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Unveiling the biocontrol potential of Harmonia axyridis: functional response to eggs of S. litura and S. frugiperda

Published online by Cambridge University Press:  09 October 2025

Arzlan Abbas
Affiliation:
College of Plant Protection, Jilin Agricultural University, Changchun, China
Ayesha Iftikhar
Affiliation:
Entomological Research Institute, Ayub Agricultural Research Institute, Faisalabad, PB, Pakistan
Muhammad Yasir Ali
Affiliation:
Guangdong Key Laboratory of Animal Conservation and Resource Utilization, Guangdong Public Laboratory of Wild Animal Conservation and Utilization, Institute of Zoology, Guangdong Academy of Sciences, Guangzhou, China MARA-CABI Joint Laboratory for Bio-safety, Institute of Plant Protection, Chinese Academy of Agricultural Sciences, Beijing, China
Hasnain Ali
Affiliation:
College of Plant Protection, Nanjing Agricultural University, Nanjing, China
Sarah I. Othman
Affiliation:
Department of Biology, College of Science, Princess Nourah bint Abdulrahman University, Riyadh, Saudi Arabia
Rasha E. Abo-Eleneen
Affiliation:
Department of Zoology, Faculty of Science, Bnei-Suef University, Bnei-Suef, Egypt
Faisal Hafeez
Affiliation:
Entomological Research Institute, Ayub Agricultural Research Institute, Faisalabad, PB, Pakistan Wheat Research Institute, Ayub Agricultural Research Institute, Faisalabad, PB, Pakistan
Chen Ri Zhao*
Affiliation:
College of Plant Protection, Jilin Agricultural University, Changchun, China
*
Corresponding author: Chen Ri Zhao; Email: rizhaochen@jlau.edu.cn

Abstract

Understanding predator-prey dynamics is pivotal for advancing sustainable pest management strategies. This study examined the functional response of Harmonia axyridis across six developmental stages when preying upon the eggs of two destructive lepidopteran pests including Spodoptera litura and Spodoptera frugiperda. Using logistic regression and Holling’s disc equation, a clear Type II functional response was observed across all stages except first instars, indicating a density-dependent predation pattern constrained by handling time at higher prey densities. Adult females consistently emerged as the most potent predators, demonstrating the highest effectiveness of predation (1.591 on S. litura; 1.736 on S. frugiperda) and maximum predation rates (113.7 and 120.9 eggs, respectively). Adult males and fourth instar larvae also showed high predation capacities, with maximum consumption nearing 99 and 95 eggs. In contrast, first instars exhibited minimal predatory potential (effectiveness <0.017; maximum consumption <10 eggs), highlighting the critical role of developmental maturity in predation performance. Notably, predation on S. frugiperda eggs slightly surpassed that on S. litura, suggesting host-specific traits may modulate predator efficiency. The functional response curves confirmed a classic decelerating intake rate at high prey densities, characteristic of Type II predators. These findings affirm the high consumptive potential of H. axyridis, particularly adult females, as efficient natural enemies against Spodoptera spp. eggs, and provide actionable insights for their integration into targeted, stage-specific biological control programs.

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Research Paper
Copyright
© The Author(s), 2025. Published by Cambridge University Press.

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Footnotes

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These authors contributed equally to this paper.

