Tanen toleranslı Agelastica alni L., 1758 (Coleoptera: Chrysomelidae) larvalarının biyolojik mücadelesinde Paenibacillus alvei (Cheshire & Cheyne) Ash et al. (Bacillii: Paenibacillaceae) ve tanen aktivitesinin belirlenmesi

Öz

Tanenler, bitkiler tarafından sentezlenen en bol ikincil metabolitler arasındadır. Agelastica alni L., 1758 (Coleoptera: Chrysomelidae) önemli bir orman zararlısıdır. Bu çalışmada, Paenibacillus alvei (Cheshire & Cheyne) Ash et al. (Bacillii: Paenibacillaceae) ve tanenlerin A. alni larvaları üzerindeki etkisi araştırılmıştır. Larvalar 2022 yılında Rize ili Çayeli ilçesinden toplanmıştır. Besleme deneylerinde, %1.25, %2.5 ve %5 tanen içeren yapay diyetler hazırlanmıştır. Enfekte gruplara 100 ve 200 µl P. alvei uygulanmıştır. Farklı diyetlerle beslenen larvaların beslenme indeksleri, pupal kütleleri, fenoloksidaz aktiviteleri, antioksidan enzim aktiviteleri ve ölüm oranları incelenmiştir. Nisbi tüketim oranı (RCR), tüm gruplarda tanen konsantrasyonu ile artmıştır. Nisbi büyüme oranı (RGR), tüm gruplarda tanen konsantrasyonunun artmasıyla yükselmiştir. Enfekte gruplarda tanen konsantrasyonundaki artış, gelişim süresinde azalmaya neden olmuştur. Enfekte olmayan larvalarda süperoksit dismutaz ve fenoloksidaz aktiviteleri tanen konsantrasyonu ile azalırken, katalaz ve glutatyon peroksidaz aktiviteleri artmıştır. Enfekte larvalarda ise tanen konsantrasyonundaki artış katalaz aktivitesinin azalmasına neden olmuştur. P. alvei dozu, süperoksit dismutaz ve fenoloksidaz aktivitelerinde artışa yol açarken, katalaz ve glutatyon peroksidaz aktivitelerini etkilememiştir. %5 tanik asit içeren diyet, en düşük ölüm oranına sahip olmuştur.

Anahtar Kelimeler

• Agelastica alni
• antioksidan sistem
• biyolojik mücadele
• Paenibacillus alvei
• tanen tolerant

Determination of tannin activity and Paenibacillus alvei (Cheshire & Cheyne) Ash et al. (Bacillii: Paenibacillaceae) on the biocontrol of tannin-tolerant Agelastica alni L., 1758 (Coleoptera: Chrysomelidae) larvae

Abstract

Tannins are among the most abundant secondary metabolites synthesized by plants. Agelastica alni L., 1758 (Coleoptera: Chrysomelidae) is a critical forest pest. This study investigated the effect of Paenibacillus alvei (Cheshire & Cheyne) Ash et al. (Bacillii: Paenibacillaceae) and tannins against A. alni larvae. The larvae were collected from the Çayeli district of Rize province in 2022. In the feeding experiments, artificial diets containing 1.25%, 2.5% and 5% tannins were prepared. 100 and 200 µl of P. alvei were applied to the infected groups. Nutritional indices, pupal masses, phenoloxidase activities, antioxidant enzyme activities and mortality rates of larvae fed with different diets were studied. Relative consumption rate (RCR) increased with tannin concentration in all groups. Relative growth rate (RGR) increased with rising tannin concentrations across all groups. In the infected groups, the increase in tannin concentration caused a decrease in developmental time. While superoxide dismutase and phenoloxidase activities of uninfected larvae decreased with tannin concentration, catalase and glutathione peroxidase activities of larvae increased. In infected larvae, catalase activity decreased with increasing tannin concentration. The dose of P. alvei caused an increase in superoxide dismutase and phenoloxidase activities, but did not affect catalase and glutathione peroxidase activities. The diet containing 5% tannic acid had the lowest mortality rate.

