# Induced tomato defenses mediated by jasmonic acid do not have a major effect on the density of predator biological control agents

M. Bohloolzadeh, J. M. Alba, D. Serrano-Carnero, A. Elragig, A.

Rodríguez-Gómez, P. Bielza, S. Legarrea, M. Navajas, M S Tixier, A. Paspati, et al.

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## To cite this version:

M. Bohloolzadeh, J. M. Alba, D. Serrano-Carnero, A. Elragig, A. Rodríguez-Gómez, et al. Induced tomato defenses mediated by jasmonic acid do not have a major effect on the density of predator biological control agents. Journal of Pest Science, In press, 10.1007/s10340-025-01941-y. hal-05162853

HAL Id: hal-05162853

https://hal.inrae.fr/hal-05162853v1

Submitted on 15 Jul 2025

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Distributed under a Creative Commons Attribution 4.0 International License
# Induced tomato defenses mediated by jasmonic acid do not have a major effect on the density of predator biological control agents

M. Bohloolzadeh<fnref n="1" />,<fnref n="9" /> Ⓓ J. M. Alba<fnref n="1" /> Ⓓ D. Serrano-Carnero<fnref n="1" /> Ⓓ A. Elragig<fnref n="2" /> Ⓓ A. Rodríguez-Gómez<fnref n="3" /> Ⓓ P. Bielza<fnref n="3" /> Ⓓ

S. Legarrea<fnref n="4" /> Ⓓ M. Navajas<fnref n="5" /> Ⓓ M. S. Tixier<fnref n="6" /> Ⓓ A. Paspati<fnref n="7" /> Ⓓ M. Recker<fnref n="2" />,<fnref n="8" /> Ⓓ M. Montserrat<fnref n="1" />

Received: 16 September 2024 / Accepted: 13 June 2025
© The Author(s) 2025

## Abstract

Plants have developed different defense mechanisms to protect themselves from the attack of herbivores. Plant defenses can be categorized into two types: constitutive, which are present before herbivore attack, and induced, which are activated upon attack. Some herbivores have developed the ability to neutralize either or both types of plant defenses, and plant defenses may act against their own interest when they negatively affect herbivore's natural enemies such predator insects and mites. Here we investigated whether herbivore-induced tomato defenses mediated by jasmonic acid (JA) affect the density of predator biological control agents and thus affect biological pest control negatively. Specifically, we assessed predator-herbivore abundances in greenhouse experiments on two tomato genotypes, a wild type (*Castlemart*) expressing the JA-mediated defense pathway and a mutant of the wild type (*def-1*) unable to activate this defense path. Plants were infested with either *Bemisia tabaci*, a pest that suppresses the activation of the JA defense path, or *Frankliniella occidentalis*, a pest species that induces JA defenses. As predators, we used four species of natural enemies, two phytoseiid mites and two predatory bugs, one of each pair able to colonize tomato crops (*Typhlodromus (A.) recki*, *Macrolophus pygmaeus*) and the other not (*Amblyseius swirskii*, *Orius laevigatus*). Results suggest that JA-mediated defenses do not have a negative impact on predator density. Instead, glandular trichomes likely contributed to the unsuccessful pest control. Yet, JA-mediated defenses are key for plant protection against herbivore species that cannot avoid this line of defense.

**Keywords** Predatory mites • Predatory insects • Phytoseiidae • Anthocoridae • Miridae • Biological pest control

Communicated by Antonio Biondi.

M. Recker and M. Montserrat have shared senior authorship.

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M. Montserrat
mmontserrat@eelm.csic.es

## Introduction

Plants and herbivores have been engaged in an evolutionary arms race during their ca 350 million years of co-existence, in which plants have evolved an array of defenses to resist or evade herbivore attacks (Gatehouse

<footnote n="1">¹ Institute for Mediterranean and Subtropical Horticulture "La Mayora" - University of Málaga - Spanish National Research Council (IHSM-UMA-CSIC), Avda Dr Weinberg s/n, 29750 Algarrobo-Costa, Málaga, Spain</footnote>

<footnote n="2">² Centre for Ecology & Conservation, University of Exeter, Penryn Campus, Penryn, UK</footnote>

<footnote n="3">³ Agronomic Engineer Department, Polytechnic University of Cartagena, Cartagena, Spain</footnote>

<footnote n="4">⁴ Institute for Biodiversity and Ecosystem Dynamics, University of Amsterdam, Amsterdam, The Netherlands</footnote>

<footnote n="5">5 CBGP, INRAE, CIRAD, IRD, Institut Agro, Univ Montpellier, Montpellier, France</footnote>

<footnote n="6">6 CBGP, CIRAD, INRAE, Institut Agro, IRD, Univ Montpellier, Montpellier, France</footnote>

<footnote n="7">7 Hellenic Agricultural Organization "DIMITRA", Institute of Olive Tree, Subtropical Crops and Viticulture, Heraklion, Greece</footnote>

<footnote n="8">⁸ Institute for Tropical Medicine, University of Tübingen, Tübingen, Germany</footnote>

