Control Effectiveness of Kaolin Clay and Neem on Agonoscena pistaciae in Pistachio Orchards

Abstract

The pistachio psyllid (Agonoscena pistaciae) is a major pest threatening pistachio production in Siirt province, Türkiye. This study evaluated the efficacy of a clay mineral, kaolin, and a botanical insecticide, neem extract, in managing this pest, aiming to reduce the reliance on chemical pesticides. Field experiments were conducted to compare the performance of these treatments with that of the synthetic insecticide spirotetramat SC 100 at various application rates. The results demonstrated that kaolin significantly reduced oviposition rates, achieving up to 100% deterrence, while neem extract exhibited substantial nymph mortality rates of up to 84.75%. These findings highlight the potential of mineral- and plant-based alternatives as effective components of integrated pest management strategies for pistachio psyllid control, offering sustainable and environmentally friendly solutions for minimizing economic losses and pesticide residues in pistachio production.

1. Introduction

Pistachio (Pistacia vera L.; Anacardiaceae) is known for its high quality and nutritional benefits and has significant economic value both globally and in Türkiye. According to FAO data, worldwide pistachio production increased from 77,078 tons in 1972 to 915,718 tons in 2021, reflecting an annual growth rate of 9.62%. Although Türkiye ranks second in the world in terms of production area, its yield remains below the global average due to significant losses caused by pests. One of the most important pests is Agonoscena pistaciae Burckhardt & Lauterer (Hemiptera: Psyllidae), which has emerged as a significant threat in pistachio orchards in the Southeastern Anatolia region as well as other major pistachio-producing countries, such as Iran, Armenia, Tajikistan, Greece, and Afghanistan [1,2,3,4,5]. It has been associated with significant yield losses, leading to extensive research on its biology and management [6,7,8]. In general, chemical pesticides are among the most commonly used methods for controlling A. pistaciae; however, their indiscriminate use has raised significant environmental and health concerns. Excessive pesticide application has been linked to biodiversity loss, environmental pollution, and the development of pesticide resistance in numerous insect species [9,10,11,12]. The pistachio psyllid, A. pistaciae, is a major pest that has developed resistance to various pesticide groups due to its high reproductive capacity and short life cycle [13], and to control it, organophosphates, neonicotinoids, and insect growth regulators have been widely used [6,14]. However, the frequent application of chemicals has exacerbated the problem of resistance. In response to these challenges, researchers have explored alternative eco-friendly approaches to pest management with organic insecticides derived from natural sources, such as garlic (Sirinol), black pepper (Tondexir), and eucalyptus extract (Palysin), which show promise in controlling A. pistaciae [15]. These botanical insecticides offer a safer and more sustainable approach to pest control, aligning with the principles of organic agriculture and integrated pest management.

In recent years, there has been increasing interest in exploring environmentally friendly alternatives for pest management. Kaolin is a naturally occurring clay mineral that has gained attention for its potential to control various insect pests. In its natural state, kaolin is a soft, white powder consisting principally of the mineral kaolinite, which, under an electron microscope, is revealed to comprise roughly hexagonal, platy crystals ranging in size from about 0.1 to 10 μm or even larger [16]. It acts as a physical barrier, deterring feeding and oviposition. Studies have shown that kaolin is effective against a wide range of pests, including aphids, codling moths, and psyllids [15,17,18,19,20]. In addition, kaolin clay offers various benefits to plants, including protection against harsh environmental conditions such as heat stress and sunburn [21]. Neem (Azadirachta indica A. Juss, Meliaceae) is another promising insecticide. Its active ingredient, azadirachtin, has potent insecticidal properties, including antifeedant, growth-regulating, and repellent effects [22,23,24,25]. Neem is a versatile plant reported as a source of insecticidal compounds such as nimbin, nimbidin, azadirachtin, salannin, tionemon, and meliantriol, which are found in high concentrations in seeds, leaves, and bark [26]. Previous research on agricultural pests has shown that neem extract effectively controls over 350 insect species [27]. In this context, evaluating the effects of neem extract on A. pistaciae in our trials can provide valuable insights for biological pest control. There is research suggesting that neem-based biopesticides offer an eco-friendly alternative to synthetic chemicals, minimizing environmental damage while effectively managing pest populations [28].

Traditional chemical control methods of A. pistaciae have limitations due to the development of resistance and environmental concerns. To address these issues, this study aimed to evaluate the efficacy of kaolin clay and neem extract in controlling A. pistaciae in Siirt province, Türkiye. By comparing these organic treatments with the synthetic insecticide spirotetramat, this research sought to identify sustainable and environmentally friendly alternatives for pistachio pest management.

2. Materials and Methods

2.1. Active Ingredients and Their Application in the Trial

For the field trials, kaolin clay WP (100% natural) (Lazoğlu, Bursa, Türkiye), Neem Azal T/S (Trifolio-M GmbH, Lahnau, Germany), and spirotetramat SC 100 (Movento; Bayer, Dormagen, Germany), which is widely used by producers in the region as a positive control insecticide, were used, as well as control plots treated with water only. To assess the efficacy of each treatment, three different dose levels were applied: the recommended application dose for each insecticide in field conditions, and doses below and above this level. Each treatment was replicated three times, resulting in a total of 36 experimental units (

Table 1. Insecticides and their doses used in the trial.

