Eur. J. Entomol. 116: 1-9, 2019 | DOI: 10.14411/eje.2019.001
Effects of temperature on the activity of antioxidant enzymes in larvae of Bactrocera dorsalis (Diptera: Tephritidae) parasitized by Diachasmimorpha longicaudata (Hymenoptera: Braconidae): Optimizing the mass rearing of this braconid by varying the temperatureOriginal article
- 1 Institute of Beneficial Insects, Plant Protection College, Fujian Agriculture and Forestry University, 350002 Fuzhou, P.R. China; e-mails: caipumo@qq.com, 1506293481@qq.com, 602328593@qq.com, 344463987@qq.com, 523441201@qq.com, 776954169@qq.com, zhh680216@163.com, 2576680960@qq.com, jiqinge@yeah.net, jhchen34@yeah.net
- 2 State Key Laboratory of Ecological Pest Control for Fujian and Taiwan Crops, 350002 Fuzhou, P.R. China
- 3 Key Lab of Biopesticide and Chemical Biology, Ministry of Education, 350002 Fuzhou, P.R. China
Diachasmimorpha longicaudata is the most widely used endoparasitoid in biocontrol programmes against various species of tephritids and is continuously mass-reared under laboratory conditions at a constant temperature; however, little is known about how varying the temperature might affect the effectiveness of the mass rearing of immature D. longicaudata. This study aimed to determine the optimum temperature for the development of larvae D. longicaudata the larvae of its host, Bactrocera dorsalis. Third-instar B. dorsalis were exposed for 4 h to five pairs of parasitoids, and then they were kept at one of six temperatures ranging from 19°C to 34°C. The activities of three major antioxidant enzymes (CAT, POX, SOD) were individually measured 4, 24, 48 and 72 h after exposure to each of the six temperatures. The results were as follows: for CAT the highest CAT activities were recorded at 25°C (intervals 5-24 h and 25-48 h), at 28°C (interval 0-4 h) and at 31°C (interval 49-72 h), and for POX and SOD identically at 25°C (intervals 0-4 h, 5-24 h) and at 31°C (intervals 25-48 h, 49-72 h), respectively. Subsequently, the effects keeping the parasitized larvae at these different temperatures on the biological attributes of D. longicaudata reared under laboratory conditions were investigated. The percentage of their eggs that hatched, percentage of adults that emerged, pupal weight and longevity were significantly greater than that recorded for the control when the parasitized host larvae were kept at 28°C for 4 h, 25°C for 5 and 48 h and 31°C for 49 and 72 h.
Keywords: Diptera, Tephritidae, Bactrocera dorsalis, Hymenoptera, Braconidae, Diachasmimorpha longicaudata, parasitoid, altering temperatures, mass-reared, activity of antioxidants
Received: February 23, 2018; Revised: November 20, 2018; Accepted: November 20, 2018; Published online: January 4, 2019 Show citation
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References
- Abele D., Burlando B., Viarengo A. & Pörtner H.O. 1998: Exposure to elevated temperatures and hydrogen peroxide elicits oxidative stress and antioxidant response in the Antarctic intertidal limpet Nacella concinna. - Comp. Biochem. Physiol. (B) 120: 425-435.
Go to original source... - Ahmad S. 1992: Biochemical defence of pro-oxidant plant allelochemicals by herbivorous insects. - Biochem. Syst. Ecol. 20: 269-296.
Go to original source... - Ahmad S. & Pardini R.S. 1990: Mechanisms for regulating oxygen toxicity in phytophagous insects. - Free Radical Biol. Med. 8: 401-413.
Go to original source... - Ahmad S., Duval D.L., Weinhold L.C. & Pardini R.S. 1991: Cabbage looper antioxidant enzymes: tissue specificity. - Insect Biochem. 21: 563-572.
Go to original source... - Ali A., Rashid M.A., Huang Q.Y. & Lei C.L. 2017: Influence of UV-A radiation on oxidative stress and antioxidant enzymes in Mythimna separata (Lepidoptera: Noctuidae). - Environ. Sci. Pollut. Res. 24: 8392-8398.
Go to original source... - Allwood A.J., Chinajariyawong A., Kritsaneepaiboon S., Drew R.A.I, Hamacek E.L., Hancock D.L., Hengsawad C., Jipanin J.C., Jirasurat M., Krong C.K., Leong C.T.S. & Vijaysegaran S. 1999: Host plant records for fruit flies (Diptera: Tephritidae) in Southeast Asia. - Raffles B. Zool. 47: 1-92.
