The effects of different Charleston pepper cultivars on the demographic parameters and the antioxidant levels of Myzus persicae (Sulzer, 1776) (Hemiptera: Aphididae)

Abstract

Host plant diversity causes differences in the biology and adaptation of insects. In this study, variations in some biological properties and adaptive antioxidative response of Myzus persicae (Sulzer,1776) (Hemiptera: Aphididae) on five Charleston pepper, Capsicum annuum L. (Solanaceae) cultivars were investigated under laboratory conditions (25±1°C, 60±5% RH). The lowest intrinsic rate of increase (r = 0.193 d-1) of M. persicae was estimated in the tested cohort fed with the Kanyon cultivar, while the highest intrinsic rate of increase (r = 0.248 d-1) was found on the Tufan cultivar. The cohort fed with Safkan cultivar exhibited the highest levels of GST-CDNB and EST-PNPA at 562.80 and 207.64 nmol/mg protein, respectively, whereas the cohort fed with Kanyon cultivar showed the lowest levels at 317.04 and 132.14 nmol/mg protein, respectively. Analysis of life table parameters and enzymatic/non-enzymatic antioxidant levels of M. persicae showed that among the cultivars we tested, the Tufan cultivar was the most preferred host by M. persicae, while Kanyon cultivar was a less suitable host.

Keywords

• Age-stage two-sex life table
• Capsicum annuum
• enzymatic antioxidant
• Myzus persicae

Farklı Charleston biber çeşitlerinin Myzus persicae (Sulzer, 1776) (Hemiptera: Aphididae)’nin demografik parametreleri ve antioksidan seviyeleri üzerine etkileri

Öz

Konukçu bitki çeşitliliği, böceklerin biyolojisinde ve adaptasyonunda farklılıklara neden olur. Bu çalışmada, laboratuvar koşullarında (25±1°C, %60±5 orantılı nem) Myzus persicae (Sulzer,1776) (Hemiptera: Aphididae)’nin beş Çarliston biber, Capsicum annuum L. (Solanaceae) çeşidi üzerindeki bazı biyolojik özellikleri ve adaptif antioksidan tepkilerindeki değişimler incelenmiştir. Myzus persicae’nin en yüksek kalıtsal üreme oranı (r = 0.248 g-1) Tufan çeşidi üzerinde, en düşük ise (r = 0.193 g-1) Kanyon çeşidi üstünde beslenen test edilen grupta kaydedilmiştir. Safkan çeşidi üstünde beslenen grup, sırasıyla 562.80 ve 207.64 nmol/mg protein ile en yüksek GST-CDNB ve EST-PNPA seviyelerini sergilerken, Kanyon çeşidi üstünde beslenen grup sırasıyla 317.04 ve 132.14 nmol/mg protein düzeyleri ile en düşük seviyeleri göstermiştir. Myzus persicae’nin yaşam çizelgesi parametreleri ve enzimatik/enzimatik olmayan antioksidan düzeylerinin analizleri, test ettiğimiz çeşitler arasında M. persicae tarafından en çok tercih edilen konukçunun Tufan çeşidi olduğunu, Kanyon çeşidinin ise daha az uygun konukçu olduğunu göstermiştir.

Anahtar Kelimeler

• Yaş ve döneme özgü iki eşeyli yaşam çizelgesi
• Capsicum annuum
• enzimatik antioksidan
• Myzus persicae

References

1. Andrewartha, H. & L. Birch, 1954. The Distribution and Abundance of Animals: University of Chicago. Chicago, Illinois, USA, 782 pp.
2. Baldin, E. L. L., M. D. Stamm, J. P. F. Bentivenha, K. G. Koch, T. M. Heng-Moss & T.E. Hunt, 2018. Feeding behavior of Aphis glycines (Hemiptera: Aphididae) on soybeans exhibiting antibiosis, antixenosis, and tolerance resistance. Florida Entomologist, 101 (2): 223-228.
3. Bass, C., A. M. Puinean, C. T. Zimmer, I. Denholm, L. M. Field, S. P. Foster, O. Gutbrod, R. Nauen, R. Slater & M. S. Williamson, 2014. The evolution of insecticide resistance in the peach potato aphid, Myzus persicae. Insect Biochemistry and Molecular Biology, 51 (3): 41-51.
4. Berger, D., 2006. A gentle introduction to resampling techniques. Western Psychological Association Statistical Workshop. Claremont Graduate University. (Web page: http://wise.cgu.edu/wp-content/uploads/2015/04/Introduction-to-Resampling-Techniques-110901.pdf) (Date accessed: May 2016).
5. Bi, J. L. & G. W. Felton, 1995. Foliar oxidative stress and insect herbivory: primary compounds, secondary metabolites, and reactive oxygen species as components of induced resistance. Journal of Chemical Ecology, 21 (10): 1511-1530.
6. Bozokalfa, M. K. & D. Eşiyok, 2010. Biber (Capsium annum L.) aksesyonlarında genetik çeşitliliğin agronomik özellikler ile belirlenmesi. Ege Üniversitesi Ziraat Fakültesi Dergisi, 47 (2): 123-134 (in Turkish with abstract in English).
7. Bradford, M. M., 1976. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Analytical Biochemistry, 72 (1-2): 248-254.
8. Cabrera-Brandt, M. A., E. Fuentes-Contreras & C. C. Figueroa, 2010. Differences in the detoxification metabolism between two clonal lineages of the Aphid Myzus persicae (Sulzer) (Hemiptera: Aphididae) reared on tobacco (Nicotiana tabacum L.). Chilean Journal of Agricultural Research, 70 (4): 567-575.