Active Ingredient	Trade Name	Formulation Type	Company	1. Dose	2. Dose *	3. Dose	Application Volume
Spirotetramat 100 g/L	Movento®	SC (Suspension Concentrate)	Bayer, Dormagen, Germany	50 mL **	100 mL	150 mL	100 L of water
Azadrachtin A 10 g/L	Neem Azal® T/S	EC (Emulsion Concentrate	Trifolio-M GmbH, Lahnau, Germany	100 mL	200 mL	300 mL	100 L of water
Kaolin clay WP	Mikronize Kaolin Kili (100% natural)	WP (Wettable Powder)	Lazoğlu, Bursa, Türkiye	3 kg	4 kg	5 kg	100 L of water

* The application dose recommended in the package insert of the insecticide. ** All active ingredients were applied in 100 L of water.

).

A Hyundai Turbo 900 25 L (Hyundai Corporation, Seoul, Republic of Korea), gasoline sprayer was used in all applications. Spraying was conducted during the early morning hours to minimize evaporation and optimize coverage. The spraying was applied to the entire tree and covered all leaf surfaces. Based on previous observations and sampling data, the treatments were applied in mid-September, coinciding with the peak of A. pistaciae in both years. Additionally, treatments were applied when weather conditions were favorable, with no rain or wind, ensuring that environmental factors had minimal impact on the effectiveness of the treatments.

2.2. Field Experiments

This study was conducted in a fully productive pistachio orchard located in İkizbağlar village, Tillo district, Siirt province, Türkiye (41°58′41.10″ N, 37°50′17.44″ E). The experiment was performed between September and November in 2021 and 2022. The orchard consisted of trees planted in a 9 m × 5 m spacing pattern. For each treatment, nine trees were selected, and the experiment was designed as a randomized complete block design with three replicates (

Table 2. Experimental design for field trials (randomized complete block design).

Block 1	Kaolin (Dose 1)	Neem Azal (Dose 1)	Movento (Dose 1)	Kaolin (Dose 3)	Movento (Dose 2)	Neem Azal (Dose 2)	Kaolin (Dose 2)	Movento (Dose 3)	Neem Azal (Dose 3)	Control
Block 2	Neem Azal (Dose 2)	Movento (Dose 1)	Kaolin (Dose 1)	Movento (Dose 2)	Kaolin (Dose 2)	Neem Azal (Dose 1)	Movento (Dose 3)	Neem Azal (Dose 3)	Kaolin (Dose 3)	Control
Block 3	Movento (Dose 2)	Kaolin (Dose 2)	Neem Azal (Dose 1)	Movento (Dose 3)	Neem Azal (Dose 3)	Kaolin (Dose 1)	Movento (Dose 1)	Kaolin (Dose 3)	Neem Azal (Dose 2)	Control

).

In addition, the A. pistaciae population reached the economic threshold of 20–30 nymphs per 20 compound leaves. To assess the effectiveness of the treatments, samplings were conducted one day before and on the 7th, 14th, and 21st day after spraying. Fifteen compound leaves were also randomly collected from each plot, considering different heights, directions, and positions within the canopy. These leaves were brought to the laboratory in a cold chain. The numbers of live nymphs, eggs, and parasitoids on both the upper and lower surfaces were recorded. Nymphs and parasitoids on the leaves were carefully examined and counted under an Olympus SC61 stereo microscope. Any stationary individuals were gently touched with a brush, and those that moved were considered alive. Additionally, blackened nymphs or eggs were considered parasitized, as this discoloration often resulted from parasitism, indicating the death of the nymph due to parasitoid activity.

2.3. Efficacy Percentage

The oviposition deterrent percentage (O.D%) of kaolin clay was calculated according to the following formula [29] (Equation (1)). This formula is widely used in many studies [30,31,32]:

$$\mathrm{O}.\mathrm{D}.\mathrm{\%}=100\times {\displaystyle \frac{(\mathrm{B}-\mathrm{A})}{(\mathrm{A}+\mathrm{B})}}$$

(1)

where O.D.% = the oviposition deterrent percentage; A = the mean number of eggs laid on the treatment; and B = the mean number of eggs laid on the control. Mortality was observed at 7, 14, and 21 days following each administration. Dead individuals were counted under a stereo microscope, and the mortality rate was calculated in the laboratory using the Henderson–Tilton formula (Equation (2)):

$$\mathrm{E}\mathrm{f}\mathrm{f}\mathrm{i}\mathrm{c}\mathrm{a}\mathrm{c}\mathrm{y}\left(\mathrm{\%}\right)=\left[\left(1-{\displaystyle \frac{\mathrm{T}\mathrm{a}\times \mathrm{C}\mathrm{b}}{Tb\times Ca}}\right)\times 100\right]$$

(2)

where Ta = the number of nymphs after spray treatment; Tb = the number of nymphs before spray treatment; Ca = the number of nymphs in the control after the experiment; and Cb = the number of nymphs in the control before the experiment.

2.4. Statistical Analysis

The data obtained in the experiment were analyzed via a two-way analysis of variance (ANOVA), and the results were evaluated using the SPSS (version 17) software package. Subsequently, mean comparisons were performed using Duncan’s test (p < 0.05).

