Sustainable bio control strategies for managing root grub, Basilepta fulvicorne jacoby (Coleoptera: chrysomelidae) in small cardamom

Introduction

Spices add flavors, aromas, and diversity to cuisines all over the world, making them an integral element of culinary traditions. These aromatic plant compounds not only enhance the taste of our food but also have significant historical and economic value. A range of many areas cultivate spice crops, which boost regional and international economies. However, these valuable goods are still at risk from plant parasitic nematodes, which can have a big impact on the spice industry's profitability (Pervez, 2018) [11] . In addition to being valued for their ability to enhance flavor, spices like pepper, ginger, turmeric, cloves, cardamom, and cinnamon are often recognized for their medicinal properties. Many nations and cultures have a long history of using spices to give local cuisine distinctive and delectable flavors. Spice crops have a significant economic impact. For millions of people, they are an essential source of income, especially in tropical and subtropical areas. The production and export of spices is a major industry in nations like Vietnam, Indonesia, India, and Sri Lanka, supporting both their total economic growth and agricultural development. Due to the growing interest in herbal medicines and traditional medicine, as well as the growing desire for unique and exotic flavors in the food and beverage business, this economic sector has been steadily rising. Cardamom, often called the "Queen of spices," is the small-seeded variety Elettaria cardamomum L. Maton. It ranks among the world's oldest and third-most valuable spices, after saffron and vanilla, and belongs to the Zingiberaceae family.

Indigenous to the evergreen forests of India's Western Ghats, the plant thrives with 1 300-4 000 mm of annual rainfall and temperatures of 10-31.5 °C in cool, shaded sites at 600-1 400 m elevation (Murugan et al., 2024) [12] . In the hilly districts of Kerala, Karnataka and Tamil Nadu it is typically cultivated as an under-storey crop beneath forest canopy. The long-term sustainability of India's cardamom sector depends on tackling issues such as drought, deforestation, pest outbreaks, chemical residues, irrigation management and market competition, while improving traceability and adopting innovative agronomic technologies. Recent yield gains must be converted into economic benefits for growers through effective market exploitation. Low productivity is often to biotic stresses, the most important being insect pests. Major pests include thrips (Sciothrips cardamomi Ramk.), shoot, panicle and capsule borer (Dichocrocis punctiferalis Guen.), shoot fly (Formosina flavipes Mall.), red spider mite (Tetranychus urticae Koch), coconut scale (Aspidiotus destructor Sign.), aphid (Pentalonia nigronervosa Coquerel), lacewing bug (Stephanitis typicus Dist.) and whitefly (Dialeurodes cardamomi David & Subr.). Among these, cardamom thrips and root grub cause the greatest damage, with uncontrolled infestations capable of reducing yields by up to 60%. Cardamom root grub (Basilepta fulvicorne, Chrysomelidae) is a serious threat to small-cardamom roots, typically causing 29-66% yield loss, with individual cases ranging from 10% to 70% depending on infestation intensity (Varadarasan, 1993) [4] . The larvae tunnel into roots, causing leaf yellowing and progressive shoot die-back. Although chemicals such as chlorpyrifos and phorate can reduce grub numbers, repeated use harms soil microbes that underpin soil health and disrupts the Western Ghats agroforestry systems where cardamom and other spices are cultivated. Consequently, these insecticides are now banned for cardamom production. Nematodes are widespread, unsegmented roundworms, and more than 30 families contain species that associate with insects and other invertebrates (Lacey et al.). These associations range from incidental (phoretic or commensal) to obligate parasitism and pathogenicity (Stock & Hunt, 2012) [3] . Entomopathogenic nematodes (EPNs) belonging to the genera Steinernema and Heterorhabditis are the most promising insect-associated biocontrol agents. These soil-dwelling worms combine traits of parasitoids and pathogens: they locate hosts using chemoreceptors, much like parasitoids, and they carry symbiotic bacteria that kill and digest the insect, acting as pathogens (Lacey et al.,). EPNs can effectively suppress several lepidopteran, dipteran and coleopteran pests of commercial crops and can be mass-produced in liquid fermenters. Their life cycle relies on a mutualistic relationship with an enteric bacterium that is essential for killing the host insect and converting its tissues into nutrients required for nematode growth and development.

