Effect of Micronutrient Fertilizers on Digestive Enzymes Activity of Hippodamia variegata (Goeze) Fed on Myzus persicae (Sulzer)

پژوهش های حفاظت گیاهان ایران

Article 6, Volume 36, Issue 2 - Serial Number 56, June 2022, Pages 213-225   

Document Type: Research Article

DOI: 10.22067/jpp.2022.74291.1070

Authors

T. Alizamani^{* 1}; J. Shakarami²; M. Mardani Talaee³; A. Zibaee⁴

¹Department of Plant Protection, Faculty of Agriculture and Natural Resources, Lorestan University, Lorestan, Iran.

²Department of Plant Protection, College of Agriculture Lorestan University

³Department of Plant Protection, Faculty of Agriculture and Natural Resources, University of Mohaghegh Ardabili, Ardabil, Iran

⁴Department of Plant Protection, Faculty of Agriculture, University of Guilan-Rasht, Iran

Abstract

Introduction
 The green peach aphid Myzus persicae (Sulzer) (Hemiptera: Aphididae) is one of the severe pests of bell pepper Capsicum annuum L. in the greenhouse. Ladybird, Hippodamia variegata (Goeze), is an important general predator in both larval and adult stages to various aphid species, including, M. persicae. In this study, the effect of nutritional interaction among plant-herbivore-natural enemy under the influence of foliar application of iron, zinc, copper and manganese in bell pepper on the activity of digestive enzymes of the third and fourth instar larvae of H. variegata fed on M. persicae was examined.
Materials and Methods
 The experiments were performed as a completely randomized design with four replicates per treatment during 2020-2021 in the greenhouse and laboratory of the Department of Plant Protection, College of Agriculture, Lorestan University. The foliar application of micronutrient carried out at four-to six-leaf stage with a certain amount of each micronutrient fertilizer. Then, sufficient number of the third and fourth instar larvae of H. variegata were randomly collected from each treatment and replication. The samples transferred to 1 mL of distilled water, and homogenized with a hand pestle. Then, the samples centrifuged at 13000 g for 15 min at 4°C. The supernatants as the enzyme source were collected and reserved at −20°C for starting biochemical assays. The activity of digestive enzymes was measured according to the standard protocols.
Results
 The results showed that the amount of digestive enzymes activity of the third and the fourth instar larvae of H. variegata fed on M. persicae reared on the different micronutrient treatments were higher than the control treatment. The total protease and the trypsin activity were higher in the third instar larvae H. variegata reared on manganese (0.583 and 19.296 U/mg protein) and iron (0.574 and 18.426 U/mg protein), respectively. The highest and lowest activity of chymotrypsin, aminopeptidase and carboxypeptidase were found in the third instar larvae in manganese (15.518, 8.95 and 7.536 U/mg protein) and control (7.353, 2.139 and 2.665 U/ mg protein) treatments, respectively. The highest (18.952) and lowest (9.139 U/ mg protein) elastase activity were found in the third instar larvae on iron and control, respectively. The higher activity of α-amylase (25.20 U/mg protein) was observed in the third instar larvae of H. variegata in iron treatments then the other treatments. The total protease (0.183 U/ mg protein) and the chymotrypsin (10.396 U/ mg protein) of the fourth instar larvae predatory had higher activities with iron treatment and these enzymes had lower activities on control (0.036 and 6.763 U/ mg protein) and copper (0.059 and 6.655 U/ mg protein) treatments. The highest activity of trypsin and aminopeptidase were observed in the fourth instar larvae of H. variegata fed on M. persicae reared on iron (6.893 and 2.317 U/ mg protein) and the highest activity of elastase was found on iron (2.486) and zinc (2.251 U/ mg protein, respectively). Also, the lowest activity of trypsin, aminopeptidase and elastase were found on control. The carboxypeptidase activity was higher in the fourth instar larvae H. variegata fed on the all micronutrients than the control. Also, the highest and lowest activity of α-amylase were observed in the fourth instar larvae H. variegata fed on micronutrients of copper and iron (17.64 and 15.04 U/ mg protein) and control (9.160 U/mg protein), respectively.
Discussion
 The results showed that the amount of digestive enzymes activity of the third and the fourth instar larvae of H. variegata fed on M. persicae reared on different micronutrient treatments were higher than the control treatment.
 Based on the results, the foliar application of plants with micronutrient fertilizers has a positive effect on the performance of predator of H. variegata through nutritional interaction and improving of the growth quality. Thus, the quality of host plants, as the first level of nutrition, has an important effect on the physiological characteristics of the predator on the third level of nutrition and show the positive effect of prey nutrients on the physiological performance of H. variegata that can be used in M. persicae management programs.
Conclusion
 Using different micronutrient fertilizers along with biological control agents such as ladybird H. variegata could be effective in integrated management programs of M. persicae through the growth quality improvement of the host plants.

