Introduction

About 2.7 million tons of limes and lemons are produced annually in Mexico (^{FAO, 2021a}). Most of the Mexican lemon [Citrus aurantifolia (Christm.) Swingle] production is concentrated in Michoacán, in the Apatzingán Valley, with an established area of 60 thousand hectares, distributed in the municipalities of Múgica, Parácuaro, Apatzingán, Aguililla, and Tepalcatepec mainly, with a production of 1.22 million tons annually, representing an economic spillover of USD $ 328.21 million annually (^{SIAP, 2021}). However, during the Mexican lemon production process in the Apatzingán Valley, citrus growers observe the presence of pests such as the Asian psyllid Diaphorina citri (Kuwayama), red spider mite Tetranychus urticae (Koch) and Thrips (Thysanoptera: Thripidae). This last pest became the most important pest in terms of fruit damage, causing lacerations in the epidermis in the early stages of development. Consequently, at the time of harvesting, the damage that occurs in production causes a marketing problem that is reflected in lower prices and, in very severe cases, the rejection of the crop. In addition, the excess of insecticide applications (organophosphates, carbamates, neonicotinoids, pyrethroids/pyrethrins) has caused the development of multiple resistance of the pest and the mortality of most beneficial insects that can control pest populations, leaving residues in food, intoxications to users, contamination to natural resources (^{Bejarano-González, 2017}) and technological dependence.

Among several pest management options, the adoption of integrated management through biorational control and biological control by conservation has stood out. In the case of severe thrips infestations on Mexican lime, the most indicated is to reduce chemical insecticide applications and make good management of herbaceous plants, which act as a refuge for thrips predators such as Chrysoperla rufilabris, Ceraeochrysa cincta, Stetorus sp, Cycloneda sanguinea, Hippodamia convergens, Olla v-nigrum, Zelus renardii, Leptotrips sp. and several spider species (^{Atakan & Pehlivan, 2019}; ^{Miranda-Salcedo & Loera-Alvarado, 2019}).

In relation to the above, there are antecedents on the management of thrips in Mexican lime, such as the case of ^{Miranda-Salcedo et al. (2021}) who reported for the insecticide Spirotetramat at a dose of 0.5 ml L^-1, 2 days after application a decrease in the population of thrips F. occidentalis Pergande 1895 by 100 % (from 1.6 thrips to 0 thrips), in Michoacán, Mexico.

^{Monteon-Ojeda et al. (2020}) found a 73 % presence of Frankliniella invasor in the mango manila crop in Actopan, Veracruz. They reported that Spinetoram at a dose of 500 mL ha^-1, maintained an average of 0.71 thrips per inflorescence and an efficacy of 87 % at 7 daa, while garlic, chili, and cinnamon extract at a dose of 2 L ha^-1 controlled 85.46 % of the population at 14 daa.

^{Miranda-Salcedo et al. (2020}) in Michoacán Mexico, showed that Spirotetramat at a dose of 0.75 mL L^-1 decreased the population of F. occidentalis thrips on Mexican lime by 70 % (from 1.0 to 0.3 thrips) at 18 daa. In addition, they observed a wide group of natural enemies that can control the pest such as Cereaochrysa cincta Schneider, 1851, Chrysoperla rufilabris Burmeister, 1839, Cycloneda sanguinea L., 1763, Hippodamia convergens Guerin-Meneville, 1842, Leptotrips sp. and different spider species. Olla v-nigrum Mulsant, 1866, Sthetorus sp., Tamarixia radiata Waterston, 1922, Zelus renardii Kolenati, 1857. However, ^{Avendaño-Gutiérrez et al. (2020}), collected 4968 Thysanoptera on Mexican lime and identified four thrips predatory species: Scolotrhips sexmaculatus, Leptotrhips micconelli, Stomatotrhips brunneus, and Scolotrhips palidus, also in Michoacán Mexico.

In Germany, in an apple crop, ^{Viñuela et al. (1996}) showed that neem (EC, 1 % azaradactin) at a dose of 0.3 % had low toxicity (20 % mortality) on Chrysoperla carnea larvae in the field, because the substance has a repellent effect.

^{Bennison et al. (2002}) reported that rosemary plants (Rosmarinus officinalis) associated with chrysanthemum crops showed great potential as repellent plants for the California thrips Frankliniella occidentalis (Thysanoptera: Thripidae); however, there was observed evidence of a repellent effect on its biological predator Orius laevigatus (Hemiptera: Anthocoridae). This corroborates a “push-pull” strategy based on the combination of stimuli, which modifies the distribution and abundance of arthropod pests and their enemies (^{Salas et al., 2021}).

Therefore, through the application of biorational insecticides along with conservation and management of natural enemies, good thrips management is obtained for the Mexican lemon crop. This study aimed to evaluate the effect of biorational products on thrips management and to record the impact on their natural enemies, for the Mexican lemon crop in Michoacán, Mexico.

Material and Methods

Study variables

The measurement of the study variables was structured in two categories, the first one contemplates the variable of insect pest: 1) Number of thrips F. occidentalis. The second, contemplates three variables of the arthropods considered as natural enemies: 2) Number of Olla v-nigrum (Mulsant, 1866) catarinae (Coleoptera: Coccinellidae); 3) Number of lacewings Chrysoperla rufilabris (Burmeister, 1839) (Neuroptera: Chrysopidae); 4) Number of phytoseiids [predatory mites] Phytoseiulus persimilis (Athias-Henriot, 1957) (Acari: Tetranychidae: Phytoseiidae). To convert the number of insects of the variables into percentages, Equation 1 was used.

