Sugarcane (Saccharum officinarum L.) is one of the world's most important crops, providing a primary source of sugar and bioethanol. It is extensively cultivated across tropical and subtropical regions, and its by-products are utilized in various industries, such as energy and animal feed (Oliveira et al., 2022). Despite its significant global importance, sugarcane cultivation faces substantial challenges due to various insect pests that can cause severe yield and quality losses.

The most damaging pests include borers, such as the sugarcane borer (Diatraea saccharalis), root borer (Diaprepes abbreviatus), and stalk borer (Chilo spp.). Sucking insects, including the sugarcane aphid (Melanaphis sacchari), whitefly (Aleurolobus barodensis), and mealybugs (Saccharicoccus sacchari), pose substantial threats by feeding directly on plant sap and transmitting viral diseases. Soil insects like white grubs (Phyllophaga spp.) and termites (Coptotermes spp.) further exacerbate crop losses by damaging roots and hindering plant establishment (Saini et al., 2019). The economic impact of these pests is significant, resulting in reduced yields, increased management costs, and decreased profitability for farmers.

Biological control methods have emerged as a sustainable alternative to chemical pesticides for managing sugarcane pests. These methods involve the use of natural enemies such as parasitoids, predators, and entomopathogens to control pest populations. Biological control offers several advantages over chemical pesticides, including reduced environmental impact, preservation of beneficial insects, and the potential for long-term pest management. For instance, the parasitoid Cotesia flavipes has been successfully used to control the sugarcane borer, Diatraea saccharalis, in Brazil, covering approximately 1.7 million hectares (Huang et al., 2018). Similarly, entomopathogenic fungi like Beauveria brongniartii have been commercialized for controlling white grubs.

The aim of this systematic review is to assess the advancements in biological control methods for managing sugarcane pests. The review will focus on three main approaches: classical biological control, augmentative biological control, and conservation biological control. Classical biological control involves the introduction and establishment of natural enemies from the pest's native range. Augmentative biological control includes the mass production and periodic release of natural enemies, while conservation biological control focuses on modifying the environment to enhance the effectiveness of existing natural enemies (Iqbal et al., 2021). By evaluating these methods, the review seeks to provide a comprehensive understanding of their efficacy, challenges, and future prospects in sustainable sugarcane pest management.

1 Major Insect Pests of Sugarcane

1.1 Borers (Scirpophaga excerptalis, Chilo infuscatellus, Chilo sacchariphagus indicus)

Sugarcane (Saccharum officinarum L.) is a vital crop grown globally for sugar production. However, its cultivation is significantly hampered by various insect pests, which cause substantial yield and sugar losses. The major insect pests of sugarcane can be categorized into borers, sucking pests, and soil insects.

Borers are among the most destructive pests of sugarcane, causing significant damage to the crop. The sugarcane top borer (Scirpophaga excerptalis), the sugarcane stem borer (Chilo infuscatellus), and the internode borer (Chilo sacchariphagus) indicus are the primary borer species affecting sugarcane (Singh and Lal, 2020). Biological control strategies, such as the use of parasitoids like Trichogramma chilonis and Cotesia flavipes, have shown promising results in managing these pests (Gulzar et al., 2022). Additionally, genetic engineering approaches, including the overexpression of cry proteins and proteinase inhibitors, have been explored to enhance resistance against these borers.

1.2 Sucking pests (Ceratovacuna lanigera, Melanaspis glomerata)

Sucking pests, such as the sugarcane woolly aphid (Ceratovacuna lanigera) and the sugarcane scale insect (Melanaspis glomerata), feed on the plant sap, leading to reduced vigor and yield. Biological control methods, including the use of natural predators and parasitoids, have been employed to manage these pests effectively. For instance, the introduction and conservation of natural enemies have been integral to the biological control programs in various regions (Shukla and Sharma, 2019). Moreover, integrated pest management (IPM) approaches that combine biological control with other methods, such as cultural and chemical controls, have been recommended for sustainable pest management.

1.3 Soil insects (Holotrichia serrata, Odontotermes spp.)

Soil insects, including the white grub (Holotrichia serrata) and termites (Odontotermes spp.), pose a significant threat to sugarcane by damaging the roots and underground parts of the plant. Biological control agents, such as entomopathogenic fungi (e.g., Beauveria brongniartii) and bacteria (e.g., Bacillus thuringiensis), have been developed and commercialized for controlling these soil pests (Singh et al., 2020). The use of these biocontrol agents has been shown to be effective in reducing pest populations and minimizing crop damage. The advances in biological control methods for managing sugarcane insect pests have provided sustainable and eco-friendly alternatives to chemical pesticides. The integration of biological control agents, genetic engineering, and IPM strategies holds great promise for the effective management of major insect pests in sugarcane cultivation.

