Article History Keywords Efficiency, Neonicotinoids, Sulfoxaflor, Sucking

Egypt. J. Plant Prot. Res. Inst. (2020), 3 (1): 316 - 325

Egyptian Journal of Plant Protection Research Institute

www.ejppri.eg.net

Effects of neonicotinoids and sulfoxaflor application against sucking pests infesting watermelon and their associated predators Ahmed, A. Barrania Plant Protection Research Institute, Etay El-Baroud, Agricultural Research Station, Agricultural Research Center, Egypt. ARTICLE INFO Abstract: Article History Field studies were carried out during 2018 and 2019 summer Received: 1 / 2/ 2020 seasons, at Nubarya district, El-Beheira Governorate to evaluate the Accepted: 19/ 3/2020 effects of some neonicotinoid insecticides (Imidacloprid, clothianidin, Keywords thiamethoxam and acetamiprid) compared with sulfoxaflor, at Efficiency, recommended rates against sucking pests infesting watermelon and neonicotinoids, their associated predators. Results showed that, all treatments exhibited sulfoxaflor, sucking excellent and fast action activity against Bemisia tabaci (Gennadius) insects, predators (‎Hemiptera: Aleyrodidae) and the least reduction percentages were and watermelon. recorded by acetamiprid at both seasons. Under the same conditions, neonicotinoid insecticides have toxic effect on predators; Chrysoperla carnea (Stephens) (Neuroptera:‎Chrysopidae), Paederus alfierii Koch. (Coleoptera: Staphylinidae) and Coccinella spp.) (‎Coleoptera‎: ‎Coccinellidae) while, sulfoxaflor has slightly toxic effect. The present study suggests neonicotinoid insecticides can be disruptive to natural and biological control by reducing insect predators populations, so the population of Tetranychus urticae Koch. (Acari: Tetranychidae) will be increased during both seasons. Yet, sulfoxaflor is also reported as being slightly harmful to biological control agents, it as a preferred insecticide, with less harmful effects on the fitness components of natural enemies, for integrated pest management of sucking insects (B. tabaci) on watermelon plantations.

Introduction Watermelon, a popular summer Aleyrodidae) and Spodoptera sp. vegetable crop worldwide (Wu et al., (Lepidoptera: Noctuidae) larvae (Wu et 2014) is an important crop and provides al., 2012). The sweet potato whitefly, B. phytochemicals. However, watermelon is tabaci attacks watermelon and a wide susceptible to numerous diseases and range of other plant species and on a pests, such as Tetranychus urticae Koch. global scale. In addition to injuries from (Acari: Tetranychidae), Aphis direct feeding, problems from this pest gossypii Glover (Hemiptera: Aphididae), are intensified because its vectors Bemisia tabaci (Gennadius) (‎Hemiptera:

