1 Introduction

Sitophilus oryzae, commonly known as the rice weevil, is a significant pest affecting stored cereal grains worldwide, including rice (Wu and Yan, 2018). This pest is notorious for its ability to infest and damage stored grains, rendering them unsuitable for consumption, processing, and export (Singh et al., 2021). The rice weevil's lifecycle and reproductive capabilities allow it to proliferate rapidly under favorable conditions, leading to substantial economic losses in the agricultural sector (Pal et al., 2021). The pest's adaptability to various storage environments and its resistance to common insecticides further complicate management efforts (Tesfaye et al., 2021).

Addressing infestations of S. oryzae is crucial for several reasons. Firstly, the economic impact of rice weevil infestations is profound, as they lead to significant post-harvest losses. For instance, in regions like southern India and Nepal, infestations have been reported to cause substantial grain damage and weight loss, affecting both local consumption and international trade (Guru-Pirasanna-Pandi et al., 2018). Secondly, the presence of S. oryzae in stored grains can lead to contamination and spoilage, posing health risks to consumers (Hu et al., 2018). Moreover, the development of resistance to conventional insecticides, such as deltamethrin, necessitates the exploration of alternative control methods to ensure sustainable pest management (Nasr et al., 2022).

This study evaluates the current strategies and challenges in managing S. oryzae infestations in rice. This includes an assessment of chemical, biological, and eco-friendly control methods, as well as the identification of resistant rice genotypes and the role of genetic resistance in pest management. This study also explores the geographical distribution of S. oryzae and its related species, providing insights into regional pest management practices.

2 Biology and Behavior of Sitophilus oryzae

2.1 Life cycle and reproductive patterns

The life cycle of Sitophilus oryzae, commonly known as the rice weevil, involves several stages: egg, larva, pupa, and adult. The duration of each stage can vary depending on environmental conditions and the type of grain the weevil infests. For instance, research has shown that the total life cycle period of S. oryzae is longer when the weevil is fed on mixed grains compared to a single cultivar like HPW-2361. Additionally, the reproductive success of S. oryzae can be influenced by the type of grain, with certain rice varieties showing higher rates of adult emergence and grain consumption, indicating susceptibility (Mehta et al., 2021). The presence of fissures in the grain is a significant morphological characteristic that determines the susceptibility or resistance of rice varieties to S. oryzae (Costa et al., 2016).

2.2 Feeding behavior and damage to rice grains

S. oryzae primarily feeds on the endosperm of grains, while the larvae target the germ, leading to reduced germination and nutritional value of the grains (Singh et al., 2021). The feeding behavior of S. oryzae can be monitored using ultrasonic insect feeding monitors, which have revealed that weevils reared in grains with higher moisture content develop faster and have fewer instars compared to those in drier conditions (Hu et al., 2018). The damage inflicted by S. oryzae varies among different grain types, with polished rice being the most preferred and heavily damaged, while rough rice is less affected8. The weevil's feeding not only reduces the weight and quality of the grains but also affects their germination rates, as observed in various wheat cultivars (Baker, 1988).

2.3 Environmental factors influencing infestation levels

Environmental factors such as temperature, humidity, and grain moisture content significantly influence the infestation levels of S. oryzae. For example, weevils reared in grains with lower humidity levels exhibit longer development times and may undergo supernumerary molts as a stress response to low moisture conditions (Pittendrigh et al., 1997). Additionally, a logistic model simulating environmental changes has shown that temperature and grain moisture content are critical parameters affecting the development, survivorship, and oviposition rates of S. oryzae (HarDIan, 1978). The model also predicts that cooling and drying grains can be effective strategies to mitigate weevil infestations (Parisot et al., 2021). Furthermore, the presence of fungal cues, such as those from Aspergillus flavus, can influence the foraging behavior of S. oryzae, with certain fungal life stages attracting the weevils more than others. By understanding the biology and behavior of S. oryzae, including its life cycle, feeding habits, and the environmental factors that influence its infestation levels, effective strategies can be developed to combat this pest and protect rice grains from significant damage (Ponce et al., 2022).

3 Current Strategies for Managing Sitophilus oryzae

3.1 Chemical control methods

Chemical control remains a primary strategy for managing Sitophilus oryzae in stored rice. Commonly used insecticides include synthetic pyrethroids such as deltamethrin. However, the extensive use of these chemicals has led to significant resistance issues. For instance, a study in India identified a super kdr mutation, T929I, in S. oryzae, which confers resistance to deltamethrin, highlighting the need for alternative control measures (Adarkwah et al., 2019).

