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Full Research Article

Toxicity of Some Pesticides against Oligonychus afrasiaticus (Mcgregor) (Acari: Tetranychidae) in Tunisian Oases and Analysis of Their Residues in Date Fruits

Samah Ben Chaaban1,2,*, Rakia Ben Slimen1, Sihem Ben Maachia1, Kamel Mahjoubi1, Safwa Hamad1, Ibtissem Mahmoudi1, Sabrine Nsir3
  • http://orcid.org/0000-0002-6332-6169
1Laboratory of Entomology, Regional Research Center of Oasis Agriculture, Degache, Tunisia.
2Laboratory of Biotechnology Applied to Agriculture, National Agricultural Research Institute of Tunisia (INRAT), University of Carthage, Tunis, Tunisia.
3Sabrine Nsir Ministry of Agriculture, Water Resources and Fisheries, Tunisia.

ABSTRACT

Background: In Tunisia, the date palm mite Oligonychus afrasiaticus McGregor (Acarina: Tetranychidae) is one of the most important pests of the date palm Phoenix dactylifera L. (Arecaceae). The control of Oligonychus afrasiaticus in Tunisian oases requires the use of safe and effective acaricides.

Methods: In this study, the toxicity of pesticides (sulfur, hexythiazox, bifenazate and spinosad) against O. afrasiaticus in date palms was investigated in the field. The aim of this study was also to evaluate the dissipation of bifenazate, hexythiazox and spinosad in date fruits by the QuEChERS method.

Result: Bifenazate was effective with a reduction of 90.2 and 89.4% of O. afrasiaticus motile forms and eggs, respectively, up to 21 days after application of this insecticide. Within 21 days of spraying, hexythiazox was an effective acaricide, reducing eggs and motile forms to 98.5% and 82.5%, respectively. Spinosad was effective for up to 14 days. Under the conditions of the Tunisian oases, the sulfur toxicity applied in July may remain effective for <14 days after treatment. Regarding, the dissipation of tested pesticides, the results showed that bifenzate deposited faster in date fruits than hexythiazox and spinosad. The initial deposition of bifenzate and spinosad decreased and was no longer detected after 7 and 14 days, respectively. Hexythiazox was detected at harvest when the date fruits were treated twice, but the residues were lower than the residue levels recommended by the European Union. These results would be useful to improve the control of O. afrasiaticus based on the efficacy, persistence and toxicity of these pesticides.

INTRODUCTION

The date palm (Phoenix dactylifera L.) sector plays an important role in Tunisia. The production of dates is estimated at 340 thousand tons for 2021-2022 (Onagri, 2023). Tunisia is the largest exporter of dates in the world in terms of value (GIFruits, 2022). There is a growing demand on the international market for dates of excellent quality that are free from pesticide residues. However. dates are affected by numerous diseases and pests that affect their yield and quality. such as Oligonychus afrasiaticus. Farmers tend to use more acaricides to control this pest. In Saudi Arabia Al-Doghairi (2004) evaluated the efficacy of eight acaricides such as Neoron (Bromopropylate 25% EC). Kelthane (Dicofol 18.5 EC). Tedion (Tetradifon 75.2 g L-1). Top cop (73% S + 6.4% Cu. w/v). Microthiol special (Sulfur 80%WP). Ekatin (Thiometon 25% EC). Transact (Abamectin 1.8% EC) and Peropal (Azocyclotin 25% WP). Aldosari (2009) evaluated the efficacy of the botanical compound (Biaco) as compared with some acaricides such as Vertamic 1.8% EC. Salocide 40% EC. Amitraz 20% EC and Perpol 25% WP. In Iran. Arbabi et al., (2017) evaluated the efficacy of different acaricides such as Amitraz 20% EC. Fenpropathrin 10% EC. Fenpyroximate 5% SC. Fenazaquin 20% SC. Propargite 57% EC. Tetradifon 18.5% EC. Hexythiazox 10%. In Egypt Fakeer and Eraky  (2019) tested  five acaricides abamectin (1.8% EC). chlorfenapyr (36% SC). fenopyroximate (5% EC). cyflumetofen (20% SC) and hexythiazox (10% WP).
       
The excessive and improper use of these agrochemicals can lead to an increase in pesticide residues in may leach in the soil. water and even remain in the crop residues and food products. From there they enter in human food chain posing serious health hazards (Padaliya et al., 2020).                        