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Barrania, 2020 over 100 plant viruses (Jones, 2003 and The sulfoximines are a new class of Simmons et al., 2010). As it is farmed insecticides targeting sap-feeding insects primarily by protected and successive including the aphids, whiteflies, hoppers, cultivation techniques, many pesticides and lygus (Nawaz et al., 2018; Babcock are required for the control of pests (Park et al., 2011 and Zhu et al., 2011), that are et al., 2010). resistant to other classes of insecticides, Neonicotinoid insecticides and that are resistant to the represent the fastest-growing class of neonicotinoids (Sparks et al., 2013). insecticides introduced to the market Sulfoxaflor is the initial compound in this since the launch of pyrethroids (Nauen class selected for commercial and Bretschneider, 2002) and are the development and is an agonist at insect most used class of insecticides for nicotinic acetylcholine receptors controlling sucking insects (Jiang et al., (nAChRs) (Liao et al.,2017; Watson et 2019). Neonicotinoids interfere with the al., 2017 and Sparks et al., 2013). Yet, nicotinic acetylcholine receptor and sulfoxaflor is also reported as being therefore have specific activity against slightly harmful to biological control the insect nervous system (Maienfisch et agents, including Nesidiocoris tenuis al., 2001). It is considered an important (Reuter) (Hemiptera: Miridae), group of insecticides being used against Chrysoperla carnea (Stephens) sucking insects for several years (Neuroptera: Chrysopidae), and Adalia (Muhammad et al., 2011), especially bipunctata (L.) (Coleoptera: active on hemipteran pest species such as Coccinellidae) (Sparks et al. ,2013; aphids, whiteflies, thrips, leaf miners and Wanumen et al., 2016 and Nawaz et al., plant hoppers, but also commercialized to 2018). control many coleopteran and some Therefore, two field experiments lepidopteran pest species (Elbert et al., were carried out during 2018 and 2019 1998 and Nauen et al., 2003). Due to the summer seasons, at Nubarya district, El- potent systemic characteristics, they can Beheira Governorate to evaluate the side be absorbed via the roots and transferred effect of sulfoxaflor and some to almost all parts of targeted crops neonicotinoids treatment against sucking (Jeschke and Nauen, 2008). But this pests infesting watermelon and their irreversible uniting effect may not vary associated predators at recommended much between target and non-target rates. species, inducing similar detrimental Materials and methods impacts on the biocontrol agents 1.Tested compounds: (predators) (Cloyd and Bethke, 2011). Sulfoxaflor (Closer 24% SC) was Currently, global concerns about the provided by Dow Agro Sciences Co., negative influence of neonicotinoids on Ltd. Imidacloprid (Gaucho® 70%WS) non-target organisms (particularly bees) was provided by Bayer Crop Science. and human have led to the regulation by Clothianidin (Supertox-1® 48%SC) was the European Union (EU) since 2013, to provided by Jiangs Jiag chemical industry date, the use of three typical Co. Ltd China. Thiamethoxam (Actara neonicotinoids i.e. imidacloprid, 25% WG) provided by Syngenta thiamethoxam and clothianidin has been Company. Acetamiprid (Mospilan 20% totally banned on field crops by EU SP) provided by Nippon Soda Chemical (Jiang et al., 2019). Industry Co. Ltd.

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Egypt. J. Plant Prot. Res. Inst. (2020), 3 (1): 316 - 325

2. Field trials: aphid lion, C. carnea, the rove beetle, Field experiments were carried out Paederus alfierii and the lady birds, throughout two successive seasons (2018 Coccinella spp. were counted. Counts and 2019) during summer plantation in were done by the lenses in the early Nubarya district, El-Beheira Governorate. morning when flight activity is minimal These experiments were cultivated with according to Butler et al. (1988). watermelon. The experimental site was Percentage of pest reduction numbers divided into 24 plots, each plot 1/100 were calculated according to Henderson feddan (42m²). Randomized complete and Tilton equation (1955) and blocks design was used with four subjected to analysis of variance replicates for each treatment with the (ANOVA) (CoStat Statistical control plots. Field concentrations were software,1998). 40ml, 60gm, 1000ml, 60gm and Results and discussion 50gm/200 liter per feddan for sulfoxaflor, In this study, field evaluation of some imidacloprid, clothianidin, insecticides treatments against B. tabaci thiamethoxam, and acetamiprid, immature stages on watermelon respectively. The insecticides were plantation at 2018 and 2019 seasons was sprayed by Knapsack sprayer equipment carried out. The % reductions of B. (CP3). For counting the numbers of tabaci caused by sulfoxaflor, whiteflies, B. tabaci (immature stages), imidacloprid, clothianidin, and T. urticae, samples of 25 leaves thiamethoxam, and acetamiprid (from three different levels of the plants) formulation were summarized in Table were collected at random in the morning (1). Mean of % reduction was 95.47, for both diagonals of the inner square 95.35, 91.25, 92.87 and 85.25%, area of each experimental plot. Pre- respectively at 2018, while were 95.62, treatment counts were done in the early 91.17, 93.27, 92.97 and 79.72%, morning just before application while respectively at 2019 season. In both post-treatment counts were done on 1, 4, seasons, the highest reduction 7and 10 days after treatment. In the same percentages were achieved sulfoxaflor time, sample of 25 watermelon plants where the least reduction percentages were examined and the number of the were recorded by acetamiprid. Table (1): Efficacy of certain treatments against Bemisia tabaci immature stages on watermelon plantations. Season Tested Rate / %Reduction After compounds feddan 1-day 4-days 7-days 10-days Mean Sulfoxaflor 40ml 85.4 96.5 100.0 100.0 95.47a Imidacloprid 60g 88.5 94.5 98.4 100.0 95.35a

