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Article

Acaricidal Effect of Zeolite and Kaolin Against Tyrophagus putrescentiae on Wheat

by
Christos G. Athanassiou
1,
Christos I. Rumbos
2,
Paraskevi Agrafioti
1,* and
Maria K. Sakka
1
1
Laboratory of Entomology and Agricultural Zoology, Department of Agriculture, Crop Production and Rural Environment, University of Thessaly, Phytokou Str., 38446 Nea Ionia, Greece
2
Department of Agriculture, University of Patras, 30200 Messolonghi, Greece
*
Author to whom correspondence should be addressed.
Agronomy 2025, 15(4), 799; https://doi.org/10.3390/agronomy15040799
Submission received: 13 January 2025 / Revised: 17 March 2025 / Accepted: 23 March 2025 / Published: 24 March 2025
(This article belongs to the Section Pest and Disease Management)
Versions Notes

Abstract

:
Different inert materials have been tested as grain protectants against stored-product mites with variable results. Most of the studies are focused on the efficacy of diatomaceous earth, but there are few comparable data on other types of inert dust. In this study, we have tested two inert materials, zeolite and kaolin, against the cheese mite Tyrophagus putrescentiae (Schrank) (Astigmata: Acaridae) on wheat. Mites were reared in the laboratory under controlled conditions of 25 °C and 80% relative humidity. Bioassays were conducted to assess the acaricidal effects of zeolite and kaolin. These formulations were applied to wheat kernels at 100, 500, and 1000 ppm. The treated wheat was manually mixed and divided into 1 g subsamples, each containing ten T. putrescentiae. Mortality was recorded after 3 and 7 days, while progeny production was assessed after 42 days. Control samples without treatment were also included, and all experiments were conducted under the same controlled conditions. Our results indicated that zeolite was more effective than kaolin, regardless of the dose rates tested. Parental mortality reached 100% on wheat treated with 1000 ppm of zeolite after only 3 days of exposure. In contrast, survival of T. putrescentiae was noted in all doses of kaolin. Moreover, progeny production in the treated substrate was not avoided even in the highest dose of kaolin but was totally (100%) suppressed at 500 and 1000 ppm. Our results illustrate that zeolite was very effective for the control of this species, even at short exposure intervals, and hence, can be considered further as a grain protectant.