- Aluja M., Sivinski J., Ovruski S., Guillén L., López M., Cancino J., Torres-Anaya A., Gallegos-Chan G. & Ruíz L. 2009: Colonization and domestication of seven species of native new world hymenopterous larval-prepupal and pupal fruit fly (Diptera: Tephritidae) parasitoids. - Biocontrol Sci. Techn. 19: 49-79.
Go to original source... - An M.I. & Choi C.Y. 2010: Activity of antioxidant enzymes and physiological responses in ark shell, Scapharca broughtonii, exposed to thermal and osmotic stress: effects on hemolymph and biochemical parameters. - Comp. Biochem. Phys. (B) 155: 34-42.
Go to original source... - Baranowski R., Glenn H. & Sivinski J. 1993: Biological control of the Caribbean fruit fly (Diptera: Tephritidae). - Fla Entomol. 76: 245-251.
Go to original source... - Bradford M.M. 1976: A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. - Anal. Biochem. 72: 248-254.
Go to original source... - Cai P.M., Gu X.H., Yao M.Y., Zhang H.H., Huang J., Idress A., Ji Q.E., Chen J.H. & Yang J.Q. 2017: The optimal age and radiation dose for Bactrocera dorsalis (Hendel) (Diptera: Tephritidae) eggs as hosts for mass-reared Fopius arisanus (Sonan) (Hymenoptera: Braconidae). - Biol. Control 108: 89-97.
Go to original source... - Cai P.M., Hong J.F., Wang C., Yang Y.C., Zhang Q.W., Ji Q.E. & Chen J.H. 2018a: Radiation of Bactrocera dorsalis (Diptera: Tephritidae) eggs to improve the mass rearing of Diachasmimorpha longicaudata (Hymenoptera: Braconidae). - J. Econ. Entomol. 111: 1157-1163.
Go to original source... - Cai P.M., Hong J.F., Wang C., Yang Y.C., Yi C.D., Chen J.H. & Ji Q.E. 2018b: Effects of Co-60 radiation on the activities of three main antioxidant enzymes in Bactrocera dorsalis (Hendel) (Diptera: Tephritidae). - J. Asia-Pac. Entomol. 21: 345-351.
Go to original source... - Carton Y., Poirié M. & Nappi A.J. 2008: Insect immune resistance to parasitoids. - Insect Sci. 15: 67-87.
Go to original source... - Chihrane J. & Laugé G. 1996: Loss of parasitization efficiency of Trichogramma brassicae (Hym.: Trichogrammatidae) under high-temperature conditions. - Biol. Control 7: 95-99.
Go to original source... - Chinajariyawong A., Clarke A., Jirasurat M., Kritsaneepiboon S., Lahey H., Vijaysegaran S. & Walter G. 2000: Survey of opiine parasitoids of fruit flies (Diptera: Tephritidae) in Thailand and Malaysia. - Raffles Bull. Zool. 48: 71-101.
- Clarke A.R., Allwood A., Chinajariyawong A., Drew R.A., Hengsawad C., Jirasurat M., Krong C.K., Kritsaneepaiboon S. & Vijaysegaran S. 2001: Seasonal abundance and host use patterns of seven Bactrocera Macquart species (Diptera: Tephritidae) in Thailand and Peninsular Malaysia. - Raffles Bull. Zool. 49: 207-220.
- Costa M.L.Z., Pacheco M.G., Lopes L.A., Botteon V.W. & Mastrangelo T. 2016: Irradiation of Anastrepha fraterculus (Diptera: Tephritidae) eggs to inhibit fly emergence in the mass-rearing of Diachasmimorpha longicaudata (Hymenoptera: Braconidae). - J. Insect Sci. 16: 1-9.
Go to original source... - Dubovskiy I.M., Martemyanov V.V., Vorontsova Y.L., Rantala M.J., Gryzanova E.V. & Glupov V.V. 2008: Effect of bacterial infection on antioxidant activity and lipid peroxidation in the midgut of Galleria mellonella L. larvae (Lepidoptera, Pyralidae). - Comp. Biochem. Phys. (C) 148: 1-5.
Go to original source... - Firake D.M. & Khan M.A. 2014: Alternating temperatures affect the performance of Trichogramma species. - J. Insect Sci. 14: 41, 14 pp.
Go to original source... - Foyer C.H., Descourvieres P. & Kunert K.J. 1994: Protection against oxygen radicals: an important defence mechanism studied in transgenic plants. - Plant Cell Environ. 17: 507-523.
Go to original source... - Griswold C.M., Matthews A.L., Bewley K.E. & Mahaffey J.W. 1993: Molecular characterization and rescue of acatalasemic mutants of Drosophila melanogaster. - Genetics 134: 781-788.
