Sharma, Prajjval ¹ ; Sharma, Prem Lal² ; Verma, Subhash Chander³ ; Chandel, Rajeshwar Singh⁴ and Sharma, Shubham ⁵

¹Department of Entomology. Dr. Y S Parmar University of Horticulture and Forestry, Nauni, Solan (HP) 173230, India.
²Department of Entomology. Dr. Y S Parmar University of Horticulture and Forestry, Nauni, Solan (HP) 173230, India.
³Department of Entomology. Dr. Y S Parmar University of Horticulture and Forestry, Nauni, Solan (HP) 173230, India.
⁴Department of Entomology. Dr. Y S Parmar University of Horticulture and Forestry, Nauni, Solan (HP) 173230, India.
⁵✉ Department of Entomology. Dr. Y S Parmar University of Horticulture and Forestry, Nauni, Solan (HP) 173230, India.

2025 - Volume: 65 Issue: 1 pages: 116-129

Original research

Keywords

Abstract

Introduction

Integrated Pest Management (IPM) is an important approach that combines biological, cultural, and chemical methods to effectively manage pest populations, while reducing the sole reliance on pesticides (de Araújo et al. 2024; Wang et al. 2024). This strategy is widely implemented in economically significant crops to minimize costs and achieve sustainable pest control (Elhalawany et al. 2024b; Noorinahad et al. 2024). Tomato (Solanum lycopersicum L.) is one of the world's most important vegetable crops, both economically and nutritionally, ranking second only to potato in terms of area and production (Ouattara and Konate 2024). However, tomato cultivation faces significant threats from various pests and diseases throughout its growth cycle (Shirvani et al. 2023b; Islam et al. 2024). Among these, fungal pathogens can cause substantial crop losses if left unmanaged (Panno et al. 2021). In response, farmers often resort to chemical fungicides, which, despite advancements in more sustainable pest control approaches, remain essential for managing fungal outbreaks (Ye et al. 2020). In addition to fungal pathogens, invertebrate pests including spider mites such as Tetranychus urticae Koch (Acari: Tetranychidae) also significantly affect tomato production (Monjarás-Barrera et al. 2024). These mites feed on chlorophyll, leading to leaf defoliation and reduced plant vigor, especially in the hot, dry conditions that favor tomato production (Nag et al. 2020; Bhullar et al. 2021).

Due to extensive pesticide use for mite management, T. urticae populations have developed resistance to various acaricides (Ay et al. 2024), necessitating the application of biological control strategies. Phytoseiid mites are considered as an excellent predators of spider mites in diverse cropping environments (Shirvani et al. 2023a; Dalir et al. 2024; Wang et al. 2024; Yaşar et al. 2024). The predatory mite, Neoseiulus longispinosus (Evans) (Acari: Phytoseiidae) has shown its effectiveness in reducing T. urticae populations, feeding on all life stages of this pest (Biswas et al. 2022). This phytoseiid predator is well-known in IPM programmes for tomato and other crops (Bernard et al. 2010). However, in tomato cultivation, the extensive use of conventional fungicides such as mancozeb, metalaxyl, thiophanate methyl, and copper oxychloride raises concerns about their potential non-target effects on natural enemies like N. longispinosus.

Estimating the predatory potential of a biocontrol agent against pests is vital for understanding its effectiveness in integrated pest management (IPM) programmes (Adly 2024; Elhalawany et al. 2024a). However, the presence of toxicants, such as pesticides or fungicides, can significantly alter the predatory potential of biocontrol agents. These chemicals may impair the agents' ability to locate, capture, or consume pests, thus reducing overall efficiency (Musa et al. 2023; Havasi and Kheradmand 2024). Furthermore, sublethal doses of toxicants may also affect the predatory potential due to changes in behaviour, reproduction, or survival of the predator, potentially compromising its role in pest management. Therefore, evaluating the impact of toxicants on predatory behavior is vital to ensure the compatibility of biocontrol agents with chemical pest control practices (Stark and Banks 2003). Given these considerations, the present study investigated the influence of commonly used fungicides on the predatory potential of N. longispinosus against T. urticae on tomato plants. This study aimed to understand the compatibility of chemical and biological control methods, which is useful for optimizing IPM strategies in tomato cropping systems.