Keywords

Digestive enzymes; Hippodamia variegata; Micronutrient fertilizers

References

1. Alizamani, T., Shakarami, J., Mardani- Talaee, M., Zibaee, A., & Serrão,E. (2020). Direct interaction between micronutrients and bell pepper (Capsicum annuum L.), to affect fitness of Myzus persicae (Sulzer). Journal of Plant Protection Research 60: 253-262. https://doi.org/10.24425/jppr.2020.133319.
2. Alizamani, T., Shakarami, J., Mardani- Talaee, M., Zibaee, A., & Serrao, J.E. (2021a). Micronutrient fertilizers affect the digestibility, intermediary metabolism, and oxidative stress in Myzus persicae (Sulzer). Neotropical Entomoloy 50: 940- https://doi.org/10.1007/s13744-021-00893-z.
3. Alizamani, T., Shakarami, J., Mardani- Talaee, M., Zibaee, A., & Serrao, J.E. (2021b). Induce of antibiotic resistance in bell pepper, Capsicum annuum L, against green peach aphid, Myzus persicae (Sulzer), by micronutrient fertilizers. Iranian Journal of Plant Protection Science 52(2): 73-85. https://doi.org/22059/IJPPS.2021.319609.1006969.
4. Bernfeld, P. (1955). Amylases, α and β. Methods in Enzymology 1: 149- https://doi.org/10.1016/0076-6879(55)01021-5.
5. Bigham, M., & Hosseininaveh, V. (2010). Digestive proteolytic activity in the pistachio green stink bug, Brachynema germari Kolenati (Hemiptera: Pentatomidae). Journal of Asia Pacific Entomology 13: 221- https://doi.org/10.1016/j.aspen.2010.03.004.
6. Broadway, R.M., & Duffey, S.S. (1988). The effect of plant protein quality on insect digestive physiology and the toxicity of plant proteinase inhibitors. Journal of Insect Physiology 34: 1111- https://doi.org/10.1016/0022-1910(88)90213-2.
7. De Clercq, P., Merlevede, F., & Tirry L. (1998). Unnatural prey and artificial diets for rearing Podisus maculiventris (Heteroptera: Pentatomidae). Biological Control 12: 137-
8. Elpidina, E.N., Vinokurov, K.S., Gromenko, V.A., Rudenskaya, Y.A., Dunaevsky, Y.E., & Zhuzhikov, D.P. (2001). Compartmentalization of proteinases and amylases in Nauphoeta cinerea Archives of Insect Biochemistry and Physiology 48: 206-216. https://doi.org/10.1002/arch.10000.
9. Felton, G.W. (1996). Nutritive quality of plant protein: sources of variation and insect herbivore responses. Archives of Insect Biochemistry and Physiology 32: 107-130.
10. Fenton, B., Kasprowicz, L., Malloch, G., & Pickup, J. (2010). Reproductive performance of asexual clones of the peach-potato aphid, Myzus persicae, (Homoptera: Aphididae), colonising Scotland in relation to host plant and field ecology. Bulletin of entomological research 100: 451-460.
11. Ferreira, C., & Terra, W.R. (1983). Physical and kinetic properties of a plasma-membrane-bound P-Dglucosidase (cellobiase) from midgut cells of an insect Rhynchosciara americana Biochemical Journal 213: 43-51.
12. Franco, O.L., Rigden, D.J., Melo, F.R., Bloch, C.Jr., Silva, C.P., & Grossi, de Sá M.F. (2000). Activity of wheat α‐amylase inhibitors towards bruchid α‐amylases and structural explanation of observed specificities. European Journal of Biochemistry 267: 2166- https://doi.org/10.1046/j.1432-1327.2000. 01199.x.
