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Article

Evaluation of the Varietal Impact of Two Citrus Species on Fluctuations of Tetranychus urticae (Acari: Tetranychidae) and Beneficial Phytoseiid Mites

1
Laboratory of Functional Ecology and Environment, Faculty of Sciences and Technology, Sidi Mohamed Ben Abdellah University, Imouzzer Street, Fez P.O. Box 2202, Morocco
2
Laboratory of Applied Organic Chemistry, Faculty of Sciences and Technology, Sidi Mohamed Ben Abdellah University, Imouzzer Street, Fez P.O. Box 2202, Morocco
3
Department of Pharmacognosy, College of Pharmacy, King Saud University, P.O. Box 2455, Riyadh 11451, Saudi Arabia
4
Department of Plant Protection, Faculty of Agriculture, Ataturk University, Erzurum 25240, Turkey
5
Department of Zoology, College of Science, King Saud University, P.O. Box 2455, Riyadh 11451, Saudi Arabia
6
Zoology Department, Faculty of Science, Cairo University, Giza 12613, Egypt
7
Department of Vegetable and Herbal Crops, University of Life Sciences, Lublin 50A Doświadczalna Street, 20-280 Lublin, Poland
*
Author to whom correspondence should be addressed.
Sustainability 2022, 14(5), 3088; https://doi.org/10.3390/su14053088
Submission received: 1 February 2022 / Revised: 20 February 2022 / Accepted: 3 March 2022 / Published: 7 March 2022
(This article belongs to the Special Issue Agroecology and Sustainable Organic Farming Systems)

Abstract

:
The activity of Tetranychus urticae Koch, 1836, and its predators (Euseius stipulatus Athias-Henriot, 1960, Typhlodromus sp., and Phytoseiulus persimilis Athias-Henriot, 1957) on two citrus varieties (Nules (Mandarin) and Valencia late (Orange)) was studied in citrus orchards in Machraa Belksiri at the Gharb region of Morocco in the years 2020–2021. In this trial, during the first year of monitoring, we detected that on the Valencia late variety (Citrus sinensis), the occupancy of leaves by T. urticae was important, with 3200 mobile forms (50%). The predator Typhlodromus sp. presented 1385 (22%), followed by E. stipilatus with 1186 mobile forms (18%), while P. persimilis presented the lowest number with 621 forms (10%). Conversely, on the Nules variety (Citrus Clementina), we found (52%) 2475 forms for the pest T. urticae. E. stipulatis was the most abandoning predator, with 1344 (28%), followed by Typhlodromus sp., with 944 (22%); however, the predator P. persimilis was absent. From our results, it can be concluded that synergistic control by these predators can reduce the rate of T. urticae and constitutes a sustainable alternative method in the absence of chemical control. Regarding the effect of the variety of the different mites studied, the varieties Nules and Valencia late showed no impact on the rates of E. 1tipulates and T. urticae, with relatively similar averages, while on the predator Typhlodromus sp. and P. persimilis, the varietal impact was important.

