Managing Strawberry Pests with Chemical Pesticides and Non-Chemical Alternatives

ABSTRACT

Western tarnished bug or lygus bug (Lygus hesperus) is a major pest of California strawberries causing significant yield reduction. Other common insect pests include aphids (Chaetosiphon fragaefolii and Myzus persicae), greenhouse whitefly (Trialeurodes vaporariorum), and western flower thrips (Frankliniella occidentalis). Growers mainly depend on chemical pesticides for managing these pests. Limited control with some of the available chemical pesticides and the risk of resistance development due to their repeated use warrant a strong integrated pest management program where multiple tools can be utilized. Field studies conducted in commercial strawberry fields from 2012–14 in Santa Maria with an emphasis on managing L. hesperus demonstrated the potential of botanical and microbial pesticides. Replacing one or more applications of chemical pesticides with botanical and microbial alternatives and using them in different combinations can make a significant contribution to a sustainable management strategy.

KEYWORDS:

• Integrated pest management
• strawberry
• Lygus hesperus
• microbial control
• Beauveria bassiana
• Metarhizium brunneum
• azadirachtin

Introduction

Strawberry is an important commodity in California with an annual crop value of $2.2 billion (NASS, 2015). Western tarnished plant bug, Lygus hesperus Knight, is a major pest of strawberries in California causing significant reduction in marketable berry yield due to fruit deformation and is a target of several pesticide applications during the fruit production season (CDPR, 2014; Zalom et al., 2014). Many growers are unable to manage L. hesperus populations to manageable levels even with multiple applications of a variety of chemical pesticides (Dara, 2014). Various species of aphids, including the green peach aphid, Myzus persicae Sulzer; the strawberry aphid, Chaetosiphon fragaefolii (Cockerell); and other pests, such as the greenhouse whitefly, Trialeurodes vaporariorum (Westwood), and the western flower thrips, Frankliniella occidentalis (Pergande), cause varying levels of damage and some of them are important as vectors of the virus decline of strawberry (Dara, 2015; Zalom et al., 2014). According to the Pesticide Use Report of California Department of Pesticide Regulation (CDPR, 2014), nearly 91 tons of chemical insecticide and miticide active ingredients were used on strawberries in 2012. Among ~23 tons of biorational active ingredients that were additionally applied, 97% were Bacillus thuringiensis products used against lepidopteran pests. Apart from the release of various species of predatory mites against the twospotted spider mite, Tetranychus urticae Koch, pest management in strawberries is mainly dependent on chemical pesticides; integrated pest management (IPM) is generally limited to the rotation of pesticides in different modes of action groups. Since effective control of pests, such as L. hesperus, is a challenge with current management practices, there is a need to evaluate additional tools to improve control efficacy as well as reduce the risk of pesticide resistance with an overall goal of sustainable agriculture through a sound IPM program.

Entomopathogenic fungi, such as Beauveria bassiana (Balsamo) Vuillemin and Metarhizium brunneum Petch, are pathogenic to various strawberry pests and their close relatives (Liu et al., 2002; Ludwig and Oetting, 2002; Maniania et al., 2003; McGuire et al., 2006; Quesada-Moraga et al., 2006; Shi et al., 2008), but their potential for pest management in California strawberries is unknown. Field studies were conducted in commercial strawberry fields in Santa Maria, California from 2012 to 2014 in an effort to evaluate and integrate biopesticides based on entomopathogenic fungi (B. bassiana and M. brunneum), bacterium (Chromobacterium subtsugae), and neem (azadirachtin) with chemical pesticides. Rotating chemical pesticides among different modes of action groups and using botanical and microbial pesticides is expected to reduce the risk of insecticide resistance and chemical pesticide use in general.

Materials and methods

Various chemical and non-chemical pesticides were evaluated alone and in combination or rotation with each other in conventional strawberry fields in Santa Maria, California. In some treatments, biopesticides were used with reduced rates of chemicals in an effort to increase the pest control through additive or synergistic interactions. Treatments were administered by growers’ commercial spray equipment by professional pesticide applicators.

