Bioinoculants do not alter the foraging behavior of a predatory mite on soybean plants infested by Tetranychus urticae (Acari: Tetranychidae)

Bioinoculantes não alteram o comportamento de forrageamento de um ácaro predador em plantas de soja infestadas por Tetranychus urticae (Acari: Tetranychidae)

Abstract

Microorganisms and arthropods can interact indirectly through plant-mediated volatile communication. Different microorganisms compose agricultural bioinoculants and are widely used to optimize plant nutrition and physiological performance. However, the effects of inoculation on plant defense mechanisms are not fully understood, as plant responses vary according to the crop species, herbivore, and nutritional status. This study aimed to evaluate whether bioinoculated soybean plants affect the foraging behavior of the predatory mite Neoseiulus californicus. Plants were bioinoculated with BRM 119 (Bacillus megaterium) + BRM 2084 (Bacillus subtilis); BRM 119 (Bacillus megaterium) + BRM 2084 (Bacillus subtilis) + Bradyrhizobium; Azospirillum; Azospirillum + BRM 119 (Bacillus megaterium) + BRM 2084 (Bacillus subtilis); a non-inoculated control treatment supplemented with 0.37 g of NPK; and a control treatment supplemented with 0.75 g of NPK (10:10:10). For the foraging assays with N. californicus, a Y-tube olfactometer was used. The results indicate that bioinoculation in soybean does not alter the foraging behavior of the predator toward plants infested by its prey, Tetranychus urticae, suggesting that the use of bioinoculants does not interfere with the potential efficiency of biological control exerted by this natural enemy.

Keywords:
tritrophic interactions; biological control; plant growth-promoting microorganisms

Resumo

Microorganismos e artrópodes podem interagir indiretamente, por meio de comunicação mediada por voláteis de plantas. Diferentes microrganismos compõem bioinoculantes agrícolas e são amplamente empregados com o objetivo de otimizar a nutrição e o desempenho fisiológico das plantas. Contudo, o efeito de inoculações sobre os mecanismos de defesa em plantas, não é totalmente esclarecido. As respostas das plantas variam em função da cultura, do herbivoro e do estado nutricional. Nosso objetivo foi avaliar se plantas de soja bioinoculadas afetam o forrageamento do ácaro predador, Neoseiulus californicus. As plantas foram bioinoculadas com BRM 119 (Bacillus megaterium) + BRM 2084 (Bacillus subtilis); BRM 119 (Bacillus megaterium) + BRM 2084 (Bacillus subtilis) + Bradyrhizobium; Azospirillum; Azospirillum + BRM 119 (Bacillus megaterium) + BRM 2084 (Bacillus subtilis); tratamento controle sem bioinoculação + 0,37 gramas de NPK e tratamento controle + 0,75 gramas de NPK (10:10:10). Para os testes de forrageamento com N. californicus, utilizou-se um olfatômetro em “Y. Os resultados mostram que a bioinoculação em soja não modifica o comportamento de busca do predador N. californicus por plantas infestadas por sua presa, Tetranychus urticae, sugerindo que o uso de bioinoculantes não interfere na eficiência potencial do controle biológico exercido por esse inimigo natural.

Palavras-chave:
interações tritróficas; controle biológico; microrganismos promotores de crescimento

1. Introduction

The two-spotted spider mite, Tetranychus urticae Koch (Acari: Tetranychidae), stands out as one of the most economically important pests in several crops, and its management has traditionally relied on the application of synthetic acaricides (Reichert et al., 2024). However, the adverse effects of these products and the rapid selection of resistant populations have driven the adoption of alternative strategies, such as biological control through the release of predatory mites, including Phytoseiulus macropilis (Bank) (Acari: Phytoseiidae) and Neoseiulus californicus (McGregor, 1954) (Acari: Phytoseiidae) (Marafeli et al., 2014; Reichert et al., 2017), which have demonstrated effectiveness in controlling T. urticae (Oliveira et al., 2007; Montazersaheb et al., 2023).