Clothianidin 1000ml 82.2 92.3 96.5 94.0 91.25b Thiamethoxam 60g 81.5 94.2 97.4 98.4 92.87b

2018 Acetamiprid 50ml 77.4 85.1 88.7 89.8 85.25c Sulfoxaflor 40ml 88.1 94.4 100.0 100.0 95.62a Imidacloprid 60g 78.2 90.2 96.3 100.0 91.17a Clothianidin 1000ml 80.5 96.3 100.0 96.3 93.27a Thiamethoxam 60g 81.3 100.0 96.3 94.3 92.97a

Acetamiprid 50ml 72.3 80.0 84.3 82.3 79.72b 2019 Means within the same column followed by the same letters are not significantly different according to the LSD0.05 for the same season.

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Barrania, 2020 This result indicates that, C. carnea, P. alfierii and Coccinella spp. neonicotinoids provides excellent control caused by sulfoxaflor, imidacloprid, B. tabaci (Kuhar et al., 2002). clothianidin, thiamethoxam, and Muhammad et al. (2011 and 2013) acetamiprid. For C. carnea were 31.47, reported that, B. tabaci has developed 49.55, 47.67, 44.55 and 37.50%, resistance to some of neonicotinoids. respectively at 2018 and 30.15, 48.85, Sulfoxaflor is also effective against a 54.52, 43.10and 33.90%, respectively at wide range of sap-feeding insect pests 2019, and for P. alfierii were 28.35, that are resistant to other classes of 28.90, 43.00, 42.75 and 38.17, insecticides, including many that are respectively at 2018 and 35.85, 49.37, resistant to the neonicotinoids (Zhu et al., 51.15, 47.27 and 45.47%, respectively at 2011; Sparks et al., 2013; Jeschke et al., 2019. While reduction percentages of 2015; Liao et al., 2017 and Wang et al., Coccinella spp. caused by sulfoxaflor, 2017). flupyradifurone, clothianidin, In this study, field evaluation of the thiamethoxam, and acetamiprid were side effect of certain treatments against 29.60, 34.50, 47.77, 45.80 and 31.77%, some predators (C. carnea, P. alfierii and respectively at 2018 and 39.20, 51.55, Coccinella spp.) and spider mites (T. 53.55, 52.02 and 46.85%, respectively at urticae) on watermelon plantations at 2019. Concerning data, all treatments 2018 and 2019 seasons. have toxic effect on natural enemies Data from Tables (2, 3 and 4) except sulfoxaflor have slightly toxic indicated that, reduction percentages of effect.

Table (2): Side effect of certain treatments against Chysoperla carnea on watermelon plantations.

Season Tested compounds Rate / %Reduction After feddan 1-day 4-days 7-days 10-days Mean Sulfoxaflor 40ml 32.4 34.3 30.4 28.8 31.47c

Imidacloprid 60g 44.4 52.6 52.6 48.6 49.55a

Clothianidin 1000ml 42.5 55.3 48.2 44.7 47.67ab

Thiamethoxam 60g 45.5 45.5 54.5 32.7 44.55ab

Acetamiprid 50ml 34.4 40.2 36.3 39.1 37.50bc 2018 Sulfoxaflor 40ml 28.2 33.6 32.4 26.4 30.15d

Imidacloprid 60g 44.6 52.6 50.0 48.2 48.85b

Clothianidin 1000ml 55.3 60.2 52.6 50.0 54.52a

Thiamethoxam 60g 39.1 42.4 46.5 44.4 43.10c

Acetamiprid 50ml 32.2 44.6 28.4 30.4 33.90d 2019 Means within the same column followed by the same letters are not significantly different according to the LSD0.05 for the same season.