Each treatment had seven 22.9-m long and 1.4-m wide strawberry beds replicated four times in a randomized block design. Observations were made 5 or 6 days after each spray application to monitor various insect pest and natural enemy populations. On each observation date, 20 randomly selected plants from the middle three beds of each plot were sampled by beat tray method, where each sample plant was gently beaten with the lid of a container 3–4 times and the number of insects and natural enemies dislodged into the container were counted. Two beds on either side of the middle three sampling beds acted as a buffer. Natural enemies that were monitored during the period included bigeyed bug (Geocoris spp.), minute pirate bug (Orius spp.), lacewing (Chrysoperla spp. and Chrysopa spp.), damsel bug (Nabis spp.), lady beetle (multiple species), parasitoids (multiple species), and spiders (multiple species). Data were analyzed using ANOVA and significant means were separated using Tukey’s HSD test. Pest and natural enemy numbers were presented based on pre-treatment and post-treatment (average of three counts after each spray application) are presented.

2012 study

Strawberry cultivar PS-4634 was planted in Nov. 2011. Treatments were applied on 31 July, 8 Aug., and 15 Aug., 2012 using tractor-mounted equipment, with hollow cone nozzles on a spray boom that covered seven beds. Treatments included: (i) untreated control, (ii) acetamiprid (Assail 70 WP, United Phosphorus, Inc., King of Prussia, PA) at 210.2 g/ac, (iii) novaluron (Rimon 0.83EC, Chemtura Corp., Middlebury, CT) at 877 ml/ha + bifenthrin (Brigade WSB, FMC Corp., Philadelphia, PA) at 1.1 kg/ha, (iv) B. bassiana (BotaniGard 22WP, BioWorks, Inc., Rochester, NY) at 2.2 kg/ha, (v) B. bassiana at 2.2 kg/ha + azadirachtin (Molt-X, BioWorks, Inc., Rochester, NY) at 584.6 ml/ha, (vi) B. bassiana (BotaniGard 22WP) at 2.2 kg/ha + fenpropathrin (Danitol 2.4 EC, Valent USA Corp., Walnut Creek, CA) at 387.3 ml/ha (half the label rate), (vii) B. bassiana (BotaniGard 22WP) at 2.2 kg/ha + acetamiprid (Assail 70 WP) at 105.1 g/ha (half the label rate), (viii) azadirachtin (AzaGuard, BioSafe Systems, East Hartford, CT) at 584.6 ml/ha, and (ix) azadirachtin (AzaGuard) at 1169.3 ml/ha, all in 467.6 L/ha of spray volume. Non-ionic surfactant at 0.125% vol/vol concentration was used with B. bassiana at 0.25% concentration for the rest of the treatments. In 2012, treatment materials were not rotated during weekly applications.

2013 study

Experimental and sampling protocols were similar to those used in 2012 and the list of treatments is included in Table 1. Strawberry cultivar Virtue was planted in Oct. 2012 and treatments were administered on 14, 22, and 29 May 2013.

Table 1. List of active ingredients used in 2013 field study and their application rates per hectare.

Treatment	1st application (rate/acre)	2nd application (rate/acre)	3rd application (rate/acre)
1	Untreated	Untreated	Untreated
2	Acetamiprid (Assail 70 WP) 210.2 g	Acetamiprid 210.2 g	Acetamiprid 210.2 g
3	Flonicamid (Beleaf 50 SG, FMC Corp.) 196.2 g	Flonicamid 196.2 g	Bifenthrin + avermectin B1 (Athena, FMC Corp.) 1242.3 ml
4	Bifenthrin + avermectin B1 1242.3 ml	Bifenthrin + avermectin B1 1242.3 ml	Flonicamid 196.2 g
5	Novaluron 877 ml + bifenthrin 1.1 kg	Novaluron 877 ml + bifenthrin 1.1 kg	Piperonyl butoxide + pyrethrins (EverGreen Crop Protection EC 60-6, Valent USA) 1169.3 ml
6	Novaluron 877 ml + bifenthrin 1.1 kg	B. bassiana (BotaniGard ES, BioWorks, Inc.) 4.7 L + azadirachtin (Molt-X, BioWorks, Inc.) 584.6 ml	B. bassiana 4.7 L + azadirachtin 584.6 ml
7	Chromobacterium subtsugae (Grandevo, Marrone Bio Innovations, Davis, CA) 2.2 kg	C. subtsugae 2.2 kg	C. subtsugae 2.2 kg
8	B. bassiana 4.7 L + azadirachtin 584.6 ml	C. subtsugae 2.2 kg	Flonicamid 196.2 g
9	Piperonyl butoxide + pyrethrins 1169.3 ml	Piperonyl butoxide + pyrethrins 1169.3 ml	Acetamiprid 210.2 g
10	B. bassiana 4.7 L + low acetamiprid 105.1 g	B. bassiana 4.7 L + low flonicamid 98.1 g	B. bassiana 4.7 L + low bifenthrin + avermectin B1 730.8 ml
11	Sulfoxaflor (Sequoia, Dow AgroSciences, Indianapolis, IN) 328.9 ml	Sulfoxaflor 328.9 ml	B. bassiana 4.7 L + C. subtsugae 2.2 kg
12	Sulfoxaflor 219.2 ml	Sulfoxaflor 219.2 ml	Flonicamid 196.2 g