References

Abbas, A, Ullah, F, Hafeez, M, Han, X, Dara, MZN, Gul, H and Zhao, CR (2022) Biological control of fall armyworm, Spodoptera frugiperda. Agronomy 12(11), 2704. https://doi.org/10.3390/agronomy12112704CrossRefGoogle Scholar
Abbas, A, Wei‐Bo, Q, Hafeez, F, Hasnain, A, Shoukat, K, Ali, J, Xiao, F, Liu, JL, Ghramh, HA, Khan, KA, Ullah, F and Chen, RZ (2025) Unveiling the feeding response of Spodoptera litura to natural host and artificial diet. Entomologia Experimentalis Et Applicata 173(3), 218231. https://doi.org/10.1111/eea.13537CrossRefGoogle Scholar
Abdel‐Salam, A and Abdel‐Baky, N (2001) Life table and biological studies of Harmonia axyridis Pallas (Col., Coccinellidae) reared on the grain moth eggs of Sitotroga cerealella Olivier (Lep., Gelechiidae). Journal of Applied Entomology 125(8), 455462. https://doi.org/10.1046/j.1439-0418.2001.00574.xCrossRefGoogle Scholar
Atwal, A and Dhaliwal, G (2009) Agricultural Pests of South East Asia and Their Management. Ludhiana. In: College of agriculture. New Delhi: India: Kalyani Publishers.Google Scholar
Church, SH, Donoughe, S, De Medeiros, BA and Extavour, CG (2019) Insect egg size and shape evolve with ecology but not developmental rate. Nature 571(7763), 5862. https://doi.org/10.1038/s41586-019-1302-4CrossRefGoogle Scholar
de Castro-guedes, CF, de Almeida, LM, Do Rocio Chiarello Penteado, S and Moura, MO (2016) Effect of different diets on biology, reproductive variables and life and fertility tables of Harmonia axyridis (Pallas)(Coleoptera, Coccinellidae). Revista Brasileira de Entomologia 60, 260266. https://doi.org/10.1016/j.rbe.2016.03.003CrossRefGoogle Scholar
DeLong, JP and Uiterwaal, SF (2022) Predator functional responses and the biocontrol of aphids and mites. BioControl 67(2), 161172. https://doi.org/10.1007/s10526-021-10127-1CrossRefGoogle Scholar
DeLong, JP, Uiterwaal, SF and Dell, AI (2021) Trait-based variation in the foraging performance of individuals. Frontiers in Ecology and Evolution 9, 649542. https://doi.org/10.3389/fevo.2021.649542CrossRefGoogle Scholar
Desneux, N, Decourtye, A and Delpuech, JM (2007) The sublethal effects of pesticides on beneficial arthropods. Annual Review of Entomology 52(1), 81106. https://doi.org/10.1146/annurev.ento.52.110405.091440CrossRefGoogle ScholarPubMed
Di, N, Zhang, K, Xu, Q, Zhang, F, Harwood, JD, Wang, S and Desneux, N (2021) Predatory ability of Harmonia axyridis (Coleoptera: Coccinellidae) and Orius sauteri (Hemiptera: Anthocoridae) for suppression of fall armyworm Spodoptera frugiperda (Lepidoptera: Noctuidae). Insects 12(12), 1063. https://doi.org/10.3390/insects12121063CrossRefGoogle ScholarPubMed
Eisner, T, Eisner, M, Rossini, C, Iyengar, VK, Roach, BL, Benedikt, E and Meinwald, J (2000) Chemical defense against predation in an insect egg. Proceedings of the National Academy of Sciences 97(4), 16341639. https://doi.org/10.1073/pnas.030532797CrossRefGoogle Scholar
Feng, Y, Zhou, ZX, An, MR, Yu, XL and Liu, TX (2018) The effects of prey distribution and digestion on functional response of Harmonia axyridis (Coleoptera: Coccinellidae). Biological Control 124, 7481. https://doi.org/10.1016/j.biocontrol.2018.04.009CrossRefGoogle Scholar
Gontijo, LM (2019) Engineering natural enemy shelters to enhance conservation biological control in field crops. Biological Control 130, 155163. https://doi.org/10.1016/j.biocontrol.2018.10.014CrossRefGoogle Scholar
Guo, Z, Guo, Z, Gao, J, Huang, G, Wan, H, He, S, Xie, Y, Li, J and Ma, K (2024) Detection of insecticide susceptibility and target-site mutations in field populations of Spodoptera frugiperda (Lepidoptera: Noctuidae). International Journal of Pest Management 70(4), 880890. https://doi.org/10.1080/09670874.2022.2050835CrossRefGoogle Scholar