9. Cameron, R., E. B. Lang, I. B. Annan, H. E. Portillo & J. M. Alvarez, 2013. Use of fluorescence, a novel technique to determine reduction in Bemisia tabaci (Hemiptera: Aleyrodidae) nymph feeding when exposed to Benevia and other insecticides. Journal of Economic Entomology, 106 (2): 597-603.
10. Cao, H. H., M. Z. Pan, H. R. Liu, S. H. Wang & T. X. Liu, 2015. Antibiosis and tolerance but not antixenosis to the grain aphid, Sitobion avenae (Hemiptera: Aphididae), are essential mechanisms of resistance in a wheat cultivar. Bulletin of Entomological Research, 105 (4): 448-455.
11. Chi, H. & H. Liu, 1985. Two new methods for the study of insect population ecology. Bulletin of the Institute of Zoology, Academia Sinica, 24 (2): 225-240.
12. Chi, H. & H. Y. Su, 2006. Age-Stage, Two-sex life tables of Aphidius gifuensis (Ashmead) (Hymenoptera: Braconidae) and its Host Myzus persicae (Sulzer) (Homoptera: Aphididae) with mathematical proof of the relationship between female fecundity and the net reproductive Rate. Environmental Entomology, 35 (1): 10-21.
13. Chi, H., 1988. Life-table analysis incorporating both sexes and variable development rates among individuals. Environmental Entomology, 17 (1): 26-34.
14. Chi, H., 1990. Timing of control based on the stage structure of pest populations: a simulation approach. Journal of Economic Entomology, 83 (4): 1143-1150.
15. Chi, H., 2022a. TWOSEX-MSChart: a computer program for the age-stage, two-sex life table analysis. National Chung Hsing University, Taichung, Taiwan., TWOSEX-MSChart: (Web page: http://140.120.197.173/Ecology/Download/ Twosex-MSChart-exe-B100000.rar) (Date accessed: 2022).
16. Chi, H., 2022b. TIMING-MSChart: A computer program for the population projection based on age-stage, two-sex life table. National Chung Hsing University, Taichung, Taiwan. TIMING-MSChart: (Web page: http://140.120.197.173/ Ecology/Download/TIMING-MSChart-exe.rar) (Date accessed: 2022).
17. Chi, H., M. You, R. Atlıhan, C. L. Smith, A. Kavousi, M. S. Özgökçe, A. Güncan, S. J. Tuan, J. W. Fu, Y. Y. Xu, F. Q. Zheng, B. H. Ye, D. Chu, Y. Yu, G. Gharekhani, P. Saska, T. Gotoh, M. I. Schneider, P. Bussaman, A. Gökçe & T. X. Liu, 2020. Age-Stage, two-sex life table: an introduction to theory, data analysis, and application. Entomologia Generalis, 40 (2): 103-124.
18. Cruz, P. L. & E. L. Baldin, 2017. Performance of Bemisia tabaci Biotype B on Soybean Genotypes. Neotropical Entomology, 46 (1): 210-215.
19. Downer, R. G., 1985. Lipid metabolism. Comprehensive İnsect Physiology, Biochemistry and Pharmacology, 10 (1): 77-113.
20. Efron, B., 1982. The Jackknife, the Bootstrap, and Other Resampling Plans. CBMS-NSF Regional Conference Series in Applied Mathematics, 85 pp.
21. Efron, B. & R. J. Tibshirani, 1994. An Introduction to the Bootstrap. Chapman and Hall/CRC, CRC Press, 456 pp.
22. Eşiyok, D., 2006. Biberin anavatanı ve yayılışı. (Web page: http://www.dunyagida.com.tr/haber/biberin-anavatani-ve-yayilisi/2045) (Date accessed: 08.04.2019) (in Turkish).
23. FAO, 2020. Food and Agriculture Organization of the United Nations. (Web page: http://www.fao.org/faostat/en/#home) (Date accessed: May 2016).
24. Fisher, R. A., 1930. The Genetical Theory of Natural Selection. Dover, Clarendon Press, Oxford, 310 pp.
25. Goodman, D., 1982. Optimal life histories, optimal notation, and the value of reproductive value. The American Naturalist, 119 (6): 803-823.