<footnote n="9">⁹ R&D_Production Department, Bioline Agrosciences_ Iberia S.L., Pol. Ind. la Redonda, C. Bremen, 2, 04710 Santa María del Águila, Almería, Spain</footnote>
2002; Kessler and Baldwin 2002; Glazebrook 2005). Plant defenses against arthropod herbivores can be broadly categorized into two types: constitutive, that is, defenses that are always active, and induced, that is, defenses that are activated upon herbivore attack. Some examples of constitutive defenses are the formation of physical barriers via lignification of cellular walls to hinder herbivory (Hanley et al. 2007), the synthesis and accumulation of compounds that are toxic to herbivores (review by Kant et al. 2015; Schimmel et al. 2018), or the development of glandular trichomes containing toxic or sticky substances, such as acylsugar, methyl ketones, and other terpenes, typical of tomato plants (Alba et al. 2009; Glas et al. 2012). Induced defenses involve the synthesis of phytohormones immediately after the herbivore attack. Two phytohormones play a key role at modulating the defense response: salicylic acid (SA) and jasmonate acid (JA) (Walling 2000; Thaler et al. 2012). While JA-mediated defenses are typically activated in response to herbivores and necrotrophic pathogens, SA-mediated defenses are mostly activated against hemi/biotrophic pathogens (Monte 2023), yet phloem-feeding insects can also activate SA-mediated defenses (Walling 2000). Both phytohormones function as a signal to mediate the accumulation of various secondary metabolites or proteins that negatively affect the survival or development of the herbivore (Wang and Wu 2013).

In this evolutionary arms race, however, herbivores are not passive actors and have evolved mechanisms to cope with plant defenses (Kant et al. 2008; Alba et al. 2015). A well-known mechanism is the ability of some herbivore species to sequester toxic plants defense compounds (see the recent review by Beran and Petschenka 2022), or the ability of some herbivores to suppress the activation of JA-mediated plant defenses (Kant et al. 2008; Sarmento et al. 2011; Alba et al. 2015). Furthermore, constitutive and induced plant defenses are rarely target specific and thus have the potential to affect the enemies of herbivores as well, such as predators, which otherwise work as allies to plants (Riddick and Simmons 2014; Ataide et al. 2016). For example, a recent work showed that tomato glandular trichomes strongly determine the ability of an important group of natural enemies, the predatory mites of the family Phytoseiidae, to control the populations of their pest (Legarrea et al. 2022). Similarly, the defensive compounds produced in response to JA signaling can sometimes be harmful to natural enemies (Thaler 2002), either because toxic components ingested by herbivores from plants intoxicate their predators or because predator abundance is affected by the lower quality and/or lower abundance of herbivores (Ataide et al. 2016; Thaler 1999). For example, in a field experiment Thaler (2002) found significantly less number of eggs of syrphid flies close to aphid colonies foraging on tomato plants sprayed with JA than on tomato plants sprayed with water.

Tomato (Solanum lycopersicum L.) plants are host for many different pests, including whiteflies [e.g., *Trialeurodes vaporariorum* (Westwood) and *Bemisia tabaci* (Gennadius) (Hemiptera: Aleyrodidae)], leafminers [e.g., *Tuta absoluta* (Meyrick) (Lepidoptera: Gelechiidae) and *Liriomyza trifolii* (Diptera: Agromyzidae)], fruit borers [e.g., *Helicoverpa armigera* (Hubner) (Lepidoptera: Noctuidae)], aphids [e.g., the potato aphid *Macrosiphum euphorbiae* (Sulzer) (Hemiptera: Aphididae)], spider mites [e.g., *Tetranychus urticae* Koch (Acari: Tetranychidae)], which cause significant yield losses (Zoebisch et al. 1984; Schuster et al. 1991; Johnson et al. 1992; Goggin et al. 2001; Ferrero et al. 2011; Ramos et al. 2018; Buragohain et al. 2021). In response to herbivore threads, tomato plants are heavily protected by both constitutive (glandular trichomes that produce large quantities of secondary metabolites) and induced (mostly mediated by JA) plant defenses. Yet, while tomato glandular trichomes are well known to negatively affect the foraging efficiency of some predator species (Legarrea et al. 2022), whether JA-mediated plant defenses affect them is variable and not fully understood (Kaplan and Thaler 2011).

