Investigation of biodegradable insecticidal properties of different plant lectins on Tropinota (Epicometis) hirta (Poda, 1761) (Coleoptera: Cetoniidae)

Abstract

Tropinota (Epicometis) hirta (Poda, 1761) (Coleoptera: Cetoniidae), a polyphagous agricultural pest that causes significant economic damage to fruits, vegetables and cereals. Due to its presence during the same period as bees, chemical control methods are not recommended. This study aims to evaluate the effectiveness of plant lectins as bioinsecticides in comparison to synthetic insecticides. Adult insects were collected from various locations in İvrindi district of Balıkesir, Türkiye, between March 25 and June 6, 2024. The insects were fed in vivo with lectins from Wisteria floribunda (Willd.) DC. (Fabales: Fabaceae) (WF), Phaseolus vulgaris L. (Fabales: Fabaceae) (PV), Triticum vulgaris L. (Poales: Poaceae) (TV) and Phytolacca americana L. (Caryophyllales: Phytolaccaceae) (PA) at concentrations of 200, 250 and 300 mg/g for 7 days. The highest lethal effect among the applied lectin doses was detected at the PA300 dose. Upon examining the insect gut tissues, it was found that the TV300 lectin dose contained higher levels of oxidants compared to the synthetic insecticide. Additionally, the applied lectins exhibited inhibitory effects on the activity of various digestive enzyme in insects. Our findings suggest that lectins can be used as a biodegradable alternative to chemical insecticides for controlling T. hirta.

Keywords

• Bioinsecticides
• digestive enzymes
• lectins
• oxidative stress
• apple blossom beetle

Tropinota (Epicometis) hirta (Poda, 1761) (Coleoptera: Cetoniidae) üzerinde farklı bitki lektinlerinin biyolojik olarak parçalanabilir insektisit özelliklerinin araştırılması

Öz

Tropinota (Epicometis) hirta (Poda, 1761) (Coleoptera: Cetoniidae), meyve, sebze ve tahıllara önemli ekonomik zararlar veren polifag bir tarımsal zararlıdır. Arılarla aynı dönemde bulunması nedeniyle kimyasal kontrol yöntemleri önerilmemektedir. Bu çalışma, sentetik insektisitlere kıyasla biyoinsektisit olarak bitki lektinlerinin etkinliğini değerlendirmeyi amaçlamaktadır. Ergin böcekler, 25 Mart-06 Haziran 2024 tarihleri arasında Türkiye'nin İvrindi (Balıkesir) ilçesinin çeşitli lokasyonlarından toplanmıştır. Böcekler, 7 gün boyunca Wisteria floribunda (Willd.) DC. (Fabales: Fabaceae) (WF), Phaseolus vulgaris L. (Fabales: Fabaceae) (PV), Triticum vulgaris L. (Poales: Poaceae) (TV) ve Phytolacca americana L. (Caryophyllales: Phytolaccaceae) (PA) lektinlerin 200, 250 ve 300 mg/g konsantrasyonuyla in vivo olarak beslenmiştir. Uygulanan lektin dozları arasında en yüksek öldürücü etki PA300 dozunda tespit edilmiştir. Böcek bağırsak dokuları incelendiğinde, TV300 lektin dozunun sentetik insektisit ile karşılaştırıldığında daha yüksek düzeyde oksidan içerdiği tespit edilmiştir. Ek olarak, uygulanan lektinler böceklerdeki çeşitli sindirim enzimlerinin aktivitesi üzerinde inhibitör etki göstermiştir. Bulgularımız, lektinlerin T. hirta'nın kontrolünde kimyasal pestisitlere alternatif biyolojik olarak parçalanabilen bir insektisit olarak kullanılabileceğini göstermektedir.