13. Gatehouse, A.M.R., Norton, E., Davidson, G.M., Babbe, S.M., & Newell, C.A. (1999). Digestive proteolytic activity in larvae of tomato moth, Lacenobia oleracea; effects of plant protease inhibitors in vitro and in vivo. Journal of Insect Physiology 45: 545-
14. Habibi, J., Backus, E.A., Coudron, T.A., & Brandt, S.L. (2001). Effect of different host substrates on hemipteran salivary protein profiles. Entomologia Experimentalis et Applicata 98: 369-
15. Hansch, R., & Mendel, R.R. (2009). Physiological functions of mineral micronutrients (Cu, Zn, Mn, Fe, Ni, Mo, B, Cl). Current Opinion in Plant Biology 12: 259- https://doi.org/10.1016/j.pbi.2009.05.006.
16. Jansen, B., & Groot, A. (2004). Occurrence, biological activity and synthesis of drimane sesquiterpenoids. Natural Product Reports Article 21: 449-477. https://doi.org/1039/b311170a.
17. Kalushkov, P., & Hodek, I. (2004). The effects of thirteen species of aphids on some life history parameters of the ladybird Coccinella septempunctata. Biological Control 50: 223-
18. Kontodimas, D.C., & Stathas, G.J. (2005). Phenology, fecundity and life table parameters of the predator Hippodamia variegata reared on Dysaphis crataegi. Biocontrol 50: 223-233. https://doi.org/10.1007/s10526-004-0455-7.
19. Lu, Z.X., Yu, X.P., Heong, K.L., & Hu, C. (2007). Effect of nitrogen fertilizer on herbivores and its stimulation to major insect pests in rice. Rice Science 14: 56-66. https://doi.org/10.1016/S1672-6308(07)60009-2.
20. Mardani-Talaee, M., Zibaee, A., Nouri-Ganblani,, & Razmjou, J. (2016). Chemical and organic fertilizers affect physiological performance and antioxidant activities in Myzus persicae (Hemiptera: Aphididae). Invertebrate Survival Journal 13: 122-133.
21. Mendiola-Olaya, E., Valencia-Jimenez, A., Valdés-Rodrı́guez, S., Delano-Frier, J., & Blanco-Labra, A. (2000). Digestive amylase from the larger grain borer, Prostephanus truncatus Comparative Biochemistry and Physiology Part B: Biochemistry and Molecular Biology 126: 425-433.
22. Mirab-balou, M., & Alizamani, T. (2022). The effect of nutritional interaction between micronutrient fertilizers and Capsicum annuum on the population growth of Aphidoletes aphidimyza Rondani as predator of green peach aphid. Journal of Iranian Plant Protection Research 35(4): 481-494. https://doi.org/10.22067/JPP.2021.70745.1028.
23. Mottaghinia, L., Hassanpour, M., Razmjou, J., Chamani, E., & Hosseini, M. (2015). The effect of vermicompost on some biological characteristics of the melon aphid Aphis gossypii Glover and the predatory gall midge Aphidoletes aphidimyza Rondani on two cultivars of greenhouse cucumber. Applied research in plant protection 4(2): 56-70.
24. Musa, P.D., & Ren, S.X. (2005). Development and reproduction of Bemisia tabaci (Homoptera: Aleyrodidae) on three bean species. Insect Science 12: 25-30. https://doi.org/1111/j.1672-9609.2005.00004.x.
25. Nation, J.L. (2008). Insect physiology and biochemistry (2th ed.), London, CRC press, UK.
26. Obrycki, J.J., & Kring, T.J. (1998). Predaceous coccinellidae in biological control. Annual Review of Entomology l43: 295- https://doi.org/10.1146/annure.ento.43.1.295.