In this work, we investigated the impact of JA-mediated plant defenses on the density of predators to assess whether such defenses have an indirect negative effect on biological control agents. We used two tomato genotypes, a wild type (*Castlemart*, CM hereafter) with the JA-induced defense fully functional and a mutant (*def-1*) unable to activate this defense path. These two genotypes have been typically used in studies addressing the role of JA-mediated defenses on the evolution of herbivore-plant interactions (Kant et al. 2004; Alba et al. 2015). Indeed, tomato is a crop species for which several mutants are available that express or lack the expression of different type of defense mechanism (Li et al. 2004). We also used two herbivore species, *B. tabaci*, a species that suppresses the activation of the JA defense path (van de Ven et al. 2000), or *F. occidentalis*, a species unable to do so (Abe et al. 2009). As predators, we used four species of natural enemies, including two phytoseiid mites and two predatory bugs, one of each pair able to colonize tomato crops [*Typhlodromus (Anthoseius) recki* Wainstein and *Macrolophus pygmaeus* (Rambur)], and the other not (*Amblyseius swirskii* Athias-Henriot and *Orius laevigatus* (Fieber)]. Each predator-herbivore pair was chosen according to what herbivore species the predator is usually used against (i.e., *A. swirskii* and *M. pygmaeus* against whiteflies, and *O. laevigatus* against thrips), except for the predatory mite *T. (A. recki. Typhlodromus (A.) recki)*. This species develops well on different cultivars of tomato (Tabary et al. 2024), and it was tested against the two herbivores. To our knowledge, this species, not yet commercialized, has only been tested thus far against *T. urticae*, *T. evansi* (Baker & Pritchard) (Acari: Tetranychidae), and *Aculops lycopersici* (Tryon) (Acari: Eriophyidae) (Tixier et al. 2020a; Ersin et al. 2021).

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We are aware that we included predator species known to be unsuccessful at controlling the abundance of herbivores in tomato crops. Yet, we still expected to detect differences in predator and herbivore densities if the induction of jasmonic acid would influence the predator's survival, foraging capabilities, etc. Also, because jasmonic acid might play a role in the formation of glandular trichomes (Li et al. 2004), we estimated predator entrapment at the end of the experiment to be able to account for genotype-dependent effects of tomato constitutive defenses on the density of predators.

# Material and methods

## Animal and plant materials

Amblyseius swirskii was obtained from the rearing that is kept at the Institute for Mediterranean and Subtropical Horticulture "La Mayora" (IHSM) facilities, which was started in 2017 from ca. 600 individuals collected in citrus orchards at two different locations in Israel [(32° 56'36.43" N; 35° 6'1.26" E) and (33° 9'54.57" N; 35° 35'17.43" E)]. *Typhlodromus* (A.) *recki* were kindly supplied by Prof Dr. Marie-Stéphane Tixier, from Institut Agro Montpellier, France, in 2021. *Macrolophus pygmaeus* and *Frankliniella occidentalis* were kindly supplied by Biobest Group, Belgium. *Orius laevigatus* were kindly supplied by the Prof Dr. Pablo Bielza, from Universidad Politécnica de Cartagena, Spain. *Bemisia tabaci* [Mediterranean (MED) species, formerly Q biotype], indigenous to the Mediterranean region and characterized first from Spain (Guirao et al. 1997), were obtained from populations kept at the IHSM facilities (see below).

To evaluate effects of induced defenses on the performance of predator BCAs, we used plants of *Solanum lycopersicum* var. Castlemart (CM), which can activate JA-mediated defenses upon damage, and the mutant *def-1*, in the genetic background of CM, which is unable to accumulate the JA hormone. Tomato seeds of the two accessions of *S. lycopersicum* were originally obtained from the UC Davis/ C.M. Rick Tomato Genetics Resource Center, Department of Plant Sciences, University of California, Davis, CA 95616 (https://tgrc.ucdav.is.edu/). Seeds were kept and propagated at the University of Amsterdam greenhouse facilities, and they were kindly supplied to us by Prof. Dr. Merijn Kant. Plants used in the experiments of the two cultivars were grown inside a climate chamber at 25 ± 2 °C, 70 ± 10% RH, and 16:8 h L:D (light:dark).

## Insect and mite cultures

Predatory mites (*A. swirskii* and *T. (A. recki*) were cultured at the laboratory facilities of the IHSM "La Mayora."

Rearing units consisted of a plastic sheet, placed on top of a water-saturated foam covered by a wet layer of cotton, and placed in a plastic tray, half-filled with water. The margins of the plastic sheet were surrounded by strips of moistened filter paper which served as a source of water and a physical barrier that helped to dissuade and prevent predators from escaping. Cotton threads were provided as oviposition substrates to enhance the oviposition of predatory mites on flat surfaces, and small pieces of roof shape plastic were placed on top of them, to provide shelter to the mites. New cultures of similar-aged individuals (egg waves) were made weekly by transferring the cotton threads filled with eggs to the new rearing units. Mites were fed 3 times per week ad libitum with pollen of *Carpobrotus edulis* (L.) (Caryophyllales: Aizoaceae). Colonies were cultured in a climate chamber at 25 ± 2 °C, 70 ± 10% RH, and 16:8 h L:D (light:dark) photoperiod. Pollen of *C. edulis* was obtained from the pink-petal flower phenotype. When flowers were about to open, sepals and petals were taken to the laboratory, and stamens were removed and dried on a stove at 37 °C for 48 h and sieved through 0.25-mm and 0.075-mm sieves, consecutively, to obtain pollen free of impurities. Lastly, pollen was stored in a freeze at -20 °C until it was needed.

*Bemisia tabaci* (MED) was reared on melon (Cucumis melo L. cv. ANC42, IHSM seedbank collection) plants inside wooden cages covered with insect-proof nets, in an insect-proof glasshouse with temperature controlled (22-27 °C day and 17-20 °C night) and light supplementation when needed.