1. Introduction

Stored-product mites are considered important pests of stored products that, apart from the direct infestation that they can cause, are able to cause serious degradations, and their presence may endanger human health [1,2,3,4,5]. Tyrophagus putrescentiae (Schrank) (Astigmata: Acaridae), commonly known as the cheese mite, is a significant pest of stored food products, causing both direct damage to commodities and indirect effects on food quality and human health [1,2,3,4,5]. Infestations are common in high-protein and high-fat stored products such as cheese, grains, dried fruits, flour, animal feed, and cured meats [4,5]. The damage symptoms of T. putrescentiae include physical deterioration of stored products, unpleasant odors, fungal contamination, and health risks [2,3,4,5,6]. Early detection and proper storage management are essential to prevent economic losses and food safety concerns.
In theory, methods that are applied for the control of stored-product insects are considered effective for stored-product mites; however, data show that certain stored-product mites are tolerant to some of the currently used insecticides. For instance, pyrethroids and organophosphates have been tested against T. putrescentiae and indicated that this species may develop tolerance to these compounds [6]. Furthermore, fumigants have been widely used for the control of stored-product insects and mites [7,8]. Due to the phase-out of methyl bromide [9], phosphine has become much more important as a fumigant for the control of stored products [10,11]. Nevertheless, inappropriate application of phosphine (inadequate sealing, leaks), coupled with its continuous usage, has resulted in the emergence of resistance among diverse stored-product insect populations, which is proliferating in several regions globally [12,13]. For instance, Hasan et al. [7] found that eggs of the cheese mite T. putrescentiae, which is one of the most important stored-product mite species globally, could survive fumigants at concentrations that are lethal for most stored-product insects. Similarly, the bacterial insecticide spinosad, which is highly effective for a wide range of stored-product insect species of the orders Coleoptera, Lepidoptera, and Psocopetra, was completely ineffective against T. putrescentiae [8,14]. As a result, traditional control methods rely mostly on chemical treatments, but increasing concerns about resistance, food safety requirements, and environmental effects have prompted researchers to investigate a shift toward alternative approaches, such as inert dust.
Inert materials have been proven effective both as admixture with the grains as well as surface treatment agents [5,15,16,17,18,19,20]. Diatomaceous earths (DEs) have been extensively studied for their efficacy in the control of stored-product insects, including a plethora of published papers in this area over the last decade [21,22,23,24,25,26]. For example, DEs have been used successfully to control major stored-product insects such as the red flour beetle, Tribolium castaneum (Herbst) (Coleoptera: Tenebrionidae), the rice weevil, Sitophilus oryzae (L.) (Coleoptera: Curculionidae), and the lesser grain borer, Rhyzopertha dominica (F.) (Coleoptera: Bostrychidae) [23,27]. Moreover, DEs are effective against mites, including T. putrescentae [24,25,26,28,29,30,31,32,33]. Specifically, Iatrou et al. [29] have shown that DEs can successfully control mite populations, including T. putrescentiae, but their effectiveness varies depending on the formulation, grain type, and environmental conditions. Moreover, Palyvos et al. [18] found that T. putrescentiae was extremely susceptible to DEs after exposure for 48 h on DE-treated grains. In fact, this species seems to be more susceptible than other stored-product mite species, such as Cheyletus malaccensis (Oudemans) (Prostigmata: Cheyletidae) and Blattisocius keegani Fox (Mesostigmata: Blattisociidae) as mentioned by Palyvos et al. [18] and Athanassiou and Palyvos [17].
In recent years, research into alternate inert dusts has expanded to include zeolite and kaolin, which may have different advantages over DEs. Zeolite is a very porous aluminosilicate mineral with remarkable adsorption and ion exchange capabilities, making it extremely effective for moisture management and cuticular lipid absorption [25]. Its unusual physicochemical properties indicate high acaricidal capability, although there is little information on its use against stored-product mites. Kaolin, a naturally occurring clay mineral, is recognized for its small particle size and coating capabilities, which can operate as a barrier against arthropod pests [34]. While kaolin has been studied as an insect repellent, its efficacy as an acaricide remains unknown. However, there is a noticeable lack of comparative data on their acaricidal efficacy, particularly against stored-product mites. Despite having promised physiochemical properties, zeolite and kaolin have not been sufficiently studied for their acaricidal potential. Thus, the research gap is in the lack of data on how effective these dusts are, particularly when applied against stored-product mites.
Considering the fact that most of the data available on the control of species are focused on DEs, research into other inert dusts has expanded to include zeolite and kaolin, which offer additional benefits such as higher adsorption capacity. The aim of this study is to evaluate a formulation of zeolite and a formulation of kaolin against T. putrescentiae in stored wheat in an effort to shed some more light on this direction, using non-chemical grain protectants. Apart from the parental mortality, progeny production suppression was also evaluated.

2. Materials and Methods

2.1. Rearings

Mites were reared in the laboratory under conditions described by Palyvos et al. [18] and Iatrou et al. [29]. In brief, rearings were placed in a mixture of diets as recommended by Palyvos et al. [18] in plastic boxes at controlled conditions of 25 °C and 80% relative humidity (r.h.). From the individuals of the rearings, care was taken in order to select large-bodied individuals, which, according to Palyvos et al. [18], is more likely to correspond to adults. This was due to the fact that progeny production was also estimated in this study, and “parental individuals” can be considered adults despite the fact that deviations might have occurred.