3. Results

To evaluate the effectiveness of kaolin, azadirachtin, and spirotetramat against A. pistaciae and its parasitoids, field trials were conducted in Siirt province in 2021 and 2022, and the effects of different concentrations of these treatments on nymph and egg populations and parasitoid abundance were evaluated. The results are presented in

Table 3. The oviposition deterrent percentage (O.D %) and nymph mortality after treatment (%) of kaolin, neem, and spirotetramat in 2021 and 2022.

			Doses
			Kaolin			Neem			Spirotetramat
Years	Samplings	n *	3 kg K ** D1 ***	4 kg K D2	5 kg K D3	100 mL D1	200 mL D2	300 mL D3	50 mL D1	100 mL D2	150 mL D3
2021	7 days	15	%63.07	%69.61	%96.56	%12.82	%73.80	%84.75	%53.92	%74.09	%83.55
	14 days	15	%77.05	%80.46	%89.92	%51.7	%65.72	%79.20	%87.08	%90.68	%98.22
	21 days	15	%64.84	%31.33	%57.50	%31.01	%66.87	%72.90	%71.90	%79.64	%86.38
2022	7 days	15	%40.42	%69.23	%62.28	%34.03	%71.88	%64.43	%25.82	%64.15	%54.14
	14 days	15	%100	%100	%84.61	%74.54	%81.24	%67.51	%51.74	%90.26	%78.94
	21 days	15	%11.03	%100	%68.09	%35.11	%60.74	%61.62	%76.69	%91.32	%88.13

* n: number of trees evaluated for each Neem Azal application. ** All active ingredients were applied in 100 L of water. *** D1: Dose 1; D2: Dose 2; D3: Dose 3.

, showing that the tested kaolin clay doses were effective on pistachio psyllid eggs in both years (Table 3). The highest efficiency of kaolin clay in deterring pest egg laying was determined to be 100% for Dose 1 at 14 days and the same rate for Dose 2 at both 14 and 21 days after treatment. The results showed that the tested kaolin clay doses were effective on pistachio psyllid eggs in both years (Table 3). The mortality rates achieved with Neem Azal T/S and Movento were found to be significant in this study on A. pistaciae nymphs. For neem, the highest nymph mortality rate was found to be 84.75% at a concentration of 300 mL/100 L (Dose 3) at 7 days after treatment. Although neem was judged to be as effective as spirotetramat over the first 7 days, the mortality rate decreased from the 14th day. However, in the case of spirotetramat, the highest nymph mortality rate at Dose 3 was found to be 98.22% on the 14th day. In addition, the mortality rates of spirotetramat at Dose 1, Dose 2, and Dose 3 were found to be high at 14 and 21 days after treatment (Table 3).

In the experiments in the first year (2021), kaolin (K) clay treatments significantly reduced the number of live A. pistaciae nymphs per leaf at 7, 14, and 21 days post-treatment compared to the control and pre-treatment groups (p < 0.05) (

Table 4. The effects (mean ± standard error) of different concentrations of kaolin, neem, and spirotetramat applications on A. pistaciae in the 2021 field trial.