Anahtar Kelimeler

• Biyo-insektisit
• sindirim enzimleri
• lektinler
• oksidatif stres
• çiçek zınnı

Kaynakça

1. Akpınar, F., E. Yüksel & R. Canhilal, 2020. Potential of local entomopathogenic nematode isolates to control the adults of the scarab beetle, Epicometis hirta (Coleoptera: Scarabaeidae). Uluslararası Tarım ve Yaban Hayatı Bilimleri Dergisi, 6 (3): 461-468.
2. Albuquerque, L. P., T. H. Procópio, C. C. S. Guedes, E. V. Pontual, P. M. G. Paiva & T. H. Napoleão, 2020. Antinutritional effects of the chitin-binding lectin from Microgramma vacciniifolia rhizome (MvRL) on Sitophilus zeamais. Journal of Stored Products Research, 88: 101652.
3. Atmaca, S., G. Pekbey & R. Canhilal, 2018. Bazı entomopatojen fungusların baklazınnı, Epicometis hirta (Poda) (Coleoptera: Scarabaeidae) erginlerine karşı virülensliği. Iğdır Üniversitesi Fen Bilimleri Enstitüsü Dergisi, 8 (2): 37-42 (in Turkish with abstract in English).
4. Buşmachiu, G. & L. Toderaş, 2014. Some observation on Tropinota (Epicometis) hirta (Poda, 1761) (Coleoptera: Scarabaeoidea, Cetoniidae) from the Republic of Moldova. Marisia, Studii și Materiale. Ştiinţele Naturii Numărul, 33-34: 123-130.
5. Camaroti, J. R. S. L., W. A. Almeida, B. R. Belmonte, A. P. S. Oliveira, T. A. Lima, M. R. A. Ferreira, P. M. G. Paiva, L. A. Soares, E. V. Pontual & T. H. Napoleão, 2018. Sitophilus zeamais adults have survival and nutrition affected by Schinus terebinthifolius leaf extract and its lectin (SteLL). Industrial Crops and Products, 116 (2018): 81-89.
6. Carey, J. R. & P. Liedo, 1999. Mortality dynamics of insects: general principles derived from aging research on the mediterranean fruit fly (Diptera: Tephritidae). American Entomologist, 45 (1): 49-55.
7. Carlini, C. R. & M. F. Grossi-De-Sá, 2002. Plant toxic proteins with insecticidal properties. A review on their potentialities as bioinsecticides. Toxicon, 40 (11): 1515-1539.
8. Chakrabarti, P., S. Rana, S. Sarkar, B. Smith & P. Basu, 2015. Pesticide-induced oxidative stress in laboratory and field populations of native honey bees along intensive agricultural landscapes in two Eastern Indian states. Apidologie, 46 (1): 107-129.