2014 study

Strawberry cultivar Del Rey was planted in Nov. 2013 and the treatments were applied on 4, 12, and 20 June 2014. A list of treatments is included in Table 2. The experimental procedure was similar to the previous years except that 1028.5 L/ha of spray volume were used due to the configuration of the grower’s spray equipment. Diatomaceous earth dust was applied using a backpack dust applicator.

Table 2. List of active ingredients used in 2014 field study and their application rates per hectare.

Treatment	1st application (rate/acre)	2nd application (rate/acre)	3rd application (rate/acre)
1	Untreated	Untreated	Untreated
2	Acetamiprid (Assail 70 WP) 210.2 g	Acetamiprid WP 210.2 g	Acetamiprid WP 210.2 g
3	Novaluron 877 ml + Acetamiprid (Assail 30SG) 483.4 g	Novaluron 877 ml + Sulfoxaflor 328.9 ml	Novaluron 877 ml + Acetamiprid SG 483.4 g
4	Novaluron 877 ml + Bifenthrin 1.1 kg	B. bassiana 4.7 L + Azadirachtin (Molt-X, BioWorks, Inc.) 584.6 ml	B. bassiana 4.7 L + Azadirachtin 584.6 ml
5	Novaluron 877 ml + Acetamiprid SG 483.4 g	Novaluron 877 ml + Flonicamid 196.2 g	Novaluron 877 ml + Acetamiprid SG 483.4 g
6	B. bassiana 4.7 L + Azadirachtin 584.6 ml	B. bassiana 4.7 L + low Flonicamid 98.1 g	Low B. bassiana 2.3 L + low Sulfoxaflor 210.2 g
7	Thiamethoxam 280.2 g	Thiamethoxam (Actara, Syngenta Crop Protection, Greensboro, NC) 280.2 g + Abamectin (Agri-Mek SC, Syngenta Crop Protection) 255.8 ml	B. bassiana 4.7 L + Azadirachtin 584.6 ml
8	High Sulfoxaflor 315.2 g	High Sulfoxaflor 315.2 g	High Sulfoxaflor 315.2 g
9	Low Sulfoxaflor 210.2 g	Low Sulfoxaflor 210.2 g	Low Sulfoxaflor 210.2 g
10	High Diatomaceous earth (Diafil 570, Imerys Performance Minerals, Cornwall, UK) slurry 78.5 kg	Low B. bassiana 2.3 L + low Sulfoxaflor 210.2 g	M. brunneum (Met 52EC, Novozymes BioAg Inc., Salem, VA) 1169.3 ml + Acetamiprid WP 210.2 g
11	Low Diatomaceous earth slurry 39.2 kg	Low Sulfoxaflor 210.2 g + Azadirachtin 584.6 ml	M. brunneum 1169.3 ml
12	High Diatomaceous earth dust 78.5 kg	Low B. bassiana 2.3 L + Acetamiprid WP 210.2 g	M. brunneum 1169.3 ml + Azadirachtin 584.6 ml

All treatments were administered in the evening except for those on 22 and 29 May 2013 due to logistics issues. Spray equipment, volume of the liquid, and surfactant concentrations in 2013 and 2014 were the same as in 2012. Applying entomopathogenic fungi in the evening provides several hours of favorable conditions for fungal establishment in the pest habitat. Cooler temperatures and leaf wetness during the night are beneficial for the fungus.

Results

Data from 2012, 2013, and 2014 studies are presented in Tables 3, 4, and 5, respectively.

Table 3. Mean number of various pest and natural enemy populations per 20 plants before (Pre) and after three pesticide applications (Post) during 2012 study.