Material and methods

The present study was conducted under laboratory conditions at a temperature of 25 ± 0.5 °C, 70 ± 5% relative humidity, and a 12-hour light: 12-hour dark photoperiod. The tomato and strawberry plants used for maintaining the mass culture and conducting experiments were grown in a polyhouse at the experimental farm of the Department of Entomology, Dr. YS Parmar University of Horticulture and Forestry Solan, Himachal Pradesh, India (1275 m above mean sea level; 31.28°N, 76.94°E).

Stock cultures

Neoseiulus longispinosus and Tetranychus urticae cultures were obtained from the Biocontrol Laboratory, Department of Entomology, Dr. YS Parmar University of Horticulture and Forestry, Solan, Himachal Pradesh, India. The T. urticae colony was initially inoculated and established on tomato plants (Solanum lycopersicum L., variety: Solan Lalima) cultivated in a polyhouse. In the laboratory, T. urticae was transferred to strawberry leaves, which were placed with the abaxial side facing up on a sponge saturated with water. After 2-3 days of infestation, N. longispinosus was introduced onto the strawberry leaves. To ensure a continuous food supply for the predatory mite, the older leaves were regularly replaced with fresh T. urticae-infested ones. Before being used in experiments, the T. urticae culture was transferred to tomato leaves and maintained for one generation. Similarly, N. longispinosus was placed on T. urticae-infested tomato leaves and maintained for one generation.

Treatment of Neoseiulus longispinosus with fungicides

To determine the impact of four fungicides on the predatory potential of Neoseiulus longispinosus, the wettable powder (WP) formulations of mancozeb 75% WP (Indofil M-45®; 2500 ppm), copper oxychloride 50% WP (Blitox® 50 W; 3000 ppm), thiophanate methyl 70% WP (Roko®; 1000 ppm), and metalaxyl 4% + mancozeb 64% WP (Ridomil Gold®; 2500 ppm) were used. Tomato leaf discs (3 cm × 3 cm) from the ′Solan Lalima′ variety were treated with these fungicides at the recommended doses using a modified leaf dip technique based on the method of Helle and Overmeer (1985). Each leaf disc was immersed in the fungicide solution for 15 seconds, while control discs were dipped in distilled water. After air drying for three hours, the treated discs were placed upside down on a damp sponge within experimental trays. Concurrently, tomato plants of the same variety grown in a polyhouse were sprayed with the respective fungicides using the knapsack sprayer for the residual toxicity experiments. For each treatment and control, 600 gravid females of N. longispinosus (5 days old) were individually placed on the treated leaf discs over a water saturated sponge in plastic trays. Each treatment included two experimental setups. In the first setup, 300 gravid females were provided with T. urticae eggs ad libitum as prey, while in the second setup, 300 N. longispinosus females were provided with T. urticae protonymphs ad libitum for a 48-hour exposure period. Six plastic trays, each containing 50 tomato leaf discs, were used for each setup within a treatment. To observe the mortality of N. longispinosus females after the exposure period, the leaves were transferred using forceps onto a wet sponge placed in a Petri plate and examined under a binocular microscope. The predatory mite females that exhibited no appendage movement when touched were considered dead. A cohort of 100 N. longispinosus eggs from each experimental setup were collected from the surviving females in each treatment and control group for further experiments.