1. Introduction

In Morocco, the area cultivated with citrus has exceeded 130,000 ha, with a total annual production of more than 2.2 million tons, thanks to the strategies developed by the Ministry of Agriculture [1]. In addition, government policy has forecasted an estimated production of 2.5 to 3.5 million tons by 2022 [2]. The citrus fruits are mainly produced in the regions of Moulouya, Souss, Tadla, Haouz, Loukkos, Berkane, and Gharb [3]. Currently, the national citrus market is undergoing an extraordinary change, with a significant decline in exports to the European Union, from 70% to only 25–30%. In comparison, exports to Russia have increased from 45% to 50% of all Moroccan exports [4]. Unfortunately, this sector has been seriously affected in recent years by biotic and abiotic factors [5]. In addition to production and marketing complications, many pests and diseases have reduced the quantity and quality of citrus fruit [6]. Pests of primary economic importance include spider mites, thrips, aphids, medflies, and diaspine scales. [7,8,9].
Tetranychus urticae C. L. Koch, 1836, is native to the temperate zone, but it is frequently introduced in the tropical zone [10]. It is a phytophagous mite of the family Tetranychidae; this species is a highly polyphagous herbivore and a major agricultural pest worldwide that causes hard damages to economic crops [11,12,13]; it presents a notable pest of field crops, ornamentals, and annual and perennial plants [14]. It attacks (i) fruit trees, including apple, citrus, raspberry, and pear shrubs [15]; (ii) vegetables, including okra, cotton, cucumber, bean, tomato, and eggplant [16,17,18,19]; (iii) ornamentals, including dahlia, rose, gerbera, zinnia, and ganda [20]; and medicinal plants, including moringa (Moringa oleifera Lam.), metel (Datura metel L.), Alfalfa (Medicago sativa L.), Peppermint (Mentha piperita L.), rosemary (Salvia rosmarinus Spenn.), and common vervain (Verbena offlicinalis L.) [21,22,23,24,25].
Euseius stipulatus Athias-Henriot, 1960, (Acari: Phytoseiidae) was found in the Mediterranean citrus orchards [24]. It feeds on Panonychus citri and T. urticae and consumes pollen [26]. In Morocco, this predator was observed preying on P. citri, T. urticae, and Tetranychus cinnabarinus and played a role in biological control [27].
Phytoseiulus persimilis Athias-Henriot, 1957, (Acari: Phytoseiidae) is a specialist predator that feeds particularly on Tetranychus species and whose survival depends on the presence and quality of its prey [28]. In the Mediterranean zone, Phytoseiulus persimilis is a principal predator of T. urticae in open fields and in greenhouses [29].
Typhlodromus sp. are predacious mites preying on either tetranychid or eriophyid mites. Certain species are successfully used as biological agents [30]. Typhlodromus mites have a global distribution. In Africa, species have been recorded from Algeria, Morocco, Egypt, Sudan, Congo, and South Africa [31]. In Morocco, Typhlodromus sp. was often observed preying on T. urticae and T. cinnabarinus [27]. The goal of this study is to evaluate the varietal impact of two citrus species (Nules (Mandarin) and Valencia late (Orange)), on fluctuations of T. urticae and beneficial phytoseid mites (E. stipulatus, Typhlodromus sp., and P. persimilis) during a two-year span.

2. Materials and Methods

2.1. Study Area

This study was performed in Mechra Bel Ksiri (34°34′00″ N, 5°57′00″ W), located north of Oued Sebou in the Gharb region at an altitude of 300–500 m above sea level (Figure 1). The Gharb area is Morocco’s largest agricultural region (600 km2) [32]. This area is well known for the production of cereals, citrus, and vegetables due to the suitable climate and soil characteristics [33]. This zone is characterized by its Mediterranean climate, with annual precipitations ranging between 460 and 600 mm, and an average temperature of 27 °C during summer and 13 °C during winter.

2.2. Sampling Design

This experiment was conducted on two plots without chemical practices; the first is a plot of 4 Ha planted with the variety Valencia late (Citrus sinensis). The second one is a 4 Ha plot planted with the variety Clementine Nules (Citrus clementina). In this trial, the activity of T. urticae and its predators (E. stipulatus, Typhlodromus sp., and P. persimilis) was monitored weekly.
In both plots, 10 trees belonging to a square block were selected and monitored weekly; on each tree, 10 leaves collected from different sun exposure sectors (North, East, South, and West) were inspected during 8 weeks (10 repetitions were performed independently) [34,35,36]. In the open field, the total number of predators and phytophagous mites (T. urticae) found were counted on both surfaces of the leaf using a professional 10× eye loupe. Surveys were conducted for 8 consecutive weeks per year during a two-year span. The dates for each week and year were as follows: in 2020, 12 April (week 1), 19 April (week 2), 26 April (week 3), 3 May (week 4), 10 May (week 5), 17 May (week 6), 24 May (week 7), and 1 June (week 8). In 2021, 16 April (week 1), 23 April (week 2), 30 April (week 3), 08 May (week 4), 15 May (week 5), 22 May (week 6), 29 May (week 7), and 6 June (week 8). Temperature data were collected in the field, using Davis Instruments Vantage Pro2.