9. Coelho, M. B., S. Marangoni & M. L. R. Macedo, 2007. Insecticidal action of Annona coriacea lectin against the flour moth Anagasta kuehniella and the rice moth Corcyra cephalonica (Lepidoptera: Pyralidae). Comparative Biochemistry and Physiology, Part C, 146 (3): 406-414.
10. Czapla, T. H. & B. A. Lang, 1990. Effect of plant lectins on the larval development of European corn borer (Lepidoptera: Pyralidae) and southern corn rootworm (Coleoptera: Chrysomelidae). Journal of Economic Entomology, 83 (6): 2480-2485.
11. Çelik, V. B. & B. Yaşar, 2021. The effects of traps hung in different places in the cherry orchard on the capture and flower damage of Tropinota (Epicometis) hirta (Poda, 1761) (Coleoptera: Cetoniidae). Journal of Advanced Research in Natural and Applied Sciences, 7 (4): 582-589.
12. De Sá, L. F. R., T. T. Wermelinger, E. S. Ribeiro, G. A. Gravina, K. V. S. Fernandes, J. Xavier-Filho, T. M. Venancio, G. L. Rezende & A. E. A. Oliveira, 2014. Effects of Phaseolus vulgaris (Fabaceae) seed coat on the embryonic and larval development of the cowpea weevil Callosobruchus maculatus (Coleoptera: Bruchidae). Journal of Insect Physiology, 60 (1): 50-57.
13. Douglas, A. E., 2012. “Alimentary Canal, Digestion and Absorption, 46-80”. In: The Insects: Structure and Function (Eds. R. F. Chapman). Cambridge University, New York, USA, 929 pp.
14. Erdem, M., S. C. Karahan, A. Menteşe, S. O. Yaman & S. Demir, 2021. The Assessment of oxidative stress biomarkers in different serum and plasma specimens. Erciyes Medical Journal, 43 (6): 541-547.
15. Gatehouse, A. M. R., F. M. Dewey, J. Dove, K. A. Fenton & A. Pusztai, 1984. Effect of seed lectins from Phaseolus vulgaris on the development of larvae of Callosobruchus maculatus; mechanism of toxicity. Journal of the Science of Food Agriculture, 35 (4): 373-380.
16. Gholamzadeh Chitgar, M., M. Ghadamyari & M. Sharifi, 2013. Identification and characterization of gut proteases in the fig tree skeletoniser moth, Choreutis nemorana Hübner (Lepidoptera: Choreutidae). Plant Protection Science, 49 (1): 19-26.
17. Habibi, J., E. A. Backus & T. H. Czapla, 1993. Plant lectins affect survival of the potato leafhopper (Homoptera: Cicadellidae). Journal of Economic Entomology, 86 (3): 945-951.
18. Hamadah, K., K. Ghoneim, M. Tanani, A. Basiouny & H. Waheeb, 2016. Deteriorated acid and alkaline phosphatase activities in certain tissues of Spodoptera littoralis (Lepidoptera: Noctuidae) by some novel chitin synthesis inhibitors. International Journal of Advanced Research, 4 (2): 611-624.
19. Huber, M., T. Roder, S. Irmisch, A. Riedel, S. Gablenz, J. Fricke, P. Rahfeld, M. Reichelt, C. Paetz, N. Liechti, L. Hu, Z. Bont, Y. Meng, W. Huang, C. A. Robert, J. Gershenzon & M. Erb, 2021. A beta-glucosidase of an insect herbivore determines both toxicity and deterrence of a dandelion defense metabolite. eLife, 10: e68642.
20. Jaber, K., E. Haubruge & F. Francis, 2010. Development of entomotoxic molecules as control agents: Illustration of some protein potential uses and limits of lectins (Review). Biotechnology, Agronomy, Society and Environmental, 14 (1): 225-241.
21. Kara, K., 1995. Tropinota (Epicometis) hirta (Poda) (Coleoptera, Scarabeidae) ’nin Tokat ve çevresindeki konukçuları, yayılışı, zarar düzeyi, bazı biyolojik özellikleri üzerine araştırmalar. Gaziosmanpaşa Üniversitesi Ziraat Fakültesi Dergisi, 12 (1): 15-26 (in Turkish with abstract in English).
