treatment in 2012. Bars with no or same letters are not significantly different using Tukey’s HSD (P ≥ 0.05).

Fig. (4). Number of B. brassicae per plot before and after (average of six sampling dates) treatment in 2012. Bars with no or same letters are not significantly different using Tukey’s HSD (P ≥ 0.05).

Since entomopathogenic fungi take time for the infection process, combining B. bassiana with other insecticides might improve its efficacy against vegetable pests. Such a positive impact was seen against F. occidentalis and other pests in California strawberries when B. bassiana was combined with chemical pesticides or azadirachtin [26]. Similarly, root aphids in organic celery were effectively controlled when B. bassiana was used in combination with azadirachtin [27].

These studies demonstrate the efficacy of various chemical insecticides and B. bassiana against some of the lettuce and broccoli pests and provide useful information for growers. While chemical pesticides are more readily used by growers due to various reasons including low cost and generally perceived higher efficacy, microbial pesticides such as those based on B. bassiana are also important for reducing the risk of pesticide resistance and maintaining environmental sustainability. However, limited information is available on microbial control of vegetable pests especially in California. Current studies evaluated the potential of B. bassiana in vegetable IPM. In circumstances where microbial pesticides alone are not very effective, combining or rotating them with chemical pesticides or other control options can be effective [28]. Using insecticides with different modes of action along with non-chemical alternatives is critical for sustainable pest management practices.

CONFLICT OF INTEREST

The authors confirm that this article content has no conflict of interest.

ACKNOWLEDGEMENTS

Thanks to Frank Costa, Oceanview Flowers, Lompoc and San Ysidro Farms, Nipomo for allowing to conduct research on their farms, pesticide industry partners for the financial support, and Thomas Crottogini and Pedro Villela for the technical assistance.

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