The development of resistance to chemical insecticides is a growing concern. The aforementioned T929I mutation in S. oryzae populations in India has resulted in a 134-fold increase in resistance to deltamethrin compared to susceptible strains (Riudavets et al., 2021). This necessitates the identification of synergists or alternative insecticides to manage resistant populations effectively. Additionally, the use of botanical oils, such as those derived from Simmondsia chinensis and Rosmarinus officinalis, has shown promise as they exhibit significant insecticidal activity against S. oryzae and could be integrated into pest management programs to mitigate resistance development (Shawer et al., 2022).

3.2 Biological control methods

Biological control using natural predators and parasitoids offers a sustainable alternative to chemical methods. The parasitoid Anisopteromalus calandrae has been shown to effectively control S. oryzae populations in stored rice. In large-scale trials, A. calandrae reduced weevil populations by approximately 60% in big bags of paddy rice (Adak et al., 2020). Additionally, the combined use of the predator Xylocoris flavipes and the parasitoid Theocolax elegans has demonstrated a synergistic effect, significantly reducing S. oryzae progeny in stored rice (Khoobdel et al., 2022). Entomopathogenic fungi, such as Metarhizium anisopliae, have been investigated for their potential to control S. oryzae. Studies have shown that higher concentrations of M. anisopliae result in increased mortality rates of S. oryzae, with an effective concentration (LC50) of 31.88% (Fouad et al., 2021). These fungi offer a promising biological control method that can be integrated into pest management strategies to reduce reliance on chemical insecticides.

3.3 Physical control methods

Manipulating environmental conditions such as temperature and humidity can effectively control S. oryzae infestations. Lowering the temperature and reducing humidity levels in storage facilities can inhibit the development and reproduction of the weevils, thereby reducing their populations (Kłyś et al., 2020). Controlled atmosphere storage, including the use of CO₂ fumigation, is another effective physical control method. This technique involves altering the atmospheric composition within storage containers to create conditions that are lethal to pests like S. oryzae. It is a chemical-free method that can be used in conjunction with other control strategies to enhance overall effectiveness.

3.4 Cultural and integrated pest management (IPM) approaches

Cultural practices such as crop rotation and maintaining high levels of sanitation in storage facilities are crucial components of integrated pest management (IPM). These practices help to reduce the initial pest load and prevent the establishment and spread of S. oryzae populations. Combining multiple control strategies, including chemical, biological, physical, and cultural methods, can enhance the overall effectiveness of pest management programs. For example, integrating the use of botanical oils with biological control agents like A. calandrae and M. anisopliae can provide a more comprehensive approach to managing S. oryzae infestations (Figure 1) (Tarore et al., 2023). This integrated approach not only improves control efficacy but also reduces the risk of resistance development and minimizes environmental impact.

Figure 1 (a-b): Imago S. oryzae attacked by M. anisopliae pathogen in the laboratory, (a) Imago S. oryzae healthy and (b) Imago S. oryzae stricken M. anisopliae (Adopted from Tarore et al., 2023)

Tarore et al. (2023) found that the entomopathogenic fungus Metarhizium anisopliae is highly effective in infecting and eventually killing Sitophilus oryzae (rice weevil) under laboratory conditions. The study observed significant differences between healthy and infected rice weevils, highlighting the pathogenic impact of M. anisopliae. The infected weevils exhibited visible growths of conidia and mycelia, which are key reproductive structures of the fungus, leading to the eventual death of the host. This pathogen has potential applications in biological control strategies against pests like S. oryzae, offering a natural alternative to chemical pesticides. The research supports the viability of using fungal pathogens for pest management in stored grain environments, contributing to sustainable agricultural practices by reducing reliance on harmful synthetic chemicals. The findings underscore the importance of further research into optimizing the use of M. anisopliae in pest control programs.

4 Challenges in Combatting Sitophilus oryzae

4.1 Emergence of resistance to chemical treatments

One of the significant challenges in managing Sitophilus oryzae is the emergence of resistance to chemical treatments. For instance, the recurrent use of deltamethrin, a synthetic pyrethroid insecticide, has led to genetic resistance in S. oryzae populations in southern India. Research has identified a super kdr mutation, T929I, in the voltage-gated sodium channel gene, which confers resistance to deltamethrin. This mutation has resulted in some populations being 134-fold more resistant compared to susceptible strains, necessitating the need for alternative control strategies or synergists to enhance the efficacy of existing treatments (Zhou and Wang, 2016). Additionally, the indiscriminate use of phosphine gas for fumigation has also led to heritable resistance in S. oryzae, complicating the management of this pest (Lucas and Riudavets, 2002).