27. Omkar James, B.E. (2004). Influence of prey species on immature survival, development, predation and reproduction of Coccinella transversalis Fabricius (Col.: Coccinellidae). Journal of Applied Entomology 128: 150- https://doi.org/10.1111/j.1439-0418.2004.00826.x.
28. Özgökçe, M.S., Chi, H., Atlıhan, R., & Kara, H. (2018). Demography and population projection of Myzus persicae (Sulzer.) (Hemiptera: Aphididae) on five pepper (Capsicum annuum) cultivars. Phytoparasitica 46:153-167. https://doi.org/10.1007/s12600-018-0651-0.
29. Pascual-Ruiz, S., Carrilo, L., Alvarez-Alfageme, F., Ruiz, M., Castanera, P., & Ortego, F. (2009). The effects of different prey regimes on the proteolytic digestion of nymphs of the spined soldier bug, Podisus maculiventris (Hemiptera: Pentatomidae). Bulletin of Entomological Research 99: 487-491. https://doi.org/1017/S0007485308006561.
30. Price, P.W., Bouton, C.E., Gross, P., McPheron, B.A., Thompson, J.N., & Weis, A. (1980). Interactions among three trophic levels: Influence of plants on interactions between insect herbivores and natural enemies. Annual Reviews of Ecology and Systematics 11: 41-65. https://doi.org/1146/annurev.es.11.110180.000353.
31. Rahbe, Y., Deraison, C., Bonade-Bottino, M., Girard, C., Nardon, C., & Jouanin, L. (2003). Effects of the cysteine protease inhibitor oryzacystatin (OC-I) on different aphids and reduced performance of Myzus persicae on OC-I expressing transgenic oilseed rape. Plant Science 164: 441- https://doi.org/10.1016/S0168-9452(02)00405-8.
32. Schädler, M., Brandl, R., & Kempel, A. (2010). Host plant genotype determines bottom-up effects in an aphid-parasitoid-predator system. Entomologia Experimentalis et Applicata 135: 162-169. https://doi.org/1111/j.1570-7458.2010.00976.x.
33. Scholler, M., Prozell, S.A., Al-Kirshi, G., & Reichmuth, C. (1997). Towards biological control as a major component of integrated pest management in stored product protection. Journal of Stored Products Research 33: 81-97.
34. Silva, L.B., Silva, W., Macedo, M.L.R., & Peres, M.T.L.P. (2009). Effects of croton urucurana extracts and crude resin on Anagasta kuehniella (Lepidoptera: Pyralidae). Brazilian Archives of Biology and Technology 52: 653-664.
35. Sorkhabi-Abdolmaleki, S., Zibaee, A., Hosseini, R., & Hoda, H. (2013). Effects of different prey regimes on activities of digestive enzymes in Andrallus spinidens (Hem.: Pentatomidae). Journal of Entomological Society of Iran 33: 57-68. (In Persian with English abstract)
36. Thompson, S.N. (1999). Nutrition and culture of entomophagous insects. Annual Review of Entomology 44: 561-592. https://doi.org/1146/annurev.ento.44.1.561.
37. Walker, A.J., Ford, L., Majerus, M.E.N., Geoghegan, I.E., Birch, N., Gatehouse, J.A., & Gatehouse, A.M.R. (1998). Characterization of the mid-gut digestive proteinase activity of the two-spot ladybird (Adalia bipunctata ) and its sensitivity to proteinase inhibitors. Insect Biochemistry and Molecular Biology 28: 173-180.
38. Yassen, A., Abou El-Nour, E., & Shedeed S. (2010). Response of wheat to foliar Spray with urea and micronutrients. Journal of American Science 6: 14-22.