Additionally, mite communities are influenced by environmental conditions and management practices in crops such as soybean (Ribeiro et al., 2023; Reichert et al., 2024; Fernandes et al., 2025). These practices include the use of microorganisms, particularly plant growth-promoting bacteria (PGPB), which have the ability to stimulate plant growth and defense systems against pathogens and herbivores by enhancing nutrient availability, nutrient uptake, and hormone biosynthesis (Pineda et al., 2020), highlighting the indirect interactions between microorganisms and arthropods mediated by plants (Stout et al., 2006; Khaitov et al., 2015).

The interaction between rhizobacterias and plants is triggered by the recognition of microbe-associated molecular patterns (MAMPs) by root cells, which activates signaling pathways associated with induced systemic resistance (ISR). This process begins in the roots and is systemically transmitted to aerial tissues, promoting the activation of hormonal pathways, especially those mediated by salicylic acid (SA) and jasmonic acid (JA). As a consequence, gene expression related to the synthesis of defense proteins, enzymes, and secondary metabolites is regulated, including alkaloids, phenolic compounds, non-volatile terpenes, and volatile organic compounds (VOCs), which play a key role in plant responses to biotic stress (Disi et al., 2018; Espadas-Pinacho et al., 2021).

Among the groups of rhizobacterias studied for their synergistic interactions with plants, the genus Bacillus stands out due to its multifunctional capacity to produce siderophores, which contribute to phosphate solubilization and promote plant development (Timofeeva et al., 2023). This group of bacteria has been used in microbial consortia with other bacterias, such as Azospirillum (Ribeiro et al., 2022) and Bradyrhizobium (Prando et al., 2020), to enhance plant growth and increase crop yields in maize and soybean (Abreu et al., 2017; Hungria et al., 2001).

Some PGPB enhance plant defense mechanisms against phytopathogens and herbivorous insects through induced systemic resistance (ISR) (Yu et al., 2022). In addition, these bacteria may increase the foraging efficiency of natural enemies due to the emission of volatile organic compounds (VOCs), which contribute to reducing herbivore pressure (Disi et al., 2018).

Epiphytic bacterias can affect the composition of volatile compounds released by plants and, consequently, the behavior of other organisms associated with the plant, such as herbivores and/or pathogens (Karamanoli et al., 2020). However, although the use of such microorganisms is beneficial to plants, their combined effects and relative contributions regarding host plant selection and the attraction of associated natural enemies remain poorly understood.

Therefore, this study aimed to evaluate whether the inoculation of soybean plants with the bioinoculants BRM 119 (Bacillus megaterium) and BRM 2084 (Bacillus subtilis), as well as Bradyrhizobium and Azospirillum, applied individually or in combination, influences plant-induced indirect defenses, particularly in relation to the foraging behavior of the predatory mite Neoseiulus californicus.

2. Materials and Methods

2.1. Plants

Jack bean plants (Canavalia ensiformis (L.)) were grown from seeds in plastic pots (6.3 L) filled with commercial substrate (Terral Solo®) and maintained in aphid-proof screen cages in a greenhouse (25 ± 5 °C, 70 ± 20% relative humidity). Plants were watered daily and replaced whenever necessary.

For the experiment, three soybean seeds (Glycine max (L.) Merrill, cv. BRS Valiosa) were sown in 1.0 L plastic pots containing soil collected from Embrapa Maize and Sorghum [pH (H₂O) 6.1; OM (g kg⁻¹) 19; P Mehlich (g kg⁻¹) 7; K Mehlich (mmolc kg⁻¹) 2.4; Ca (mmolc kg⁻¹) 24; Mg (mmolc kg⁻¹) 11; Al (mmolc kg⁻¹) 0; H+Al (mmolc kg⁻¹) 23; sum of bases (mmolc kg⁻¹) 37; CEC (mmolc kg⁻¹) 60; base saturation (%) 62; Al saturation (%) 0], and maintained inside aphid-proof screen cages in a greenhouse. A single commercial soybean cultivar (BRS 7780 IPRO) was used throughout all experiments to minimize variation associated with plant genotype. Therefore, the differences observed in the foraging behavior of N. californicus can be attributed to the experimental treatments, ensuring the reproducibility of the results under the conditions evaluated.

2.2. Rearing of the two-spotted spider mite and acquisition of the predatory mite

The population of the two-spotted spider mite, T. urticae, was established from individuals collected on sorghum plants (Sorghum bicolor). After initial collection, the mites were transferred to untreated jack bean leaves (C. ensiformis). The leaves were placed on water-soaked foam inside plastic trays, with the abaxial surface facing upward, and surrounded by moistened cotton to prevent mite escape.

