Efficacy of Endophytic Fungi in the Management of Spoladea recurvalis (Lepidoptera: Crambidae) on Amaranth (Amaranthus dubius)

Abstract

Amaranth is a Traditional African Vegetable (TAV) that in recent years has gained global popularity due to its exceptional nutritional, medicinal and economic attributes. However, its production is significantly limited by insect pest infestations, mainly lepidopteran defoliators. Spoladea recurvalis, commonly known as Hawaiian beet webworm has been reported as the major pest that feeds voraciously on the leaves leading to substantial yield losses of up to 100% under severe pest infestation. Chemical control remains a widely used method for the management of S. recurvalis. The use of fungal endophytes has emerged as a promising, sustainable and eco-friendly alternative to chemical pesticides in the management of insect pests. Therefore, this study evaluated the efficacy of selected 15 fungal isolates to endophytically colonize Amaranthus dubius host plant. Only two fungal isolates Hypocrea lixii F3ST1 and Trichoderma asperellum M2RT4 were found to be endophytic to A. dubius with varied colonization rates among them. The results revealed that both endophytes successfully colonized over 90% of all the examined plant tissues (root, stem and leaves). The two fungal isolates were further evaluated for their endophytic persistence, effect on host plant growth promotion and insecticidal activity against S. recurvalis life cycle and F1 progeny. Also, the behavioral and chemical mechanism through which the presence of the most potent endophytes H. lixii F3ST1 and T. asperellum M2RT4 within amaranth plants influence S. recurvalis host selection and herbivory were investigated. Both endophytes persisted in the host plant throughout the four-week assessment period exhibiting varying colonization rates influenced by significant interaction between time, fungal isolates and plant parts. Although T. asperellum M2RT4 outperformed H. lixii F3ST1 in the weekly assessment on plant growth promotion, the two endophytes significantly improved plant height, the number of leaves, leaf length and leaf width. Trichoderma asperellum M2RT4 significantly enhanced dry shoot biomass when compared with H. lixii F3ST1 and the control. Further, both endophytes significantly reduced number of egg masses laid, egg hatchability, increased larval mortality, reduce pupae formation, adult emergence and reduced survival/longevity of F1 progeny. Amaranthus dubius plants endophytically colonized by H. lixii F3ST1 significantly recorded the lowest number of egg masses (3.75 ± 1.11) resulting in 5% and 49.8% reductions, followed by T. asperellum M2RT4 (36.75 ± 3.77) compared to (73.25 ± 5.14) in the control. Upon egg hatching, H. lixii F3ST1 endophytically colonized plants significantly recorded the lowest number of larvae (13.75 ± 1.75) followed by T. asperellum M2RT4 (94.5 ± 11.66) compared to 196.5 ± 22.14 in the control. There was no significant difference in larval mortality by H. lixii F3ST1 endophytically colonized (40 ± 0.82%) and T. asperellum M2RT4 plants (42 ± 0.74%) compared to (2.91 ± 0.29%) in the control. Fewer pupae were obtained in H. lixii F3ST1 (3.75 ± 1.75) followed T. asperellum M2RT4 (44.5 ± 1.94) compared to 76.25 ± 1.43 in the control. Besides, adult emergence of S. recurvalis varied significantly between the fungal isolates with the lowest number of moths emerging from H. lixii F3ST1 endophytically colonized plants (3.25 ± 0.25) followed by T. asperellum M2RT4 (38.5 ± 1.19) compared to the control (66.5 ± 2.25). Furthermore, the two endophytes H. lixii F3ST1 and T. asperellum M2RT4 significantly reduced the survival of S. recurvalis F1 progenies. The behavioral bioassay using the Y-tube olfactometer revealed that S. recurvalis showed a preference for non-colonized amaranth plants over those colonized by both endophytes. Nevertheless, the findings showed that S. recurvalis moths were not attracted to either infested non-colonized or infested endophyte-colonized amaranth plants. Gas chromatography-mass spectrometry (GC-MS) analysis of volatiles emitted from non-inoculated, inoculated, non-inoculated infested, and inoculated infested amaranth plants colonized by H. lixii F3ST1 and T. asperellum M2RT4 revealed the presence of 80 and 74 volatile organic compounds (VOCs), respectively. Similarity percentage analysis highlighted the major compounds contributing to the differences observed among treatments. In H. lixii F3ST1-colonized plants, key discriminating VOCs included (Z)-3-Hexenyl acetate, pentadecane, α-Cedrene, o-Xylene, and (E)-β-Ocimene while for T. asperellum M2RT4-colonized plants, predominant differentiating compounds were Germacrene D, (Z)-3-hexenol, 1,3-Dimethylbenzene, Tetradecane, and 2,4,4-Trimethyl-1-pentene. The distinct VOC profiles linked to their colonization and treatment status suggest that these endophytes may influence plant defense signaling pathways, further contributing to their biocontrol efficacy for the management of S. recurvalis. Hence, providing insights for their integration into environmentally friendly pest management strategies in amaranth cropping systems. However, further studies are warranted to assess the effects of the key identified synthetic compounds on the pest and validate the results under field conditions.