3. Statistics

Experimental data were performed in Minitab software, version 1.1.19, LLC, State College, PA, USA [37]. The results were given as the SD amd mean. In addition, to evaluate the abandonment of each species of the studied mites, we calculated the percentage of mobile forms of T. urticae and their predators (E. stipulatus, Typhlodromus sp., and P. persimilis) (specimen in question/total species studied). We checked the normality and homogeneity of the variance for all variables with the Kolmogorov–Smirnov test. To assess the impact of varietal and monitoring dates on mite evolution, we used the one-way analysis of variance test, followed by a Tukey post hoc test at p < 0.05 [38].

4. Results

4.1. Leaf Occupancy Rate by Mites in the Different Plots

After the first year of follow-up, on the variety Valencia late (Figure 2), the occupation of the leaves by T. urticae was most important with 50% (n = 3200) of mobile forms. The predator Typhlodromus sp. presented 22% (n = 1385), while the proportion of E. stipulatus was 18% (n = 1186); P. persimilis was the least with a percentage of 10% (n = 621).
The rate of leaf occupancy by these species on the variety Nules (Figure 3) was 52% (n = 2475) for the pest T. urticae. E. stipulatis was the most abundant predator on the trees of this variety with a proportion of 28% (n = 1344), followed by Typhlodromus sp. with 20% (n = 944), whereas the predator P. persimilis was absent.
During the second year of monitoring, in the plot planted with the Valencia late variety, we registered 2779 mobile specimens of T. urticae (45%). For the predator Typhlodromus sp., we recorded 1344 mobile specimens (22%). E. stipulatus was recorded with 1240 mobile specimens (20%). P. persimilis presented the lowest percentage, with 14% (n = 847).
On the Nules variety, we had 2573 mobile specimens of T. urticae (48%), 810 for Tyhphlodromus sp. (15%), and 1412 for E. stipulatus (26%), and P. persimilis had 547 mobile specimens (10%).

4.2. Varietal Impact on Mite Populations

Regarding the effect of the variety on the different mites studied (Figure 4), following the first year of monitoring, the Nules (V2) and Valencia late variety (V1) showed a significant impact on the evolution of T. urticae pests (Table 1), with an average of 40.00A ± 4.59 on Valencia late and 30.94B ± 3.17 on Nules. On the predator Typhlodromus sp., the varietal impact was important; on Valencia late, the average was 17.31A ± 1.86, while on Nules, it was 11.80B ± 1.33. On the other hand, the two varieties did not show any influence on E. stipulates, with an average of 14.82A ± 1.51 on Valencia late and 16.80A ± 1.41 on Nules. P. persimilis was absent on Nules and low on Valencia late, with an average of 7.76A ± 1.40.
In the second year of follow-up (Figure 4), the two varieties did not have an influence on the evolution of T. urticae and E. stipulates, with 34.74A ± 3.35 on Valencia late and 32.16A ± 3.42 on Nules for T. urticae. There were 17.65A ± 2.34 on Valencia late and 15.50A ± 1.78 on Nules for E. stipulatus.
On the contrary, for Typhlodromus sp. and P. persimilis, the varietal impact was significant (Table 1), with an average of 16.80A ± 2.21 on Valencia late and 10.12B ± 1.94 on the Nules variety for the first one and 10.59A ± 2.51 on Valencia late and 06.84B ± 1.56 on the Nules variety for the second one.