			Kaolin			Neem Azal			Spirotetramat
Year	Samplings	n	D1 AN 1	D1 E 2	D1 P 3	D1 AN	D1 E	D1 P	D1 AN	D1 E	D1 P
2021	Before spraying	15	111.13 ± 29.18 ab	51.33 ± 13.1 ab	0.13 ± 0.13 a	74.07 ± 10.94 cd	38.53 ± 11.23 abc	0.13 ± 0.13 b	100.2 ± 26.37 bc	49.4 ± 8.64 ab	0.47 ± 0.32 ab
	Control	15	133.07 ± 20.24 ab	67.73 ± 18 a	0.80 ± 0.54 a	133.07 ± 20.24 ab	67.73 ± 18 a	0.8 ± 0.54 a	133.07 ± 20.24 ab	67.73 ± 18 a	0.8 ± 0.54 a
	7 days	15	81.93 ± 19.49 b	12.07 ± 6.42 b	0.0 ± 0.0 a	74.53 ± 16.78 cd	7 ± 1.49 c	0.07 ± 0.07 b	53.27 ± 16.05 cd	17.47 ± 5.91 bc	0.07 ± 0.07 ab
	Control 7 days	15	153.60 ± 16.22 a	53.20 ± 16.11 ab	0.07 ± 0.06	153.60 ± 16.22 a	53.20 ± 16.11 ab	0.07 ± 0.07 b	153.60 ± 16.22 a	53.20 ± 16.11 ab	0.07 ± 0.07 ab
	14 days	15	21.87 ± 5.99 c	3.33 ± 0.98 c	0.47 ± 0.4 a	26.8 ± 6.25 e	14.73 ± 6.09 c	0.07 ± 0.07 b	15.13 ± 4.51 d	26.27 ± 12.2 bc	0.33 ± 0.19 ab
	Control 14 days	15	101.26 ± 10.07 b	25.60 ± 6.16 bc	0.06 ± 0.06	101.26 ± 10.07 bc	25.60 ± 6.16 bc	0.06 ± 0.06 b	101.26 ± 10.07 bc	25.60 ± 6.16 bc	0.06 ± 0.06 ab
	21 days	15	13.93 ± 3.28 c	2.53 ± 1.22 c	0.33 ± 0.19 a	38.47 ± 8.41 de	31.07 ± 7.64 bc	0.13 ± 0.13 b	32.67 ± 11.04 d	33.87 ± 12.33 abc	0.07 ± 0.07 ab
	Control 21 days	15	99.53 ± 12.90 b	11.86 ± 12.73 c	0.0 ± 0.0 a	99.53 ± 12.90 bc	11.86 ± 12.73 c	0.0 ± 0.0	99.53 ± 12.90 bc	11.86 ± 12.73 c	0.0 ± 0.0 b
			D2 AN	D2 E	D2 P	D2 AN	D2 E	D2 P	D2 AN	D2 E	D2 P
	Before spraying	15	165.2 ± 47.1 a	76.73 ± 24.57 a	0.13 ± 0.09 b	73.67 ± 19.92 c	59.13 ± 20.85 ab	0.0 ± 0.0 b	198.47 ± 21.14 a	63.47 ± 19.3 ab	1.2 ± 0.49 a
	Control	15	133.07 ± 20.24 abc	67.73 ± 18 a	0.80 ± 0.54 a	133.07 ± 20.24 ab	67.73 ± 18 a	0.8 ± 0.54 ab	133.07 ± 20.24 bc	67.73 ± 18 a	0.8 ± 0.54 ab
	7 days	15	79.27 ± 18.72 c	9.53 ± 3.3 c	0.0 ± 0.0 b	22.8 ± 6.28 d	10.6 ± 4.4 c	0.33 ± 0.27 ab	59.93 ± 13.01 de	15.07 ± 6.26 cd	0.47 ± 0.34 ab
	Control 7 days	15	153.60 ± 16.22 ab	53.20 ± 16.11 ab	0.07 ± 0.07 b	153.60 ± 16.22 a	53.20 ± 16.11 ab	0.07 ± 0.07	153.60 ± 16.22 b	53.20 ± 16.11 abc	0.07 ± 0.07 b
	14 days	15	8.27 ± 2.13 d	5.0 ± 1.62 c	0.0 ± 0.0 b	19.87 ± 9.31 d	24.33 ± 8.53 bc	0.93 ± 0.51 a	14.2 ± 5.46 f	20.07 ± 6.69 cd	0.47 ± 0.34 ab
	Control 14 days	15	101.26 ± 10.07abc	25.60 ± 6.16 bc	0.0 ± 0.0 b	101.26 ± 10.07 bc	25.60 ± 6.16 bc	0.0 ± 0.0 b	101.26 ± 10.07 cd	25.60 ± 6.16 bcd	0.0 ± 0.0 b
	21 days	15	17 ± 5.14 d	6.2 ± 2.5 c	0.0 ± 0.0 b	18.67 ± 4.26 d	30 ± 7.17 bc	0.13 ± 0.13 ab	30.47 ± 7.77 ef	48.47 ± 12.47 abcd	0.27 ± 0.21 ab
	Control 21 days	15	99.53 ± 12.90 bc	11.86 ± 3.28 c	0.13 ± 0.07 b	99.53 ± 12.90 bc	11.86 ± 3.28 c	0.13 ± 0.07 ab	99.53 ± 12.90 cd	11.86 ± 3.28 d	0.0 ± 0.0 b
			D3 AN	D3 E	D3 P	D3 AN	D3 E	D3 P	D3 AN	D3 E	D3 P
	Before spraying	15	170.8 ± 41.35 a	65.6 ± 18.9 a	0.0 ± 0.0 c	114.47 ± 15.77 b	36.2 ± 8.77 abc	0.0 ± 0.0 b	148.47 ± 34.56 ab	49.47 ± 10.72 ab	0.4 ± 0.34 a
	Control	15	133.07 ± 20.24 ab	67.73 ± 18 a	0.80 ± 0.54 a	133.07 ± 20.24 ab	67.73 ± 18 a	0.8 ± 0.54 a	133.07 ± 20.24 ab	67.73 ± 18 a	0.8 ± 0.54 a
	7 days	15	47.2 ± 12.55 cd	0.93 ± 0.3 c	0.27 ± 0.21 ab	20.73 ± 6.14 c	11.4 ± 4.28 c	0.07 ± 0.07 b	28.27 ± 6.76 c	5.4 ± 2.32 a	0.2 ± 0.14 a
	Control 7 days	15	153.60 ± 16.22 ab	53.20 ± 16.11 ab	0.07 ± 0.06 c	153.60 ± 16.22 a	53.20 ± 16.11 ab	0.07 ± 0.07 b	153.60 ± 16.22 a	53.20 ± 16.11 ab	0.07 ± 0.07 a
	14 days	15	12.2 ± 4.37 d	1.33 ± 0.55 c	0.2 ± 0.2 ab	18.47 ± 6.65 c	33 ± 11.02 bc	0.07 ± 0.07 b	2.53 ± 0.66 c	7.33 ± 1.71 c	0.0 ± 0.0 a
	Control 14 days	15	101.26 ± 10.07 bc	25.60 ± 6.16 bc	0.0 ± 0.0 c	101.26 ± 10.07 b	25.60 ± 6.16 bc	0.0 ± 0.0 b	101.26 ± 10.07 b	25.60 ± 6.16 bc	0.0 ± 0.0 a
	21 days	15	11.53 ± 1.65 d	3.2 ± 1.39 c	0.07 ± 0.07 c	23 ± 5.11 c	30.93 ± 9.21 bc	0.07 ± 0.07 b	15.87 ± 4.75 c	53.33 ± 13.74 ab	0.4 ± 0.27 a
	Control 21 days	15	99.53 ± 12.90 bc	11.86 ± 3.28 c	0.13 ± 0.07 c	99.53 ± 12.90 b	11.86 ± 3.28 c	0.13 ± 0.07 ab	99.53 ± 12.90 b	11.86 ± 3.28 c	0.0 ± 0.00 a