Pesticide exposure in people can happen both directly and indirectly. Pesticides can immediately damage the skin. eyes. mouth and respiratory system. for example. when they are sprayed on crops (Sangha et al., 2023; Sahoo  et al., 2024).
       
For this reason. pesticide residues in food are strictly regulated by governments around the world to determine whether the concentration of pesticides used exceeds the maximum residue limits (MRLs) set by the Codex Alimentarius (CA) and the European Union (EU) (EFSA. 2021). Studies have detected pesticide residues in marketed dates. namely in Saudi Arabia in 2018 (Abdallah et al., 2018) and in the United Arab Emirates (UAE) in 2020 (El-Mageed  et al. 2022).  In addition. compliance with pesticide regulations and safety certification are crucial for market access. Due to this reason. many pesticides are banned in several countries. including key export markets such as Europe. which is an important export market for Tunisian products.
       
To avoid health risks for consumers. it is therefore important to consider the effects of the pesticide on date fruits when searching for pesticides that effectively control O. afrasiaticus in the Tunisian oasis. Therefore. the aim of this work was (1) to evaluate the toxicity of pesticides (sulfur. hexythiazox. bifenazate and spinosad) against O. afrasiaticus and (1) to measure the residue levels of bifenazate. hexythiazox and spinosad after different intervals of last field application. The results will be useful to establish a list of recommended registered acaricides for use on Tunisian date palms in Tunisia.

METRIALS AND METHODS

Acaricides/Insecticides
 
The aim of this insecticide trial was to evaluate the effectiveness of commercial pesticides. hexythiazox (cesar 10 WP. Nippon Soda CO Ltd. Tokyo. Japan). spinosad (Tracer 240 SC Dow Agrosciences USA Spinosad. 240 g/l. SC) at a rate of. bifenazate (Floramite 240 SC CHEMTURA/ARYSTA . Japon) and sulfur (azumo) were purchased from local suppliers.
 
Field application of insecticides
 
The field trial was conducted from July to November 2021 in the Chekmou oasis (3359023.7300 N. 814049.7900 E. Tozeur. southern Tunisia). It is a modern type of oasis with an average planting distance of 10 x 10 m and ten-year-old date palms (Deglet Noor variety).
       
The experiment has a total of Five treatments (one water control and for pesticides) and each treatment was replicated 3 times in a randomized complete block design (replicate size: three palms for each treatment).
       
Each test plot was sprayed on 30/7/2021with the active ingredient at the recommended dosage: 50 g ha-1 hexythiazox. 300 g ha-1 sulfur. 60 mL/100 L spinosad and 60 mL/100 L bifenazate.

Sampling mites on fruit
 
From each replicate. a sample of 10 fruits was taken from each date palm (total of 30 fruits per replicate). A total of 90 fruits per treatment were sampled before treatment and 3. 7. 14 and 21 days after treatment.
       
The mites in the fruits were counted under a stereo microscope. We determined the average number of eggs and motile forms of O. afrasiaticus per sampling date.  The efficacy of each pesticide against O. afrasiaticus was calculated using the equation (Henderson and Tilton. 1955).
 
  
  
Where.  
n = Number of motile stages or eggs.
T = Treated.
Co = Control.
 
Residues
 
Application of pesticides
 
To evaluate the persistence of bifenazate. hexythiazox and spinosad in date fruits. test plots were selected (the residue of sulfur is not investigated as it is biological). In the first plot. the date palms were sprayed once on 30/7/2021. In the second plot. the date palms were sprayed twice. on 30/7/2021 and 1/9/2021. In each plot. the experimental design was a randomized complete block with three treatments (three pesticides). three blocks and three palms (Deglet Noor variety) in each plot for each treatment.
 
Date samples collection and preparation
 
Approximately 1 kg of date palm fruits were randomly collected from each tree on 7 and 14 days after insecticide/acaricide treatment and at harvest on 29/9/2021. The seeds were discarded and the pulp was homogenized with a blender and stored at -20oC until analysis.
 
Analysis of residues
 
The “Quick. Easy. Cheap. Effective. Rugged and Safe” (QuEChERS) method was used to detect residues of spinosad. hexythiazox and bifenazate in palm fabrics (Attia  et  al., 2019). The samples were analyzed at the Laboratory for the Control and Analysis of Pesticides (LCAP) of the Ministry of Agriculture in Tunisia. It uses dispersive solid phase extraction (SPE) followed by chromatographic analysis of the extracts (Solomon  et al., 1993).
       