4.3. Evolution of Mites on the Two Varieties according to the Follow-Up Dates

On the Valencia late variety, during the first year of follow-up (2020), we noticed that the average of T. urticae was low between the first week (12 April) and the fourth week (3 May) (Figure 5). These averages were between 7.60E ± 1.90 and 12.90D ± 1.18 when the temperature was between 23 °C and 27 °C (Table 2). From the 5th week (10 May) when the temperature was higher than 30 °C, the average of T. urticae had an important increase, increasing from 33.20C ± 4.18 (10 May) to 89.40A ± 6.05 (1 June; week 8). Similarly, the predator E. stipulatus showed a significant increase from the first week to the last week of monitoring; this average increased from 2.20D ± 1.23 (12 April) to 37.81A ± 5.20 (1 June). Equally, the predator Typhlodrumus sp. gradually increased from 5.8E ± 1.93 (12 April; 25 °C) to 32.50A ± 3.97 (1 June; 37 °C). P. persimilis increased from the first week (0.50D ± 0.1) to the last week (15.50A ± 3.50).
During the second year of monitoring, 2021 (Figure 5), in the plot planted with Valencia late variety, the average of T. urticae remained low during the first 4 weeks with similar statistical means, with 7.30D ± 1.93 in week 1 (16 April) and 10.80D ± 2.45 in week 4 (8 May). Hereafter, the average of T. urticae increased significantly to reach 74.10A ± 6.41 on the last date of sampling (6 June). The same results were observed for the three phytoseiid mites, with stability in the number from week 1 to week 4, with 7.40D ± 2.01 for Typhlodromus sp., 2.80D ± 1.01 for E. stipulatus, and 5.20C ± 1.52 for P. persimilis. Then, a significant increase of the averages during the last 4 weeks was observed to reach 26.40A ± 4.10 for Typhlodromus sp., 34.80A ± 4.13 for E. stipulatus, and 17.60A ± 2.34 for P. persimilis in week 8.
On the Nules variety, during the first year of follow-up (2020), Figure 6 shows that T. urticae, E. stipulatus, and Typhlodromus sp. had a significant increase from week 1 (12 April) to week 8 (June 1), while P. persimilis was absent. The averages of T. urticae, E. stipulatus, and Typhlodromus sp. increased from 3.20E ± 1.03, 3.30E ± 1.25, and 2.80C ± 1.47 (12 April; 25 °C) to 58.40A ± 3.86, 35.70A ± 5.97, and 16.00A ± 2.76 (1 June; 37 °C), respectively.
During the second year (2021), T. urticae had a significant increase from the third week where it was 9.60D ± 1.73 (30 April) to reach 56.40A ± 6.43 in the last week (6 June). Typhlodromus sp. did not have a significant increase, as we experienced, during the first year; the average remained almost stable from the third week, with 9.20A ± 2.36, to the last week, with 12.70A ± 2.88. Conversely, P. persimilis appeared on this variety since the first week (16 April), with an average of 2.20E ± 0.76, to reach 11.60A ± 2.14 in the last week (6 June). On both varieties, the density of phtoseiid mites was higher than that of T. urticae during the first four weeks of monitoring, whereas the density of T. urticae exceeded that of the phtoseiid mites during the last four weeks.

5. Discussion

According to our nationwide investigation, this is the first research that has focused on the study of the varietal impact on the evolution of spider mites and beneficial phytoseiid populations. These results are the first data provided to compare the evolution of mites on different citrus varieties in Africa, which is of great importance for further comparative research in order to know the infestation rates and the spread rate of pests according to the variety category.
During the two years of follow-up, without the use of any chemical intervention, we noticed that the evolution of T. urticae exceeded that of their predators (E. stipulatus, Typhlodromus sp., and P. persimilis). Much research conducted in the open field and in greenhouses confirms that pests are a problem of diverse global crops [39,40]. It is a generalist species that can feed on hundreds of host plants and produces a significant destruction to field, greenhouse, and horticultural crops. It can produce silk threads to protect itself from predators or to disperse from plant to plant [41,42]. On the Valencia late variety, during the two years of monitoring, the abundance of the three predators (E. stipulatus, Typhlodromus sp., and P. persimilis) exceeded 50%. Likewise, on the Nules variety, the rate of these predators was approximately 50%, which presented the same rate of T. urticae; from our results it can be concluded that the synergic control by these predators can reduce the rate of T. urticae. A study conducted in Italy showed that the simultaneous release of beneficial phytoseiid mites, Amblyseius aberrans and Typhlodromus pyri, in a vineyard infested by Panonychus ulmi provided significant control [43]. In Morocco, the new introduction in citrus orchards of the predators Neoseiulus californicus McGregor (Acari: Phytoseiidae) and Amblyseius swirskii Athias-Henriot (Acari: Phytoseiidae) against the oriental mite Eutetranychus orientalis and T. urticae ensures good results [5]. Similarly, in Spain, the control of T. urticae through releases of the predatory mites P. persimilis, N. californicus, A. swirskii Athias-Henriot, 1962, and Orius laevigatus Fieber, 1860, (Hemiptera: Anthocoridae) showed significant results. Besides, the combined release of O. laevigatus with A. swirskii gave efficient control of the principal pests of bell pepper [44].
During the second year, the emergence of P. persimilis on the Nules variety caused a decrease in the number of Typhlodromus sp. throughout the monitoring period (8 weeks). In the similar results found by [45] in Spain, the release of P. persimilis alone was better than combined releases. A study was conducted in Florida to develop a sustainable control method (“Predator-In-First” (PIF)) against pepper pests. The use of the phytoseiid mite Amblyseius swirskii in the regulation of several pepper pests (Bemisia tabaci Gennadius, 1889, Frankliniella occidentalis Pergande, 1895, and Polyphagotarsonemus latus Banks) under greenhouse and field conditions was very effective. Results suggest that the application of A. swirskii alone can help regulate several pepper pests and ensure improved crop yield [46]. However, a simultaneous release of multiple predators may cause competition between the species [47].
In the first year of monitoring, our results show that the two varieties of Nules and valencia late have a significant impact on the evolution of T. urticae and the two predators (Typhlodromus sp. and P. persimilis). The same results were obtained by [48,49], who showed that the variety could induce an impact on the evolution of the pests and predators. Another study was performed in the open field on five cotton varieties to compare the infestation degree by the pests Aphis gossypii Glover, 1877, (Hemiptera: Aphididae) and Amrasca devastans Dist. (Hemiptera: Cicadellidae). The results showed that the type of variety could influence the infestation level [50].
Our results show that the rate of T. urticae increased significantly from the first week (12 April) to the last week of monitoring (1 June); this was due to the fluctuation in temperature from 25 °C to 37 °C recorded during the follow-up. Identical results were obtained on clementine in the Gharb region (Morocco), where the orchards were isolated for 3 cropping annuals and without the practice of acaricide treatments in order to investigate the severity of infestation by T. urticae [51]; this study showed that the infestation degree of the trees was 10% in mid-April and increased rapidly to 87% in July. A study realized by [52] confirmed that temperature is the most important environmental factor affecting insect population dynamics.