Throughout the experimental period, jack bean leaves were used to maintain colonies of T. urticae in a climate-controlled chamber (BOD type) at 25 ± 1 °C, relative humidity of 70 ± 10%, and a 12 h photophase.

The predatory mite N. californicus used in the olfactometry assays was obtained from the company Koppert under the commercial name SPICAL®. Only active, healthy-looking adult females exhibiting normal locomotion were used in the olfactometry assays, whereas individuals showing reduced mobility or abnormal behavior were discarded.

2.3. Soybean plant inoculation

A total of 24 soybean plants were used, distributed across six treatments, with four replicates each. The treatments consisted of: control plants receiving only NPK fertilizer (10:10:10) applied at a rate of 0.375 g at sowing, supplemented with 1 mL of a micronutrient solution containing iron, manganese, zinc, copper, molybdenum, and boron; the remaining treatments, except for the positive phosphorus control, received the same fertilization with NPK (10:10:10) and the micronutrient solution.

The bacterial strains used were BRM 119 (B. megaterium) and BRM 2084 (B. subtilis), both with phosphate-solubilizing capacity, isolated from different edaphoclimatic conditions in agricultural areas of Brazil (Abreu et al., 2017; Oliveira-Paiva et al., 2021).

The bacterial treatment consisted of inoculating these strains at a rate equivalent to 100 mL ha⁻¹, using a 1 mL aliquot of the suspension applied directly onto the seeds at sowing. In another treatment, the same bacterial strains were applied under the same conditions, combined with co-inoculation with Bradyrhizobium, aiming to simulate conditions closer to those found in the field. Additionally, a treatment with Azospirillum inoculation (10⁹ colony-forming units – CFU) was conducted, as well as a treatment with co-inoculation of Azospirillum and the strains BRM 119 (B. megaterium) and BRM 2084 (B. subtilis).

Furthermore, a treatment with mineral fertilization was established, in which the equivalent of 0.75 of the recommended dose of NPK (10:10:10) per pot was applied. After seedling emergence, thinning was performed, maintaining one plant per pot. Irrigation and other cultural practices were carried out as needed.

2.4. Preference of Neoseiulus californicus in a Y-tube olfactometer

Infestations with the two-spotted spider mite T. urticae were established using 100 adult females, 24 hours prior to the experiment (Rocha et al., 2021, 2023). Plants were then transferred to a Y-tube olfactometer (Sabelis and van de Baan, 1983), consisting of arms 21.0 cm in length and 3.5 cm in diameter.

Treatments were arranged at the distal ends of the olfactometer as follows: (i) air vs. air; (ii) clean control plants vs. air; (iii) clean plants inoculated with B. megaterium (BRM 119) + B. subtilis (BRM 2084) vs. inoculated plants infested with T. urticae; (iv) clean plants inoculated with Azospirillum vs. inoculated plants infested with T. urticae; (v) clean plants inoculated with B. megaterium (BRM 119) + B. subtilis (BRM 2084) + Bradyrhizobium vs. inoculated plants infested with T. urticae; and (vi) clean plants inoculated with B. megaterium (BRM 119) + B. subtilis (BRM 2084) + Azospirillum vs. inoculated plants infested with T. urticae.

All treatment combinations were tested with three replicates, each consisting of a set of plants and 20 valid responses from predatory mites. Individuals of N. californicus were introduced individually into the olfactometer, and each female was allowed to choose between the two arms. A choice was recorded when the mite reached approximately one-third of the length of one arm within a maximum period of 5 minutes. Females that did not make a choice within this period were recorded as non-responders.

After each choice, or after a maximum observation period of 5 min, the mite was removed and replaced by a new individual (Janssen, 1999). Following each release, the Y-tube olfactometer was completely disassembled and thoroughly washed with running water and neutral soap to eliminate any residual chemical cues. The apparatus was then rinsed with running water, allowed to air dry completely, and reassembled before the next replicate. In addition, the positions of the odor sources were alternated after every five responses to avoid positional bias. Individuals that left the pathway or were lost from the observer’s view were excluded from the analysis.