	Lygus bug—All life stages		Lygus bug—Different life stages						Aphids		Western flower thrips		Greenhouse whitefly adults		Natural enemy complex
			1–3 instars		4–5 instars		Adults
Treatment	Pre	Post	Pre	Post	Pre	Post	Pre	Post	Pre	Post	Pre	Post	Pre	Post	Pre	Post
1	8.3	9.3	6.3	7.7	0.3	0.6	1.5	1.1	6.5	41.9a^z	1.3	12.5	55.0	32.5	10.8	6.8
2	14.0	2.0	12.8	1.1	0.0	0.0	1.0	0.9	13.5	2.9c	5.0	5.5	52.0	21.0	12.5	3.8
3	13.3	4.9	7.5	6.0	1.5	1.5	1.3	1.3	2.3	28.7abc	3.0	11.3	43.0	38.3	12.3	4.6
4	9.5	8.8	7.0	4.0	0.3	0.4	0.0	0.3	8.5	29.9abc	4.3	9.1	44.3	32.1	11.3	5.6
5	15.0	4.7	5.3	8.3	0.5	0.8	2.5	1.3	7.0	8.3bc	1.0	14.8	43.8	32.3	16.0	5.4
6	5.8	10.4	8.0	2.6	0.0	0.2	0.3	0.6	10.5	38.3ab	2.8	11.8	43.0	31.4	11.3	3.8
7	10.0	3.3	5.8	6.1	0.5	0.4	1.8	1.1	9.0	5.1c	3.5	8.2	54.0	28.8	9.3	3.8
8	6.8	7.6	13.3	4.8	0.3	0.3	0.5	0.7	12.5	36.3ab	2.8	13.5	42.5	35.9	11.8	5.0
9	14.8	5.8	11.0	3.8	0.5	0.3	0.0	0.8	11.3	19.3abc	2.5	11.3	45.5	35.6	13.5	5.3
P value	0.69	0.24	0.52	0.26	0.14	0.11	0.12	0.66	0.62	0.0005	0.76	0.11	0.55	0.10	0.60	0.09

^zMeans followed by the same or no letter are not statistically different using Tukey’s HSD.

Aphids

In 2012, aphid populations increased during the treatment period with more than a five-fold increase in untreated control (Table 3). During this time, acetamiprid standalone treatment caused nearly 78% reduction and the combination of B. bassiana and half the label rate of acetamiprid caused about 44% reduction in aphid numbers. Among the remaining treatments, where aphid populations increased, the combination of B. bassiana and azadirachtin limited the increase to 19%. In 2013, very low numbers of aphid infestations occurred during the study period. Average numbers varied from 0 to 0.33 per 20 plants during the post-treatment period, but there was no statistically significant difference among different treatments (P ≥ 0.05, data not shown). In 2014, a negligible number of aphids was seen only in a few treatments (data not shown).

Western tarnished plant bug

In 2012, the total number of nymphs and adults was similar in untreated control during the experimental period. Acetamiprid caused an 86% reduction (from 14 to 2 per 20 plants) in L. hesperus populations after three spray applications (Table 3). Beauveria bassiana standalone treatment caused a 58% reduction in L. hesperus numbers with the first application and only 11% with the second one (data not shown). But, B. bassiana could not limit increasing numbers afterwards and as a result the average control was only 8%. However, the combinations of B. bassiana with azadirachtin and half the label rate of acetamiprid caused 69% and 67% reduction, respectively, in L. hesperus numbers. While the lower rate of azadirachtin was similar to the untreated control, the higher rate brought down L. hesperus numbers by 60%. In general, the 1st to 3rd instar nymphs dominated L. hesperus populations compared to other life stages. Although there were no statistical differences (P ≥ 0.05), many treatments reduced the number of younger nymphs.