Keywords

• Agelastica alni
• antioxidant system
• biocontrol
• Paenibacillus alvei
• tannin-tolerant

Kaynakça

1. Adesanya, A., N. Liu & D. W. Held, 2016. Host suitability and diet mixing influence activities of detoxification enzymes in adult Japanese beetles. Journal of Insect Physiology, 88: 55-62.
2. Aebi, H., 1984. Catalase in vitro. Methods in Enzymology, 105: 121-126.
3. Ahmad, S. & R. S. Pardini, 1990. Mechanisms for regulating oxygen toxicity in phytophagous insects. Free Radical Biology and Medicine, 8 (4): 401-413.
4. Ali, S., Z. Huang, H. Li, M. H. Bashir & S. Ren, 2013. Antioxidant enzyme influences germination, stress tolerance, and virulence of Isaria fumosorosea. Journal of Basic Microbiology, 53 (6): 489-97.
5. Ardia, D. R., J. E. Gantz, B. C. Schneider & S. Strebel, 2012. Costs of immunity in insects: an induced immune response increases metabolic rate and decreases antimicrobial activity. Functional Ecology, 26 (3): 732-739.
6. Ashida, M. & P. Brey, 1997. “Recent Advances in Research on the Insect Prophenoloxidase Cascade, 135- 171”. In: Molecular Mechanisms of Immune Responses in Insects (Eds. P. Brey & D. Hultmark). Chapman & Hall, London, UK, 325 pp.
7. Atanasova-Pancevska, N. & D. Kungulovski, 2018. In vitro potential of Paenibacillus alvei DZ-3 as a biocontrol agent against several phytopathogenic fungi. Biologija, 64 (1): 65-72.
8. Barbehen, R. V. & M. M. Martin, 1992. The protective role of the peritrophic membrane in the tannin-tolerant larvae of Orgyia leucostigma (Lepidoptera). Journal of Insect Physiology, 38 (12): 973-980.