Effect of fungicides on the predatory potential of Neoseiulus longispinosus

The effects of residual toxicity of the fungicides on the predatory potential of N. longispinosus against the eggs and protonymphs of T. urticae were evaluated. To account for population variability in each treatment and control group, only one egg per alive female was collected within a 12-hour period to form a cohort of 100 predator eggs. In each treatment, these predatory mite eggs were individually transferred to fresh tomato leaf discs (3 cm × 3 cm) from the fungicide-sprayed plants using a fine brush and a binocular microscope. In addition, the other progeny from these females were simultaneously reared as a reserve culture in their respective fungicidal and control groups to obtain males for future pairing. The leaf discs were placed upside down on a water-saturated sponge inside plastic trays. Unsprayed plant leaves were used for the control group. After egg hatching, the larval, protonymph, and deutonymph stages of N. longispinosus were each provided separately with 15 eggs and 10 protonymphs of T. urticae daily for each treatment and control group. Similarly, adult males of N. longispinosus were provided daily with 20 eggs and 15 protonymphs of T. urticae in different set ups of each treatment and control group. The males that emerged from the experimental cohort were used solely to collect data on prey consumption and not for mating. Upon reaching adulthood, the females were paired with males from the reserve culture of the same fungicidal group, and these pairs were kept together until death. Each pair was provided daily with 30 T. urticae eggs and 25 protonymphs. The leaf arenas and prey were replaced with fresh ones every 24 hours to ensure a continuous and adequate food supply for the predatory mite. The presence of exuviae on the leaf disc confirmed that moulting had occurred. The number of replicates for prey consumption by N. longispinosus in each treatment and the control group varied depending on stage-specific survival (n) of the predatory mite.

Data on prey consumption by different stages of the predatory mite were recorded every 24 hours until the last adult died. The daily prey consumption by adult predator females was assessed by subtracting the mean number of prey eaten by N. longispinosus males (kept alone) from the total number of prey consumed by the male-female predator pairs. This data was used to calculate the feeding potential parameters of N. longispinosus against the eggs and protonymphs of T. urticae. In these calculations, x represents the age in days, j denotes the stage, and m indicates the number of stages. The variables l_x, s_xj , and c_xj correspond to age-specific survival, age-stage survival, and age-stage predation, respectively. The prey consumption by each stage of the predatory mite and following feeding potential parameters were analyzed using the computer program CONSUME-MSChart (Chi 2025a).

• i) Age-specific predation rate (k_x ):

\[k_x=\frac{\sum_{j=1}^m s_{x j} c_{x j} }{\sum_{j=1}^m s_{x j} }\]

• ii) Net age-specific predation rate (q_x ):

\[q_x=k_x l_x\]

• iii) Cumulative consumption (C₀ ):

\[C_0=\sum q_x=\sum l_x k_x\]

• iv) Stable predation rate (ψ):

\[\psi=\sum_{x=o}^{\infty} \sum_{j=1}^\beta a_{x j} c_{x j}\]

• v) Finite predation rate (ω):

\[\omega=\lambda \psi\]

• vi) Transformation rate (Q_p ):

\[Q_P=C_o / R_0\]

Projection of prey consumption

The prey consumption by N. longispinosus was projected over a period of 90 days using computer simulation program TIMING (Chi, 1990; Chi, 2025b) with an initial population of 10 predator eggs. The prey consumption (p) at time t was calculated as:

\[p(t)=\sum_{j=1}^m\left(\sum_{x=0}^{\infty} c_{x j} n_{x j, t}\right)\]

where, n_xj,t is the number of individuals of age x and stage j at time t.

Data analysis

Means and standard errors (SE) of stage wise prey consumption and feeding potential parameters were determined using 100,000 bootstrap replicates. Differences in daily prey consumption by different predator stages among different treatments were analysed using a one-way ANOVA, followed by Tukey's HSD test (p < 0.05) in SPSS v26.0. Feeding potential parameters were compared with the help of a paired bootstrap test based on the 95% confidence interval of difference (p < 0.05) in TWO-SEXMS Chart computer program (Chi 2025c).