Huang, YH, Escalona, HE, Sun, YF, Zhang, PF, Du, XY, Gong, SR, Tang, XF, Liang, YS, Yang, D, Chen, PT, Yang, HY (2025) Molecular evolution of dietary shifts in ladybird beetles (Coleoptera: Coccinellidae): From fungivory to carnivory and herbivory. BMC Biology 23, 67. https://doi.org/10.1186/s12915-025-02174-2.CrossRefGoogle ScholarPubMed
Islam, Y, Güncan, A, Zhou, X, Naeem, A and Shah, FM (2022a) Effect of temperature on the life cycle of Harmonia axyridis (Pallas), and its predation rate on the Spodoptera litura (Fabricius) eggs. Scientific Reports 12(1), 15303. https://doi.org/10.1038/s41598-022-18166-zCrossRefGoogle Scholar
Islam, Y, Shah, FM, Güncan, A, DeLong, JP and Zhou, X (2022b) Functional response of Harmonia axyridis to the larvae of Spodoptera litura: The combined effect of temperatures and prey instars. Frontiers in Plant Science 13, 849574. https://doi.org/10.3389/fpls.2022.849574CrossRefGoogle Scholar
Islam, Y, Shah, FM, Rubing, X, Razaq, M, Yabo, M, Xihong, L and Zhou, X (2021) Functional response of Harmonia axyridis preying on Acyrthosiphon pisum nymphs: The effect of temperature. Scientific Reports 11(1), 13565. https://doi.org/10.1038/s41598-021-92954-xCrossRefGoogle ScholarPubMed
Islam, Y, Shah, FM, Shah, MA, Musa Khan, M, Rasheed, MA, Ur Rehman, S, Ali, S and Zhou, X (2020) Temperature-dependent functional response of Harmonia axyridis (Coleoptera: Coccinellidae) on the eggs of Spodoptera litura (Lepidoptera: Noctuidae) in laboratory. Insects 11(9), 583. https://doi.org/10.3390/insects11090583CrossRefGoogle ScholarPubMed
Jaworski, CC, Bompard, A, Genies, L, Amiens-Desneux, E and Desneux, N (2013) Preference and prey switching in a generalist predator attacking local and invasive alien pests. PloS One 8(12), e82231. https://doi.org/10.1371/journal.pone.0082231CrossRefGoogle Scholar
Juliano, SA (2001) Nonlinear curve fitting: Predation and functional response curves.In. Cheiner, S and Gurven, J (eds), Design and Analysis of Ecological Experiments. 2nd Edn. Oxford: Oxford UniversityPress, 178196.10.1093/oso/9780195131871.003.0010CrossRefGoogle Scholar
Kenis, M, Benelli, G, Biondi, A, Calatayud, PA, Day, R, Desneux, N, Harrison, RD, Kriticos, D, Rwomushana, I and Van den Berg, J (2023) Invasiveness, biology, ecology, and management of the fall armyworm, Spodoptera frugiperda. Entomologia Generalis 43(2), 187241. https://doi.org/10.1127/entomologia/2022/1659CrossRefGoogle Scholar
Kivelä, SM, Davis, RB, Esperk, T, Gotthard, K, Mutanen, M, Valdma, D and Tammaru, T (2020) Comparative analysis of larval growth in Lepidoptera reveals instar‐level constraints. Functional Ecology 34(7), 13911403. https://doi.org/10.1111/1365-2435.13556CrossRefGoogle Scholar
Koch, R (2003) The multicolored Asian lady beetle, Harmonia axyridis: A review of its biology, uses in biological control, and non-target impacts. Journal of Insect Science 3(1), 32. https://doi.org/10.1093/jis/3.1.32CrossRefGoogle ScholarPubMed
Koch, R, Hutchison, W, Venette, R and Heimpel, G (2003) Susceptibility of immature monarch butterfly, Danaus plexippus (Lepidoptera: Nymphalidae: Danainae), to predation by Harmonia axyridis (Coleoptera: Coccinellidae). Biological Control 28(2), 265270. https://doi.org/10.1016/S1049-9644(03)00102-6CrossRefGoogle Scholar
Lee, JH and Kang, TJ (2004) Functional response of Harmonia axyridis (Pallas)(Coleoptera: Coccinellidae) to Aphis gossypii Glover (Homoptera: Aphididae) in the laboratory. Biological Control 31(3), 306310. https://doi.org/10.1016/j.biocontrol.2004.04.011CrossRefGoogle Scholar