Go to original source... - Heck D.E., Vetrano A.M., Mariano T.M. & Laskin J.D. 2003: UVB light stimulates production of reactive oxygen species: unexpected role for catalase. - J. Biol. Chem. 278: 22432-22436.
Go to original source... - Ji Q.E., Bi K. & Chen J.H. 2016: Response of egg-pupal parasitoid Fopius arisanus (Sonan) to infochemicals from the host eggs' surface of Bactrocera dorsalis (Hendel). - J. Asia-Pac. Entomol. 19: 1151-1157.
Go to original source... - Jia F.X., Dou W., Hu F. & Wang J.J. 2011: Effects of thermal stress on lipid peroxidation and antioxidant enzyme activities of oriental fruit fly, Bactrocera dorsalis (Diptera: Tephritidae). - Fla Entomol. 94: 956-963.
Go to original source... - Julsirikul D., Haymer D.S. & Kitthawee S. 2017: Genetic structure and diversity of the Diachasmimorpha longicaudata species complex in Thailand: SSCP analysis of mitochondrial 16S rDNA and COI DNA sequences. - Biochem. Syst. Ecol. 71: 59-68.
Go to original source... - Lee K.S., Kim S.R., Park N.S., Kim I., Kang P.D., Sohn B.H., Choi K.H., Kang S.W., Je Y.H., Lee S.M., Sohn H.D. & Jin B.R. 2005: Characterization of a silkworm thioredoxin peroxidase that is induced by external temperature stimulus and viral infection. - Insect Biochem. Mol. Biol. 35: 73-84.
Go to original source... - Lesser M.P. 2006: Oxidative stress in marine environments: biochemistry and physiological ecology. - Annu. Rev. Physiol. 68: 253-278.
Go to original source... - Liang G.H., Chen Y.R. & Huang J.C. 2007: Effects of parasitism on the activity of peroxidase in the larvae of Bactrocera dorsalis (Diptera: Tephritidae). - J. Cent. South Univ. For. Techn. 27: 48-51.
- Lin L., Huang J.C., Chen J.H., Ji Q.E. & Yang J.Q. 2006: Parasitical efficiency of Diachasmimorpha longicaudata on Bactrocera dorsalis. - Entomol. J. East China 15: 288-290.
- Liu C.Y., Chen K.W. & Zeng L. 2012: Effects of temperature on the development and fecundity of Diachasmimorpha longicaudata (Ashmead). - Chin. J. Appl. Ecol. 23: 3051-3056.
- Livingstone D.R. 2001: Contaminant-stimulated reactive oxygen species production and oxidative damage in aquatic organisms. - Mar. Poll. Bull. 42: 656-666.
Go to original source... - Lopez-Martinez G., Elnitsky M.A., Benoit J.B., Lee R.E. & Denlinger D.L. 2008: High resistance to oxidative damage in the Antarctic midge Belgica antarctica, and developmentally linked expression of genes encoding superoxide dismutase, catalase and heat shock proteins. - Insect Biochem. Mol. Biol. 38: 796-804.
Go to original source... - Luck H. 1971: Bergmeyer H.U. (ed.): Catalase. Methods of Enzymatic Analysis. Academic Press, New York, pp. 885-893.
- Maceda A., Hohmann C.L. & Santos H.R. 2003: Temperature effects on Trichogramma pretiosum Riley and Trichogrammatoidea annulata de Santis. - Braz. Arch. Biol. Techn. 46: 27-32.
Go to original source... - Mannino M.C., Rivarola M., Scannapieco A.C., González S., Farber M., Cladera J.L. & Lanzavecchia S.B. 2016: Transcriptome profiling of Diachasmimorpha longicaudata towards useful molecular tools for population management. - BMC Genomics 17: 793, 13 pp.
Go to original source... - Marklund S. & Marklund G. 1974: Involvement of the superoxide anion radical in the autoxidation of pyrogallol and a convenient assay for superoxide dismutase. - Eur. J. Biochem. 47: 469-474.
Go to original source... - Meirelles R.N., Redaelli L.R. & Ourique C.B. 2013: Comparative biology of Diachasmimorpha longicaudata (Hymenoptera: Braconidae) reared on Anastrepha fraterculus and Ceratitis capitata (Diptera: Tephritidae). - Fla Entomol. 96: 412-418.
Go to original source... - Meirelles R.N., Redaelli L.R. & Ourique C.B. 2015: Thermal requirements and annual number of generations of Diachasmimorpha longicaudata (Hymenoptera: Braconidae) reared in the South American fruit fly and the Mediterranean fruit fly (Diptera: Tephritidae). - Fla Entomol. 98: 1223-1226.