D1: Dose 1; D2: Dose 2; D3: Dose 3; K: kaolin; AN: alive nymphs; E: egg; P: parasitization; differences between means signed in the same column with the same letters are not significantly important (p < 0.05). AN ¹: the number of alive nymphs per leaf; E ²: the number of alive eggs per leaf; P ³: the number of parasitized nymphs per leaf.

). This effect was observed across all the tested doses (D1, D2, and D3). Additionally, kaolin significantly reduced egg numbers compared to the control and pre-treatment groups (p < 0.05). However, no significant impact on parasitoid populations was detected for D1 and D3. For D2, parasitized nymphs were not observed in the post-treatment samples (p < 0.05). Similarly, neem treatments led to a significant reduction in nymph populations at 7, 14, and 21 days post-treatment for D2 and D3 (p < 0.05) (Table 4). Egg numbers were also significantly lower in all the neem treatments compared to the control and pre-treatment groups (p < 0.05). However, no significant impact on parasitoid populations was observed for any neem treatment.

Spirotetramat treatment significantly reduced the number of live nymphs per leaf at 7, 14, and 21 days post-treatment for D1, D2, and D3 compared to the control and pre-treatment groups (p < 0.05) (Table 4). Additionally, spirotetramat significantly reduced egg numbers compared to the control and pre-treatment groups at 14 and 21 days post-treatment (p < 0.05). However, no significant impact on parasitoid populations was observed for any spirotetramat treatment (Table 4).

In 2022, kaolin clay treatments at dose D1 did not show a significant difference in nymph populations. However, D2 and D3 significantly reduced the number of live nymphs per leaf at all the observation time points compared to both the pre-treatment and control groups (p < 0.05) (

Table 5. The effects (mean ± standard error) of different concentrations of kaolin, neem, and spirotetramat applications on A. pistaciae in the 2022 field trial.