2.2. Experimental Procedure

Following the rearing of mites, the experimental procedures were designed to evaluate the acaricidal effects of the treatments. The bioassays were carried out with two commercial formulations, Zeofeed (Zeoprofit Hellas P.C., Thessaloniki, Greece) and Surround (Hellafarm S.A., Athens, Greece). These were added to a mixture of whole hard wheat kernels with 5% cracked kernels. The inert materials were placed within the substrate at three doses each, i.e., 100, 500, and 1000 ppm. Five hundred grams of wheat samples were placed along with the respective inert material quantities in 1 lt glass jars, which were shaken manually for 3 min in order to achieve a uniform distribution of the dust within the grain mass. Then, these quantities were separated into 1 g subsamples, which were subsequently placed in small vials, as recommended by Palyvos et al. [18]. Then, within each vial, ten individuals of T. pytrescentiae were placed, while mortality was recorded after 3 and 7 days of exposure. The vials were maintained under the same conditions for an additional 42 days, during which progeny production was recorded individually. The conditions of the experiments were the same as above, while a separate series of jars and vials with untreated commodity (zero ppm) was used as a control.

2.3. Statistical Analysis

Data were analyzed by using the MANOVA fit repeated-measures procedure with exposure interval (3 and 7 days) as the repeated variable and treatment (zeolite and kaolin), as well as dose rate (0, 100, 500, and 1000 ppm) as the main effects. Progeny production was analyzed by using a two-way ANOVA to determine the effect of treatment (zeolite and kaolin) and dose rate (0, 100, 500, and 1000 ppm), as well as their associated interaction, on offspring numbers. Mortality and progeny data were submitted to one-way ANOVA in order to identify the differences between the doses for each treatment and exposure interval. Means were separated by using the Tukey–Kramer HSD test, p < 0.05. Finally, Student’s t-test was performed to compare the means of mortality, as well as progeny counts, on kaolin-treated or zeolite-treated cracked wheat for each exposure interval and within each dose rate (p < 0.05).

3. Results

3.1. Mortality

The mortality of T. putrescentiae adults was significantly affected by the dose rate, whereas the treatment effect and the effect of their associated interaction were not significant (Table 1). In the case of zeolite, mortality of T. putrescentiae adults was high and reached 61 and 100% already after 3 days of exposure to cracked wheat treated with 500 and 1000 ppm, respectively. Mortality rates further increased with the increase in the exposure interval and reached 43 and 98% for 100 and 500 ppm, respectively, 7 d after exposure to the zeolite-treated substrate. Slightly lower mortality rates were recorded for kaolin, for which complete control (100% mortality) was not achieved, even at the highest dose rate (1000 ppm) and exposure interval (7 days). More specifically, 53 and 84% of T. putrescentiae adults were dead after 3 days of exposure to cracked wheat treated with kaolin at 500 and 1000 ppm, whereas the respective figures were 85 and 93% after 7 days of exposure (Table 2).

3.2. Progeny Production

Offspring emergence of T. putrescentiae was significantly affected both by the dose rate and the treatment but not by their associated interaction (Table 3). In the case of zeolite, mean progeny production in untreated cracked wheat was 57 individuals/vial and, in all cases, differed significantly from the one in zeolite-treated wheat for all dose rates. Particularly, progeny production in zeolite-treated wheat was totally suppressed at dose rates higher than 500 ppm. When cracked wheat was treated with kaolin, progeny production was not completely suppressed even at the highest dose rate (4 individuals/vial). Instead, considerable offspring emergence was recorded in wheat treated with kaolin at 100 and 500 ppm, i.e., 74 and 40 individuals/vial (Table 4).

