Rice is a staple food for more than half of the world's population, providing a primary source of nutrition and energy to billions of people. Its cultivation is of paramount importance to global food security. However, rice production is frequently threatened by a variety of pests, including insects like planthoppers, stem borers, and leaf folders, which can cause significant yield losses (Peng et al., 2020). The management of these pests is a critical aspect of rice farming and has traditionally relied on chemical pesticides. However, the use of such chemicals has raised concerns due to their environmental impact, effects on non-target organisms, and the development of pest resistance.

Rice pests pose a significant challenge to agricultural productivity. The rice planthopper, for example, is a major pest that not only damages the rice plants directly but also acts as a vector for plant diseases (Peng et al., 2020). The control of these pests is essential to maintain rice yields and ensure food security.

Biological control methods offer an environmentally friendly alternative to chemical pesticides. These methods involve the use of living organisms to suppress pest populations. Entomopathogenic fungi are a group of naturally occurring fungi that infect and kill insects. They have been recognized as promising biological control agents due to their specificity to target pests and minimal impact on non-target species, including humans and beneficial insects. These fungi can also play additional ecological roles, such as promoting plant growth and antagonizing plant pathogens (Vega et al., 2009; Jaber and Ownley, 2018).

This study attempts to provide a comprehensive overview of the current research status and case analysis in this field to demonstrate the application and effectiveness of these fungi, emphasizing the potential of insect pathogenic fungi for sustainable pest management in rice production, particularly their impact on pest populations, non target organisms, and overall plant health. The aim is to understand the practical significance of using insect pathogenic fungi and identify areas that require further research to optimize their use in integrated pest management strategies.

1 Types and Effects of Rice Pests

1.1 Major pest species

Rice crops are susceptible to a variety of pests, among which stem borers, leafhoppers, and planthoppers are particularly detrimental. These pests not only cause direct damage to the plants but also act as vectors for disease, further exacerbating their impact on rice cultivation.

Stem borers are a group of insects whose larvae bore into the stems of rice plants, causing dead hearts and whiteheads which lead to significant yield losses. Leafhoppers and planthoppers, on the other hand, are sap-sucking insects that can cause damage through feeding and also by transmitting viruses such as the rice ragged stunt virus and rice grassy stunt virus (Vega et al., 2009; Peng et al., 2020; Wakil et al., 2021). The life cycles and behaviors of these pests are closely linked to environmental conditions, and understanding these factors is crucial for developing effective control strategies.

1.2 Impact on crop yields and quality

The presence of pests like stem borers, leafhoppers, and planthoppers can lead to substantial quantitative and qualitative impacts on rice crops. Infestations can result in yield losses due to reduced grain filling and increased rates of unfilled or partially filled grains (Budiarti and Nuryanti, 2022). Moreover, the quality of the rice grains can be compromised, affecting marketability and price.

Economic repercussions of pest infestations are significant, as they can lead to increased costs for pest management and reduced income due to lower yields and quality (Figure 1). The use of chemical pesticides has been the traditional method for controlling these pests, but concerns over environmental and human health impacts have led to a search for alternative strategies, such as the use of entomopathogenic fungi (Wakil et al., 2021).

In the figure, a comparison of caged and non-caged plots reveals the actual effectiveness of different pest management methods. By releasing IPM adults, these experiments aim to reduce reliance on chemical pesticides while maximizing pest control. The use of entomopathogenic fungi as biological control agents is a promising alternative strategy. This method uses fungi to infect and kill pests, reducing pest populations without negatively impacting the environment and human health.

Entomopathogenic fungi, such as Metarhizium anisopliae, have shown potential as biological control agents against rice pests. Studies have demonstrated that these fungi can suppress populations of rice planthoppers effectively, with control efficiency comparable to chemical treatments and without significant effects on the rice microbiota (Peng et al., 2020). This suggests that entomopathogenic fungi could be integrated into pest management programs to reduce reliance on chemical pesticides, thereby mitigating their negative impacts while maintaining crop yields and quality.

2 Biological Characteristics and Pest Control Mechanisms of Entomopathogenic Fungi

2.1 Biological characteristics

Entomopathogenic fungi are a diverse group of organisms that play a crucial role in the biological control of insect pests. These fungi belong to various taxa, with the majority being from the phyla Ascomycota and Basidiomycota, including prominent genera such as Metarhizium, Beauveria, and Aspergillus (Afandhi et al., 2020; Budiarti and Nuryanti, 2022; Mangais et al., 2023). They exhibit a complex life cycle that involves the production of infective propagules, which can be conidia or blastospores, that adhere to the insect host's cuticle (Figure 2) (Sharma et al., 2020; Mathulwe et al., 2022). The reproductive mechanisms of these fungi are adapted to ensure the widespread distribution and infection of their insect hosts, with some species capable of both sexual and asexual reproduction (Sharma et al., 2020).