9. Barbehenn, R. V., S. L. Bumgarner, E. F. Roosen & M. M. Martin, 2001. Antioxidant defenses in caterpillars: role of the ascorbate-recycling system in the midgut lumen. Journal of Insect Physiology, 47 (4-5): 349-357. Barbahenn, R. V. & C. P. Constabel, 2011. Tannins in plant-herbivore interactions. Phytochemistry, 72 (13): 1551-1565.
10. Baud, O., A. E., Greene, J. Li, H. Wang, J. J. Volpe & P. A. Rosenberg, 2004. Glutathione peroxidase-catalase cooperativity is required for resistance to hydrogen peroxide by mature rat oligodendrocytes. Journal of Neuroscience Research, 24 (7): 1531-1540.
11. Bayramoğlu, Z., I. Demir, C. Inan & Z. Demirbağ, 2018. Efficacy of native entomopathogenic nematodes from Turkey against the alder leaf beetle, Agelastica alni L. (Coleoptera: Chrysomelidae), under laboratory conditions. Egyptian Journal of Biological Pest Control, 28: 17 (1-5).
12. Beauchamp, C. & I. Fridovich, 1971. Superoxide dismutase: improved assays and an assay applicable to acrylamide gels. Analytical Biochemistry, 44 (1): 276-287.
13. Bekircan, Ç., M. Cüce & A. Sökmen, 2014. Antifeedant activity of the essential oils from four different Lamiaceae species against Agelastica alni L. (Coleoptera: Chrysomelidae). Advances in Zoology and Botany 2 (4): 57-62.
14. Bradford, M. M., 1976. A rapid and sensitive for the quantitation of microgram quantitites of protein utilizing the principle of protein-dye binding. Analytical Biochemistry, 72 (1-2): 248-254.
15. Cory, J. S. & K. Hoover, 2006. Plant-mediated effects in insect-pathogen interactions. Trends in Ecology & Evolution, 21 (5): 278-286.
16. Czypionka, L. & M. P. Hill, 2007. The relationship between female pupal mass and fecundity of Gratiana spadicea (Klug, 1829) (Coleoptera: Chrysomelidae). African Entomology, 15 (2): 380-382.
17. Deml, R., T. Meise & K. Dettner, 1999. Effects of Bacillus thuringiensis d-endotoxins on food utilization, growth, and survival of selected phytophagous insects. Journal of Applied Entomology, 123 (1): 55-64.
18. Djilali, A.B., R. Mehraz, K. Bouacem, A. Benseddik, I. Moualek, M. Nabiev & A. Benzara, 2021. Bioactive substances of Cydonia oblonga fruit: insecticidal effect of tannins on Tribuliumm confusum. International Journal of Fruit Science, 21 (1): 721-731.
19. Djukic, M., D. Becker, A. Poehlein, S. Voget & R. Daniel, 2012. Genome sequence of Paenibacillus alvei DSM 29, a secondary invader during European foulbrood outbreaks. Journal of Bacteriology, 194 (22): 6365. Drotar, A., P. Phelps & R. Fall, 1985. Evidence for glutathione peroxidase activities in cultured cells. Plant Science, 42 (1): 35-40.
20. Eleftherianos, I. & C. Revenis, 2011. Role and importance of phenoloxidase in insect hemostasis. Journal of Innate Immunity, 3 (1): 28-33.
21. Farrar, R. R., J. D. Barbour & G. G. Kennedy, 1989. Quantifying food consumption and growth in insects. Annals of the Entomological Society of America, 82 (5): 593-598.
22. Gillespie, J. P., M. R. Kanost & T. Trenczek, 1997. Biological mediators of insect immunity. Annual Review of Entomology, 42 (1): 611-643.
23. Grady, E. N., J. MacDonald, L. Liu, A. Richman & Z. C. Yuan, 2016. Current knowledge and perspectives of Paenibacillus: a review. Microbial Cell Factories, 15: 203 (1-18).
24. Hafeez, M., S. Liu, S. Jan, A. Gulzar, G. M. Fernández-Grandon, M. Qasim, K. A. Khan, B. Ali, S. J. Kedir, M. Fahad & M. Wang, 2019. Enhanced effects of dietary tannic acid with chlorantraniliprole on life table parameters and nutritional physiology of Spodoptera exigua (Hübner). Pesticide Biochemistry and Physiology,155: 108-118.
25. Hristov, Y. V., M. H. Allsopp & T. C. Wossler, 2022. Apis mellifera capensis larvae show low resistance to a highly virulent Paenibacillus larvae field strain. Journal of Apiccultural Research, 61 (4): 502-510.
26. Huarte-Bonnet, C., P. Juárez & N. Pedrini, 2015. Oxidative stress in entomopathogenic fungi grown on insect‑like hydrocarbons. Current Genetics, 61 (3): 289-297.
27. Ibrahim, S. A. M., H. H. A. Salem & M. A. Taha, 2019. Dual application of entomopathogenic nematodes and fungi on immune and antioxidant enzymes of the greater wax moth, Galleria mellonella L. Egyptian Journal of Biological Pest Control, 29: 20 (1-7).
28. Isayama, S., T. Suzuki, M. Nakai & Y. Kunimi, 2011. Influences of tannic acid and polyphenols in the leaves of strawberry, Fragaria x ananassa, and perilla, Perilla frutescens viridis on the insecticidal activity of Bacillus thuringiensis formulation against the common cutworm, Spodoptera litura (Lepidoptera: Noctuidae). Japanese Journal of Applied Entomology and Zoology, 55 (2): 49-57.