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Table (3): Side effect of certain treatments against Paederus alfierii on watermelon plantations. Season Tested Rate / %Reduction After compounds feddan 1-day 4-days 7-days 10-days Mean Sulfoxaflor 40ml 26.3 34.4 28.2 24.5 28.35c Imidacloprid 60g 30.2 34.4 26.6 24.4 28.90c Clothianidin 1000ml 44.5 46.5 42.4 38.6 43.00a Thiamethoxam 60g 40.0 46.4 44.4 40.2 42.75a

Acetamiprid 50ml 33.3 42.5 40.5 36.4 38.17b 2018 Sulfoxaflor 40ml 32.2 34.4 40.2 36.6 35.85c Imidacloprid 60g 42.5 50.0 50.0 55.0 49.37ab Clothianidin 1000ml 50.0 56.4 50.0 48.2 51.15a Thiamethoxam 60g 46.5 50.0 48.2 44.4 47.27ab

Acetamiprid 50ml 40.2 45.3 50.0 46.4 45.47b 2019 Means within the same column followed by the same letters are not significantly different according to the LSD0.05 for the same season. Insecticides can be disruptive to costly, safe on the environmental natural and biological control by reducing constituents. Neonicotinoid insecticides natural enemy populations (Johnson and are considered an important group of Tabashnik, 1999 and Nasr and Keratum, insecticides being used against sucking, 2009). Our results were comparable with but also commercialized to control many Rizk et al. (1999) and Omar and El- coleopteran and some lepidopteran pest Kholy (2001), where they reported that, species. But this irreversible uniting the possibility of controlling sucking effect may not vary much between target pests by a combination of biological and and non-target species (predators) (Cloyd chemical methods had proved to be less and Bethke, 2011). Table (4): Side effect of certain treatments against Coccinella spp. on watermelon plantations. Season Tested Rate / %Reduction After compounds feddan 1-day 4-days 7-days 10-days Mean Sulfoxaflor 40ml 22.2 28.4 34.4 33.4 29.60c Imidacloprid 60g 32.5 35.4 36.6 33.5 34.50b Clothianidin 1000ml 44.5 48.2 50.0 48.4 47.77a Thiamethoxam 60g 40.2 50.0 48.6 44.4 45.80a

Acetamiprid 50ml 28.4 32.5 34.0 32.2 31.77bc 2018 Sulfoxaflor 40ml 38.4 42.4 40.0 36.0 39.20c Imidacloprid 60g 50.0 55.3 52.5 48.4 51.55a Clothianidin 1000ml 52.5 55.4 56.3 50.0 53.55a Thiamethoxam 60g 46.5 52.2 57.1 52.3 52.02a

Acetamiprid 50ml 44.6 48.2 48.2 46.4 46.85b 2019 Means within the same column followed by the same letters are not significantly different according to the LSD0.05 for the same season. Predators are very effective and agents, including, C. carnea and practical in biological control programs Clitemnestra bipunctata (Say) ( against sucking insect pests such as, C. Hymenoptera: Crabronidae). carnea and Coccinella spp. (Brook and Neonicotinoids have negative impact Barnard, 1990). Sparks et al. (2013); coccinellids through several routes of Wanumen et al. (2016) and Nawaz et al. entry, including: topical contact, residual (2018) reported that, sulfoxaflor is contact, inhalation of volatiles, ingestion slightly harmful to biological control of toxified plant products and ingestion