22. Kaur, M., K. Singh, P. J. Rup, A. K. Saxena, R. H. Khan, M. T. Ashraf, S. S. Kamboj & J. Singh, 2006. A tuber lectin from Arisaema helleborifolium Schott with anti-insect activity against melon fruit fly, Bactrocera cucurbitae (Coquillett) and anti-cancer effect on human cancer cell lines. Archives of Biochemistry and Biophysics, 445 (1): 156-165.
23. Khoobdel, M., V. Rahimi, A. Ebadollahi & P. Krutmuang, 2022. Evaluation of the potential of a lectin extracted from Polygonum persicaria L. as a biorational agent against Sitophilus oryzae L. Molecules, 27 (3): 793 (1-17).
24. Krishnan, N. & F. Sehnal, 2006. Compartmentalization of oxidative stress and antioxidant defense in the larval gut of Spodoptera littoralis. Archives of Insect Biochemistry and Physiology, 63 (1): 1-10.
25. Kutinkova, H. & R. Andreev, 2004. Integrated pest management in sweet cherry (Prunus avium L.) orchards in Bulgaria. Journal of Fruit and Ornamental Plant Research, 12 (1): 41-47.
26. Lazarević, J. & M. Janković-Tomanić, 2015. Dietary and phylogenetic correlates of digestive trypsin activity in insect pests. Entomologia Experimentalis et Applicata,157 (2): 123-151.
27. Lima, T. A., K. M. Fernandes, A. P. S. Oliveira, L. P. Dornelles, G. F. Martins, T. H. Napoleão & P. M. G. Paiva, 2016. Termiticidal lectins from Myracrodruon urundeuva (Anacardiaceae) cause midgut damages when ingested by Nasutitermes corniger (Isoptera; Termitidae) workers. Pest Management Science, 73 (5): 991-998.
28. Lima, T. A., L. P. Dornelles, A. P. S. Oliveira, C. C. S. Guedes, S. O. Souza, R. A. Sá, R. B. Zingali, T. H. Napoleão & P. M. G. Paiva, 2018. Binding targets of termiticidal lectins from the bark and leaf of Myracrodruon urundeuva in the gut of Nasutitermes corniger workers. Pest Management Science, 74 (7): 1593-1599.
29. Lodos, N., F. Önder, E. Pehlivan, R. Atalay, E. Erkin, Y. Karsavuran, S. Tezcan & S. Aksoy, 1999. Faunistic Studies on Scarabaeoidea (Aphodiidae, Cetoniidae, Dynastidae, Geotrupidae, Glaphyridae, Hybosoridae, Melolonthidae, Ochodaeidae, Rutelidae, Scarabaeidae) (Coleoptera) of Western Black Sea, Central Anatolia and Mediterranean Regions of Turkey. Ege Üniversity, Bornova, İzmir, 64 pp.
30. Macedo, M. L. R., M. G. M. Freire, J. C. Novello & S. Marangoni, 2002. Talisia esculenta lectin and larval development of Callosobruchus maculatus and Zabrotes subfasciatus (Coleoptera: Bruchidae). Biochimica et Biophysica Acta, 1571 (2): 83-88.
31. Macedo, M. L. R., M. G. M. Freire, M. B. R. Silva & L. C. B. B. Coelho, 2007. Insecticidal action of Bauhinia monandra leaf lectin (BmoLL) against Anagasta kuehniella (Lepidoptera: Pyralidae), Zabrotes subfasciatus and Callosobruchus maculatus (Coleoptera: Bruchidae). Comparative Biochemistry and Physiology, Part A: Molecular & Integrative Physiology, 146 (4): 486-498.
32. Mantzoukas, S., G. Korbou, A. Magita, P. A. Eliopoulos & K. Poulas, 2020. Leguminous seeds powder diet reduces the survival and development of the khapra beetle, Trogoderma granarium Everts (Coleoptera: Dermestidae). Biology, 9 (8): 204 (1-9).
33. Martinez, D. S. T., M. G. M. Freire, P. Mazzafera, R. T. Araujo-Júnior, R. D. Bueno & M. L. R. Macedo, 2012. Insecticidal effect of labramin, a lectin-like protein isolated from seeds of the beach apricot tree, Labramia bojeri, on the Mediterranean flour moth, Ephestia kuehniella. Journal of Insect Science, 12 (62): 1-11.