26. Habig, W. H., M. J. Pabst & W. B. Jakoby, 1974. Glutathione S-transferases the first enzymatic step in mercapturic acid formation. Journal of biological Chemistry, 249 (22): 7130-7139.
27. Hong, F., H. L. Han, P. Pu, D. Wei, J. Wang & Y. Liu, 2019. Effects of five host plant species on the life history and population growth parameters of Myzus persicae (Hemiptera: Aphididae). Journal of Insect Science, 19 (6): 803-823.
28. Huang, Y. B. & H. Chi, 2011. The age-stage, two-sex life table with an offspring sex ratio dependent on female age. Journal of Agriculture & Forestry, 60 (4): 337-345.
29. Huang, Y. B. & H. Chi, 2012. Assessing the application of the jackknife and bootstrap techniques to the estimation of the variability of the net reproductive rate and gross reproductive rate: A case study in Bactrocera cucurbitae (Coquillett) (Diptera: Tephritidae). Journal of Agriculture and Forestry, 61 (1): 37-45.
30. Huang, Y. B. & H. Chi, 2013. Life tables of Bactrocera cucurbitae (Diptera: Tephritidae): With an invalidation of the jackknife technique. Journal of Applied Entomology, 137 (5): 327-339.
31. Huang, Z., J. T. Pinto, H. Deng & J. P. Richie Jr, 2008. Inhibition of caspase-3 activity and activation by protein glutathionylation. Biochemical Pharmacology, 75 (11): 2234-2244.
32. Jamieson, D., 1989. Oxygen toxicity and reactive oxygen metabolites in mammals. Free Radical Biology and Medicine, 7 (1): 87-108.
33. Jha, R. K., H. Chi & L. C. Tang, 2012. Life Table of Helicoverpa armigera (Hübner) (Lepidoptera: Noctuidae) with a discussion on jackknife vs. bootstrap techniques and variations on the euler-lotka equation. Formosan Entomology, 32: 355-375.
34. Kazek, M., A. Kaczmarek, A. K. Wrońska & M. I. Boguś, 2020. Conidiobolus coronatus induces oxidative stress and autophagy response in Galleria mellonella larvae. PLoS ONE, 15 (2): e0228407.
35. Kogan, M. & E. F. Ortman, 1978. Antixenosis-a new term proposed to define Painter's “nonpreference” modality of resistance. Bulletin of the ESA, 24 (2): 175-176.
36. Konuş, M., 2014. Analysing resistance of different Tuta absoluta (Meyrick) (Lepidoptera: Gelechiidae) strains to abamectin insecticide. Turkish Journal of Biochemistry, 39 (3): 291-297.
37. Konuş, M., S. U. Karaagaç & M. Iscan, 2014. Analysis of molecular resistance mechanisms in Helicoverpa armigera (Hübner) (Noctuidae: Lepidoptera) populations under pyrethroid stress in Turkey. Journal of the Entomological Research Society, 16 (2): 81-92.
38. 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: Published in Collaboration with the Entomological Society of America, 63 (1): 1-10.
39. la Rossa, F. R., A. Vasicek & M. C. Lopez, 2013. Effects of pepper (Capsicum annuum) cultivars on the biology and life table parameters of Myzus persicae (Sulz.) (Hemiptera: Aphididae). Neotropical Entomology, 42 (1): 634-641.
40. Lukasik, I. & S. Goławska, 2013. Effect of host plant on levels of reactive oxygen species and antioxidants in the cereal aphids Sitobion avenae and Rhopalosiphum padi. Biochemical Systematics & Ecology, 51 (1): 232-239.
41. Lukasik, I., S. Golawska, A. Wojcicka & A. Golawski, 2011. Effect of host plants on antioxidant system of pea aphid Acyrthosiphon pisum. Bulletin of Insectology, 64 (2): 153-158.
42. Luo, S. l., S. J. Zhang & D. T. Zhang Sun, 2003. Investigation on aphid species of Capsicum annuum [J]. Journal of Biology, 20 (1): 22-24.
43. Musaogullari, A., A. Mandato & Y. C. Chai, 2020. Role of glutathione depletion and reactive oxygen species generation on caspase-3 activation: a study with the kinase inhibitor staurosporine. Frontiers in Physiology, 11 (1): 998-1005.