			Kaolin			Neem Azal			Spirotetramat
Year	Samplings	n	D1 AN 1	D1 E 2	D1 P 3	D1 AN	D1 E	D1 P	D1 AN	D1 E	D1 P
2022	Before spraying	15	142.13 ± 51.94 b	79.47 ± 20.73 a	0.4 ± 0.163 b	130.07 ± 10.72 bc	79.33 ± 29.88 a	0.2 ± 0.11 a	82.93 ± 20.73 c	91 ± 19.01 a	1.0 ± 0.33 a
	Control	15	101.4 ± 24.53 b	76.80 ± 15.95 a	0.13 ± 0.9 b	101.40 ± 24.53 cd	76.80 ± 15.95 a	0.13 ± 0.90 a	101.4 ± 24.53 bc	76.80 ± 15.95 a	0.13 ± 0.9 bc
	7 days	15	135.8 ± 44.35 b	14.8 ± 3.17 bc	0.53 ± 0.26 b	46.53 ± 9.24 d	33.07 ± 8.41 ab	1.4 ± 0.51 a	64.07 ± 17.86 c	37.4 ± 9.23 b	0.07 ± 0.07 c
	Control 7 days	15	105.86 ± 18.34 b	33.26 ± 5.37 b	0.66 ± 0.25 b	105.86 ± 18.34 bc	33.26 ± 5.37 ab	0.66 ± 0.25 a	105.86 ± 18.34 bc	33.26 ± 5.37 b	0.67 ± 0.25 ab
	14 days	15	238.13 ± 43.41 ab	0.0 ± 0.0 c	0.20 ± 0.15 b	95.67 ± 24.36 cd	55 ± 15.35 ab	0.87 ± 0.55 a	115.07 ± 30.59 ab	33.4 ± 9.51 b	0.4 ± 0.19 bc
	Control 14 days		290.80 ± 55.34 a	12.13 ± 4.20 bc	0.13 ± 0.9 b	290.80 ± 55.34 a	12.13 ± 4.20 b	0.13 ± 0.90 a	290.80 ± 55.34 a	12.13 ± 4.20 b	0.13 ± 0.9 bc
	21 days	15	180.33 ± 59.95 ab	14.47 ± 8.09 bc	2.47 ± 1.49 a	157.47 ± 29.68 bc	47.53 ± 20.06 ab	1.4 ± 0.79 a	36.4 ± 8.43 c	34.27 ± 11.49 b	0.27 ± 0.12 bc
	Control 21 days	15	188.20 ± 28.18 ab	18.06 ± 5.04 bc	0.26 ± 0.15 b	188.20 ± 28.18 b	8.06 ± 5.04 b	0.26 ± 0.15 a	188.20 ± 28.18 b	8.06 ± 5.04 b	0.26 ± 0.15 bc
			D2 AN	D2 E	D2 P	D2 AN	D2 E	D2 P	D2 AN	D2 E	D2 P
	Before spraying	15	126.93 ± 25.98 bc	39.8 ± 11,41 b	0.07 ± 0.07 c	130.6 ± 21.71 bc	44.8 ± 20.96 b	0.53 ± 0.29 ab	161.73 ± 28.9 bc	24.8 ± 6.42 b	1.47 ± 0.46 a
	Control	15	101.4 ± 24.53 bc	76.80 ± 15.95 a	0.13 ± 0.9 bc	101.40 ± 24.53 cd	76.80 ± 15.95 a	0.13 ± 0.90 a	101.4 ± 24.53 bc	76.80 ± 15.95 a	0.13 ± 0.9 bc
	7 days	15	114.73 ± 45.76bc	6.67 ± 1.98 c	0.4 ± 0.24 abc	38.73 ± 6.01 d	27.33 ± 5.83 bc	0.93 ± 0.33 a	60.93 ± 16.87 d	29.6 ± 8.65 b	1.07 ± 0.55 ab
	Control 7 days		105.86 ± 18.34bc	33.26 ± 5.37 bc	0.67 ± 0.25 ab	105.86 ± 18.34 cd	33.26 ± 5.37 bc	0.7 ± 0.25 ab	105.86 ± 18.34 cd	33.26 ± 5.37 b	0.7 ± 0.25 ab
	14 days	15	113.47 ± 33.91 bc	0.0 ± 0.0 d	0.13 ± 0.09 bc	70.13 ± 8.82 bc	30.87 ± 6.73 bc	0.67 ± 0.19 ab	45.73 ± 12.22 d	34 ± 13.45 b	0.13 ± 0.09 a
	Control 14 days	15	290.80 ± 55.34 a	12.13 ± 4.20 cd	0.13 ± 0.09 bc	290.80 ± 55.34 a	12.13 ± 4.20 c	0.13 ± 0.09 b	290.80 ± 55.34 a	12.13 ± 4.20 b	0.13 ± 0.09 b
	21 day	15	77.33 ± 22.83 c	0.0 ± 0.0 d	0.73 ± 0.28 a	95.27 ± 22.85 ab	3.8 ± 2.45 c	0.4 ± 0.19 ab	26.07 ± 9.16 d	26.6 ± 11.61 b	1.13 ± 0.45 ab
	Control 21 days	15	188.20 ± 28.18 b	8.06 ± 5.04 d	0.26 ± 0.15 bc	188.20 ± 28.18 b	8.06 ± 5.04 c	0.26 ± 0.15 ab	188.20 ± 28.18 b	8.06 ± 5.04 b	0.26 ± 0.15 b
			D3 AN	D3 E	D3 P	D3 AN	D3 E	D3 P	D3 AN	D3 E	D3 P
	Before spraying	15	154.8 ± 26.23 bc	23.4 ± 7.67 bc	2.8 ± 1.08 ab	119.13 ± 20.19 bc	45.47 ± 12.36 b	0.07 ± 0.07 b	86.4 ± 35.73 c	57.33 ± 13.47 ab	0.6 ± 0.35 a
	Control	15	101.4 ± 24.53 bcd	76.80 ± 15.95 a	0.13 ± 0.9 c	101.40 ± 24.53 bc	76.80 ± 15.95 a	0.13 ± 0.90 a	101.4 ± 24.53 c	76.80 ± 15.95 a	0.13 ± 0.9 a
	7 days	15	49.33 ± 13.88 d	7.73 ± 3.20 b	1.07 ± 0.67 bc	44.33 ± 9.75 c	27.2 ± 6.11 bcde	0.27 ± 0.12 ab	41.67 ± 13.8 c	16.53 ± 5.59 c	0.87 ± 0.31 a
	Control 7 days	15	105.86 ± 18.34 bd	33.26 ± 5.37 b	0.66 ± 0.25 bc	105.86 ± 18.34 bc	33.26 ± 5.37 bcd	0.66 ± 0.25 a	105.86 ± 18.34 c	33.26 ± 5.37 bc	0.66 ± 0.25 a
	14 days	15	81.8 ± 23.05 cd	1 ± 0.66 d	0.67 ± 0.33 bc	111.07 ± 25.97 bc	40.6 ± 16.83 bc	0.33 ± 0.13 ab	52.07 ± 14.61 c	24.73 ± 7.48 bc	0.67 ± 0.21 a
	Control 14 days	15	290.80 ± 55.34 a	12.13 ± 4.20 cd	0.13 ± 0.9 c	290.80 ± 55.34 a	12.13 ± 4.20 cde	0.13 ± 0.90 b	290.80 ± 55.34 a	12.13 ± 4.20 c	0.13 ± 0.9 a
	21 days	15	60.0 ± 20.89 d	1.53 ± 1.39 cd	3.73 ± 1.68 a	85 ± 18.01 c	1.67 ± 1.46 e	0.2 ± 0.15 b	19.47 ± 6.87 c	22.73 ± 8.01 c	0.33 ± 0.23 a
	Control 21 days	15	188.20 ± 28.18 b	8.06 ± 5.04 cd	0.26 ± 0.15 c	188.20 ± 28.18 b	8.06 ± 5.04 de	0.26 ± 0.15 ab	188.20 ± 28.18 b	8.06 ± 5.04 c	0.26 ± 0.15 a

D1: Dose 1; D2: Dose 2; D3: Dose 3; K: kaolin; AN: alive nymphs; E: egg; P: parasitization; differences between means signed in the same column with the same letters are not significantly important (p < 0.05). AN ¹: the number of alive nymphs per leaf; E ²: the number of alive eggs per leaf; P ³: the number of parasitized nymphs per leaf.