Results

Prey consumption

In all fungicidal treatments, Neoseiulus longispinosus larvae did not feed on either of the tested prey stages of Tetranychus urticae. Prey consumption by the predatory mite began at the protonymph stage. On T. urticae eggs, a significant reduction from control in the pre-adult prey consumption was observed in all fungicidal treatments (F_4,339: 20.047; p < 0.001). The pre-adult consumption was lowest in the metalaxyl + mancozeb treatment (5.21 eggs) which was statistically similar with mancozeb (5.25 eggs) and copper oxychloride (5.61 eggs) treatments (Table 1). Similarly, in all fungicidal treatments, significant reductions from the control were recorded in egg consumption by adult females, adult males, and over the entire lifespan of N. longispinosus (Adult Female – F_4,191: 31.138; p < 0.001; Adult Male – F_4,143: 15.114; p < 0.001; Life-long – F_4,339: 28.473; p < 0.001). The highest egg consumption across treatments by adult females (37.50 eggs) of the predatory mite occurred in the thiophanate methyl treatment which was at par with the copper oxychloride treatment (35.00 eggs) whereas, in metalaxyl + mancozeb and mancozeb treatments, significant reductions from control was observed in the prey consumption by adult females. This trend was also observed in the total life-long consumption of T. urticae eggs by N. longispinosus, with the maximum consumption recorded in the thiophanate methyl treatment (38.53 eggs) and the minimum in the metalaxyl + mancozeb treatment (31.86 eggs). Here, the life-long consumption includes both adult male and female individuals of N. longispinosus. Egg consumption by N. longispinosus males decreased significantly compared to the control and was statistically similar across all treatments.

When fed on the protonymphs of T. urticae, N. longispinosus showed a significant reduction in prey consumption during the pre-adult period in the mancozeb treatment (F_4,311: 2.658; p = 0.033). However, prey consumption by the predatory mite throughout its lifespan, as well as by adult females and males, was significantly reduced compared to the control across all treatments (Adult Female – F_4,179: 35.944; p < 0.001; Adult Male – F_4,127: 21.843; p < 0.001; Life-long – F_4,311: 20.577; p < 0.001). Among the fungicidal treatments, prey consumption of T. urticae protonymphs by adult N. longispinosus females and males was statistically similar. However, all fungicidal treatments showed a significant reduction compared to the control (Table 2).

Feeding potential and projection of prey consumption

The feeding potential of N. longispinosus on T. urticae eggs and protonymphs was assessed using various parameters: Cumulative consumption (C₀ ), Transformation rate (Q_p ), Stable predation rate (ψ), and Finite predation rate (ω). The cumulative consumption of T. urticae eggs was highest in the thiophanate methyl treatment (C₀ = 29.64 eggs/predator), which was statistically similar to the untreated control (Table 3). The transformation rate (Q_p ) and stable predation rate (ψ) of the predatory mite in the copper oxychloride and thiophanate methyl treatments were also comparable to those of the untreated control. Among the fungicidal groups, the highest finite predation rate (ω) was observed in the thiophanate methyl treatment (ω = 0.87), which was on par with the control (ω = 0.97) and the copper oxychloride treatment (ω = 0.84). The lowest finite predation rate was recorded in the metalaxyl + mancozeb treatment (ω = 0.73), which was on par with the mancozeb treatment (ω = 0.87) (Table 3).

When fed T. urticae protonymphs, a significant reduction was observed in the stable predation rate (ψ) of N. longispinosus as compared to the control group in the metalaxyl + mancozeb treatment (ψ = 0.47) (Table 4). The cumulative consumption (C₀ ) was highest in the thiophanate methyl treatment (C₀ = 20.48), and showed no significant difference from the control (C₀ = 26.60) and copper oxychloride treatment (C₀ = 17.72). The transformation rate remained unaffected in all the fungicidal treatments. The finite predation rate (ω) was significantly reduced from the control in both the mancozeb (ω = 0.59) and metalaxyl + mancozeb (ω = 0.51) treatments (Table 4).