44. Naranjo, S. E. & J. P. Legg, 2010. “Biology and Ecology of Bemisia tabaci, 105-107”. In: Bemisia: Bionomics and Management of a Global Pest (Eds. P. A. Stansly & S. E. Naranjo). Springer, Dordrecht, 540 pp.
45. Nikolakakis, N., J. Margaritopoulos & J. Tsitsipis, 2003. Performance of Myzus persicae (Hemiptera: Aphididae) clones on different host-plants and their host preference. Bulletin of Entomological Research, 93 (3): 235-242.
46. Ologundudu, F., 2021. Antioxidant enzymes and non-enzymatic antioxidants as defense mechanism of salinity stress in cowpea (Vigna unguiculate L. Walp)-Ife brown and Ife bpc. Bulletin of the National Research Centre, 45 (1): 152-156.
47. Orozco-Cardenas, M. & C. A. Ryan, 1999. Hydrogen peroxide is generated systemically in plant leaves by wounding and systemin via the octadecanoid pathway. Proceedings of the National Academy of Sciences, 96 (11): 6553-6557.
48. Özgökçe, M. S., H. Chi, R. Atlıhan & H. Kara, 2018. Demography and population projection of Myzus persicae (Sulz.) (Hemiptera: Aphididae) on five pepper (Capsicum annuum L.) cultivars. Phytoparasitica, 46 (1): 153-167.
49. Painter, R. H., 1951. Insect resistance in crop plants. Soil Science, 72 (6): 481-481.
50. Panda, N. & G. Khush, 1995. Host Plant Resistance to Insects. CAB international, Wallingford, UK, 436 pp.
51. Petitt, F., C. Loader & M. Schon, 1994. Reduction of nitrogen concentration in the hydroponic solution on population growth rate of the aphids (Homoptera: Aphididae) Aphis gossypii on cucumber and Myzus persicae on pepper. Environmental Entomology, 23 (4): 930-936.
52. Qayyum, A., M. A. Aziz, A. Iftikhar, F. Hafeez & R. Atlihan, 2018. Demographic Parameters of Lipaphis erysimi (Hemiptera: Aphididae) on Different Cultivars of Brassica Vegetables. Journal of Economic Entomology, 111 (4): 1885-1894.
53. Qing, C., 2002. A study on the correlation between several chemical substances and Capsicum cultivar resistance to Myzus persicae (Sulzer). Acta Horticulturae Sinica, 29 (6): 533-536.
54. Ramsey, J. S., D. S. Rider, T. K. Walsh, M. De Vos, K. H. Gordon, L. Ponnala, S. L. Macmil, B. A. Roe & G. Jander, 2010. Comparative analysis of detoxification enzymes in Acyrthosiphon pisum and Myzus persicae. Insect Molecular Biology, 19 (1): 155-164.
55. Razazzian, S., M. R. Hassani, S. Imani & M. Shojai, 2015. Life table parameters of Plodia interpunctella (Lepidoptera: Pyralidae) on four commercial pistachio cultivars. Journal of Asia-Pacific Entomology, 18 (1): 55-59.
56. Razmjou, J. & A. Golizadeh, 2010. Performance of corn leaf aphid, Rhopalosiphum maidis (Fitch) (Homoptera: Aphididae) on selected maize hybrids under laboratory conditions. Applied Entomology and Zoology, 45 (2): 267-274.
57. Sedlak, J. & R. H. Lindsay, 1968. Estimation of total, protein-bound, and nonprotein sulfhydryl groups in tissue with Ellman's reagent. Analytical Biochemistry, 25 (1): 192-205.
58. Silva, J. P. G. F., E. L. L. Baldin, E. S. Souza & A. L. Lourenção, 2012. Assessing Bemisia tabaci (Genn.) biotype B resistance in soybean genotypes: Antixenosis and antibiosis. Chilean Journal of Agricultural Research, 72 (4): 516-522.
59. Singh, R. R. & K. M. Reindl, 2021. Glutathione S-transferases in cancer. Antioxidants, 10 (5): 701-726.
60. Smith, C. M. & S. L. Clement, 2012. Molecular bases of plant resistance to arthropods. Annual Review of Entomology, 57: 309-328.