6. Conclusions

Our results highlight two key pieces of information: (1) The data register that variety can induce an impact on the evolution of pests and predators. (2) The density of the mites can change according to the monitoring dates. In addition, the establishment of an integrated long-term ecological monitoring program and the incorporation of new technologies into surveillance programs is an urgent need to control pests. These programs must take into consideration climatic conditions, plant and pest phenology, infestation rates, and the rate of spread of the pests in each country. All these elements are proposed to control the pests, respect the environment, and promote the expansion of predators.

Author Contributions

Methodology, data curation, software, A.A.; writing—supervision, editing, A.L. and A.F.; supervision, editing, R.U. and Y.B.K.; funding, resource, editing R.A.; supervision, editing, validation, Revision, A.N.; Editing, Writing, A.A.S. All authors have read and agreed to the published version of the manuscript.

Funding

This research was funded by Researchers Supporting Project number (RSP-2021/96), King Saud University, Riyadh, Saudi Arabia.

Institutional Review Board Statement

Not applicable.

Informed Consent Statement

Not applicable.

Data Availability Statement

All related data are within the manuscript.

Acknowledgments

The authors would like to extend their sincere appreciation to the Researchers Supporting Project number (RSP-2021/96), King Saud University, Riyadh, Saudi Arabia.

Conflicts of Interest

The authors declare no conflict of interest.