29. Isayama, S., T. Suzuki, M. Nakai & Y. Kunimi, 2021. Influence of tannic acid on the insecticidal activity of a Bacillus thuringiensis serovar aizawai formulation against Spodoptera litura Fabricius (Lepidoptera: Noctuidae). Biological Control, 157 (2021): 104558 (1-9).
30. Janceva, S., T. Dizhbite, G. Telisheva, U. Spulle, L. Klavinsh & M. Dzenis, 2011. “Tannins of deciduous trees bark as a potential source for obtaining ecologically safe wood adhesives, 265-270”. Proceedings of the 8th International Scientific and Practical Conference (20-22 June 2011, Rēzekne, RA Izdevniecība), 353 pp.
31. Jayaraj, R., P. Megha & P. Sreedev, 2016. Organochlorine pesticides, their toxic effects on living organisms and their fate in the environment. Interdisciplinary Toxicology, 9 (3-4): 90-100.
32. Jiang, D., S. Wu, M. Tan, Q. Wang, L. Zheng & S. Yan, 2021. The high adaptability of Hyphantria cunea larvae to cinnamic acid involves in detoxification, antioxidation and gut microbiota response. Pesticide Biochemistry and Physiology, 174 (2021): 104805 (1-9).
33. Jovanovic ́-Galovic, A., D. P. Blagojević, G. Grubor-Lajšić, R. Worland & M. B. Spasić, 2004. Role of antioxidant defense during different stages of preadult life cycle in European corn borer (Ostrinia nubilalis, Hubn.): Diapause and metamorphosis. Archives of Insect Biochemistry and Physiology, 55 (2): 79-89.
34. Karthi, S., K. Vaideki, M. S. Shivakumar, A. Ponsankar, A. Thanigaivel, M. Chellappandian, P. Vasantha-Srinivasan, C. K. Muthu-Pandian, W. B. Hunter & S. Senthil-Nathan, 2018. Effect of Aspergillus flavus on the mortality and activity of antioxidant enzymes of Spodoptera litura Fab. (Lepidoptera: Noctuidae) larvae. Pesticide Biochemistry and Physiology, 149: 54-60.
35. Keating, S. T., W. J. McCarthy & W. G. Yendol, 1989. Gypsy moth (Lymantria dispar) larval susceptibility to a baculovirus affected by selected nutrients, hydrogen lons (pH), and plant allelochemicals in artificial diets. Journal of Invertebrate Pathology, 54 (2): 165-174.
36. Korayem, A. M., M. M. Khodairy, A. A. Abdel-Aal & A. A. M. El-Sonbaty, 2012. The protective strategy of antioxidant enzymes against hydrogen peroxide in honey bee, Apis mellifera during two different seasons. Journal of Biology and Earth Science, 2 (2): 93-109.
37. Krongdang, S., J. D. Evans, Y. Chen, W. Mookhploy & P. Chantawannakul, 2019. Comparative susceptibility and immune responses of Asian and European honey bees to the American foulbrood pathogen, Paenibacillus larvae. Insect Science, 26 (5): 831-842.
38. Lalitha, K., S. Karthi, G. Vengateswari, R. Karthikraja, P. Perumal & M. S. Shivakumar, 2018. Effect of entomopathogenic nematode of Heterorhabditis indica infection on immune and antioxidant system in Lepidopteran pest Spodoptera litura (Lepidoptera: Noctuidae). Journal of Parasitic Disease, 42 (2): 204-211.
39. Lee, K. P., J. S. Simpson & K. Wilson, 2008. Dietary protein-quality influences melanization and immune function in an insect. Functional Ecology, 22 (6): 1052-1061.
40. Lee, K. P., S. T. Behmer, S. J. Simpson & D. Raubenheimer, 2002. A geometric analysis of nutrient regulation in the generalist caterpillar Spodoptera littoralis (Boisduval). Journal of Insect Physiology, 48 (6): 655-665.
41. Lindroth, R. L., S. Y. Hwang & T. L. Osier, 1999. Phytochemical variation in quaking aspen: Effects on gypsy moth susceptibility to nuclear polyhedrosis virus. Journal of Chemical Ecology, 25 (6): 1331-1341.
42. Liu, W., X. ChaoBin, Z. JingJing, Y. JinFeng & L. WanChun, 2010. Inhibitory effect of tannic acid on growth, development and phenoloxidase activity of Spodoptera exigua larva. Journal of Plant Resources and Environment, 19 (1): 32-37.
43. Meşe, Y., B. Tunçsoy & P. Özalp, 2022. Effects of Cu, Zn and their mixtures on bioaccumulation and antioxidant enzyme activities in Galleria mellonella L. (Lepidoptera: Pyralidae). Ecotoxicology, 31 (4): 649-656.
44. Mostafa, M., H. Hossain, H. Hossain, P. Biswas & M. Haque, 2012. Insecticidal activity of plant extracts against Tribolium castaneum Herbst. Journal of Advanced Scientific Research, 3 (3): 80-84.
45. Mrdaković, M., V. Perić Mataruga, L. Ilıjin, M. Vlahović, M. Janković Tomanić, D. Mirčić & J. Lazarević, 2013. Response of Lymantria dispar (Lepidoptera: Lymantriidae) larvae from differently adapted populations to allelochemical stress: Effects of tannic acid. European Journal of Entomology, 110 (1): 55-63.