In 2013, L. hesperus numbers were relatively low (Table 4). Post-treatment averages showed significant differences (P < 0.05) among various treatments. When change in lygus populations as a result of treatments was considered, there was a 211% increase in treatment 7 (C. subtsugae) followed by 84%, 56%, and 46% in treatments 9 (two applications of piperonyl butroxide+pyrethrins and acetamiprid), 8 (B. bassiana, C. subtsugae, and flonicamid), and untreated control, respectively. A 61% reduction in L. hesperus was seen in treatment 10 (B. bassiana with low rates of acetamiprid, flonicamid, and bifenthrin+avermectin B1) followed by 53% in treatment 5 (two applications of novaluron+bifenthrin and piperonyl butoxide+pyrethrins), 50% in treatment 6 (novaluron+bifenthrin and two applications of B. bassiana+azadirachtin), 47% in treatment 12 (two applications of sulfoxaflor at low rate and flonicamid), and 46% in treatment 11 (two applications of sulfoxaflor at high rate and B. bassiana+C. subtsugae). When the average for nymphal and adult stages for post-treatment period was considered, the lowest number was found in treatments 5 and 10 followed by treatments 11 and 6 (Table 4). When individual life stages were considered, there were no statistically significant differences in the number of 4th and 5th instar nymphs and adults post-treatment (P ≥ 0.05). However, treatments 11, 5, and 3 (two applications of flonicamid and bifenthrin+avermectin) had the lowest number of 1st to 3rd instar nymphs (P < 0.0001). When pre- and post-treatment numbers were compared, many treatments failed to stop the increase of nymphal stages except for treatments 5 and 12 that resulted in 68% and 23% reduction in 4th and 5th instar nymphs, respectively.

Table 4. Mean number of various pest and natural enemy populations per 20 plants before (Pre) and after three pesticide applications (Post) during 2013 study.

Treatment	Lygus bug—All life stages		Lygus bug—Different life stages						Western flower thrips		Greenhouse whitefly adults	Natural enemy complex
			1–3 instars		4–5 instars		Adults
	Pre	Post	Pre	Post	Pre	Post	Pre	Post	Pre	Post	Post	Pre	Post
1	1.3	1.8ab^z	0.0	0.6bc	0.3	0.6	1.0	0.7	19.3	38.91	6.1ab	5.0	3.3a
2	1.5	1.8ab	0.0	0.8ab	0.3	0.7	1.3	0.3	29.3	31.59	5.1ab	6.3	2.3abc
3	1.0	1.0b	0.0	0.2c	0.3	0.3	0.8	0.5	30.3	31.25	4.3b	5.5	1.7abc
4	1.3	1.3ab	0.0	0.4bc	0.0	0.3	1.3	0.5	25.0	29.33	6.3ab	5.8	2.3abc
5	1.3	0.6b	0.3	0.2c	0.3	0.1	0.8	0.3	23.0	29.09	6.8ab	4.5	0.8c
6	1.5	0.8b	0.3	0.3bc	0.0	0.3	1.3	0.2	23.0	36.17	6.7ab	3.5	1.3bc
7	0.8	2.3ab	0.0	1.3a	0.3	0.8	0.5	0.3	19.3	36.17	7.5ab	5.5	2.0abc
8	0.8	1.2ab	0.0	0.5bc	0.0	0.3	0.8	0.4	28.5	38.58	8.9a	6.5	1.4abc
9	0.5	0.9b	0.0	0.3bc	0.3	0.3	0.3	0.3	26.5	33.7	5.9ab	6.5	2.4abc
10	1.5	0.6b	0.0	0.3bc	0.3	0.1	1.3	0.3	28.5	31.8	4.3b	4.8	1.6abc
11	1.3	0.7b	0.0	0.1c	0.0	0.3	1.3	0.3	27.3	34.8	6.6ab	5.8	1.9abc
12	1.8	0.9b	0.0	0.8bc	0.8	0.6	1.0	0.2	24.3	37.6	4.2b	3.0	3.0ab
P value	0.74	0.003	0.56	0.00001	0.29	0.35	0.87	0.62	0.42	0.14	0.02	0.98	0.002

^zMeans followed by the same or no letter are not statistically different using Tukey’s HSD.

In 2014, L. hesperus numbers increased in all treatments after treatment and there were no statistical differences among treatments (P ≥ 0.05) (Table 5). However, when the percent change post-treatment was considered, population buildup was less in some treatments. The high rate of sulfoxaflor (treatment 8) limited the increase to 14% followed by 17% from the rotation of diatomaceous earth high rate–B. bassiana+acetamiprid–M. brunneum+azadirachtin (treatment 10). When B. bassiana+azadirachtin combination was applied twice after the novaluron+bifenthrin combination (treatment 4) there was a 54% increase in population buildup. Untreated control and acetamiprid WP had the highest lygus numbers with 383% and 1083% increase, respectively. Younger instar nymphs increased in all treatments after spray applications, but older nymph and adult numbers were reduced in some treatments.

Table 5. Mean number of various pest and natural enemy populations per 20 plants before (Pre) and after three pesticide applications (Post) during 2014 study.