Natural damage and symptoms of attack of root grub

Soil-dwelling insects such as white grubs, cutworms, termites and root grubs are responsible for 24-40% yield reductions in a range of crops including sugarcane, maize, arecanut, cardamom, groundnut, potato, banana, guava, turmeric, pulses, vegetables and grasses with overall direct losses ranging from 20% to 60%. The larvae of these root-feeding pests live in the rhizosphere, where they consume roots, leading to leaf yellowing, wilting and eventual plant death. Ongoing deforestation, depletion of soil organic carbon, suppression of microbial activity and loss of natural antagonists driven by human activity and geological changes have weakened the ecological balance, allowing these subterranean insects to spread more widely and pose a growing threat to agricultural production. Root grub is a serious threat to cardamom because its feeding on roots limits nutrient uptake, leading to leaf yellowing; the damage is especially severe in poorly shaded areas. The adult beetle is a small (4-6 mm) shiny insect that may be metallic blue, green or brown, with females larger than males. They are active on cardamom leaves in the early morning and late evening but do not feed on the crop; instead they graze on leaves of jackfruit, mango, guava and similar trees. Adult populations peak in March-April and again in August-September. Females lay 124-393 eggs in batches of 12-63 on dry cardamom leaves or mulch. The creamy-white larvae hatch, drop to the ground, locate the root zone and begin feeding. There are two larval periods: April-July and September-January. The larvae are short, stout, C-shaped and become mature in 45-60 days. Pupation occurs inside an earthen cocoon. The first generation (March-August) lasts 65-102 days, while the second generation (September-February) takes 73-111 days.

Material and Methods

Nematodes can be produced on a large scale and applied with ordinary farm equipment such as sprayers and drip-irrigation systems. For in-vivo multiplication, wax-moth (Galleria mellonella) larvae are inoculated with infective juveniles (IJs) of the chosen entomopathogenic nematode (EPN); after the larvae die, the IJs are recovered from the cadavers. Field trials were conducted from 2021 to 2023 in Santhanpara and Vandanmedu villages of Idukki district, Kerala. Two small-cardamom cultivars, 'Njallani' and 'Bhoomi', were planted in 3 m × 3 m plots at the end of June 2021, and all standard agronomic practices were followed except for root-grub control. Five treatments plus an untreated control (see Table 1) were arranged in a randomized block design with three replications. The EPN powder was mixed with water (5 g L⁻¹) and drenched at the base of each plant (≈5 L per plant, delivering 2 × 10⁵ -4 × 10⁵ IJs). The nematodes emerge from the cadavers in the soil, locate root grubs, and kill them, with applications timed for May-June and September-October. Root-grub counts were recorded from 25 plants per treatment one day before treatment and at 15, 30, and 45 days after application. Data were analyzed using the method of Gomez and Gomez (1998) [8] .

Results and Discussion:

The data in Tables 1 and2 show that Heterorhabditis indica gave the greatest reduction in root-grub numbers, cutting the population by 12.05% (2022) and 20% (2023) at 15 days after treatment, followed by H. bacteriophora (5.65% and 15%) and Steinernema carpocapsae (4.15% and 6.75%) relative to the untreated control. At 30 days, the reductions were 35% for H. indica, 25% for H. bacteriophora and 10% for S. carpocapsae. By 45 days the figures rose to 65%, 36% and 32% respectively, and after 60 days the corresponding decreases were 95%, 65.75% and 45.70% compared with the untreated plots. All differences were statistically significant. Our results align with Menti et al. (2000) [14] , who noted that the pathogenicity of entomopathogenic nematodes can vary markedly between and within species because infective juveniles (IJs) differ in their ability to locate and invade hosts. In our trials, Heterorhabditis indica IJs penetrated root-grub larvae more efficiently than H. bacteriophora or Steinernema carpocapsae, and the penetration rate reflected each isolate's infection strategy. This variation may stem from intrinsic