Individuals of *M. pygmaeus*, *F. occidentalis*, and *O. laevigatus* used in our experiments were used upon arrival to our facilities.

## Effects of JA-mediated defenses on predator and herbivore density

Experiments were carried out at the IHSM La Mayora-CSIC in a plastic greenhouse containing four tables (2.5 × 1.5 m). Either four or eight (see the specifics for each predator/pest combination) cages (90×45×45 cm) containing two tomato plants with three full grown leaves, each with 5 leaflets, were placed on the tables. Half of the cages per table contained the CM genotype and the other half the *def-1* genotype. Experiments were not designed to compare the performance among BCAs, but they aimed at testing the effects of plant defenses mediated by JA on the performance of four BCAs. Each predator/herbivore system tested had four replicates per treatment. The initial number of predators and herbivores introduced in the cages was specific to each predator/herbivore system and based on information from the literature (see below):

*Amblyseius swirskii / Bemisia tabaci:* All the tomato plants were infested with 15 and 5 females *B. tabaci* on
<table><caption>**Table 1** Results of the generalized linear models applied to the cumulative number of the pest, for each predator–pest system separately: (a) *A. swirskii*—*B. tabaci*; (b) *M. pygmaeus*—*B. tabaci*; (c) *O. laevigatus*—*F. occidentalis*; (d) *T. (A. recki*—*B. tabaci*; (e) *T. (A. recki*—*F. occidentalis*; (f) Results of the generalized linear models applied to the number of individuals found entrapped on glandular trichomes</caption><thead><tr><th>Sources of variation</th><th>LR Chisq</th><th>Df</th><th>Pr(&gt; Chisq)</th></tr></thead><tbody><tr><td colspan="4">(a) Response: juveniles of <i>Bemisia tabaci</i>; predator: <i>Amblyseius swirskii</i></td></tr><tr><td>TOM_GENOTYPE</td><td>0.009</td><td>1</td><td>0.925</td></tr><tr><td>PREDATOR</td><td>0.414</td><td>1</td><td>0.520</td></tr><tr><td>TOM_GENOTYPE:PREDATOR</td><td>0.516</td><td>1</td><td>0.472</td></tr><tr><td colspan="4">(b) Response: juveniles of <i>Bemisia tabaci</i>; predator: <i>Macrolophus pygmaeus</i></td></tr><tr><td>TOM_GENOTYPE</td><td>0.040</td><td>1</td><td>0.841</td></tr><tr><td>PREDATOR</td><td>8.927</td><td>1</td><td>0.003 **</td></tr><tr><td>TOM_GENOTYPE:PREDATOR</td><td>0.0024</td><td>1</td><td>0.961</td></tr><tr><td colspan="4">(c) Response: mobile stages of <i>Frankliniella occidentalis</i>; predator <i>Orius laevigatus</i></td></tr><tr><td>TOM_GENOTYPE</td><td>31.170</td><td>1</td><td>&lt;0.001 ***</td></tr><tr><td>PREDATOR</td><td>1.333</td><td>1</td><td>0.248</td></tr><tr><td>TOM_GENOTYPE:PREDATOR</td><td>0.820</td><td>1</td><td>0.365</td></tr><tr><td colspan="4">(d) Response: juveniles of <i>Bemisia tabaci</i>; predator: <i>Typhlodromus (A.) recki</i></td></tr><tr><td>TOM_GENOTYPE</td><td>0.015</td><td>1</td><td>0.901</td></tr><tr><td>PREDATOR</td><td>0.272</td><td>1</td><td>0.602</td></tr><tr><td>TOM_GENOTYPE:PREDATOR</td><td>0.589</td><td>1</td><td>0.443</td></tr><tr><td colspan="4">(e) Response: mobile stages of <i>Frankliniella occidentalis</i>; predator: <i>Typhlodromus (A.) recki</i></td></tr><tr><td>TOM_GENOTYPE</td><td>11.007</td><td>1</td><td>&lt;0.001 ***</td></tr><tr><td>PREDATOR</td><td>1.502</td><td>1</td><td>0.220</td></tr><tr><td>TOM_GENOTYPE:PREDATOR</td><td>0.315</td><td>1</td><td>0.575</td></tr><tr><td colspan="4">(f) Response: entrapment</td></tr><tr><td>TOM_GENOTYPE</td><td>1.812</td><td>1</td><td>0.178</td></tr><tr><td>PREDATOR</td><td>48.768</td><td>3</td><td>&lt;0.001 ***</td></tr><tr><td>TOM_GENOTYPE:PREDATOR</td><td>0.737</td><td>3</td><td>0.864</td></tr></tbody></table>

Sources of variation included in the models were “tomato genotype” (2 levels: CM and def-1) and “predator” (2 levels, Yes and No) as categorical variables

week 0 and 1, respectively. At week 1, half of the cages per tomato genotype received 15 females of *A. swirskii* (10–12 days old, since egg hatching) per plant (5 per tomato leaf) (Calvo et al. 2011). The other cages received no predator. All the treatments were randomly allocated to a position within each table. Each week, from the second week till week 9, the number of juvenile whiteflies (i.e., all the immature sessile stages: 2nd and 3rd larval stage and pupa) and mobile forms of the predatory mites (i.e., all the developmental stages except eggs) were counted in situ on 3 leaflets per cage from the top, medium, and bottom strata, chosen at random, and the three values were summed.