4. Discussion

Our data show that both formulations tested here were able to cause parental mortality of T. pytrescentiae, along with progeny production suppression. Regarding the latter, we have to mention that only the number of live individuals was recorded, but we also noted mite individuals that were dead, which underlines the “residual effect” of inert materials [25]. In an earlier study, Athanassiou et al. [35] found that DEs could provide a considerable level of protection on both wheat and barley against the rice weevil Sitophilus oryzae (L.) (Coleoptera: Curculionidae). Considering our data, we assume that, at longer exposure intervals, mite mortality would have been higher, especially during the progeny production evaluation stage. This is due to the fact that inert materials act through the cuticle, and hence, soft-bodied individuals may be more susceptible [21]. Nevertheless, this is not the case with stored-product psocids, which, although soft-bodied as well, seem to have a mechanism to moderate water loss [16,25].
From the two formulations tested here, zeolite was found to be more effective than kaolin. In an earlier study evaluating kaolin as a grain protectant, Panagiotakis et al. [34] found that the same formulation as the one tested here was unable to control adults of the larger grain borer, Prostephanus truncatus (Horn) (Coleoptera: Bostrychidae). While the mode of action of both formulations we used in the current tests is similar, differences among the physicochemical properties of these formulations (particle size, particle shape, etc.) might have affected their efficacy. Zeolite has a highly porous, crystalline structure with a huge surface area, allowing it to effectively adsorb moisture and cuticular lipids from mites, resulting in fast desiccation and death. Its uneven, sharp-edged particles also cause mechanical abrasion of the mite’s exoskeleton, which increases water loss. On the other hand, kaolin has a smoother, less porous structure with less adsorption capacity effect. Furthermore, zeolite’s cation exchange ability may interrupt mite physiological processes, which adds to its effectiveness. These combined characteristics account for zeolite’s excellent effectiveness in mortality and offspring suppression. In an earlier study, Kavallieratos et al. [15] used the same zeolite formulation and found that this formulation was effective for the control of this species, but its efficacy varied according to the life stage of T. putrescentiae tested. Moreover, in that study, the authors noted that T. putrescentiae was more susceptible to the zeolite-treated substrate than the flour mite Acarus siro L. (Astigmata: Acaridae) [15]. In our work, we found the mortality levels that were higher than those of Kavallieratos et al. [15], which could be attributed to the experimental conditions, but, in principle, the efficacy data reported here are comparable with that work. This study’s results showed that zeolite was fully effective (100% mortality) at doses of 500 and 1000 ppm after just 3 days, whereas kaolin never achieved complete mortality. This suggests that for practical grain storage applications, zeolite concentrations above 500 ppm are likely to be the most effective. Additionally, more precise application methods, such as uniform distribution via mechanical agitators or high-pressure air dispersal, should be considered to improve the consistency of dust distribution within the grain mass [24]. Previous research has highlighted the importance of uniform dust application in maximizing the efficacy of inert materials against stored-product pests [36].
Although mites are considered very susceptible to inert materials, we saw here that the lowest dose (100 ppm) used here was not effective. In fact, progeny production levels in the vials that were treated with 100 ppm were comparable with those in the control vials. Progeny production is perhaps more important than parental mortality, given that inert dusts have no ovicidal effect [21,25], which means that the “speed of kill” is of utmost importance, and newly hatched individuals may continue to cause grain damage. Inert materials, being slower-acting than conventional grain protectants, may allow for colonization through this mechanism, which partially explains the presence of dead individuals that were recorded during the progeny production evaluation stage. Nevertheless, delayed mortality is likely to occur through the contact of inert materials with the newly hatched individuals, as demonstrated in the case of the confused flour beetle, Tribolium confusum Jacquelin du Val (Coleoptera: Tenebronidae) [27,36].
In summary, we have found that both inert materials tested here were effective for the control of T. putrescentiae, with zeolite being more effective than kaolin. Due to variations in their physicochemical characteristics, including particle size and shape, zeolite is more effective than kaolin. The acaricidal effects of zeolite and kaolin against T. putrescentiae are primarily based on physical and physiological interactions rather than direct toxicity. These inert dusts function by disrupting the mites’ external structures, leading to desiccation, mechanical damage, and physiological stress. However, zeolite demonstrates superior acaricidal properties compared to kaolin due to differences in particle structure, adsorption capacity, and ion exchange properties. Aside from the mechanism of the dusts, some other factors might also be involved, such as differences in surface characteristics and chemical makeup that impact how they interact with mites. For example, variations in hydrophilic or hydrophobic properties may affect how the mites’ cuticular lipids are adsorbed, resulting in different degrees of desiccation and death [9]. According to earlier research, the size and form of the particles in inert dusts, such as diatomaceous earths (DEs), affect how well they absorb cuticular lipids and dehydrate arthropods [21]. Moreover, we have underlined the fact that even if parental mortality is high, progeny production cannot be avoided, but even this progeny can be gradually suppressed through contact with the inert material particles. The results of this study show that inert materials can be further evaluated on the basis of a non-chemical strategy in grain protection.
This study highlights the potential of inert materials, specifically zeolite and kaolin, in order to control T. putrescentiae, a significant pest in stored products. The results underscore the superior efficacy of zeolite, which achieved 100% mortality at higher doses (500 and 1000 ppm) within a short exposure period while also completely suppressing progeny production. In contrast, kaolin showed limited efficacy, with lower mortality rates and incomplete suppression of progeny, even at the highest concentration. These differences are likely due to variations in the physicochemical properties of the materials, such as particle size and shape, which influence their interaction with the pests. The findings reaffirm the potential of zeolite as a sustainable and non-chemical alternative for pest control in grain storage, particularly for species like T. putrescentiae that exhibit tolerance to conventional pesticides. The use of inert materials also aligns with the growing demand for environmentally friendly pest management strategies, reducing reliance on chemical treatments that may pose risks to human health and the environment.