The age-specific predation rates of N. longispinosus on T. urticae eggs and protonymphs are presented in Figures 1 and 2, respectively. These figures illustrate the trend in the mean number of prey consumed by the predator at each age (x). Using equations (i) and (ii), we calculated the age-specific predation rate (k_x ) and the net age-specific predation rate (q_x ) of the cohort, which were then plotted by combining all stages of the predatory mite. The net age-specific predation rate accounts for cohort survival, adjusting proportionately to reveal the predator's weighted predation rate. For both prey stages of T. urticae, the peak values of q_x were lowest in the metalaxyl + mancozeb treatment due to higher mortality during the immature stages of the predatory mite.

The prey consumption of N. longispinosus on the tested stages of T. urticae was projected on a log scale using prey consumption data from the various fungicidal treatments (Figure 3). Over a simulation period of 90 days, the maximum consumption of T. urticae eggs and protonymphs by N. longispinosus followed a similar trend across the different fungicidal treatments. On the 90th day, the projected consumption on the log scale was highest in the thiophanate methyl treatment (eggs: 6.47; protonymphs: 6.07), followed by copper oxychloride (eggs: 6.33; protonymphs: 5.43), mancozeb (eggs: 4.95; protonymphs: 4.67), and metalaxyl + mancozeb (eggs: 4.19; protonymphs: 3.62).

Discussion

The use of natural enemies in agro-ecosystems is an important component of Integrated Pest Management. This practice reduces the over dependence of farmers on pesticides during the management of insect pests and diseases (Crowther et al. 2024; Yaşar et al. 2024). Predatory arthropods contribute to pest mortality and alter pest behavior; however, the factors affecting the feeding behavior of natural enemies are less understood (Kasap et al. 2023; Pakyari and Zemek 2023; Pakyari et al. 2024). Therefore, assessing the predatory potential of natural enemies is essential for understanding their role in regulating pest populations and maintaining ecological stability within predator-prey dynamics (Ferreira et al. 2023; Sun et al. 2024). This predator-prey interaction forms the basis of biological control, where natural enemies are deployed to sustainably manage pest populations (Kheradmand et al. 2024). However, in agroecosystems where chemical treatments, such as fungicides, are frequently applied, it is important to understand how these treatments may impact predator efficiency and prey dynamics (Döker et al. 2024; Sharma et al. 2024c). The presence of toxicants on crop surfaces is a major factor that influences the predatory potential and preference of natural enemies (Havasi et al. 2023; Mousavi et al. 2023). The effects of these toxicants on the developmental and reproductive biology of non-target organisms are well studied (Döker et al. 2024), but their effects on prey consumption remain largely unknown for most of the natural enemy species. Our findings indicate that exposure of Neoseiulus longispinosus to field-relevant concentrations of fungicides led to a significant reduction in feeding across all developmental stages of the predator when fed on eggs and nymphs of T. urticae. These results highlight the importance of studying the effects of plant protection chemicals on the feeding behavior of natural enemies, in addition to their biological and demographic effects.