). Additionally, all the kaolin treatments (D1, D2, and D3) significantly reduced egg populations compared to the pre-treatment and control groups (p < 0.05), with D3 being the most effective (Table 5). However, no significant differences were observed in parasitoid populations across all kaolin treatments, indicating a minimal impact on natural enemies.

For neem, D1, D2, and D3 significantly reduced the number of live nymphs at 14 days after treatment, while D3 remained effective even at 21 days post-treatment (p < 0.05) (Table 5). While D1 and D2 did not significantly differ from the pre-treatment and control groups in terms of egg reduction, D3 significantly reduced the number of eggs 21 days post-treatment (p < 0.05). Similarly to kaolin, azadirachtin treatments did not cause significant changes in parasitoid populations.

Spirotetramat exhibited strong efficacy, significantly reducing nymph populations at D1 on days 7 and 21 after treatment, as well as at all observation points for D2 and D3 (p < 0.05) (Table 5). However, no significant impact on parasitoid populations was observed across all spirotetramat treatments, suggesting it could be a compatible option for integrated pest management. Overall, kaolin and neem were effective in controlling A. pistaciae; however, a slight increase in pest density was observed 14 days post-treatment. Kaolin was particularly effective in reducing egg numbers, which may aid in long-term pest suppression. Spirotetramat demonstrated the most consistent nymph reduction across all doses, making it a promising control option.

4. Discussion

This study shows that both kaolin and azadirachtin are effective against A. pistaciae. Despite a slight increase in pest density, particularly at 14 days after treatment, kaolin effectively reduced the number of A. pistaciae eggs. Overall, these findings support the efficacy of these organic alternatives in managing this pest. Integrating organic alternatives like kaolin and neem extract into broader integrated pest management (IPM) strategies offers several advantages. Kaolin functions by creating a physical barrier that deters pests from feeding and ovipositing on plants, which has been supported by research demonstrating that kaolin can effectively reduce pests’ damage by disrupting their feeding behavior [33,34,35]. Neem extract, which contains azadirachtin, disrupts pest growth through hormonal interference, which is effective in managing various pest populations [24,25]. Kaolin clay is considered safe for human health and is used in a range of toothpastes. The kaolin used in our study is a white, non-porous, non-swelling, non-abrasive, fine-grained, flat aluminosilicate mineral [Al₄Si₄O₁₀(OH)₈] and is chemically inert over a wide pH range [19]. Kaolin clay is also increasingly being used for various agricultural purposes; specifically, kaolin is the most common particulate clay mineral recommended for sunburn protection in vegetables and fruits. According to previous studies, kaolin has been shown to lower the temperature on leaf and fruit surfaces, enhancing photosynthesis, carbon assimilation, and water use in plants, thereby improving yield and fruit color [36]. Additionally, kaolin possesses insect repellent and irritant properties [34], playing a significant role in protecting plants against pathogens and various arthropod species [19]. The effects of kaolin on many important insect pest species have been revealed in previous studies conducted in different countries. It has been used against several key pest species, including Ceratitis capitata (Wiedemann) (Diptera: Tephritidae) [37,38], Myzus persicae (Sulzer) [39], Aphis gossypii Glover [40], Lipaphis erysimi Kalt. [41], Bemisia tabaci (Gennadius) [42,43], Spodoptera exigua (Hübner) [44], Cydia pomonella (L.) [45], and Thrips tabaci (Lindeman) [46]. While the effects of kaolin on the management of some important insect species belonging to the Psyllidae family have been investigated [19,20,47,48], there are few reported studies on the efficacy of kaolin against pistachio leaf psyllid. In this study, it was determined that kaolin treatments significantly reduced the number of eggs and nymphs on the leaves. The number of nymphs on the leaves was found to be statistically significant when compared to both the before-spraying and control groups. It was also observed that significantly fewer eggs were laid on leaves treated with kaolin clay compared to all treatments with azadirachtin and spirotetramat. Moreover, it was observed that adult A. pistaciae individuals did not prefer to lay eggs on the treated leaves of Siirt pistachio trees after kaolin treatments. These results suggest that kaolin acts as a barrier, reducing feeding and development of nymphs on the leaves.

In this study, the number of eggs and nymphs on the leaves was reduced by treatments of kaolin in Siirt pistachio orchards. The highest efficiency of kaolin clay in deterring the oviposition of the pest was determined to be 100% at a concentration of Dose 1 at 14 days and at Dose 2 at 14 and 21 days after treatment in 2021. Additionally, this study indicated that all kaolin doses significantly decreased the number of eggs found on the leaves. Kaolin clay at Dose 3 showed very high efficacy in 2022. The highest decrease in nymph population density was reported with a 7.5% concentration of kaolin particle film [15]. In addition, leaf treatment with kaolin particle film resulted in fewer adults, nymphs, and eggs of the potato psyllid, Bactericera cockerelli, than treatments with water. Similarly, kaolin used against the insect pest Agonoscena targionii significantly reduced the number of adults and nymphs compared to the control treatment [47]. In [49], kaolin treatments exhibited significantly higher efficacy against Cacopsylla pyri compared to mineral oil and untreated controls. The results indicated a 99% reduction in egg numbers and a 100% reduction in nymphs on kaolin-treated plants, and no phytotoxic effects were observed in trees treated with kaolin. Moreover, a 5% kaolin application reduced the number of psylla nymphs more effectively than acetamiprid in all spraying experiments conducted in pistachio fields. The authors of [50] reported that, based on two years of data, 5% and 10% kaolin positively influenced the yield traits of pistachio trees. The results of this study for kaolin clay application were in line with those reported for many species of the Psyllidae family. In general, kaolin treatments significantly reduced the egg and nymph density of psyllid pest species compared to the control and other insecticides. In pistachio trees where all leaves were thoroughly treated with kaolin, the number of eggs and nymphs was found to be below the economic damage threshold at very low levels, without the use of chemical pesticides for pest control.