Technique and instruments for field data collection

The technique used to record pest insect infestation in the field was “tapping sampling”. The materials used were a 38 x 21 cm wooden board lined with blue adhesive paper and a wooden handle 30 cm long and 3 cm in diameter. One lateral branch per tree was selected at approximately 1.50 m of height and three light blows were given with the wooden handle so that arthropods fell on the board and at the same moment they were identified, counted in situ and capture data recorded (Miranda-Ramírez et al., 2021).

For data collection, a previous sampling was done as a starting point for the study and comparison. After the application of the treatments, sampling was carried out at 3, 6, 12, 20, 26, 35 and 41 days after application (daa).

Experimental design and statistical analysis

The design used was completely randomized, with twelve treatments, and ten replications; the experimental unit was a tree. For the statistical analysis, the Post Hoc test of homogeneity of variances data, ANDEVA, and Tukey’s test of comparison of means (p ≤ 0.05) were performed, using the statistical package Statistica version 13 (^{StatSoft Inc., 2017}).

Results and Discussion

Discussion

The present work corroborates an analysis of the agronomic management of thrips and its natural enemies in the Mexican lemon crop. The results showed that there is a sustainable alternative for the management of thrips populations, supported by some commercial botanical insecticides and the biorational effect on natural enemies.

There is a large number of chemical products that control thrips, but they may also affect its natural enemies, which increases damage to Mexican lemon foliage and fruit (^{Miranda-Salcedo et al., 2020}; ^{Miranda-Salcedo et al., 2021}). ^{Argolo et al. (2014}), reported persistence of secondary effects of Spirotetramat for Phytoseiulus persimilis of zero days, with mortality ranging from 30 to 79 %. This insecticide has a rapid and temporary impact on insect populations and citrus growers prefer to use it, because it seems easy to obtain visible results with a rapid decrease in insect populations, including beneficial insects (^{Xiao et al., 2010}; ^{Raza et al., 2017}). On the other hand, ^{Ferragut et al. (1990}) pointed out, that phytoseiid mites found on wild plants, exhibit good tolerance to some insecticides, and are very common in field crops and feed on small-sized arthropods such as pest thrips.

^{Argolo et al. (2013}), reported in Spain, mortality of less than 30 % of phytoseiids with the application of neem oil (azadirachtin) and a persistence effect of zero days for citrus. The control efficiency of these phytoseiid mites on thrips pests depends largely on the percentage decrease caused by the effect of insecticides, which are used during the management of this pest. ^{Argolo et al. (2014)}, found that the phytoseiid species most sensitive to mineral oils is Phytoseiulus persimilis.

Phytoseiid mites can show persistence to plant Spinosina for up to seven days, with a decrease of 30 to 79 % (^{San-Andres et al., 2006}; ^{Argolo et al., 2013}). However, to identify biorational insecticides that could be used in combination with a biological control strategy, it is important to know any side effects on natural enemies (^{Sterk et al., 1999}). One way to control F. occidentalis thrips is by releasing native phytoseiid mites (^{Urbaneja et al., 2005}) which at one point in time and in the near future may eventually reduce the excess application of insecticides in the Apatzingán valley.

^{Esparza-Díaz et al. (2010}) pointed out that the effect of azadirachtin depends on its dose and the pest species to be controlled since it can reduce feeding, survival, nymph viability, progeny, and can even produce acute toxicity. This oil acts as an alarm pheromone and makes insects stop eating, and its active substances are biodegradable and non-toxic to humans and domestic animals (^{Guerra-Maldonado, 2021}).

In relation to chrysopids, ^{Luna-Cruz et al. (2018}) applied an insecticide composed of argemonin (Chicalote, Argemone mexicana L.), berberine (Berberis sp.) ricinine (higuerilla, Ricinus communis L.) and α-Terthienyl by direct contact and reported a mortality of 9 % at 24 h, the highest mortality of 11 % at 98 h, under laboratory conditions.

^{Planes et al. (2013}) pointed out, that the conservation of natural enemies is key to being able to carry out an effective “Integrated Management” of pests in citrus since a major part of the pests are naturally controlled by some of these natural enemies.

Conclusions

Tolfenpyrad product proved to be a very efficient chemical insecticide in reducing the number of thrips during all sampling dates and remained constant with a range of 41.40 to 98.78 % mortality. However, for the number of coccinellids, the effect was devastating, showing a reduction in the population of 100 % in all the samplings except for 35 daa; for lacewings, it also reached levels of decrease in the population up to 100 %, so it is considered of high impact for the natural enemies of thrips.

The insecticides that showed a decrease in the population of thrips based on plant extracts were garlic extract + chamomile and rue extract, castor oil, Neem + castor oil + governess oil + cinnamon oil + garlic oil + mustard oil, neem oil, and vegetable Spinosin on all sampling dates and with the effect observed up to 41 daa. Garlic oil proved to be a good option for the control of thrips by reducing their population by an average of 60 %, and in phytoseiid mites, there was an increase of an average of 800 %. These extracts may represent an alternative for the control of thrips on Mexican lime in the Apatzingán Valley.