*Macrolophus pygmaeus/Bemisia tabaci*: All the plants were infested with 40 and 10 females *B. tabaci* on week 0 and 1, respectively. At week 1, half of the cages/tomato genotype received 5 females of *M. pygmaeus* per plant (Sanchez et al. 2018). The other half received no predator. Countings of whiteflies juveniles and of nymphs and adults of *M. pygmaeus* were done in situ, as above, in three-leaflets from the top, medium, and bottom strata, and the three values were summed.

*Orius laevigatus / Frankliniella occidentalis*: All the plants were infested with 50 and 20 females *F. occidentalis* on week 0 and 1, respectively. At week 1, half of the cages/tomato genotype received 5 females of *O. laevigatus* per plant (Weintraub et al. 2011). The other half received no predator. To stimulate *Orius* females to remain on the plant, we initially enclosed the predatory bugs inside clip-on cages clipped on a leaflet, and we provided eggs of *Ephestia kuehniella* as food to force females to oviposit on the plant (as in Pallipparambil et al. 2015). Clip-ons were removed after 1 week, and thus, samplings were done from week 3 to week 10. The number of mobile stages of thrips (1st and 2nd larva and adults) and predators (all stages but eggs) was done in situ on 3 leaflets per cage from the top, medium, and bottom strata, chosen at random, and the three values were summed.

*Typhlodromus (A.) recki/Bemisia tabaci* or *Frankliniella occidentalis*: In this experiment, the initial conditions of predatory mites and whiteflies, and of thrips, were the same as those used in the experiments above. As in the previous experiments, there were two releases of prey at weeks 0 and 1, at week one 15 predator females were released in the half of the cages, and similar counting as above was done weekly from week 2 on.

As proxy for effects of constitutive defenses (i.e., glandular trichomes), at the end of all the experiments we counted the number of *A. swirskii*, *M. pygmaeus*, *O. laevigatus*, or *T. (A. recki*) entrapped on glandular hairs present in 6 petioles of leaves chosen at random, under the binocular magnifier (×10) in the laboratory. The total number of individuals entrapped per replica was used as dependent variable.

## Statistical analyses

All statistical analyses were performed using the computer environment R (R Core Team 2023). To increase the power to detect differences in predator and prey densities between tomato genotypes, we used the cumulative number of either predators or prey in the last counting of the experiment as the dependent variable. Analyses were done applying Generalized Linear Models (package glm2) using log-link functions and Poisson distribution of errors or using quasi-Poisson correction when overdispersion of data was detected.
<figure><img src="image_5.png" /><figcaption>**Fig. 1** Cumulative number (a) and number/ week (b) of *B. tabaci* juveniles, i.e., all the immature feeding stages (2nd and 3rd larval stage and pupa) (average number ± S.E., N=4), on two types of tomato plants [var. Castlemart (black dots) or *def-1* (white dots)], in the presence (solid line) or absence (dashed line) of the predatory</figcaption></figure>

mite *A. swirskii*. Cumulative number (c) and number/week (d) of mobile stages (that is, all the developmental stages but eggs) of *A. swirskii* on tomato plants var Castlemart (black dots) or *def-1* (white dots) infested by *B. tabaci*

Data of species abundance were analyzed for each predator–prey system separately:

*A. swirskii/B. tabaci* and *M. pygmaeus/B. tabaci*: The cumulative number of juvenile whiteflies at week 9 was analyzed using GLM, with “tomato genotype” (2 levels: CM and *def-1*) and “predator” (2 levels, Yes and No) as categorical variables. The cumulative number of predators was analyzed using only treatments where the predator was present, with “tomato genotype” as categorical variable.

*O. laevigatus/F. occidentalis*: The cumulative number of mobile stages (adults and juveniles) of *F. occidentalis* at week 10 was analyzed using GLM with “tomato genotype” (2 levels: CM and *def-1*) and “predator” (2 levels: Yes and No) as categorical variables. The cumulative number of mobile stages of *O. laevigatus* at week 10 was analyzed including only treatments with the predator present, as in above.

*T. (A). recki/B. tabaci* or *F. occidentalis*: The cumulative number of either juvenile *B. tabaci* or mobile stages of *F. occidentalis* at week 9 were analyzed separately using GLM, with “tomato genotype” (2 levels: CM and *def-1*) and “predator” (2 levels: Yes and No) as categorical variables. The cumulative number of predators at week 9 was analyzed including only treatments with the predator present, as in above.

The number of predators entrapped on glandular trichomes was analyzed using GLM with “tomato genotype” (2 levels: CM and *def-1*) and “predator” (4 levels: *A. swirskii*, *O. laevigatus*, *T. (A). recki_BT* and *T. (A). recki_FO*) as categorical variables. *Macrolophus pygmaeus* was not included in this analysis because no predators were found trapped on glandular hairs.

Post hoc were done applying Tukey HSD tests, when applicable.