Treatment	Lygus bug—all life stages		Lygus bug—Different life stages						Western flower thrips		Greenhouse whitefly adults		Natural enemy complex
			1–3 instars		4–5 instars		Adults
	Pre	Post	Pre	Post	Pre	Post	Pre	Post	Pre	Post	Pre	Post	Pre	Post
1	1.0	4.8	0.3	3.8	0.5	0.4	0.3	0.7	282.3	145.7ab^z	3.3	3.7	53.3	31.5a
2	0.5	5.9	0.3	5.2	0.0	0.4	0.3	0.3	272.3	177.2a	5.0	2.8	56.3	7.7d
3	1.5	4.0	0.8	3.6	0.0	0.2	0.8	0.3	252.3	101.6b	1.5	1.1	45.3	21.1abc
4	2.8	4.0	1.0	3.2	0.3	0.2	1.5	0.6	248.3	118.7ab	3.0	1.8	57.0	7.2d
5	1.8	2.6	1.5	2.0	0.0	0.3	0.3	0.3	248.3	104.3ab	3.5	0.8	50.3	12.8cd
6	1.3	5.1	0.8	4.4	0.5	0.5	0.0	0.2	207.0	125.0ab	2.8	1.5	56.8	24.8ab
7	1.3	4.8	0.5	3.9	0.5	0.5	0.3	0.3	284.5	120.0ab	2.3	2.1	53.0	8.8d
8	4.3	4.8	3.5	4.4	0.8	0.2	0.0	0.3	240.5	122.2ab	5.0	1.8	65.8	12.2cd
9	1.8	3.2	0.5	2.3	0.8	0.3	0.5	0.6	231.8	127.3ab	7.3	1.6	53.8	14.9bcd
10	1.8	3.8	0.8	3.3	0.3	0.2	0.8	0.3	266.3	121.4ab	5.5	2.0	48.8	20.0bc
11	1.0	4.7	0.3	3.8	0.5	0.5	0.3	0.3	238.5	110.5ab	1.3	1.5	55.0	21.0bc
12	3.0	3.5	1.5	2.8	1.3	0.2	0.3	0.5	303.8	97.6b	3.3	2.2	50.3	14.4bcd
P value	0.07	0.68	0.10	0.67	0.78	0.51	0.07	0.59	0.84	0.04	0.54	0.51	0.91	0.00001

^zMeans followed by the same or no letter are not statistically different using Tukey’s HSD.

Western flower thrips

In 2012, there was a general increase in F. occidentalis numbers in all treatments (Table 3). However, the increase was relatively less in acetamiprid (10%) followed by B. bassiana (114%) and the combination of B. bassiana and low rate of acetamiprid (133%) compared to a 900% increase in untreated control. The combination of B. bassiana and azadirachtin also had a very high increase of 1375% post-treatment in F. occidentalis numbers. In 2013, there was an increase in F. occidentalis numbers after the first spray application and treatments appeared to show their effect following the second application (data not shown). When the post-treatment change was considered, there was a 102% increase in untreated control. The treatments that had the lowest population buildup were 3 (two flonicamid applications followed by bifenthrin+avermectin B1), 2 (acetamiprid), and 10 (B. bassiana with low rates of acetamiprid, flonicamid, and bifenthrin+avermectin B1) with 3%, 8%, and 12% increase in F. occidenatalis, respectively (Table 4). Unlike the previous 2 years, F. occidentalis were very high in 2014, but there was an overall reduction in their numbers post-treatment (Table 5). There was a 48% reduction in untreated control while it varied from 35% in treatment 2 (acetamiprid WP) to 68% in treatment 12 (diatomaceous earth dust high rate followed by B. bassiana+acetamiprid WP and M. brunneum+azadirachtin).

Greenhouse whitefly

In 2012, there was a general reduction in T. vaporariorum adult numbers during the observation period (Table 3). Acetamiprid alone and at the half labeled rate along with B. bassiana caused a 60% and 47% reduction, respectively. In 2013, relatively low numbers of T. vaporariorum adults were observed during the observation period (Table 4). Pre-treatment counts were not available, but the number of adults for the post-treatment period varied significantly among treatments (P = 0.03). The lowest numbers were seen in treatments 3 (two flonicamid applications followed by bifenthrin+avermectin B1), 10 (B. bassiana with low rates of acetamiprid, flonicamid, and bifenthrin+avermectin B1), and 12 (two applications of sulfoxaflor at low rate followed by flonicamid). Low T. vaporariorum numbers were seen during the 2014 study also (Table 5). In general, there was a 7% to 78% reduction after three applications among different treatments except for a 13% increase in untreated control and 20% increase in treatment 11 (low diatomaceous earth slurry–low sulfoxaflor+azadirachtin–M. brunneum).