Li, C, Yu, J, Mao, R, Kang, K, Xu, L and Wu, M (2024) Functional and numerical responses of Harmonia axyridis (Coleoptera: Coccinellidae) to Rhopalosiphum nymphaeae (Hemiptera: Aphididae) and their potential for biological control. Insects 15(9), 633. https://doi.org/10.3390/insects15090633CrossRefGoogle ScholarPubMed
Li, TH, Ma, Y, Hou, YY, Nkunika, PO, Desneux, N, Zang, LS (2023)Variation in egg mass scale thickness of three Spodoptera species and its effects on egg parasitoid performance. Journal of Pest Science 96, 13931402. https://doi.org/10.1007/s10340-023-01608-6.CrossRefGoogle Scholar
Liu, N (2015) Insecticide resistance in mosquitoes: Impact, mechanisms, and research directions. Annual Review of Entomology 60(1), 537559. https://doi.org/10.1146/annurev-ento-010814-020828CrossRefGoogle ScholarPubMed
Lu, Y, Wu, K, Jiang, Y, Guo, Y and Desneux, N (2012) Widespread adoption of Bt cotton and insecticide decrease promotes biocontrol services. Nature 487(7407), 362365. https://doi.org/10.1038/nature11153CrossRefGoogle Scholar
Lucas, É, Coderre, D and Brodeur, J (1998) Intraguild predation among aphid predators: Characterization and influence of extraguild prey density. Ecology 79, 10841092. https://doi.org/10.1890/0012-9658(1998)079[1084:IPAAPC]2.0.CO;2CrossRefGoogle Scholar
Montezano, DG, Sosa-Gómez, D, Specht, A, Roque-Specht, VF, Sousa-Silva, JC, Paula-Moraes, SD, Peterson, JA and Hunt, T (2018) Host plants of Spodoptera frugiperda (Lepidoptera: Noctuidae) in the Americas. African Entomology 26(2), 286300. https://doi.org/10.4001/003.026.0286CrossRefGoogle Scholar
Nauen, R, Bass, C, Feyereisen, R and Vontas, J (2022) The role of cytochrome P450s in insect toxicology and resistance. Annual Review of Entomology 67(1), 105124. https://doi.org/10.1146/annurev-ento-070621-061328CrossRefGoogle ScholarPubMed
Novak, M and Wootton, JT (2010) Using experimental indices to quantify the strength of species interactions. Oikos 119(7), 10571063. https://doi.org/10.1111/j.1600-0706.2009.18147.xCrossRefGoogle Scholar
Ortiz, E, Ramos-Jiliberto, R and Arim, M (2023) Prey selection along a predators’ body size gradient evidences the role of different trait-based mechanisms in food web organization. PloS One 18(10), e0292374. https://doi.org/10.1371/journal.pone.0292374CrossRefGoogle ScholarPubMed
Pandi, GGP, Paul, B, Vivek, S and Shankarganesh, K (2012) Feeding potential and biology of coccinellid predator Cheilomenes sexmaculata (Fabricius)(Coleoptera) on aphid hosts. Indian Journal of Entomology 74(4), 388393.Google Scholar
Pang, H and Li, HS (2025) New advances in the genetics and evolution of ladybird beetles for biological control. Insects 16, 753. https://doi.org/10.3390/insects16080753CrossRefGoogle ScholarPubMed
Pritchard, DW, Paterson, RA, Bovy, HC and Barrios-O’Neill, D (2017) Frair: An R package for fitting and comparing consumer functional responses. Methods in Ecology and Evolution 8, 15281534. https://doi.org/10.1111/2041-210X.12784CrossRefGoogle Scholar
Qin, H, Wang, D, Ding, J, Huang, R and Ye, Z (2006) Host plants of Spodoptera litura. Acta Agriculturae Jiangxi 18, 5158. https://doi.org/10.19386/j.cnki.jxnyxb.2006.05.017Google Scholar
Raak-van den Berg, CL (2014) Harmonia Axyridis: How to Explain Its Invasion Success in Europe. Netherlands: Wageningen University and Research.Google Scholar
Rogers, D (1972) Random search and insect population models. The Journal of Animal Ecology 41, 369383. https://doi.org/10.2307/3474CrossRefGoogle Scholar
Sanches, M and Wise, J (2024) The Arthropod Pesticide Resistance Database. East Lansing, Michigan, USA: Michigan State University. https://www.pesticideresistance.org/, (accessed on 25 January 2025).Google Scholar