Each sample was thawed naturally. then 10 g of each homogenized sample was mixed with 10 mL of acetonitrile in a centrifuge tube. After this step. a mixture of salts: 4 g MgSO4. 1 g NaCl. 1 g sodium citrate. dihydrate (C6H5Na3O7. 2H2O) and 0.5 g disodium hydrogen citrate sesquihydrate (C6H8Na2O8) were added to each sample. After vigorous shaking of the mixture. the tubes were then centrifuged at 3500 rpm for 5 minutes. Six ml of the supernatant was collected and added to a tube containing 150 mg of primary and secondary amines (PSA) and 900 mg of MgSO4. After stirring. the mixture was centrifuged at 3500 rpm for 5 minutes. The final extract was filtered and analyzed.
 
Chromatographic analyses
 
The analyses of pesticide residues in dates fruits were performed by a chromatographic liquid system coupled to a triple quadrupole mass spectrometer and interface by electrospray (LC-ESI-MS/MS) (Table 1).

Table 1: Experimental conditions of LC\MS analyses to detect residues of insecticides in dates fruits.


 
Statistical analysis
 
Significant differences in efficacy of pesticides treatments were analyzed using one-way analysis of variance (ANOVA) and the means were compared using Tukey test at P<0.05. All the analyses were performed using the SPSS statistical software version 21.0.

RESULTS AND DISCUSSION

The efficacy of pesticides for control of O. afrasiaticus
 
The efficacy of each pesticide in reducing the motile stages of O. afrasiaticus on date fruit was evaluated under field conditions (Table 2). Three days after treatment. the average number of motile stages of O. afrasiaticus was reported as 6.3. 6. 10.6 and 0 for bifenazate. hexythiazox. spinosad and sulfur. respectively. This corresponded to a percentage reduction in the mite population of 66.9. 68.7. 44.9  and 100 %. respectively. By 21 days post-treatment. the average number of motile stages increased to 25. 45. 203 and 348.3 for the bifenazate. hexythiazox. spinosad and sulfur treatments. respectively. The percentage reductions showed that bifenazate (90.2 %) and hexythiazox (82.5 %) were the most effective acaricides. Spinosad led to a population reduction of 21.4%. while sulfur had no effect in reducing the population.  As far as the ovicidal effect is concerned (Table 3). 19 eggs were counted three days after treatment. which means a reduction of 28 % in the fruits treated with sulfur. In fruits treated with hexythiazox. bifenazate and spinosad. egg counts were 0.6. 3.6 and 4.02. respectively. The greatest reduction in eggs was observed in fruits treated with hexythiazox (97 %). followed by bifenazate (86.6 %) and spinosad (84.9 %). with no significant differences in efficacy between the latter three treatments.

Table 2: Efficacy of bifenazate, hexythiazox, spinosad and sulfur on numbers of O. afrasiaticus motile stages on date fruits before and after 3, 7, 14 and 21 days of spraying of pesticides.



Table 3: Efficacy of bifenazate, hexythiazox, spinosad and sulfur on numbers of O. afrasiaticus eggs on date fruits before and after 3, 7, 14 and 21 days of spraying of pesticides.


       
Three weeks after treatment. the number of O. afrasiaticus eggs on date fruit was found to be 33.6. 4.6. 311 and 308.3 for bifenazate. hexythiazox. spinosad and sulfur. respectively. The highest reduction of eggs (98.5 %) was observed in fruits treated with hexythiazox. Bifenazate also showed a significant ovicidal effect. leading to an 89.4 % reduction in eggs. In contrast. the fruits treated with spinosad and sulfur only showed a reduction of 1.7 % and 2.7 % respectively. which did not differ statistically from the control group.
       
Bifenazate showed high efficacy in killing O. afrasiaticus. These results are consistent with previous observations that bifenazate has significant toxicity potential for the treatment of other Tetranychidae such as Panoncus citri (Wang et al., 2021) and Tetranychus urticae (Li  et al., 2017). is toxic to leaf mites at all life stages (Van Leeuwen  et al., 2007). The long duration of action of bifenazate makes it an acaricide for mite control around the world (Ochiai  et al., 2007).
       