Conclusion

In conclusion the soil application of Heterorhabditis indica in May and September would significantly effective in reducing root grub population (more than 87%) within 60 days of application and recorded highest yield of 6.20 t/ha with accounted for 37.28% higher yield than untreated control. Biological control of root grub is a suitable alternative; Entomopathogenic fungi such as Beauveria bassiana (on beetles of root grub) and Metarhizium anisopliae (on grubs) are pathogenic to the pest, but controlling under field condition is not highly effective. Entomopathogenic nematode (EPN), a native isolate Heterorhabditis indica (ICAR-NBAIR EPN) is highly effective in controlling the pest under field conditions. The technology of mass production and application of EPN, which are user-friendly, in the field, has been standardized. Several farmer groups, NGOs, a commercial firm, and KVK were trained on the technology; more than 500 farmers used EPN in their fields, and root grub problem were effectively controlled in Kerala.

Acknowledgement

AcknowledgementThe authors are grateful to the Director, ICAR-National Bureau of Agricultural Insect Resources, Bengaluru for providing the technical support of my PhD research work. The authors are also thankful to Bio-micro Biotech for the financial assistance given to carry out the research work.

References

1. Abd-Elgawad MMM. Toxic secretions of Photorhabdus and their efficacy against crop insect pests. In: Biocontrol agents: entomopathogenic and slug parasitic nematodes. Wallingford (UK): CABI; 2017. p. 231-260.
2. Askary TH, Ahmad MJ. Entomopathogenic nematodes: mass production, formulation and application. In: Biocontrol agents: entomopathogenic and slug parasitic nematodes. Wallingford (UK): CABI; 2017. p. 261-286.
3. Dillman AR, Chaston JM, Adams BJ, Ciche TA, GoodrichBlair H, Stock SP, et al. An entomopathogenic nematode by any other name. PLoS Pathogens. 2012;8(3):e1002527.
4. Coleoptera). Journal of Plantation Crops. 1993;21:191-191.
5. Kaya HK, Gaugler R. Entomopathogenic nematodes. Annual Review of Entomology. 1993;38(1):181-206.
6. Bhagat RM, Gupta RBL, Yadava CPS. Field efficacy of two entomopathogenic fungal formulations against whitegrubs in Himachal Pradesh. Indian Journal of Entomology. 2003;65(1):76-81.
7. David H, Nandagopal V, Anathanarayana K. Recent studies on the control of white grub, Holotrichia serrata Fabr. infesting sugarcane. Journal of Soil Biology and Ecology. 1986;6(2):117-127.
8. Gomez KA, Gomez AA. Statistical procedures for agricultural research. New York: John Wiley & Sons; 1984.
9. Keller S. Use of fungi for pest control in sustainable agriculture. Phytoprotection. 1998;79(4):56-60.
10. Kulye MS, Pokharkar DS. Evaluation of two species of entomopathogenic fungi against white grub, Holotrichia consanguinea (Blanchard) infesting potato in Maharashtra, India. Journal of Biological Control. 2009;23(1):1-4.
11. Pervez R. Current status of plant parasitic nematodes and their management of major spice crops. Trends in Horticulture. 2018;1(2).
12. Murugan M, Kuruvilla A, Devi I, Sabu SS, Mathews N, Ashokkumar K. Governance and strategies to address constraints for the revival of the Indian small cardamom sector. Journal of Current Opinion in Crop Science. 2024;5(2):125-144.
13. Varadarasan S, Kumaresan D, Gopakumar B. Occurrence of root grub as a pest of cardamom (Elettaria cardamomum Maton.). Current Science. 1988;57(1).
14. Menti H, Wright D, Perry R. Infectivity of populations of the entomopathogenic nematodes Steinernema feltiae and Heterorhabditis megidis in relation to temperature, age and lipid content. Nematology. 2000;2(5):515-521.
15. Tomalak M. Infectivity of entomopathogenic nematodes to soil-dwelling developmental stages of the tree leaf beetles Altica quercetorum and Agelastica alni. Entomologia Experimentalis et Applicata. 2004;110(2):125-133.
16. Mwaitulo S, Haukeland S, Saethre MG, Laudisoit A, Maerere AP. First report of entomopathogenic nematodes from Tanzania and their virulence against larvae and adults of the banana weevil Cosmopolites sordidus (Coleoptera: Curculionidae). International Journal of Tropical Insect Science. 2011;31(3):154-161.