2 Augmentative Biological Control

2.1 Mass rearing and release of natural enemies

Mass rearing and release of natural enemies have been pivotal in the success of biological control programs. In Brazil, for instance, the development of improved rearing techniques since the 1980s has positioned the country as a leader in BC for open fields. The mass production of natural enemies such as Trichogramma galloi and Cotesia flavipes has enabled the treatment of millions of hectares of sugarcane, significantly reducing pest populations and minimizing the reliance on chemical pesticides (Sharma et al., 2020). Similarly, large-scale field experiments in sugarcane fields have demonstrated the effectiveness of inundative releases of Trichogramma species against lepidopteran borers, achieving comparable yields and economic benefits to conventional chemical control methods (Srikanth, 2016).

2.2 Key agents and their targets

Several natural enemies have been identified as key agents in the biological control of sugarcane pests. Trichogramma chilonis, for example, has been extensively used in India for the control of various borers, with mass multiplication and field evaluation practices dating back to the early 20th century (Sharma et al., 2020). Other notable agents include Cotesia flavipes, which has been successfully used in Brazil to control the sugarcane borer, Diatraea saccharalis, covering extensive areas and demonstrating high efficiency (Maneerat et al., 2017). Additionally, entomopathogens such as Beauveria brongniartii and Bacillus thuringiensis have shown promise in controlling pests like the white grub and other sugarcane soil-dwelling insects (Srikanth, 2016).

2.3 Field efficacy and economic benefits

The field efficacy of augmentative biological control methods has been well-documented. Studies have shown that fields treated with biocontrol agents exhibit significantly lower pest incidence compared to untreated fields, leading to higher yields and better economic returns. In China, the use of dominant natural enemies has not only increased yield but also reduced environmental pollution and production costs, highlighting the socio-economic benefits of BC. Furthermore, the integration of habitat augmentation strategies, such as the inclusion of lac cultivation (Figure 1), has been proposed to enhance the sustainability and effectiveness of BC by providing additional resources for natural enemies (Parra and Coelho, 2022). In conclusion, augmentative biological control methods offer a sustainable and economically viable alternative to chemical pesticides for managing sugarcane pests. The mass rearing and release of natural enemies, identification of key agents, and field efficacy studies underscore the potential of these methods to improve pest management practices and promote environmental sustainability.

Figure 1 shows the biological control process of Murraya paniculata using Tamarixia radiata. The egg laying cage is a place where six jasmine plants and 300 adult Murraya paniculata are placed together for 7 days to lay eggs; Plant allocation involves dividing egg bearing plants into two groups, with 30% allocated for adult development and 70% allocated for development to the 4-5 instar nymph stage. During the developmental stage, 30% of plants develop their eggs into nymphs and then into adults, which are used to continue feeding and cycling; 70% of plants have eggs that develop into 4-5 instar nymphs and are used for parasitism. The parasitic process involves placing 12 plants with 4-5 instar nymphs into cages, and releasing 1 Asian citrus psyllid per 20 nymphs. Remove adult Murraya paniculata after 24 hours of parasitism. Cut off branches with parasitic nymphs 9 days after parasitism. Parasitic bee collection and utilization involves placing branches into a dark collection box with a lamp and a 600 mL bottle at the top to collect adult insects. The collected adults are divided into two parts, 17% for continued feeding and 83% for wild release. The release location is located in commercial orchards or urban areas where Jiulixiang is used as an ornamental plant. Adults are placed in containers containing food (mixed with honey and pollen in a 1:1 ratio) and transported to the release site through an insulated box at a temperature of approximately 18 °C. This process helps to control the population of Murraya paniculata, thereby suppressing the spread of citrus yellow dragon disease.

3 Case Studies

3.1 Successful classical biological control

Traditional pest control methods, such as chemical pesticides, pose environmental hazards and can disrupt beneficial insect populations. Consequently, biological control (BC) methods have emerged as sustainable alternatives, offering eco-friendly solutions to manage sugarcane pests effectively. Biological control involves the use of natural enemies, such as parasitoids, predators, and pathogens, to suppress pest populations. This approach has been successfully implemented in various regions, demonstrating its potential to enhance pest management in sugarcane cultivation.