In our study, providing eggs and protonymphs to N. longispinosus on the fungicide-sprayed tomato leaves resulted in a significant reduction in total prey consumption by adult females and males. In contrast, the immature stages of N. longispinosus exhibited inconsistent trends among different fungicidal treatments. The feeding potential parameters of N. longispinosus were lower in metalaxyl + mancozeb and mancozeb treatments, while those in the copper oxychloride and thiophanate methyl treatments, were nearly comparable to the control. Previous studies have also reported pronounced effects of mancozeb on the biological performance of phytoseiids. These effects result directly from individual feeding, as exposure to toxicants reduced food uptake, thereby altering biological parameters (Hamedi et al. 2009; Sharma et al. 2024b). In the metalaxyl + mancozeb and mancozeb treatments, the cumulative consumption (C₀ ) of the predatory mite significantly reduced on both prey stages. However, the copper oxychloride and thiophanate methyl treatments did not cause any significant changes. Cumulative consumption takes into account the survival of the population (l_x ), and high mortality during the early stages causes a reduction in cumulative feeding (Huang et al. 2018; Sharma et al. 2024e). Therefore, higher pre-adult mortality due to chemical exposure caused a reduction in the C₀ value in the treatments containing mancozeb. These results align with earlier reports, indicating, that mancozeb is toxic to various species of phytoseiids, such as Euseius victoriensis (Womersley) (Bernard et al. 2010), Amblyseius andersoni (Chant) (Ioriatti et al. 1992), and Typhlodromus pyri Scheuten (Gadino et al. 2011). The transformation rate (Q_p ) describes the number of prey consumed to produce one predator egg and provides a demographic measure of the relationship between the reproduction rate and the predation rate of a predator (Chi and Yang, 2003). In our study, the transformation rate remained unaffected across all treatments for both eggs and protonymphs of T. urticae. In contrast, the finite predation rate (ω) and stable predation rate (ψ) were significantly reduced in the metalaxyl + mancozeb and mancozeb treatments. The finite predation rate that indicates the predation capacity of the predator, taking into consideration its age-stage structure, age-stage predation rate, and finite rate (Farhadi et al. 2011). Similarly, the stable predation rate reflects the total predation capacity of a stable predator population, where its total size is unity (Yu et al. 2005). All of these feeding potential parameters are vital tools for assessing predator capacity under varying environmental conditions.

Overall, our study shows inferior prey consumption by N. longispinosus across all treatments and the control. The leaves of tomato contain trichomes that have been reported to hinder the movement of different phytoseiid species, including N. longispinosus (Sharma et al. 2024a). The glandular and secondary volatile secretions from these trichomes further exacerbate this hindrance, reducing its performance on tomato plants compared to other host plants (Tabary et al. 2024). However, studies have shown that phytoseiids, including N. longispinosus are effective biocontrol agents of spider mites in challenging cropping environments (Azadi-Qoort and Sedaratian-Jahromi 2024). Since successful control in inoculative releases relies on the predator's subsequent generations to regulate pest populations, understanding predatory dynamics over an extended period is important (Akca et al. 2015). Therefore, we employed computer simulations to evaluate long-term trends in prey consumption. Projecting the consumption and population of an organism is a valuable tool that insights into the damage potential of a pest or the predatory potential of an organism, based on data obtained during a single generation (Chi 2025b; Sharma et al. 2024d). Computer simulations tracking the predatory mite's consumption over 90 days revealed the cumulative effects of residual fungicides. Mancozeb and copper oxychloride showed moderate reductions in mite consumption, while metalaxyl + mancozeb had a more pronounced inhibitory effect. Thiophanate methyl caused the least reduction in prey consumption over the 90-day period.

Conclusion

Our study, which focused on the residual effects of a single application of fungicides, indicated that the predatory mite could continue to feed and control prey mites when exposed to all tested fungicides. However, since multiple applications are often required for effective disease control, the feeding potential of the predatory mite may be further affected. Therefore, additional research is needed to assess the long-term and cumulative impacts of repeated fungicide applications on the feeding behavior and biological control capacity of predatory mites. The variability in predatory responses across different developmental stages and fungicide treatments further illustrates the complexity of predator-prey interactions under chemical exposure. The reduction in cumulative consumption and finite predation rates highlights the potential long-term consequences of fungicide use on predator efficiency. Efforts should be made to use low-risk insecticides and fungicides, along with management practices that are more compatible with natural enemies, ensuring sustainable pest control while maintaining ecological stability in agroecosystems.

Conflict of interest

The authors declare that they have no conflicts of interest.

Funding

Not Applicable

Acknowledgments

The authors are thankful to Dr. YS Parmar University of Horticulture and Forestry, Nauni, Solan, Himachal Pradesh, India for providing necessary facilities to carry out the study.

Author contributions

Prajjval Sharma: Writing, Investigation and methodology; Prem Lal Sharma: supervision, methodology and editing; Subhash Chander Verma: supervision and editing; Rajeshwar Singh Chandel: supervision and formal analysis; Shubham Sharma: Investigation, writing-review and data analysis. All authors have read and approved the final manuscript.

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