5. Conclusions

This study emphasizes the importance of optimizing dosage to ensure effective pest control while minimizing costs and potential residues in treated grains. Future research should explore the long-term stability and effectiveness of zeolite in real-world storage conditions, as well as its interaction with other pest management tools. Additionally, expanding these investigations to other stored-product pests and commodities would provide valuable insights into the broader applicability of inert materials.

Author Contributions

Conceptualization, C.G.A.; methodology, C.I.R., P.A. and M.K.S.; validation, C.G.A., C.I.R., P.A. and M.K.S.; formal analysis, C.G.A. and C.I.R.; investigation, C.G.A., C.I.R., P.A., and M.K.S.; data curation, C.G.A., C.I.R., P.A. and M.K.S.; writing—original draft preparation, C.G.A., C.I.R., P.A. and M.K.S.; writing—review and editing, C.G.A., C.I.R., P.A. and M.K.S.; visualization, C.G.A.; supervision, C.G.A. and C.I.R.; project administration, C.G.A. and C.I.R. All authors have read and agreed to the published version of the manuscript.

Funding

This research received no external funding.

Data Availability Statement

The data are available upon request from the authors.

Conflicts of Interest

The authors declare no conflicts of interest.

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Table 1. Repeated-measures MANOVA parameters for mortality of Tyrophagus putrescentiae adults exposed for 3 and 7 days to untreated cracked wheat (control) and cracked wheat treated with three dose rates of zeolite and kaolin (100, 500, and 1000 ppm) [error df = 64].
Table 1. Repeated-measures MANOVA parameters for mortality of Tyrophagus putrescentiae adults exposed for 3 and 7 days to untreated cracked wheat (control) and cracked wheat treated with three dose rates of zeolite and kaolin (100, 500, and 1000 ppm) [error df = 64].
SourcedfFp
All between767.7<0.001
Intercept11426.6<0.001
Treatment13.50.066
Dose3155.4<0.001
Treatment × Dose31.3050.280
All within interaction79.5<0.001
Time after exposure1155.5<0.001
Time after exposure × Treatment10.6070.439
Time after exposure × Dose320.0<0.001
Time after exposure × Treatment × Dose32.00.126
Table 2. Mean mortality ± SE of Tyrophagus putrescentiae adults exposed for 3 and 7 days to untreated cracked wheat (control) and cracked wheat treated with three dose rates of zeolite and kaolin (100, 500, and 1000 ppm).
Table 2. Mean mortality ± SE of Tyrophagus putrescentiae adults exposed for 3 and 7 days to untreated cracked wheat (control) and cracked wheat treated with three dose rates of zeolite and kaolin (100, 500, and 1000 ppm).
Mortality (%)
DoseZeoliteKaolin
Day 3Day 7Day 3Day 7
Control7.2 ± 2.6 d21.7 ± 2.8 c12.8 ± 3.7 c22.2 ± 3.5 c
100 ppm27.8 ± 3.5 c43.3 ± 5.6 b20.0 ± 3.9 c44.4 ± 7.8 b
500 ppm61.7 ± 7.9 b98.3 ± 1.2 a53.3 ± 5.1 b85.6 ± 4.2 a *
1000 ppm100.0 ± 0.0 a100.0 ± 0.0 a84.4 ± 7.0 a *93.9 ± 4.1 a