61. Smith, C. M., 2005. Plant Resistance to Arthropods: Molecular and Conventional Approaches. Springer Science & Business Media. Dordrechet, 423 pp.
62. Stansly, P. A. & E. T. Natwick, 2009. “Integrated Systems for Managing Bemisia tabaci in Protected and Open Field Agriculture, 467-497”. In: Bemisia: Bionomics and Management of a Global Pest, (Eds. P. A. Stansly & S. E. Naranjo). Springer, Dordrecht, 544 pp.
63. Stenberg, J. A. & A. Muola, 2017. How should plant resistance to herbivores be measured? Frontiers in Plant Science, 8 (1): 663-667.
64. Stout, M. J., 2007. “Types and Mechanisms of Rapidly Induced Plant Resistance to Herbivorous Arthropods, 89-107”. In: Induced Resistance for Plant Defense (Eds. D. Walters, A. Newton & G. Lyon), Wiley, 272 pp.
65. Sulistyo, A. & A. Inayati, 2016. Mechanisms of antixenosis, antibiosis, and tolerance of fourteen soybean genotypes in response to whiteflies (Bemisia tabaci). Biodiversitas Journal of Biological Diversity, 17 (2): 447-453.
66. Tsai, J. H. & J. J. Wang, 2001. Effects of host plants on biology and life table parameters of Aphis spiraecola (Homoptera: Aphididae). Environmental Entomology, 30 (1): 44-50.
67. Tuan, S. J., C. C. Lee & H. Chi, 2014. Population and damage projection of Spodoptera litura (F.) on peanuts (Arachis hypogaea L.) under different conditions using the age-stage, two-sex life table. Pest Management Science, 70 (5): 805-813.
68. TUIK, 2022. Turkish Statistical Institute. (Web page: http://www.tuik.gov.tr/Start.do) (Date accessed: May 2022).
69. van Asperen, K., 1962. A study of housefly esterases by means of a sensitive colorimetric method. Journal of Insect Physiology, 8 (4): 401-416.
70. van Emden, H. F. & R. Harrington, 2017. Aphids as Crop Pests. (Eds. H.F. van Emden & R. Harrington), CABI Publishing, London, 717 pp.
71. Vieira, S., A. Bueno, M. Boff, R. Bueno & C. Hoffman-Campo, 2011. Resistance of soybean genotypes to Bemisia tabaci (Genn.) biotype B (Hemiptera: Aleyrodidae). Neotropical Entomology, 40 (1): 117-122.
72. Vontas, J. G., G. J. Small & J. Hemingway, 2001. Glutathione S-transferases as antioxidant defense agents confer pyrethroid resistance in Nilaparvata lugens. Biochemical Journal, 357 (1): 65-72.
73. Wei, M., H. Chi, Y. Guo, X. Li, L. Zhao & R. Ma, 2020. Demography of Cacopsylla chinensis (Hemiptera: Psyllidae) reared on four cultivars of Pyrus bretschneideri (Rosales: Rosaceae) and P. communis pears with estimations of confidence intervals of specific life table statistics. Journal of Economic Entomology, 113 (5): 2343-2353.
74. Yang, T. C. & H. Chi, 2006. Life tables and development of Bemisia argentifolii (Homoptera: Aleyrodidae) at different temperatures. Journal of Economic Entomology, 99 (3): 691-698.
75. Yılmaz, C., A. Othman Pirdawid, C. Fidan Babat, M. Konuş, D. Çetin, A. Kıvrak & A. Kurt Kızıldoğan, 2022. A thiophene derivative, 2‐Bromo‐5‐(2‐(methylthio) phenyl) thiophene, has effective anticancer potential with other biological properties. Chemistry Select, 7 (15): e202200784 (1-8).
76. Yin, W. D., G. S. Qiu, W. T. Yan, L. N. Sun, H. J. Zhang, C. S. Ma & U. P. Adaobi, 2013. Age-stage two-sex life tables of Panonychus ulmi (Acari: Tetranychidae), on different apple varieties. Journal of Economic Entomology, 106 (5): 2118-2125.
77. Yu, J. Z., H. Chi & B. H. Chen, 2013. Comparison of the life tables and predation rates of Harmonia dimidiata (F.) (Coleoptera: Coccinellidae) fed on Aphis gossypii Glover (Hemiptera: Aphididae) at different temperatures. Biological Control, 64 (1): 1-9.