Theobroma cacao L., commonly known as cacao, is a shade-loving tree that is known to be the source of chocolate products. It is mainly grown for its seeds known as cocoa beans, which are used to make cocoa mass, cocoa powder, and chocolates. It has no product substitute, making it a good investment, especially for small-holder farmers. The primary producers of cacao in the world are the Ivory Coast and Ghana, and other equatorial countries in Southeast Asian like Indonesia, Malaysia, and the Philippines (Stecker, 2011). There is a growing demand for cocoa in the form of hard pressed beans for confection products (Morgan, 2014). According to the World Cacao Foundation (Frimpong, 2013) disease and insect pest occurrences are important contribotors to the decrease in the supply of cacao worldwide, where it is estimated that 30 to 40% of the loss in cacao bean production may be due to pest damage.

With the desire of the Philippines to increase local production to meet the growing market demands, it must face the threat of insect pests, specifically the cacao mirid bug (CMB) (Helopeltis bakeri Poppius) (Dormon et al., 2004). This is one of the four Helopeltis species endemic to the Philippines (Serrana et al., 2022). It feeds and oviposits on the cacao pods causing brown and black lesions, which serve as an avenue for microbial infection (Amalin et al., 2015). CMB-infested pods produce deformed and smaller beans as compared to healthy pods. Heavy infestation of CMB results in pod malformation and premature drop. In the province of Sorsogon alone, the number of damaged pods due to CMB feeding increased from 70% to 87% in just a period of three months (Tormes and Mostoles, 2021).

Management of cacao pests is usually through the application of chemical pesticides (Mboussi et al., 2018). However, that approach only offers short-term control and poses risks of harm to people and the environment. An alternative to chemical pesticides is the use of biological control agents, which use other living organisms to control the spread of insect pests and diseases. A potential biological control against CMB is the utilization of the microscopic entomopathogenic fungal species, Metarhizium anisopliae (Metschnikoff) Sorokin. It produces acidic substances that readily penetrates the proteinaceous cuticular barrier of insects (St Leger et al., 1999). Once inside, the fungi will reproduce and upon successful invasion of the host’s tissue, will emerge from the dead host.

Another alternative to chemical pesticides is the utilization of particle clays as coating agents, also known as particle film technology, to deter insect feeding. This technology combines mineral technology, insect behavior, and light physics in controlling pests (Glenn and Puterka, 2010). When sprayed into the plants, the particle film forms a barrier that protects them from insect and microbial pests. Broadly, particle film is known to works as a repellent, irritant, and as an obstacle to feeding and oviposition. It also prevents fungal spores from propagating onto the plant. It was also noted that particle film blocks the spiracles of the insect, reduces mating success, impedes insect pest movement, alters the taste and smell of the host (Kljajić et al., 2011; Glenn and Puterka, 2010).

Particle film technology was originally based on kaolin clay, a secondary mineral that came from the weathering of primary minerals such as quartz and feldspar (Glenn and Puterka, 2010). It was patented under the commercial name Surround WP^®. The United States Food and Drug Administration (FDA) granted kaolin the GRAS (Generally Recognized as Safe) status for use on fruits crops, such as apples, pears and citrus (Mazor and Erez, 2004; Daniel et al., 2005; Ramirez-Godoy et al., 2018). In the same manner, the US Environmental Protection Agency (EPA) found that kaolin has no adverse effects on non-target organisms such as spiders and beneficial insects. And since kaolin does not dissolve in water, it does not have adverse effects on aquatic organisms. Aside from the use of kaolin, other naturally occurring particle clays such as zeolite and bentonite can also be utilized in controlling pest attacks on plants. The insecticidal effect of zeolite was tested by De Smedt et al. (2016) against Tuta absoluta Meyrick, a major insect pest attacking tomatoes. They found out that zeolite affected the egg development process by weakening the first instar larvae and increasing mortality. Bentonite can also be used as a crop protectant though the study conducted by Abd El-Aziz (2013) concluded that kaolin is more effective against onion thrips as compared to bentonite.

Previous studies have reported the synergistic effects of particle film with entomopathogenic fungi. Storm et al. (2016) investigated the improvement of the efficacy of Beauveria bassiana, an entomopathogenic fungal species, against stored grain beetles (Oryzaephilus surinamensis) with synergistic co-formulant kaolin. In the same manner, Sabbour et al. (2012) tested the synergistic effects of B. bassiana and M. anisopliae with diatomaceous earth. In both studies, it was found that the efficacy of the biopesticide improved as compared to the control (water). To date, no studies have yet investigated the synergistic effect of kaolin or zeolite with M. anisopliae.