## Results

*Amblyseius swirskii/Bemisia tabaci:* Neither plant genotype nor the presence of predators had an impact on the abundance of whiteflies (Table 1a, Fig. 1a, b). Indeed, there were little or no differences on the abundance of whiteflies between the two tomato genotypes. Similarly, tomato genotype had no influence on the abundance of predatory mites (LR χ²= 0.014, df = 1, P = 0.905). Indeed, both the cumulative number (Fig. 1c) and the number through time (Fig. 1d) of predatory mites were very low throughout the experiment.

*Macrolophus pygmaeus/Bemisia tabaci:* The control of whitefly populations exerted by *M. pygmaeus* was outstanding and independent of plant genotype (Table 1b). The
<figure><img src="image_6.png" /><figcaption>**Fig. 2** Cumulative number (a) and number/week (b) of *B. tabaci* juveniles, i.e., all the immature feeding stages (2nd and 3rd larval stage and pupa (average number ± S.E., N=4), on two types of tomato plants [var. Castlemart (black dots) or *def-1* (white dots)], in the presence (solid line) or absence (dashed line) of the predatory</figcaption></figure>

bug *M. pygmaeus*. Cumulative number (c) and number/week (d) of mobile stages, i.e., nymphs and adults, of *M. pygmaeus* on tomato plants var Castlemart (black dots) or *def-1* (white dots) infested by *B. tabaci*

cumulative number of juveniles *B. tabaci* infecting tomato plants was twice higher in the absence than in the presence of predators (Fig. 2a), and predators controlled the abundance of whiteflies through time (Fig. 2b). As in the previous treatment, the abundance of predatory insects was independent of the tomato genotype (LR $\chi^2$=0.602, df=1, *P*=0.438, Fig. 2b).

*Orius laevigatus/Frankliniella occidentalis:* The overall abundance of thrips was higher in the *def-1* than in the Castlemart genotypes (Table 1c), indicating that jasmonate-mediated defenses affected the abundance of *F. occidentalis* (Fig. 3a, b). The number and cumulative number of *O. laevigatus* were also different between tomato genotypes (LR $\chi^2$=4.327, df=1, *P*=0.037, Fig. 3c,d), probably caused by a higher numerical response of the predator due to a higher density of thrips on *def-1* (Fig. 3b), given that entrapment of predators was similar on both tomato genotypes (Table 1f, interaction Tomato genotype*predator). Yet, within tomato genotype the abundance of thrips was independent of the presence of the predators (Table 1c, interaction Tomato genotype * predator).

*Typhlodromus* (A.) *recki/Bemisia tabaci*: The cumulative number and the number/week of juvenile *B. tabaci* did not differ between genotypes, neither in the presence

or absence of predators (Table 1d, Fig. 4a, b). This might indicate that the foraging efficiency of this species on tomato plants is insufficient to control *B. tabaci* populations. The abundance of predators was not affected by tomato genotype (LR $\chi^2$=0.298, df=1, *P*=0.585, Fig. 4c, d).

*Typhlodromus* (A.) *recki* / *Frankliniella occidentalis*: The cumulative number and the number/week of thrips depended on tomato genotype, being higher on *def-1* than on Castlemart (Table 1e, Fig. 5a, b). The abundance of predators was not different between tomato genotypes (LR $\chi^2$=0.435, df=1, *P*=0.510, Fig. 5c, d). Like *O. laevigatus*, the interaction between tomato genotype and presence of predators was not significant (Table 1e, Fig. 5).

*Entrapment of predators on glandular trichomes:* As indicated before, *M. pygmaeus* was not included in the analysis because we did not find any individual entrapped on glandular trichomes. Entrapment did not differ between tomato genotypes, but it differed among species of predators (Table 1f). Indeed, the entrapment of predatory mites was much higher than that of the predatory insects (Fig. 6).

<figure><img src="image_7.png" /></figure>
<figure><img src="image_8.png" /><figcaption>**Fig. 3** Cumulative number (a) and number/week (b) of mobile stages, i.e., 1st and 2nd larva and adults, of *F. occidentalis* (average number ± S.E., N=4) on two types of tomato plants [var. Castlemart (black dots) or *def*-1 (white dots)], in the presence (solid line) or</figcaption></figure>

absence (dashed line) of the predatory bug *O. laevigatus*. Cumulative number (c) and number/week (d) of mobile stages, i.e., nymphs and adults, of *O. laevigatus* on tomato plants var Castlemart (black dots) or *def*-1 (white dots) infested by *F. occidentalis*