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Figure 1. Location of studied citrus orchards.
Figure 1. Location of studied citrus orchards.
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Figure 2. Abundance of the phytophagous mite Tetranychus urticae and their predators (Euseius 4tipulates, Typhlodromus sp., and Pytoseiulus persimilis) during the whole monitoring period on the Valencia late variety.
Figure 2. Abundance of the phytophagous mite Tetranychus urticae and their predators (Euseius 4tipulates, Typhlodromus sp., and Pytoseiulus persimilis) during the whole monitoring period on the Valencia late variety.
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Figure 3. Abundance of the phytophagous mite Tetranychus urticae and their predators (Euseius stipulatus, Typhlodromus sp. and Pytoseiulus persimilis) during the whole monitoring period on the Nules variety.
Figure 3. Abundance of the phytophagous mite Tetranychus urticae and their predators (Euseius stipulatus, Typhlodromus sp. and Pytoseiulus persimilis) during the whole monitoring period on the Nules variety.
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Figure 4. Comparison between the means of different mites, depending on the variety (V1: Valencia late variety; V2: Nules variety) in first year, 2020, and the second year, 2021. Values that do not share the same letter are significantly different (p < 0.05).
Figure 4. Comparison between the means of different mites, depending on the variety (V1: Valencia late variety; V2: Nules variety) in first year, 2020, and the second year, 2021. Values that do not share the same letter are significantly different (p < 0.05).
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Figure 5. Evolution of T. urticae and their predators on Valencia late (V1) (a) in the first year, 2020, and (b) second year, 2021, according to the different follow-up dates (Phytoseiid mites: E Stipulatus + P. persimilis + Typhlodromus sp.).
Figure 5. Evolution of T. urticae and their predators on Valencia late (V1) (a) in the first year, 2020, and (b) second year, 2021, according to the different follow-up dates (Phytoseiid mites: E Stipulatus + P. persimilis + Typhlodromus sp.).
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Figure 6. Evolution of T. urticae and its predators on Nules (V2) in first year, 2020, and second year, 2021, according to the different follow-up dates (Phytoseiid mites: E. stipulatus + Typhlodromus sp. + P. persimilis).
Figure 6. Evolution of T. urticae and its predators on Nules (V2) in first year, 2020, and second year, 2021, according to the different follow-up dates (Phytoseiid mites: E. stipulatus + Typhlodromus sp. + P. persimilis).
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Table 1. Varietal impact on different mite populations in the first (2020) and second year (2021).
Table 1. Varietal impact on different mite populations in the first (2020) and second year (2021).
YearSourceDFAdj SSAdj MSF-Valuep-Value
Varietal impact on T. urticae 141414141.24.510.035 *
Varietal impact on E. stipulatus1156.0156.00.800.373
2020Varietal impact on Typhlodromus sp.112161215.5118.150.000 *
Varietal impact on P. persimilis 124102410.26135.120.000 *
Varietal impact on T. urticae 1265265.20.380.540
Varietal impact on E. stipulatus 1184.9184.90.880.350
2021Varietal impact on Typhlodromus sp. 117821782.2346.750.000 *
Varietal impact on P. persimilis 1562.5562.5022.420.000 *
* Statistically significant p-values (p < 0.05).
Table 2. Temperatures recorded during the monitoring period.
Table 2. Temperatures recorded during the monitoring period.
Follow-Up Date, 1st Year12 April (Week 1) 19 April (Week 2)26 April (Week 3)3 May (Week 4)10 May (Week 5)17 May (Week 6)24 May (Week 7)1 June (Week 8)
Temperature, 1st year25 °C27 °C23 °C27 °C30 °C32 °C34 °C37 °C
Follow-Up date, 2nd year16 April (Week 1) 23 April (Week 2)30 April (Week 3)08 May (Week 4)15 May (Week 5)22 May (Week 6)29 May (Week 7)6 June (Week 8)
Temperature, 2nd year23 °C25 °C25 °C27 °C33 °C33 °C37 °C35 °C
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Assouguem, A.; Farah, A.; Ullah, R.; Korkmaz, Y.B.; Almeer, R.; Sayed, A.A.; Najda, A.; Lazraq, A. Evaluation of the Varietal Impact of Two Citrus Species on Fluctuations of Tetranychus urticae (Acari: Tetranychidae) and Beneficial Phytoseiid Mites. Sustainability 2022, 14, 3088. https://doi.org/10.3390/su14053088

AMA Style

Assouguem A, Farah A, Ullah R, Korkmaz YB, Almeer R, Sayed AA, Najda A, Lazraq A. Evaluation of the Varietal Impact of Two Citrus Species on Fluctuations of Tetranychus urticae (Acari: Tetranychidae) and Beneficial Phytoseiid Mites. Sustainability. 2022; 14(5):3088. https://doi.org/10.3390/su14053088

Chicago/Turabian Style

Assouguem, Amine, Abdellah Farah, Riaz Ullah, Yesim Bulak Korkmaz, Rafa Almeer, Amany A. Sayed, Agnieszka Najda, and Abderrahim Lazraq. 2022. "Evaluation of the Varietal Impact of Two Citrus Species on Fluctuations of Tetranychus urticae (Acari: Tetranychidae) and Beneficial Phytoseiid Mites" Sustainability 14, no. 5: 3088. https://doi.org/10.3390/su14053088

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