46. Müller, S., E. Garcia-Gonzalez, E. Genersch & R. D. Süssmuth, 2015. Involvement of secondary metabolites in the pathogenesis of the American foulbrood of honey bees caused by Paenibacillus larvae. Natural Product Reports, 32 (6): 765-778.
47. Navon, A., 1992. Interactions among herbivores, microbial insecticides and crop plants. Phytoparasitica, 20 (Suppl 1): 21-24.
48. Neung, S., X. H. Nguyen, K. W. Naing, Y. S. Lee &. K. Y. Kim, 2014. Insecticidal potential of Paenibacillus elgii HOA73 and its combination with organic sulfur pesticide on diamondback moth, Plutella xylostella . Journal of Korean Society for Applied Biological Chemistry, 57 (2): 181-186.
49. Parker, J. D., K. M. Parker & L. Keller, 2004. Molecular phylogenetic evidence for an extracellular Cu Zn superoxide dismutase gene in insects. Insect Molecular Biology, 13 (6): 587-594
50. Pizzi, A., H. Pasch, K. Rode & S. Giovando, 2009. Polymer structure of commercial hydrolyzable tannins by matrix-assisted laser desorption/ionizationtime- of-flight mass spectrometry. Journal of Applied Polymer Science, 113 (6): 3847-3859.
51. Poppinga, L. & E. Genersch, 2015. Molecular pathogenesis of American foulbrood: how Paenibacillus larvae kills honey bee larvae. Current Opinion in Insect Science, 10: 29-36
52. Price, D., S. Pirbay, L. Weiland, J. Zhu & E. Fuller-Thompson, 2019. Tannins as a pesticide: The impact of tannic acid on the growth rates of Myzus persicae and Arabidopsis thaliana. The Scientists, 4 (1): 26-35.
53. Sagona, S., S. Minieri, F. Coppola, D. Gatta, L. Casini, L. Palego, L. Betti, G. Giannaccini & A. Felicioli, 2021. Effects of chestnut hydrolysable tannin enrichment in the artificial diet of forager bees, Apis mellifera, Journal of Apicultural Research,63 (3): 500-506.
54. Sezen, K. & Z. I. Demirbağ, 2006. Insecticidal effects of some biological agents on Agelastica alni (Coleoptera: Chrysomelidae). Biologia, 61 (6): 687-692.
55. Shobha, R., A. H. Reddy & B. Venkatappa, 2016. Catalase activity in haemolymph of silkworm (Bombyx mori L.) following fungal infection. Journal of Biology and Nature, 5 (3): 148-153.
56. Stochoff, B. A., 1992. Diet-switching by gypsy moth: effects of diet nitrogen history vs. switching on growth, consumption, and food utilization. Entomologia Experimentalis et Applicata, 64 (3): 225-238.
57. Summers C. B. & G. W. Felton, 1996. Peritrophic envelope as a functional antioxidant. Archives of Insect Biochemistry and Physiology, 32 (1): 131-142.
58. Tan, M., H. Wu, S. Yan & D. Jiang, 2022. Evaluating the toxic effects of tannic acid treatment on Hyphantria cunea larvae. Insects, 13 (10): 872 (1-15).
59. Tomalak, M., 2004. Infectivity of entomopathogenic nematodes to soil-dwelling developmental stages of the tree leaf beetles Altica quercetorum and Agelastica alni. Entomologia Experimentalis et Applicata, 110 (2): 125-133.
60. Truzi, C. C., N.F. Vieira, J. M. de Souza & S. A. De Bortoli, 2021. Artificial diets with different protein levels for rearing Spodoptera frugiperda (Lepidoptera: Noctuidae), Journal of Insect Science, 21 (4): 2 (1-7).
61. Vengateswari, G., M. Arunthirumeni & M. S. Shivakumar, 2020. Effect of food plants on Spodoptera litura (Lepidoptera: Noctuidae) larvae immune and antioxidant properties in response to Bacillus thuringiensis infection. Toxicology Reports, 7: 1428-1437.
62. Waldbauer, G. P., 1968. The consumption and utilization of food by insects. Advances in Insect Physiology, 5: 229-288.
63. Wilson, K. W., S. C. Cotter, A. F. Reeson & J. K. Pell, 2001. Melanism and disease resistance in insects. Ecology Letters, 4 (6): 637-649.
64. Yamamoto, R. T., 1969. Mass rearing of tobacco hornworm. II. larval rearing and pupation. Journal of Economic Entomology, 62: 1427-1431.
65. Yaman, M. & Z. Demirbağ, 2000. Isolation, identification and determination of insecticidal activity of two insect-originated Bacillus spp. Biológia (Bratislava), 55 (3): 283-287.
66. Young, S. Y., J. G. Yang & G. W. Felton, 1995. Inhibitory effects of dietary tannins on the infectivity of a nuclear polyhedrosis virus to Helicoverpa zea (Noctuidae: Lepidoptera). Biological Control, 5 (2): 145-150.
67. Zhang, B. & M. G. Feng, 2018. Antioxidant enzymes and their contributions to biological control potential of fungal insect pathogens. Applied Microbiology and Biotechnology, 102 (12): 4995-5004.