On the other hand, the kaolin clay used in this study did not have any side effects on the number of individuals of Psyllaephagus sp., an important parasitoid of the pistachio leaf psyllid, which is common in Siirt pistachio orchards. Kaolin application can therefore effectively reduce pest damage without significant negative impacts on natural enemies, as it is non-toxic to humans and relatively safe for the environment [51]. Considering all the results, the organic substance kaolin used in our study was found to be an alternative to chemical insecticides for the effective control of A. pistaciae. Due to the findings of this study, kaolin can be considered an economically viable and environmentally friendly option for controlling the pistachio leaf psyllid. We consider it important for future studies to test the effectiveness of kaolin in large-scale field trials for the control of pistachio psyllids.

Interest in the use of biopesticides against phytophagous insects has increased in recent years [50]. In this context, the effect of Neem Azal, a herbal insecticide, on A. pistaciae was tested for the first time globally and in our country in this study. This insecticide is formulated as an Emulsion Concentrate (EC) and contains the active ingredient azadirachtin A, which is obtained from the seed extract of the tropical neem tree (Azadirachta indica A. Juss). Especially in IPM, the use of these natural compounds instead of commercially available chemical insecticides can protect human and environmental health, prevent insecticide-induced resistance issues, and safeguard non-target organisms [52].

After 7 days, the highest mortality rate of A. pistaciae nymphs (84.75%) was indicated via the treatment with Dose 3 (300 mL/100 L) among all doses of the neem botanical insecticide used in our study. A similar mortality rate of 80% was reported for the important pest of Paraguayan tea plants, Gyropsylla spegazziniana (Lizer) (Hemiptera: Psyllidae), after neem oil treatments [53]. In another study, the effects of three different concentrations of Neem Azal T/S (0.3%, 0.5%, and 0.7%) on Agonoscena targionii (Lichtenstein, 1874) nymphs were investigated, and the mortality rates at 0.3%, 0.5%, and 0.7% concentrations were recorded as 71.7%, 77.2%, and 93.1%, respectively [14]. Furthermore, neem-based insecticides have minimal impact on many beneficial organisms, including honeybees, predators, and parasitoids [54]. In contrast, numerous studies have shown that neem-based insecticides can be effective in controlling many pests. The authors of [50] indicated that even very low concentrations (10 ppm) of azadirachtin are effective in controlling the Asian citrus psyllid, Diaphorina citri Kuwayama (Hemiptera: Psyllidae) nymphs. The effect of neem-derived insecticides has also been reported on various other insect pest species beyond the Psyllidae family. In some laboratory and field experiments, insecticides formulated from neem seed oil were found to be highly effective against aphids [55]. Similarly, neem extract has been reported to reduce aphid infestation to levels comparable to those achieved with chemical pesticides [56]. Additionally, the combination of Neem Azal T 5% and the entomopathogenic nematode Steinernema feltiae has been shown to enhance biological control efficacy against the peach fruit fly [57]. In conclusion, neem exhibits similar potential to registered insecticides in reducing psyllid infestation. In our study, neem insecticide was found to be as effective as spirotetramat, the positive control insecticide, in reducing the number of psyllid nymphs and eggs. Additionally, no side effects of neem were observed on parasitoid populations, consistent with previous studies [58,59]. These results suggest that neem can be considered an important natural insecticide for controlling A. pistaciae, particularly in IPM. Furthermore, in addition to their effectiveness in controlling pests, the environmental impacts of kaolin and neem extract, as well as their effects on other natural enemies, should be thoroughly evaluated. Kaolin, a widely used mineral found in sedimentary rocks, has a lower environmental impact compared to chemical pesticides [21]. Neem products are advantageous due to their low persistence in the environment and low toxicity to mammals [60]. These findings indicate that kaolin and neem provide environmentally sustainable alternatives to traditional chemical pesticides.

5. Conclusions

These study results demonstrated that neem was effective in managing A. pistaciae populations, while kaolin powder acted as both a repellent and a barrier to oviposition. Both neem and kaolin treatments exhibited high efficacy against A. pistaciae nymphs and eggs without causing phytotoxicity to pistachio trees. These findings supported the inclusion of neem and kaolin in integrated pest management (IPM) programs for pistachios, providing environmentally friendly alternatives to traditional pesticides. By improving pistachio quality and reducing environmental and health risks, these methods contributed to sustainable agriculture and enhanced competitiveness in international markets. This study highlighted the potential of neem and kaolin in promoting eco-friendly pest control and encouraged their adoption in sustainable farming practice.