4.2 Limitations of biological control methods

Biological control methods, while environmentally friendly, face several limitations. The use of parasitoids such as Anisopteromalus calandrae and Lariophagus distinguendus has shown promise in reducing S. oryzae populations. However, mechanical methods used in conjunction with biological control can negatively impact the survival and efficacy of these parasitoids. For example, mechanical polishing processes can reduce the nutritional quality of rice and adversely affect the survival of parasitoids, particularly A. calandrae, which shows a skewed sex ratio favoring males under such conditions (Williams and Mills, 1980). Furthermore, the effectiveness of entomopathogenic fungi like Metarhizium anisopliae is dose-dependent, with higher concentrations required to achieve significant mortality rates, which may not always be practical or cost-effective (Rojasara and Patel, 2020).

4.3 Economic and environmental impacts of control measures

The economic and environmental impacts of control measures for S. oryzae are substantial. Chemical treatments, while effective, pose risks to human health and the environment due to their toxic nature. The development of resistance further exacerbates these issues, leading to increased costs for alternative treatments and potential economic losses due to ineffective pest control. Biological control methods, although less harmful, can be costly and labor-intensive to implement on a large scale. Additionally, mechanical damage to grains during harvesting and handling can destroy inherent resistance factors in certain sorghum cultivars, making them more susceptible to S. oryzaeinfestation (Thangaraj et al., 2019). Industrial-scale radio frequency treatments offer a non-chemical alternative, but their implementation requires significant investment in equipment and infrastructure (Tarore et al., 2023).

4.4 Regulatory and logistical challenges in implementing IPM

Implementing Integrated Pest Management (IPM) strategies for S. oryzae faces several regulatory and logistical challenges. Regulatory frameworks often lag behind the rapid development of resistance in pest populations, making it difficult to enforce effective control measures. Additionally, the lack of phylogeographic structuring in S. oryzae populations across regions like India indicates significant gene flow, likely due to anthropogenic activities. This necessitates a coordinated, country-wide approach to resistance management, which can be challenging to organize and implement. Furthermore, the identification and deployment of resistant rice varieties require extensive research and breeding programs, which can be time-consuming and resource-intensive (Kosewska et al., 2023). In conclusion, combatting Sitophilus oryzae in rice involves addressing multiple challenges, including resistance to chemical treatments, limitations of biological control methods, economic and environmental impacts, and regulatory and logistical hurdles in implementing IPM strategies. Effective management will require a multifaceted approach that integrates chemical, biological, and mechanical methods while considering the economic and environmental implications (Costa et al., 2016).

5 Case Study

5.1 Background of the selected region or case

The selected case study focuses on the implementation of control strategies against Sitophilus oryzae in a rice mill located in Portugal. Sitophilus oryzae, commonly known as the rice weevil, is a significant pest affecting stored grains globally, including rice (Carvalho et al., 2012). The infestation by this pest leads to substantial economic losses due to the damage it causes to stored grains, making them unsuitable for consumption and processing. The rice mill in Portugal faced challenges in managing this pest, prompting the exploration of alternative control methods to traditional fumigation (Figure 2) (Parisot et al., 2021).

Figure 2 Sitophilus oryzae overview (Adopted from Parisot et al., 2021) Image capton: A Life cycle of cereal weevil Sitophilus oryzae. The embryo develops into a larva and pupa, and metamorphoses into a young adult, exiting the grain around 3 days after metamorphosis completion. The developmental times indicated are from a rearing condition at 27 °C and 70% relative humidity. B Photos of adult S. oryzae. Lower panel shows an adult exiting the grain (Adopted from Parisot et al., 2021)

Parisot et al. (2021) examined the life cycle of the rice weevil (Sitophilus oryzae) and identified key developmental stages that are critical for its management as a pest. The study highlighted the importance of understanding the environmental conditions that favor the development of S. oryzae, particularly temperature and humidity, which influence the duration of each stage from embryo to adult. By rearing S. oryzae at 27°C and 70% relative humidity, researchers were able to track the transformation from larvae to pupae and finally to adult weevils, with the entire process taking approximately 24 days. This information is crucial for developing targeted pest control strategies that disrupt the life cycle at vulnerable stages, such as during metamorphosis or adult emergence from the grain. The findings underscore the significance of controlling environmental factors to mitigate the impact of this pest on stored cereals, contributing to more effective pest management practices.