Natural enemy complex

All species of natural enemies were combined for the comparison. There was a general decline in natural enemy populations during the observation period in all three years (Tables 3–5). There was no statistical difference among treatments in 2012 (P ≥ 0.05), but post-treatment averages significantly differed in 2013 (P = 0.002) and 2014 (P < 0.0001). In general, untreated control had lower reduction in natural enemy populations in all 3 years compared to the rest of the treatments. Natural enemy populations were reduced by 37%, 35%, and 41% in 2012, 2013, and 2014, respectively, while the reduction in their numbers among different treatments varied from 50–69%, 61–83%, and 53–86% during those years except for no change in treatment 12 (two sulfoxaflor applications at low rate followed by flonicamid) in 2013.

Discussion

Except for a small field study in New York (Kovach and English-Loeb, 1996) and a greenhouse study in California (Dara et al., 2014), there are no large-scale field studies to demonstrate the efficacy of commercial formulations of botanical and microbial pesticides for strawberry pest management. The goal of the current studies was to evaluate the potential of biopesticides and generate information that is useful for pest management in strawberry, a high value commodity in California. Failure to achieve good control of L. hesperus populations with currently registered chemical pesticides alone warranted the need for a sound IPM program with multiple control options (Dara, 2014). Varying levels of efficacy of acetamiprid during different years in the current studies could be due to pesticide resistance issues in L. hesperus populations in the Santa Maria area. The idea behind using entomopathogenic fungi along with low rates of chemical pesticides is to increase or maintain the control efficacy while reducing the amount of chemical pesticide use as infection by entomopathogenic fungi can take time before pest populations are reduced (Dara, 2013). Since azadirachtin acts mainly as an insect growth regulator in addition to its insecticidal and repellent properties, it is a botanical equivalent of the chemical insect growth regulator, novaluron. Entomopathogenic fungi can infect all life stages, but nymphal stages could be less susceptible if they molt before infection takes place. Thus, the combination of azadirachtin and B. bassiana or M. brunneum targets immature and adult stages of various pests. Some chemical pesticides can have a synergistic effect on the growth and infectivity of entomopathogenic fungi (Dara and Hountondji, 2001, Furlong and Groden, 2001). Laboratory studies that showed improved efficacy of B. bassiana along with low rates of certain chemical pesticides against L. hesperus adults (Dara et al., 2014) led to exploring the efficacy of chemical and non-chemical combinations and rotations in the current field studies.

In general, results suggested that biopesticides can be an important component of pest management. While B. bassiana alone provided limited control of L. hesperus compared to some treatments, it either limited the population growth or reduced their numbers when used in combination with azadirachtin or chemical pesticides. Diatomaceous earth had some efficacy against L. hesperus, but left a white deposit on strawberries, which rendered them unmarketable. While the efficacy was variable due to low numbers or a general reduction in populations of other pests, azadirachtin, B. bassiana, and M. brunneum demonstrated that they can be important options in strawberry pest management especially for L. hesperus. All treatments appeared to have some negative impact on natural enemy populations, but no specific trend was observed to determine if chemical or biopesticides were better than the other.

Since conventional growers generally tend to use chemical pesticides, efficacious materials are likely to be repeatedly used over time. These studies show potential treatment options where both chemical and non-chemical pesticides are placed in a balanced manner. Using botanical and microbial pesticides in combination and rotation with effective chemical pesticides can help reduce the volume of chemical pesticides used, enhancing the efficacy of pest management that is otherwise challenging with chemicals alone. This approach also reduces the risk of pesticide resistance, and extends the longevity of new and existing chemicals. These studies support the use of biopesticides in conventional strawberry production and possibly promote their use in other cropping systems.

Acknowledgments

I wish to thank Dave Peck, Manzanita Berry Farms and Francisco Bautista, Goodwin Farms, Santa Maria for allowing to conduct research on their farms and Jacob Conway, Thomas Crottogini, Michael McNulty, Maria Murrietta, Andrew Reade, Anthony Reade, and Ryan Sheppard for their technical assistance.

Funding

I wish to thank the pesticide company partners for funding.