Classical biological control involves the introduction and establishment of natural enemies from the pest's native range to control invasive pests. In India, classical biological control has a long history, with significant successes in managing sugarcane pests. For instance, the introduction and colonization of parasitoids such as Trichogramma chilonis have been practiced since the early 20th century, leading to effective control of various borers and sucking pests (Parra et al., 2022). Similarly, in Brazil, the use of Cotesia flavipes, an exotic parasitoid, has been instrumental in controlling the sugarcane borer, Diatraea saccharalis, across millions of hectares (Figure 2) (Aya et al., 2017).

Figure 2 shows the different developmental stages of agricultural pests: the image of larva A shows that the larva is located inside the plant stem and may cause damage to the crop. The adult B image displays the adult and larval stages, indicating the life cycle of the pest. The image of pupa C and the hatching of adults from the pupa demonstrate the developmental process of the pest. These pests can be monitored through sex pheromone traps, and mechanical control and biological control are also effective management methods.

3.2 Augmentative biological control successes

Augmentative biological control involves the periodic release of large numbers of natural enemies to suppress pest populations. This method has shown promising results in sugarcane fields. Large-scale field experiments conducted between 2015 and 2019 demonstrated the effectiveness of inundative releases of Trichogramma spp. against lepidopteran borers, resulting in significantly lower pest incidence and comparable yields to chemical control methods (Maneerat et al., 2017). Additionally, the use of Trichogramma chilonis and Tetrastichus howardi in Tamil Nadu, India, has successfully managed internode borers and other borer pests, contributing to yield improvement (Behera and Mishra, 2020).

3.3 Conservation biological control impact

Conservation biological control focuses on preserving and enhancing the natural enemy populations already present in the ecosystem. This approach has been integrated into pest management strategies in various regions. In China, integrated pest management (IPM) programs emphasize the protection and utilization of natural enemies, alongside other control methods, to maintain pest populations below economic thresholds (Roy et al., 2019). Furthermore, the use of entomopathogenic fungi, such as Metarhizium anisopliae, has been effective in controlling pests like Mahanarva fimbriolata in sugarcane fields, highlighting the potential of conservation biological control in sustainable pest management (Huang et al., 2018).

Biological control methods have made significant strides in managing sugarcane pests, offering sustainable and environmentally friendly alternatives to chemical pesticides. The success of classical, augmentative, and conservation biological control strategies underscores the importance of continued research and implementation of these methods to ensure the long-term health and productivity of sugarcane crops.

4 Challenges and Limitations

The genetic complexity of sugarcane makes conventional breeding for pest resistance a challenging task. The lack of resistant genes in the sugarcane genome further complicates efforts to develop pest-resistant varieties through traditional breeding methods. Effective pest management in sugarcane requires the integration of various control methods, including biological, chemical, and cultural practices. Coordinating these methods to create an environment conducive to sugarcane growth while suppressing pest populations is a significant challenge (Bielza et al., 2020).

The use of genetically engineered crops expressing insecticidal proteins, such as Bt proteins, has shown promise in controlling pests like the sugarcane borer. However, the evolution of insect resistance to these proteins poses a major limitation, necessitating strategies like high-dose expression and refuge areas to delay resistance development. Implementing biological control methods can be economically and practically challenging (Donga et al., 2020). For instance, the mass production and field application of natural enemies or entomopathogens require substantial investment and infrastructure. Additionally, the effectiveness of these methods can be influenced by environmental factors and the availability of labor for practices like mechanical removal of pests. By addressing these challenges and limitations, and to identify potential areas for future research and development (Carbonari et al., 2020).

Biological control methods are considered environmentally friendly, yet they must be managed carefully. Impact on Natural Enemy Populations: Chemical insecticides often disrupt beneficial insect populations: Insecticide sprays for Melanaphis sacchari control reduce natural enemy populations and impact their effectiveness (Lytle and Huseth, 2021). The use of biological insecticides like Metarhizium anisopliae is less harmful to non-target species (Oliveira et al., 2022). Sustainable Habitat Management: Conservation biological control through habitat engineering offers sustainable pest management: Strategic integration of lac cultivation provides natural reservoirs of parasitoids and enhances pest control (Roy et al., 2019). Overcoming technical challenges, ensuring economic viability, and managing environmental impacts are crucial for the sustainable expansion of biological control methods in sugarcane pest management.