5.2 Description of the implemented control strategies

In the Portuguese rice mill, modified atmospheres were employed as an alternative to conventional fumigation methods to control Sitophilus oryzae (Yang et al., 2017). The strategy involved the use of high concentrations of carbon dioxide (CO₂) to create an inhospitable environment for the pests. The trials were conducted in a silo containing 40 tonnes of polished rice and in four hermetic big bags with a capacity of 1 tonne each, containing both paddy and polished rice. The atmospheric composition in these storage units ranged from 90 to 95% CO₂ and 0.7 to 2.1% O₂. Three different trials were carried out at varying temperatures and treatment durations to assess the efficacy of this method (Thangaraj et al., 2019).

5.3 Outcomes and lessons learned

The modified atmosphere treatments proved to be highly effective in controlling Sitophilus oryzae. In all trials, the mortality rate of adult weevils and eggs was close to 100%, with no emergence of the next generation (F1) recorded in any of the treated samples (Dal et al., 2000). This high level of efficacy was consistent across different temperatures and treatment durations, demonstrating the robustness of the modified atmosphere approach. The success of this method highlighted the potential of CO₂-based treatments as a viable alternative to traditional fumigation, which often involves the use of chemical agents that can leave residues on the grains (Thangaraj et al., 2016).

5.4 Implications for broader application in other regions

The successful implementation of modified atmospheres in the Portuguese rice mill suggests that this strategy could be broadly applicable in other regions facing similar challenges with Sitophilus oryzae infestations (Kosewska et al., 2023). The use of CO₂ as a control method offers several advantages, including the absence of chemical residues and the potential for use in organic grain storage systems. Additionally, this method can be adapted to various storage conditions and grain types, making it a versatile tool in integrated pest management programs. The lessons learned from this case study can inform the development of guidelines and best practices for the use of modified atmospheres in grain storage facilities worldwide, contributing to more sustainable and effective pest control strategies (Fouad et al., 2021).

6 Future Directions in Sitophilus oryzae Management

6.1 Advances in genetic and molecular research

Recent advancements in genetic and molecular research have provided significant insights into the management of Sitophilus oryzae. The identification of genetic mutations conferring resistance to insecticides, such as the T929I mutation in the vgsc gene, highlights the importance of molecular diagnostics in resistance management. This mutation has been linked to deltamethrin resistance, suggesting that genetic markers can be used to monitor and manage resistance in field populations (Thangaraj et al., 2016). Additionally, the sequencing of the S. oryzae genome has revealed extensive transposable element activity, which may influence genetic diversity and adaptability. Understanding these genetic elements can aid in developing targeted genetic interventions to control pest populations (Parisot et al., 2021).

6.2 Development of novel biocontrol agents

The development of novel biocontrol agents is a promising avenue for sustainable management of S. oryzae. The intricate relationship between S. oryzae and its endosymbiotic bacterium, Sodalis pierantonius, offers potential targets for biocontrol strategies. Disrupting this symbiotic relationship could impair the pest's development and survival. Furthermore, the identification of specific genetic markers and the understanding of population structuring can facilitate the development of biocontrol agents tailored to specific genetic profiles of S. oryzae populations (Pal et al., 2021).

6.3 Potential of precision agriculture technologies

Precision agriculture technologies hold significant potential in the management of S. oryzae. The use of advanced genetic tools, such as microsatellite markers, allows for precise monitoring of pest populations and their genetic diversity. This information can be integrated into precision agriculture systems to implement targeted pest management strategies, reducing the reliance on broad-spectrum insecticides and minimizing environmental impact (Gbaye et al., 2019). Additionally, precision agriculture can enhance the effectiveness of biocontrol agents by ensuring their application is optimized based on real-time data on pest population dynamics (Costa et al., 2016).

6.4 Policy and international collaboration for sustainable management

Effective management of S. oryzae requires robust policy frameworks and international collaboration (Sharma and James, 2018). The widespread genetic diversity and lack of population structuring across regions, as observed in India, underscore the need for coordinated efforts in resistance management. Policies should promote the use of integrated pest management (IPM) strategies that combine genetic, biological, and technological approaches. International collaboration can facilitate the sharing of genetic data, resistance management strategies, and biocontrol agents, ensuring a unified approach to combating this global pest (Derbalah et al., 2021). By leveraging advances in genetic research, developing novel biocontrol agents, utilizing precision agriculture technologies, and fostering international collaboration, sustainable management of Sitophilus oryzae can be achieved, mitigating its impact on global food security (Hu et al., 2018).

Acknowledgments

The authors thank the two anonymous peer reviewers for their thorough review of this study and for their valuable suggestions for improvement.

Conflict of Interest Disclosure

The authors affirm that this research was conducted without any commercial or financial relationships that could be construed as a potential conflict of interest.

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