Seko, T and Miura, K (2008) Functional response of the lady beetle Harmonia axyridis (Pallas)(Coleoptera: Coccinellidae) on the aphid Myzus persicae (Sulzer)(Homoptera: Aphididae). Applied Entomology and Zoology 43(3), 341345. https://doi.org/10.1303/aez.2008.341CrossRefGoogle Scholar
Sisay, B, Simiyu, J, Malusi, P, Likhayo, P, Mendesil, E, Elibariki, N, Wakgari, M, Ayalew, G and Tefera, T (2018) First report of the fall armyworm, Spodoptera frugiperda (Lepidoptera: Noctuidae), natural enemies from Africa. Journal of Applied Entomology 142(8), 800804. https://doi.org/10.1111/jen.12534CrossRefGoogle Scholar
Sloggett, JJ (2022) Diet and chemical defence in ladybird beetles (Coleoptera: Coccinellidae). European Journal of Entomology 119, 362367. https://doi.org/10.14411/eje.2022.037CrossRefGoogle Scholar
Sørensen, CH, Toft, S and Kristensen, TN (2013) Cold-acclimation increases the predatory efficiency of the aphidophagous coccinellid Adalia bipunctata. Biological Control 65(1), 8794. https://doi.org/10.1016/j.biocontrol.2012.09.016CrossRefGoogle Scholar
Tay, WT, Meagher, JRL, Czepak, C and Groot, AT (2023) Spodoptera frugiperda: Ecology, evolution, and management options of an invasive species. Annual Review of Entomology 68(1), 299317. https://doi.org/10.1146/annurev-ento-120220-102548CrossRefGoogle ScholarPubMed
Team RC (2021) R: A language and environment for statistical computing. In R Foundation for Statistical Computing, Vienna, Austria. https://www.R-project.org/Google Scholar
Ullah, MI, Arshad, M, Afzal, M, Khalid, S, Saleem, M, Mustafa, I, Iftikhar, Y, Molina-Ochoa, J and Foster, JE (2016) Incidence of Spodoptera litura (Lepidoptera: Noctuidae) and its feeding potential on various citrus (Sapindales: Rutaceae) cultivars in the Sargodha Region of Pakistan. Florida Entomologist 99(2), 192195. https://doi.org/10.1653/024.099.0206CrossRefGoogle Scholar
Walker, R, Wilder, SM and González, AL (2020) Temperature dependency of predation: Increased killing rates and prey mass consumption by predators with warming. Ecology and Evolution 10(18), 96969706. https://doi.org/10.1002/ece3.6581CrossRefGoogle ScholarPubMed
Wang, X and Zou, X (2017) Modeling the fear effect in predator–prey interactions with adaptive avoidance of predators. Bulletin of Mathematical Biology 79, 13251359. https://doi.org/10.1007/s11538-017-0287-0CrossRefGoogle ScholarPubMed
Warfe, DM and Barmuta, LA (2004) Habitat structural complexity mediates the foraging success of multiple predator species. Oecologia 141, 171178. https://doi.org/10.1007/s00442-004-1644-xCrossRefGoogle ScholarPubMed
Wasserman, RJ, Alexander, ME, Weyl, OL, Barrios‐O’Neill, D, Froneman, PW and Dalu, T (2016) Emergent effects of structural complexity and temperature on predator–prey interactions. Ecosphere 7(2), e01239. https://doi.org/10.1002/ecs2.1239CrossRefGoogle Scholar
Weisenburger, DD (1993) Human health effects of agrichemical use. Human Pathology 24(6), 571576. https://doi.org/10.1016/0046-8177(93)90234-8CrossRefGoogle ScholarPubMed
Wu, P, Zhang, J, Yan, S and Zhang, R (2018) Functional responses and intraspecific competition in the ladybird Harmonia axyridis (Coleoptera: Coccinellidae) provided with Melanaphis sacchari (Homoptera: Aphididae) as prey. European Journal of Entomology, 115. https://doi.org/10.14411/eje.2018.022Google Scholar
Yang, H, Du, J, Wang, L, Zhu, P, Li, D, Huang, J and Hu, Z (2025) Predation risk effects of Harmonia axyridis on the development and fecundity of Periphyllus koelreuteriae. Insects 16, 695. https://doi.org/10.3390/insects16070695CrossRefGoogle ScholarPubMed
Zhang, S, Cao, Z, Wang, Q, Zhang, F and Liu, TX (2014) Exposing eggs to high temperatures affects the development, survival and reproduction of Harmonia axyridis. Journal of Thermal Biology 39, 4044. https://doi.org/10.1016/j.jtherbio.2013.11.007CrossRefGoogle Scholar