With this, the objective of the study is to evaluate the efficiency of Philippine-sourced particle clays (zeolite, bentonite, and kaolin) as a coating agent to deter CMB feeding on cacao pods. By determining which particle clay is most efficient, the study also assessed its synergistic effect with the spores of M. anisopliae.

This study provides new knowledge as to the potential for particle films and entomopathogens in controlling CNB in cacao Integrated Pest Management. Results showed that both the Surround WP^® and Philippine-sourced zeolite have similar levels of performance as the insecticide thiamethoxam (Actara^®) in deterring CMB feeding. One of the most important modes of action of particle film is through masking the appearance of the target hosts. The coated pods were likely unrecognizable from the perspective of the insect pest, resulting in the deterrence of feeding, reduced oviposition, and reduced pest population in the plant (Sharma et al., 2015). The work of Glenn et al. (1999) showed that insect behavior was altered when exposed to plants coated with kaolin as compared to its behavior on natural plant surfaces. The physical barrier made by the particle film made it harder for the pest to locate its host.

There have been reports on the insecticidal properties of kaolin and zeolites. The use of kaolin as a biopesticide was documented by Daniel et al. (2005). A small field trial was conducted to determine the efficacy of kaolin as an insecticide against Cacopsylla pyri L. which attacks pear. Kaolin was introduced during the first flying period of C. pyri and its application reduced the egg laying and number of nymphs as compared to the untreated control. Kaolin-protected trees were as good as the standard insecticide, rotenone. Zeolite, on the other hand, was applied to wheat under laboratory conditions against Sitophilus oryzae and Tribolium castaneum (Kljajić et al., 2011). Results showed that there was a 94-100% mortality on both insect pests for all zeolite dosages (0.25, 0.50, 0.75 g/kg). In addition, the progeny was reduced by more than 90% 21 days after exposure to zeolite. The non-choice study herein suggests that the Philippine-sourced kaolin does not have insecticidal properties, but based on the non-choice test causes the pods to be less desirable than those that are untreated.

Another result of this present study was that zeolite has a better synergistic effect with M. anisopliae. One reason might be the particle size. Surround WP^® measures approximately 2μm in size, whereas, zeolite is approximately 25μm in size. Since the particle size of zeolite is bigger, spores have a bigger surface area for attachment, making it possible for better distribution on the treated pods. Malusá et al. (2012) noted that a good carrier of microbial inoculant may vary from 25 to 75 μm and be free of a lump. Furthermore, the same authors noted that a good carrier of beneficial bacteria and fungi must have a good moisture absorption capacity, good pH buffering capacity, and be porous. Coppin (2015) wrote that zeolite control moisture content, buffer pH of acid volcanic soils, and is porous.

There is no clear explanation yet as to the reason for the efficacy of the particle clays to carry the spores of entomopathogenic fungi. Samodra and Ibrahim (2006) observed that the cuticle of the insect was abraded due to the presence of kaolin. This gave fungal spores an avenue for easier penetration and greater conidial attachment. The increased water loss due to cuticle abrasion may result in favorable condition for spore germination and the increased stress of insects make them more susceptible to fungal infection.

Insecticides offer lethal-based control of harmful pests and diseases however, along with this comes the risks associated with these modes of action (Mahmood et al., 2016). Over time, many pest species have developed resistance to chemical pesticides which makes sustainable pest management more difficult. In this regard, biological pesticides or biological controls are becoming more attractive because they are relatively safe to humans, do not pose harm to the environment, and sometimes more economical, and pests are less likely to develop resistance and avoid pest resurgence.

This study has demonstrated that the effects of the commercially available kaolin (Surround WP^®) and the Philippine-sourced zeolite are comparable with that of the insecticide thiamethoxam (Actara^®) in deterring CMB feeding to cacao pods in both choice and no-choice tests. Between these particle clays, zeolite is more efficient in carrying the spores of M. anisopliae, an entomopathogen known to infect different insect pest species because of its particle size. The potential of the combined formulation of zeolite and M. anisopliae for the control of CMB and other insect pests attacking the cacao pods should be further explored.

The raw data supporting the conclusions of this article will be made available by the authors, without undue reservation.

SA, DA, and JW conceptualized the study. SA conducted all the experiments. SA and TC conducted the analysis under the supervision of JW. SA wrote and revised the manuscript under the supervision of DA, TC, and JW. All authors contributed to the article and approved the submitted version.