For each treatment (zeolite and kaolin) and for each exposure interval (3 and 7 days), means followed by the same lowercase letter do not differ significantly (in all cases, df = 3, 35; Tukey HSD test at p = 0.05). Means with an asterisk (*), obtained from kaolin-treated cracked wheat, are significantly different from the respective means obtained from zeolite-treated cracked wheat for each dose rate and exposure interval, according to Student’s t-test (p < 0.05).
Table 3. Two-way ANOVA parameters for main effects and associated interactions for progeny counts of Tyrophagus putrescentiae adults exposed for 3 and 7 days to untreated cracked wheat (control) and cracked wheat treated with three dose rates of zeolite and kaolin (100, 500, and 1000 ppm) [error df = 64].
Table 3. Two-way ANOVA parameters for main effects and associated interactions for progeny counts of Tyrophagus putrescentiae adults exposed for 3 and 7 days to untreated cracked wheat (control) and cracked wheat treated with three dose rates of zeolite and kaolin (100, 500, and 1000 ppm) [error df = 64].
SourcedfFp
Whole model76.8<0.001
Intercept169.8<0.001
Treatment18.00.006
Dose311.5<0.001
Treatment × Dose31.70.176
Table 4. Progeny counts (number of individuals/vial ± SE) of Tyrophagus putrescentiae adults exposed for 3 and 7 days to untreated cracked wheat (control) and cracked wheat treated with three dose rates of zeolite and kaolin (0, 100, 500, and 1000 ppm).
Table 4. Progeny counts (number of individuals/vial ± SE) of Tyrophagus putrescentiae adults exposed for 3 and 7 days to untreated cracked wheat (control) and cracked wheat treated with three dose rates of zeolite and kaolin (0, 100, 500, and 1000 ppm).
DoseZeoliteKaolin
Control57.2 ± 11.0 a62.4 ± 14.7 a
100 ppm32.0 ± 6.8 b74.2 ± 23.9 a
500 ppm0.0 ± 0.0 c40.0 ± 9.3 ab *
1000 ppm0.0 ± 0.0 c4.1 ± 1.7 b *
For each treatment (zeolite and kaolin), means followed by the same lowercase letter do not differ significantly (in all cases, df = 3, 35; Tukey HSD test at p = 0.05). Means with an asterisk (*), obtained from kaolin-treated cracked wheat, are significantly different from the respective means obtained from zeolite-treated cracked wheat for each dose rate, according to Student’s t-test (p < 0.05).
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MDPI and ACS Style

Athanassiou, C.G.; Rumbos, C.I.; Agrafioti, P.; Sakka, M.K. Acaricidal Effect of Zeolite and Kaolin Against Tyrophagus putrescentiae on Wheat. Agronomy 2025, 15, 799. https://doi.org/10.3390/agronomy15040799

AMA Style

Athanassiou CG, Rumbos CI, Agrafioti P, Sakka MK. Acaricidal Effect of Zeolite and Kaolin Against Tyrophagus putrescentiae on Wheat. Agronomy. 2025; 15(4):799. https://doi.org/10.3390/agronomy15040799

Chicago/Turabian Style

Athanassiou, Christos G., Christos I. Rumbos, Paraskevi Agrafioti, and Maria K. Sakka. 2025. "Acaricidal Effect of Zeolite and Kaolin Against Tyrophagus putrescentiae on Wheat" Agronomy 15, no. 4: 799. https://doi.org/10.3390/agronomy15040799

APA Style

Athanassiou, C. G., Rumbos, C. I., Agrafioti, P., & Sakka, M. K. (2025). Acaricidal Effect of Zeolite and Kaolin Against Tyrophagus putrescentiae on Wheat. Agronomy, 15(4), 799. https://doi.org/10.3390/agronomy15040799

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