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Barrania, 2020 of toxified prey tissues (Ruberson et al., integrated pest management programs 1998; Johnson and Tabashnik, 1999 and (IPM). Natural enemies are usually Moser and Obrycki, 2009). efficient in regulating population of pests, The field evaluation of the side effect especially in balanced ecosystem. of certain treatments against T. urticae on Pesticides alone will not solve the watermelon plantations at 2018 and 2019 problem for controlling pests. seasons was carried out (Figures, 1 and Insecticides can be disruptive to natural 2). All treatments have not toxic effect on and biological control by reducing natural spider mites at a long time, except enemy populations (Johnson and sulfoxaflor have slightly toxic effect at Tabashnik, 1999), so the population of T. short time period. In both seasons, the urticae on watermelon will be increased. highest mean numbers of T. urticae on C. carnea, P. alfierii and Coccinella spp. watermelon plantations achieved by are known that aphidophagous, consume clothianidin where 91.1 and 96.5/25 different food types because aphids are leaves at were 2018 and 2019, abundant only during a restricted time respectively. The least mean numbers period. Besides this there are other recorded at untreated plants followed by arthropod prey items documented in the sulfoxaflor and acetamiprid at the both of literature, e.g. Acari, Thysanoptera, and seasons. larvae of Diptera, Coleoptera, and Biological control approach is Lepidoptera (Hodek, 1967, 1970 and considered as a main component of the Singh et al., 1991).

140 Sulfoxaflor Imidacloprid Clothianidin 120 Thiamethoxam Acetamiprid Control

100 leaves

25 80 /

60

40 Mean numbers Mean

20

0 zero time 1-day 4-days 7-days 10-days Mean Days after treatment (2018)

Figure (1): Side effect of certain treatments against Tetranychus urticae on watermelon plantations during 2018 season. Error bars represent standard deviation of four replications. Columns within a group with the same letter are not significantly different according to (LSD at P<0.05).

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140 Sulfoxaflor Imidacloprid Clothianidin 120 Thiamethoxam Acetamiprid Control

100 leaves

25 80 /

60

40 Mean numbers Mean

20

0 zero time 1-day 4-days 7-days 10-days Mean Days after treatment (2019)

Figure (2): Side effect of certain treatments against Tetranychus urticae on watermelon plantations during 2019 season. Error bars represent standard deviation of four replications. Columns within a group with the same letter are not significantly different according to (LSD at P<0.05). References Cloyd, R.A. and Bethke, J.A. (2011): Babcock, J.M.; Gerwick, C.B. ; Impact of neonicotinoid Huang, J.X.; Loso, M.R.; insecticides on natural enemies in Nakamura, G.; Nolting, S.P.; greenhouse and interiorscape Rogers, R.B.; Sparks, T.C.; environments. Pest Manag. Sci., Thomas, J.; Watson, G.B. and 67:3–9. Zhu, Y. (2011): Biological CoStat Statistical Software (1998): characterization of sulfoxaflor, a Microcomputer program analysis novel insecticide. Pest Manag. Sci., version 6.400, CoHort Software, 67: 328–334. Berkeley, CA. Brook, S. S. and Barnard, P. C. Elbert, A.; Nauen, R. and Leicht, W. (1990): The Green Lacewing of (1998): Imidacloprid, a novel World: A Generic Review (Neu. chloronicotinyl insecticide, Chrysopidae). Bulletin of British biological activity and agricultural Museum (Natural History), importance, in: I.Ishaaya, London, England. D.Degheele (Eds.), Insecticides Butler, G. D.; Coudriet, D. L. and with Novel Modes of Action, Hennebery, T. V. (1988): Mechanism and Application, Toxicity and repellence of soybeans Springer, Berlin., 50–73. and cottonseed oils to the sweet Henderson, C. F. and Tilton, E. W. potato whitefly and the aphids on (1955): Test with acaricides against cotton in greenhouse studies. the brown wheat mite. J. Econ. Southwest, Entomol., 13: 81-96. Entomol., 48: 157-161.

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