3. Statistical Analyses

The assays were conducted in a completely randomized design. In each replicate, 20 valid responses of predatory mites to the different odor sources were considered. Proportion data were analyzed using the chi-square test at a 5% significance level. Statistical analyses were performed using the software R (Crawley, 2013; R Core Team, 2014).

4. Results

The predatory mite N. californicus showed no preference between air vs. air or between clean plants vs. air, as expected, indicating the absence of positional bias toward any specific arm of the olfactometer (Figure 11B).

Figure 1
Choice responses of adult females of the predatory mite Neoseiulus californicus in Y-tube olfactometer assays. Predators were first offered a choice between air and air (A) to verify the absence of positional bias in the olfactometer, and subsequently between air and uninfested, non-inoculated soybean plants (B) to evaluate the response to clean host plants. Bars represent the proportion of responding females choosing each odor source. Values within the bars indicate the number of responding mites selecting each treatment, whereas NR represents the number of mites that did not make a choice within 5 min.

However, a preference of the predatory mite N. californicus was observed for plants infested by T. urticae and inoculated with Azospirillum, as well as for infested plants inoculated with BRM 119 (B.megaterium) and BRM 2084 (B. subtilis), compared to clean plants under the same treatments (Figure 22B).

Figure 2
Choice responses of adult females of the predatory mite Neoseiulus californicus in Y-tube olfactometer assays to volatiles emitted by soybean plants inoculated with Azospirillum (A) or BRM 119 (Bacillus megaterium) + BRM 2084 (Bacillus subtilis) (B). For each treatment, predators were offered a choice between uninfested soybean plants and Tetranychus urticae-infested soybean plants subjected to the same inoculation regime. Bars represent the proportion of responding females choosing each odor source. Values within the bars indicate the number of responding mites selecting each treatment, whereas NR represents the number of mites that did not make a choice within 5 min.

There was also a significant preference of the predator for T. urticae-infested plants inoculated with BRM 119 (B. megaterium) + BRM 2084 (B. subtilis) + Bradyrhizobium (Figure 3A), and for infested plants inoculated with BRM 119 (B. megaterium) and BRM 2084 (B. subtilis) combined with Azospirillum (Figure 3B), compared to uninfested plants.

Figure 3
Preference of adult females of the predatory mite Neoseiulus californicus in Y-tube olfactometer assays for soybean plants inoculated with BRM 119 (Bacillus megaterium) + BRM 2084 (Bacillus subtilis) combined with Bradyrhizobium (A) or Azospirillum (B). In each comparison, predatory mites were offered a choice between clean (uninfested) soybean plants and plants infested with Tetranychus urticae under the same inoculation treatment. Bars represent the proportion of mites choosing each odor source. Numbers inside the bars indicate the number of responding mites selecting each treatment, whereas NR indicates the number of non-responding mites that made no choice within 5 min.

5. Discussion

Regarding the effects of microorganisms on the third trophic level, the results of the present study indicate that plant growth–promoting bacteria (PGPB) do not interfere with the ability of the predator N. californicus to locate plants infested by the two-spotted spider mite in soybean (Figures 22B; Figures 33B). This suggests that the primary factor determining the attraction of these mites is the presence of the herbivore on the host plant, rather than microbial inoculation.

In contrast, inoculation with Bacillus pumilus INR7 and Bacillus velezensis Fol (Bacillales: Bacillaceae) has been shown to increase the foraging efficiency of P. persimilis, enhancing its predation rate on T. urticae eggs (Montazersaheb et al., 2023). According to these authors, this effect is associated with increased emission of volatile organic compounds capable of modulating predator behavior.

In a previous study, our group demonstrated that soybean plants infested with T. urticae produce volatile compounds that attract the predatory mite N. californicus, and that this attraction is not affected by the presence of another herbivore, the soybean looper Anticarsia gemmatalis (Lepidoptera: Noctuidae) (Rocha et al., 2023). Thus, inoculation of plants with PGPB does not interfere with the trophic interactions evaluated in the present study.