The picture shows the different states of insects after fungal infection, from which different fungi can be observed to form hyphae and spores on the surface of the insect body. The infection performance of each fungus on host insects varies, for example, Beauveria bassiana usually forms a white hyphal layer on the surface of the host insect, while Metarhizium anisopliae forms a green spore layer. Through this study, it can be seen that insect pathogenic fungi play an important role in biological control. These fungi can effectively infect and kill pests, reduce dependence on chemical insecticides, and thus protect the environment and human health. These findings provide scientific basis for further promoting and applying biological control strategies, and also demonstrate the potential and advantages of using these fungi in actual agricultural production.

Classification and taxonomy of these fungi are based on morphological characteristics, such as the shape and color of mycelia and conidia, as well as genetic markers (Afandhi et al., 2020; Budiarti and Nuryanti, 2022). Recent studies have also highlighted the role of entomopathogenic fungi as endophytes, plant growth promoters, and antagonists of plant pathogens, indicating their multifaceted ecological roles (Vega et al., 2009; Sharma et al., 2020).

2.2 Mechanism of pest control

Entomopathogenic fungi infect and kill pest insects through a series of well-coordinated mechanisms. The infection process begins with the attachment of fungal spores to the insect cuticle, followed by germination and penetration of the cuticle using mechanical pressure and enzymatic degradation (Dar et al., 2017; Sharma et al., 2020). Once inside the host, the fungi proliferate, overcoming the host's immune defenses, and ultimately leading to the death of the insect (Sharma et al., 2020).

These fungi have specific adaptations that enable them to target rice pests effectively. For instance, Metarhizium anisopliae has been shown to suppress rice planthopper populations significantly without affecting the rice microbiota, demonstrating its specificity and potential as a biocontrol agent in rice ecosystems (Peng et al., 2020). The ability of these fungi to persist on rice plants for a considerable period after application and their negligible impact on non-target microorganisms, such as the indigenous microbial communities of the rice phyllosphere, further underscore their suitability for pest control in rice cultivation (Peng et al., 2020).

In summary, entomopathogenic fungi possess unique biological characteristics and mechanisms of pest control that make them effective agents for managing insect pests in rice fields. Their classification, life cycle, reproductive strategies, and specific adaptations for infecting and killing rice pests are critical for developing sustainable pest management strategies.

3 Application of Entomopathogenic Fungi in Rice Pest Control

3.1 Case study reviews

Entomopathogenic fungi have been increasingly recognized for their potential in controlling rice pests. A notable example is the fungal strain Metarhizium anisopliae CQMa421, which has demonstrated a control efficiency of over 60% against rice planthoppers, comparable to chemical treatments, while maintaining the rice microbiota intact (Peng et al., 2020). Similarly, different isolates of Beauveria bassiana and Metarhizium anisopliae have shown high efficacy against stored-grain beetle species, suggesting their potential for broader applications in pest management (Wakil et al., 2021). In another study, Beauveria bassiana, Metarhizium anisopliae, and Isaria fumosorosea were tested against the stored-grain pest Sitophilus oryzae, with varying mortality rates influenced by concentration and application method, indicating the importance of optimizing application strategies (Kavallieratos et al., 2014).

3.2 Effectiveness analysis

The effectiveness of entomopathogenic fungi varies across different environmental conditions and pest species. For instance, Metarhizium anisopliae was found to be highly virulent against Trogoderma granarium in stored grains, with mortality rates up to 98.33% (Iqbal et al., 2021). Beauveria bassiana has also been effective in controlling storage insect pests in green gram seeds, with a high mortality rate and no adverse effects on seed quality (Pande and Mishra, 2018). These findings underscore the potential of entomopathogenic fungi as a sustainable alternative to chemical pesticides, with the ability to adapt to various environmental conditions and target a wide range of pest species.

3.3 Methodologies of application

Different application techniques have been explored to maximize the efficacy of entomopathogenic fungi. For example, 'dry' conidia of Metarhizium anisopliae strain V275 were more effective than 'wet' conidia in controlling adult Culicoides biting midges, suggesting that application form can significantly influence outcomes (Ansari et al., 2011). The application of entomopathogenic fungi on surfaces where pests rest, such as manure or leaf litter, has been shown to be a promising strategy. Additionally, the study of wild fungal strains against stored product beetle pests has highlighted the potential of untested strains and the importance of specificity in application (Mantzoukas et al., 2023).