# Discussion

## Effects of JA-mediated defenses on herbivore pests

Jasmonic acid (JA) is a key elicitor of plant defenses against herbivores that mediates the expression of both direct and indirect defenses (Ament et al. 2004; Thaler et al. 2012), especially when the feeding mode of the herbivore is chewing (e.g., lepidopteran larvae) or pierce-and-sucking (e.g., thrips) (Stroud et al. 2022). For example, in *Arabidopsis thaliana* several JA defense markers are upregulated in response to the attack by the thrips *F. occidentalis* (De Vos et al. 2005). In tomato plants, JA rapidly accumulates in tissues nearby the site of herbivore attack. This accumulation triggers the synthesis and concentration of various proteins and metabolites that impair the performance of herbivorous arthropods. Examples of these defensive mechanisms include proteinase inhibitors, that interfere with digestion processes (Kant et al. 2004; Chen et al. 2005); amino acid-degrading proteins like the Threonine Deaminase 2 (Gonzales-Vigil et al. 2011); and polyphenol oxidases which, via the oxidation of dihydroxy phenolic compounds, modify essential nutrients and digestive enzymes through alkylation

reactions (Constabel et al. 1996; Constabel and Barbehenn 2008). Additionally, some secondary metabolites are also involved in defense. For example, isoprenoids are known to be repellents against whiteflies (Bleeker et al. 2012) and some alkaloids, such as physostigmine, reduce the likelihood of survival in *Spodoptera exigua* (Lepidoptera: Noctuidae) (Rivero et al. 2021). Our experiments confirmed that the activation of the JA signaling pathway has a negative effect on the population of the herbivorous thrips *F. occidentalis*. Indeed, in the treatments without predators the population of *F. occidentalis* reached higher levels on the tomato genotype that is unable to accumulate jasmonic acid.

Some herbivores, however, have evolved mechanisms to suppress induced plant defenses. For example, the attack of Colorado potato beetles *Leptinotarsa decemlineata* (Say) (Coleoptera: Chrysomelidae) and the tetranychid mite *T. evansi* suppress the transcription of genes that encode for proteinase inhibitors involved in plant defense in potato (Lawrence et al. 2008) and tomato (Sarmento et al. 2011), respectively. In the system studied here, *B. tabaci* is known to down-regulate JA-regulated defenses (van de Ven et al. 2000; Kempema et al. 2007; Zarate et al. 2007) and to
<figure><img src="image_9.png" /><figcaption>**Fig. 4** Cumulative number (**a**) and number/week (**b**) of *B. tabaci* juveniles, i.e., all the immature sessile stages (2nd and 3rd larval stage and pupa) (average number ± S.E., N=4) on two types of tomato plants [var. Castlemart (black dots) or *def*-1 (white dots)], in the presence (solid line) or absence (dashed line) of the predatory</figcaption></figure>

mite *T. (A). recki*. Cumulative number (**c**) and number/week (**d**) of mobile stages, i.e., all the developmental stages but eggs, of *T. (A). recki* on tomato plants var Castlemart (black dots) or *def*-1 (white dots) infested by *B. tabaci*

suppress the expression of JA-dependent genes in Lima bean and tomato (Kant et al. 2004; Zhang et al. 2009; Alba et al. 2015; Su et al. 2015, 2018). We expected to confirm this at the population level, and, indeed, we found no differences in *B. tabaci* abundances between the two genotypes tested here.

## Effects of JA-mediated defenses on predators

On the one hand, if induced defenses had an effect on the well-performance of predators as biological control agents, the negative impact of the presence of predators on the abundance of *F. occidentalis* (the pest species that induces the activation of the JA signaling pathway in tomato plants) should have been stronger on *def*-1, the mutant that does not accumulate JA, than on CM plants. This effect, even if small, should have been detected in the interaction term between tomato genotype and presence of predators, but this was not the case. On the other hand, if induced defenses do not affect the foraging efficiency of predators, the effect of the presence of predators on the abundance of *F. occidentalis* populations should be similar in both tomato genotypes. The results with the two predators that interacted with *F. occidentalis* were similar: The abundance of thrips through time

was influenced by plant genotype but not by the presence of predators (Table 1c and 1e), indicating that the lack of pest control was independent of the production of JA; thus, defenses other than JA affected the efficiency as predators. *Orius laevigatus* is a well-known and much used biological control agent against thrips. On tomato crops, however, *Orius* species fail to establish (Zoreh et al. 2016) and are therefore not released in these crops. In our experiments, we forced artificially the establishment of this species by imposing females to oviposit on tomato plants at the beginning of the experiment. We found *O. laevigatus* on the plants throughout the experiment, but always at low numbers. Yet, the abundance was higher on *def*-1 than on CM (Fig. 3c, d). This was likely caused by the higher abundance of thrips on the genotype unable to activate plant defenses (Fig. 3a, b).

A similar pattern was found with the other predator species tested here against thrips. *Typhlodromus (A.) recki* is a generalist species known to feed on soft bodied arthropod herbivores and on pollen. For example, it preys on all the stages of tetranychid (Ersin et al. 2021) and eriophyid (Tixier et al. 2020a) mites. *Typhlodromus (A.) recki* is one of the most commonly found predatory mite in some areas of Europe and the Middle East on Solanaceae plants, where

<figure><img src="image_10.png" /></figure>
<figure><img src="image_11.png" /><figcaption>**Fig. 5** Cumulative number (a) and number/week (b) of mobile stages, i.e., all the immature feeding stages (2nd and 3rd larval stage and pupa), of *F. occidentalis* (average number ± S.E., N=4) on two types of tomato plants [var. Castlemart (black dots) or def-1 (white dots)], in the presence (solid line) or absence (dashed line) of the predatory</figcaption></figure>

mite *T.recki*. Cumulative number (c) and number/week (d) of mobile stages, i.e., all the developmental stages but eggs, of *T. (A. recki* on tomato plants var Castlemart (black dots) or def-1 (white dots) infested by *F. occidentalis*

it inhabits both non-cultivated and cultivated plant species, including tomato (Tixier et al. 2020b). In our setup,