Interestingly, studies have shown that when T. urticae individuals treated and untreated with Beauveria bassiana (Hipocreales: Clavicipitaceae) are simultaneously available, P. persimilis preferentially consumes untreated prey compared to infected individuals after 72 hours of exposure. This behavior indicates the predator’s ability to discriminate infected prey, possibly due to changes in nutritional quality resulting from fungal infection (Seiedy 2014).

Such evidence suggests that fungal biocontrol agents may negatively affect prey quality and, consequently, predation rates, without compromising the compatibility between entomopathogenic fungi and predatory mites within integrated pest management (IPM) systems. In this context, the observed selectivity reinforces the potential for combined use of these agents. Furthermore, depending on infestation conditions, different predator species may exhibit distinct performance in controlling T. urticae, with P. macropilis being more efficient at low population densities and N. californicus showing greater efficacy at moderate densities (Siebert et al., 2025).

Additionally, the presence of PGPB may modulate plant hormonal pathways, such as jasmonic acid and salicylic acid, which are essential for activating defense responses against herbivores. Experimental evidence shows that in plants infested by T. urticae and colonized by Fusarium solani (Hypocreales: Nectriaceae), there is upregulation of marker genes associated with these pathways, as well as changes in the emission profile of volatile compounds, making plants more attractive to the predator Macrolophus pygmaeus (Hemiptera: Miridae) an important natural enemy of spider mites. In this context, protective effects against mites may involve multiple mechanisms, including antibiosis, feeding deterrence, and defense priming, as well as the attraction of natural enemies (Pappas et al., 2018; Grabka et al., 2022).

In mycorrhizal plants of Citrus reshni, a species highly susceptible to T. urticae, strong mycorrhiza-induced resistance was observed, associated with activation of jasmonic acid and abscisic acid pathways, as well as the accumulation of phenolic compounds, particularly naringenin-derived flavones implicated in plant defense. This pattern was corroborated by olfactometer bioassays, in which both T. urticae and its natural enemies, P. persimilis and N. californicus, avoided infested mycorrhizal plants, indicating an antixenosis effect mediated by volatile organic compounds (Schausberger et al., 2012).

In contrast, Citrus aurantium, a naturally more resistant species, did not exhibit a systemic response to mycorrhiza-induced resistance, indicating that the effectiveness of this resistance mechanism depends on the host species and the balance between growth- and defense-related pathways (Manresa-Grao et al., 2024). These results contrast with previous studies (Aguilar-Fenollosa et al., 2012; Widemann et al., 2021; Fatma et al., 2024), in which the specialist predatory mite P. persimilis showed preference for its prey regardless of the host plant, a pattern also observed in the present study for N. californicus in soybean (Rocha et al., 2023).

In summary, the results of this study demonstrate that inoculation with PGPB does not alter the foraging behavior of N. californicus on soybean plants infested by T. urticae, with the presence of the herbivore being the main factor determining predator preference. These findings indicate that, in this specific tritrophic system, bioinoculation does not interfere with interactions among soybean plants, the phytophagous pest, and the natural enemy.

Additionally, comparison with previous studies highlights that the effects of microorganisms on the third trophic level are highly context-dependent, varying according to plant species, associated microorganisms, and the natural enemy involved. While some microorganisms can modulate volatile emissions and positively influence predator efficiency, others do not induce detectable behavioral changes, as observed in the present study.

Therefore, it can be concluded that the use of PGPB in soybean under the evaluated conditions is compatible with biological control by N. californicus, without impairing its prey-location ability, reinforcing the potential integration of these tools in the integrated management of T. urticae.

Acknowledgements

We are grateful to each person from the ‘Federal University of São João Del Rey’ (UFSJ) and ‘Embrapa Maize and Sorghum’ institutions, who contributed to the development of this project. To ‘Minas Gerais State Research Support Foundation’ (FAPEMIG) and ‘National Council for Scientific and Technological Development’ (CNPq), for partial financial support of this research.

Data Availability Statement

The data have been archived on the GITHUNB Repository at: https://github.com/marcosfadini/Bioinoculants-do-not-alter-the-foraging-behavior-of-a-predatory-mite

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Edited by

• Editor:
  Takako Matsumura Tundisi

Publication Dates

• Publication in this collection
  11 Sept 2026
• Date of issue
  2026

History

• Received
  31 Mar 2026
• Accepted
  22 July 2026