5 Future Directions

5.1 Identify areas needing further research in sugarcane pest management

Despite the progress in biological control, several areas require further research to enhance the effectiveness and sustainability of these methods (Aya et al., 2019). For instance, the development of improved rearing techniques for natural enemies, such as Trichogramma spp., has been crucial in Brazil's success in BC (Javal et al., 2019). However, there is a need for more extensive bioecological studies to optimize mass rearing and field application of these agents (Verma et al., 2022). Additionally, understanding the interactions between different pest management strategies, such as the integration of cultural, physical, and biological controls, is essential for developing comprehensive integrated pest management (IPM) programs (Iqbal et al., 2021).

5.2 Emerging technologies to aid biological control

Advancements in genetic engineering and biotechnology offer promising avenues for enhancing biological control in sugarcane. Techniques such as host-induced gene silencing (HIGS) and CRISPR/Cas9 have shown potential in developing insect-resistant transgenic sugarcane varieties (Krishna et al., 2023). These technologies can complement traditional BC methods by reducing the reliance on chemical pesticides and enhancing the crop's inherent resistance to pests. Moreover, the application of optimal control theory and dynamic systems modeling can help in formulating effective pest control strategies through the introduction of natural enemies (Dias et al., 2021).

5.3 The potential impact of climate change on biological control agents

Climate change poses a significant threat to the efficacy of biological control agents. Changes in temperature, humidity, and precipitation patterns can affect the life cycles, distribution, and interactions of both pests and their natural enemies. For example, the effectiveness of control methods for pests like Eldana saccharina in South Africa is influenced by temperature variations (Donga et al., 2020). Therefore, it is crucial to study the potential impacts of climate change on BC agents and develop adaptive strategies to ensure their continued effectiveness under changing environmental conditions (Silva et al., 2019).

The advances in biological control methods for managing sugarcane insects have shown promising results in reducing pest populations and minimizing the use of chemical pesticides (Cherubin et al., 2021). However, further research is needed to optimize these methods, integrate emerging technologies, and address the challenges posed by climate change. By focusing on these future directions, we can develop more sustainable and effective pest management strategies for sugarcane cultivation (Krishna et al., 2023).

6 Concluding Remarks

6.1 Key insights for the integration of biological control methods

This systematic review aims to provide a comprehensive overview of the advances in biological control methods for managing sugarcane insects. By synthesizing findings from various studies, seeking to highlight key insights for the integration of biocontrol methods, discuss their implications for sustainable pest management, and offer recommendations for researchers and policymakers. The integration of biological control methods into sugarcane pest management has shown significant promise. Key insights include the importance of mass rearing and field release of natural enemies, such as parasitoids and entomopathogens, which have demonstrated effectiveness in reducing pest populations and improving crop yields. Additionally, the combination of biocontrol with genetic engineering and IPM strategies can enhance the overall efficacy of pest management programs.

6.2 Implications for sustainable pest management

Biological control methods offer a sustainable alternative to chemical pesticides, reducing environmental risks and preserving beneficial insect populations. The successful implementation of biocontrol can lead to long-term pest suppression, reduced pesticide use, and improved crop health and productivity. Moreover, the adoption of biocontrol practices aligns with the principles of sustainable agriculture, promoting ecological balance and resilience in agroecosystems.

6.3 Recommendations for researchers and policymakers

To further advance the field of biological control in sugarcane pest management, researchers should focus on enhancing mass rearing techniques, Developing efficient and cost-effective methods for mass rearing natural enemies to ensure a steady supply for field releases. Exploring genetic and molecular tools and investigating the potential of genetic engineering and molecular biology to enhance the effectiveness of biocontrol agents and develop pest-resistant sugarcane varieties. Promoting integrated pest management, encouraging the adoption of IPM strategies that combine biocontrol with other pest management practices to achieve comprehensive and sustainable pest control. Fostering collaboration between research institutions, government agencies, and the sugar industry to support coordinated research efforts, technology transfer, and the promotion of biocontrol technologies. By addressing these recommendations, researchers and policymakers can contribute to the development of effective and sustainable pest management strategies for sugarcane, ensuring the long-term viability and productivity of this essential crop.

Acknowledgments

We would like to express our gratitude to the Director of the Institute of Life Sciences at Ji Yang College of Zhejiang A&F University for reading this paper and providing valuable feedback.

Funding

This project was funded by the Institute of Life Sciences, Ji Yang College of Zhejiang A&F University.

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