34. Mehrabadi, M., A. R. Bandani, R. Mehrabadi & H. Alizadeh, 2012. Inhibitory activity of proteinaceous α-amylase inhibitors from Triticale seeds against Eurygaster integriceps salivary α-amylases: Interaction of the inhibitors and the insect digestive enzymes. Pesticide Biochemistry and Physiology, 102 (3): 220-228.
35. Metayi, M. H. A., H. S. El-Tahawe & A. M. Khorchid, 2024. Entomotoxic properties of white kidney bean and soybean lectins and their effects against two digestive enzymes of the Spiny Bollworm, Earias insulana (Boisd). Alexandria Science Exchange Journal, 45 (1): 27-34.
36. Mishra, A., A. Behura, S. Mawatwal, A. Kumar, L. Naik, S. S. Mohanty, D. Manna, P. Dokania, A. Mishra, S. K. Patra & R. Dhiman, 2019. Structure-function and application of plant lectins in disease biology and immunity. Food and Chemical Toxicology, 134: 110827.
37. Muramoto, K., 2017. Lectins as bioactive proteins in foods and feeds. Food Science and Technology Research, 23 (4): 487-494.
38. Murdock, L. L., J. E. Huesing, S. S. Nielsen, R. C. Pratt & R. E. Shade, 1990. Biological effects of plant lectins on the cowpea weevil. Phytochemistry, 29 (1): 85-89.
39. Napoleão, T.H., B. R. Belmonte, E. V. Pontual, L. P. Albuquerque, R. A. Sá, L. M. Paiva, L. C. B. B. Coelho & P. M. G. Paiva, 2013. Deleterious effects of Myracrodruon urundeuva leaf extract and lectin on the maize weevil, Sitophilus zeamais (Coleoptera, Curculionidae). Journal of Stored Products Research, 54 (2013): 26-33.
40. Oliveira, A. P. S., T. A. Lima, N. V. N. Paz, L. C. B. B. Coelho, T. H. Napoleão, D. Foguel & P. M. G. Paiva, 2023. A termiticidal and high denaturation-resistant lectin from Moringa oleifera seed cake. Journal of Natural Pesticide Research, 5: 100040.
41. Oltean, I., L. I. Macavei, I. Vasian, S. Totos, M. Varga & T. Florian, 2015. Use of Semiochemical products in monitoring and control of Epicometis hirta Poda. Bulletin University of Agricultural Sciences and Veterinary Medicine series Agriculture, 72 (2): 453-456.
42. Peumans, W. J. & E. Van Damme, 1995. Lectins as plant defense proteins. Plant Physiology, 109 (2): 347-352.
43. Powell, K. S., 2001. Antimetabolic effects of plant lectins towards nymphal stages of the planthoppers Tarophagous proserpina and Nilaparvata lugens. Entomologia Experimentalis et Applicata, 99 (1): 71-78.
44. Quandahor, P., Y. Gou, C. Lin & C. Liu, 2022. Potato (Solanum tuberosum L.) leaf extract concentration affects performance and oxidative stress in green peach aphids (Myzus persicae (Sulzer)). Plants, 11 (20): 2757.
45. Rahimi, V., J. Hajizadeh, A. Zibaee & J. Jalali Sendi, 2018. Effect of Polygonum persicaria (Polygonales: Polygonaceae) extracted agglutinin on life table and antioxidant responses in Helicoverpa armigera (Lepidoptera: Noctuidae) larvae. Journal of Economic Entomology, 111 (2): 662-671.
46. Sauvion, N., C. Nardon, G. Febvay, A. M. Gatehouse & Y. Rahbé, 2004. Binding of the insecticidal lectin Concanavalin A in pea aphid, Acyrthosiphon pisum (Harris) and induced effects on the structure of midgut epithelial cells. Journal of Insect Physiology, 50 (12): 1137-50.