Hexythiazox provides effective control of O. afrasiaticus within 21 days of application. A similar high efficacy against O. afrasiaticus on date fruit was reported by Arbabi et al., (2017) and Fakeer et al., (2019). Negm et al., (2015) also observed that hexythiazox remained toxic to O. pratensis on date fruit for up to three weeks.
       
Spinosad was effective for up to 14 days. Ismail et al., (2007) considered that spinosad had a strong ovicidal effect on T. urticae eggs. Several studies have also found significant toxicity of spinosad to larvae and adult females of T. urticae on leaf disks in laboratory bioassays (Van Leeuwen  et al., 2005; Villanueva and Walgenbach, 2006; Ismail et al., 2007). Rabbi et al., (2021) indicated a significant egg mortality by spinosad. which was 71%. We chose spinosad because we wanted to find out whether spinosad. which is normally used to control E. ceratoniae. could also indirectly control O. afrasiaticus. Previous studies have shown that spinosad is not intended for use against spider mites. but their populations are sometimes exposed to unintended effects. especially in greenhouses where the pesticide is commonly used against thrips. leafminers and caterpillars (Jones  et al., 2005; Dripps  et al., 2011; Santis et al., 2012).
       
The results of this study showed that the sulfur applied in July is no longer effective from the 14th day after treatment under the conditions of the Tunisian oases. Al-Doghairi  (2004) found that the effect of sulfur (80% WP) against O. afrasiaticus was excellent until the 35th day after treatment. The existing literature contains contradictory statements about the effect of sulfur on phytophagous mites. There is no clear pattern as the species studied. the sulfur formulations. the dosage applied and the environmental conditions vary (Kreiter, 1987, Auger  et al., 2003. Costello 2003. Beers  et al., 2009).
 
Analysis of residues
 
The changes in residue concentrations detected in date fruit over time and the European Union (EU) MRLs for bifenzate. hexythiazox and spinosad are shown in Table 4. In a single application of hexythiazox (plot 1). hexythiazox residues were not detectable at harvest. In second plot. which received two applications at harvest. the residue concentration was 0.44 and thus below the EU maximum residue level (2 mg kg-1). For straw berries. the half-life of hexythiazox residues was 2.23 days (Shalaby et al., 2022) and 6.8 days for peaches (Guo et al., 2012).

Table 4: Bifenzate, hexythiazox and spinosad residue levels (mg kg™1 ) detected in date fruits at different intervals (days after treatment DAT).


       
In bifenazate. rapid degradation began after 7 days. Studies have shown that the equivalent half-life of bifenazate in tomato fruit is 1.86 (Shalaby  et al., 2022). Mahmoud et al., (2014) found that bifenazate residues on strawberries had a degradation rate of 93 per cent at eight days after application.
       
For spinosad. no spinosad residues were detectable at two weeks after application and were thus far below the maximum residue levels for date fruit in the EU (0.02 mg kg-1). The residues of spinosad on Siwy dates in Egypt. applied at a dose of 0.2 ml/L on date fruits before storage. were measured after 28 days of treatment. The residue data obtained showed that the residues of spinosad amounted to 0.19 mg/kg (Rashed  et al., 2018). In strawberry fruits. the half-life of spinosad in the fruits was 15 days after spraying (Shalaby  et al., 2022).

CONCLUSION

The results of this study showed that. under the conditions of the Tunisian oases. the sulfur applied in July was toxic from the 14th day onwards. The high toxicity of bifenazate on eggs and motile forms of O. afrasiaticus up to 21 days after application of this acaricide. The residues of bifenazate on date fruits volatilized within 7 days. The hexythiazox can provide effective control of eggs and motile forms of O. afrasiaticus up to 21 days after application. With a single application of Hexythiazox. residues on date fruit gradually declined within 14 days. At harvest. no more Hexythiazox residues were detectable. After two applications of Hexythiazox. the residue concentration at harvest was 0.44 and thus below the EU maximum level (2 mg kg-1). Spinosad was effective for up to 14 days. No spinosad residues were found in date fruits after 7 days of treatment. These results would be helpful in developing a new strategy to control O. afrasiaticus in terms of reducing costs and residual effects.

ACKNOWLEDGEMENT

This research was supported by the Tunisia the Regional Research  Center in Oasis Agriculture of Degache Tunisia. Tunisia.
 
Disclosure statement
 
The authors confirm no relevant financial or non-financial competing interests to report.

CONFLICT OF INTEREST

The authors have no conficts of interest to declare.
 

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