In conclusion, the application of entomopathogenic fungi in rice pest control presents a promising avenue for sustainable agriculture. The methodologies of application, including spore spraying and baiting, are crucial for achieving high efficacy rates. The data suggests that these fungi can be effectively used in large-scale agricultural settings, offering an eco-friendly alternative to chemical pesticides (Kavallieratos et al., 2014; Pande and Mishra, 2018; Peng et al., 2020; Mantzoukas et al., 2023).

4 Assessment of Effectiveness and Challenges

4.1 Success rates and limitations

Entomopathogenic fungi have shown promise as biological control agents in rice pest management. Studies have demonstrated that Metarhizium anisopliae can suppress rice planthopper populations effectively, with control efficiency exceeding 60% seven days post-application, comparable to chemical treatments (Peng et al., 2020). The persistence of this fungal agent on rice plants was observed for approximately 14 days, although a decreasing trend over time was noted (Peng et al., 2020). Similarly, the combination of Trichoderma asperellum with Beauveria bassiana and Metarhizium anisopliae has been reported to significantly increase tiller numbers and reduce the intensity of rice white stemborer attack symptoms (Sutarman et al., 2023).

However, the success of entomopathogenic fungi can be limited by various factors. The existence of these fungi in the rhizosphere can be influenced by the history of land use and insecticide applications, which may affect their prevalence and efficacy (Noerfitryani and Hamzah, 2017; Budiarti and Nuryanti, 2022). Additionally, the mass production of these fungi for commercial application faces challenges, such as contamination and the suitability of substrates, which can impact the availability of resilient infective propagules (Mathulwe et al., 2022).

4.2 Environmental and economic considerations

The application of entomopathogenic fungi has been shown to have minimal impact on non-target species, including the rice microbiota. Studies have found no significant changes in the microbial communities of the rice phyllosphere after the application of Metarhizium anisopliae, suggesting that indigenous microbial communities may adapt to fungal insecticide application (Peng et al., 2020). This indicates a potential advantage of fungal applications over chemical pesticides in terms of ecosystem health.

In terms of cost-effectiveness, while the initial development and production of entomopathogenic fungi may require investment, their use could reduce the reliance on chemical pesticides, which have been associated with negative effects on human health and environmental pollution (Mathulwe et al., 2022). Furthermore, the use of these fungi as part of integrated pest management strategies can contribute to sustainable agriculture by maintaining higher diversity and species richness in rice fields (Afandhi et al., 2020).

In conclusion, entomopathogenic fungi offer a promising alternative to chemical pesticides for rice pest control. Their effectiveness, coupled with their minimal impact on non-target species and potential cost savings, underscores their value in sustainable agriculture. However, challenges such as production limitations and environmental factors must be addressed to optimize their use in the field.

5 Summary and Outlook

The utilization of entomopathogenic fungi, such as Metarhizium anisopliae, has been shown to effectively suppress populations of rice planthoppers, a major pest in rice cultivation, without adversely affecting the rice microbiota. These fungi have demonstrated control efficiencies comparable to chemical treatments and have been observed to persist on rice plants for approximately two weeks post-application. The microbial communities within the rice phyllosphere appear to adapt to the application of these fungal biocontrol agents, maintaining their richness and diversity. This suggests that entomopathogenic fungi offer a promising alternative to chemical pesticides, with the added benefit of being environmentally benign.

Biological control methods, such as the application of entomopathogenic fungi, are gaining traction as essential components of sustainable agriculture. They play a significant role in reducing the reliance on chemical pesticides, which are known to have negative impacts on human health, beneficial organisms, and the environment. The integration of these fungi into pest management strategies aligns with the global drive towards more sustainable and eco-friendly agricultural practices. Furthermore, these fungi not only control pests but also offer additional benefits such as plant growth promotion and antagonism against plant pathogens, thereby contributing to the overall health and productivity of crops.

The potential for genetic enhancement of entomopathogenic fungi is a promising avenue for increasing their efficacy and resilience. Advances in genomics and molecular biology have provided insights into the genes that contribute to fungal virulence and host interactions, paving the way for the development of genetically improved strains. Additionally, integrating these fungi with other pest control methods could lead to synergistic effects, enhancing their effectiveness and sustainability as biocontrol agents. Research into the endophytic capabilities of these fungi suggests they could be used for dual biological control of both insect pests and plant pathogens, offering a multifaceted approach to crop protection. As the understanding of the complex interactions between entomopathogenic fungi, plants, and pests deepens, the potential for these organisms to revolutionize integrated pest management and contribute to sustainable agriculture becomes increasingly apparent.

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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