47. Schmera, D., M. Tóth, M. Subchev, I. Sredkov, I. Szarukán, T. Jermy & A. Szentesi, 2004. Importance of visual and chemical cues in the development of an attractant trap for Epicometis (Tropinota) hirta Poda (Coleoptera: Scarabaeidae). Crop Protection, 23 (10): 939-944.
48. Senthil-Nathan, S., 2006. Effects of Melia azedarach on nutritional physiology and enzyme activities of the rice leaffolder Cnaphalocrocis medinalis (Guenée) (Lepidoptera: Pyralidae). Pesticide Biochemistry and Physiology, 84 (2): 98-108.
49. Senthil-Nathan, S., P. G. Chung & K. Murugan, 2006. Combined effect of biopesticides on the digestive enzymatic profiles of Cnaphalocrocis medinalis (Guenee) (the rice leaf folder) (Insecta: Lepidoptera: Pyralidae). Ecotoxicology and Environmental Safety, 64 (3): 382-389.
50. Slav, M., D. Hoza & A. Asănică, 2018. Particularities of the blossom feeder attack, Tropinota hirta Poda (Coleoptera: Scarabaeidae), on blueberry (Vaccinum corymbosum) in a commercial orchard from Vrancea county. Journal of Horticulture, Forestry and Biotechnology, 22 (4): 1-6.
51. Souza, C. S., T. F. Procópio, B. R. Belmonte, P. M. G. Paiva, L. P. Albuquerque, E. V. Pontual & T. H. Napoleăo, 2018. Effects of Opuntia ficus-indica lectin on feeding, survival, and gut enzymes of maize weevil, Sitophilus zeamais. Applied Biologica Chemistry, 61 (3): 337-343.
52. Sowa, G., A. J. Bednarska & R. Laskowski, 2024. Mortality pattern of Poecilus cupreus beetles after repeated topical exposure to insecticide-stochastic death or individual tolerance? Environmental Science and Technology, 58 (4): 1854-1864.
53. Sprawka, I., 2008. Toxicity of phytohemagglutinin (PHA) from Phaseolus vulgaris L. to the bird cherry-oat aphid (Rhopalosiphum padi L.). Pesticides, 3 (4): 101-108.
54. Sprawka, I., S. Goławska, P. Czerniewicz & H. Sytykiewicz, 2011. Insecticidal action of phytohemagglutinin (PHA) against the grain aphid, Sitobion avenae. Pesticide Biochemistry and Physiology, 100 (1): 64-69.
55. Şenyüz, Y., K. Dindar & M. Gülmez, 2015. Additions to Scarabaeoidea (Coleoptera) fauna of Eskişehir. Anadolu University Journal of Science and Technology- C - Life Sciences and Biotechnology, 4 (1): 13-23.
56. Terra, W. R. & C. Ferreira, 1994. Insect digestive enzymes: properties, compartmentalization and function. Comparative Biochemistry and Physiology Part B: Comparative Biochemistry, 109 (1): 1-62.
57. Upadhyay, S. K. & P. K. Singh, 2012. Receptors of garlic (Allium sativum) lectins and their role in insecticidal action. The Protein Journal, 31 (6): 439-446.
58. Vandenborre, G., G. Smagghe & E. J. Van Damme, 2011. Plant lectins as defense proteins against phytophagous insects. Phytochemistry, 72 (13): 1538-1550.
59. Yaşar, B. & O. A. Dahham Dahham, 2019. Farklı elma çeşitleri üzerine asılan tuzakların Tropinota hirta (Poda, 1761) (Coleoptera: Cetoniidae)’nın yakalaması üzerine etkisi. Türkiye Tarımsal Araştırmalar Dergisi, 6 (1): 57-64 (in Turkish with abstract in English).
60. Zibaee, A. & A. R. Bandani, 2010. A study on the toxicity of a medicinal plant, Artemisia annua L. (Asteracea) extracts to the sunn pest, Eurygaster integriceps Puton (Hemiptera: Scutelleridae). Journal of Plant Protection Research, 50 (1): 79-85.
61. Zibaee, A., Z. Alborzi, A. Karimi-Malati & M. Salimi, 2014. Effects of a lectin from Polygonum persicaria L. on Pieris brassicae L. (Lepidoptera: Pieridae). Journal of Plant Protection Research, 54 (3): 250-257.