<figure><img src="image_12.png" /><figcaption>**Fig. 6** Number of *A. swirskii*, *T. (A. recki* and *O. laevigatus* entrapped on glandular hairs present in 6 petioles of leaves chosen at random (N=8), at the end of the experiments. Letters indicate significant differences after Tukey HSD post hoc tests. *Macrolophus pygmaeus* was not included in the analysis because no predators were found trapped on glandular hairs</figcaption></figure>

the species persisted on tomato plants throughout the whole experiment, and with the two types of herbivores, indicating that *T. (A. recki)* foraged on both prey types. Again, its performance against thrips and whiteflies was independent of the tomato genotype, suggesting that plant defenses other than induced might have negatively influenced pest control.

Our results, thus, suggest that induced defenses mediated by JA might not have a significant effect on the abundance of predators. Short-time experiments developed by Ataide et al. (2016) showed that the oviposition rate of the mite *Phytoseiulus longipes* (Acari: Phytoseiidae), a specialist spider-mite predator, was not affected by JA defenses despite that predation rates were found to be higher on plants with weak JA defenses. Whether this effect scales up at the population level is not yet known, however, but it should be assessed to confirm potential negative effects on pest control. Furthermore, it is known that some zoophytophagous BCAs can also induce JA-mediated defenses in plants, although such induction is thought to be highly species specific (see review by Pérez-Hedo et al. 2022). To the best of our knowledge, *A. swirskii* does not puncture the plant, as shown by Nomikou et al. (2003), while it remains unknown whether this is the case for *T. (A.) reckii*. However, *O. laevigatus* and
*M. pygmaeus* were shown to induce plant defenses via the JA pathway (De Puysséleyr et al. 2011; Pérez-Hedo et al. 2015; Bouagga et al. 2018; Zhang et al. 2018). In this case, zoophytophagous predators may enhance the defensive response of the wild tomato genotype (i.e., Castlemart). A beneficial direct effect of the tomato mutant *def-1* on zoophytophagous predators cannot be ruled out in our experiments. For example, *O. laevigatus* reached higher densities on *def-1*, and although we mainly attributed this effect to a higher density of prey, this genotype may also be of higher quality for the predators. This important aspect should be included in further investigations if we are to disentangle overall effects of JA-mediated defenses on the well-functioning of BCAs at controlling pests.

Although we did not specifically address the effects of constitutive defenses on the abundance of predators, we did measure, at the end of the experiments, a proxy for entrapment of predators on glandular hairs. This way we also accounted for the formation of new glandular trichomes mediated by JA (Li et al. 2004), the effect of which would have been detected in the interaction term between tomato genotype and predator. For example, if the accumulation of JA would have induced the formation of more glandular trichomes, entrapment would have been higher in predator species that interacted with thrips (i.e., *O. laevigatus* and *T. recki-F.occidentalis*), and only on Castlemart plants, which was not the case (Table 1f). Indeed, we found high levels of entrapment in all predators except *M. pygmaeus* and in the two genotypes, (Table 1f, Fig. 6). Such level of entrapment likely explains the lack of control of herbivore populations exerted by the two species of predatory mites and *O. laevigatus*, which agrees with findings from other authors, for example, Paspati et al. (2021) and Legarrea et al. (2022) for predatory mites, and Salehi et al. (2016) for another species of *Orius*.

In conclusion, our results support that tomato JA-mediated defenses did not have a significant impact on the abundance of predators. Instead, constitutive defenses in the form of glandular trichomes probably hindered the establishment of three of the predator species tested here and were the cause of their lack of success at controlling herbivore abundance. Furthermore, our results provide experimental support for the relevant role of JA-mediated defenses in limiting the population growth of herbivores (Bleeker et al. 2009), as well as the importance for herbivores to acquire the ability to block the JA synthesis to increase plant quality to herbivores (Kant et al. 2004; Bosch et al. 2014; Alba et al. 2015).

## Author contributions

M.M. and M.R. conceived and designed research. M.B. conducted experiments. M.M. and M.R. analyzed data. M.M., M.R., JMA and M.B. wrote the manuscript. All authors read, commented, and approved the manuscript.

**Acknowledgements** The authors of this work were supported by funds from the European Union's Horizon 2020 research and innovation program under grant agreement No 773902 —"SuperPests"; and from the Spanish "Agencia Estatal de Investigación", Project "SPILL-ISLAND", grant reference PID2019-103863RB-I00. We thank three anonymous reviewers for their suggestions which contributed significantly to improve our manuscript.

**Data availability** I hereby declare that all the experimental data will be available and uploaded in a repository, if the ms is accepted.

## Declarations

**Conflict of interest** The authors declare no competing interests.

**Open Access** This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/.

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