Go to original source... - Ndlela S., Mohamed S., Ndegwa P.N., Ongama G. & Ekesi S. 2016: Release, establishment and dispersal of Diachasmimorpha longicaudata (Ashmead) and Fopius arisanus (Sonan): Hymenoptera: Braconidae, for the management of Bactrocera dorsalis in Kenya. In: Abstracts. Tephritid Workers of Europe, Africa and the Middle East (TEAM 2016), 3rd International Symposium, 11-14 April 2016, Stellenbosch, South Africa.
- Orr W.C. & Sohal R.S. 1994: Extension of life-span by overexpression of superoxide dismutase and catalase in Drosophila melanogaster. - Science 263: 1128-1130.
Go to original source... - Pak G.A. & van Lenteren J.C. 1986: Criteria and methods for the prerelease evaluation of different Trichogramma spp. strains. In Voegele J., Waage J. & Van Lenteren J. (eds): Trichogramma and Other Egg Parasites. 2nd International Symposium, INRA, Guangzhou, China, 10-15 November 1986. pp. 433-441.
- Park M.S., Jo P.G., Choi Y.K., An K.W. & Choi C.Y. 2009: Characterization and mRNA expression of Mn-SOD and physiological responses to stresses in the Pacific oyster Crassostrea gigas. - Mar. Biol. Res. 5: 451-461.
Go to original source... - Polte T. & Tyrrell R.M. 2004: Involvement of lipid peroxidation and organic peroxides in UVA-induced Matrix Metalloproteinase-1 expression. - Free Rad. Biol. Med. 36: 1566-1574.
Go to original source... - Reddy K.P., Subhani S.M., Khan P.A. & Kumar K.B. 1985: Effect of light and benzyladenine on dark-treated growing rice (Oryza sativa) leaves II. Changes in peroxidase activity. - Plant Cell Physiol. 26: 987-994.
Go to original source... - Reznik S.Y., Umarova T.Y. & Voinovich N.D. 1997: The influence of previous host age on current host acceptance in Trichogramma. - Entomol. Exp. Appl. 82: 153-157.
Go to original source... - Segura D.F., Nussenbaum A.L., Viscarret M.M., Devescovi F., Bachmann G.E., Corley J.C., Ovruski S.M. & Cladera J.L. 2016: Innate host habitat preference in the parasitoid Diachasmimorpha longicaudata: functional significance and modifications through learning. - PLoS ONE 11: e0152222, 18 pp.
Go to original source... - Shao T., Liu C.Y., Chen K.W. & Zeng L. 2008: Mass-rearing methods of Bactrocera dorsalis (Diptera: Tephritidae) and itslarval-pupal parasitoid Diachasmimorpha longicaudata (Hymenoptera: Braconidae). - J. Environ. Entomol. 30: 377-380.
- Simmonds T.J., Carrillo D. & Burke G.R. 2016: Characterization of a venom gland-associated rhabdovirus in the parasitoid wasp Diachasmimorpha longicaudata. - J. Insect Physiol. 91-92: 48-55.
Go to original source... - Spencer J.P. & Fujita B.H. 1997: A Procedural Manual for Mass Rearing Four Species of Tephritid Fruit Flies. U.S. Department of Agriculture, Anaesthetics Research Society, Honolulu, HI.
- Tabatabaie T. & Floyd R.A. 1994: Susceptibility of glutathione peroxidase and glutathione reductase to oxidative damage and the protective effect of spin trapping agents. - Arch. Biochem. Biophys. 314: 112-119.
Go to original source... - Vargas R.I., Stark J.D., Uchida G.K. & Purcell M. 1993: Opiine parasitoids (Hymenoptera: Braconidae) of oriental fruit fly (Diptera: Tephritidae) on Kauai Island, Hawaii: islandwide relative abundance and parasitism rates in wild and orchard guava habitats. - Environ. Entomol. 22: 246-253.
Go to original source... - Vargas R.I., Leblanc L., Putoa R. & Eitam A. 2007: Impact of introduction of Bactrocera dorsalis (Diptera: Tephritidae) and classical biological control releases of Fopius arisanus (Hymenoptera: Braconidae) on economically important fruit flies in French Polynesia. - J. Econ. Entomol. 100: 670-679.
Go to original source... - Vargas R.I., Leblanc L., Harris E.J. & Manoukis N.C. 2012: Regional suppression of Bactrocera fruit flies (Diptera: Tephritidae) in the pacific through biological control and prospects for future introductions into other areas of the world. - Insects 3: 727-742.
Go to original source... - Wang X.G. & Messing R.H. 2003: Intra- and interspecific competition by Fopius arisanus and Diachasmimorpha tryoni (Hymenoptera: Braconidae), parasitoids of tephritid fruit flies. - Biol. Control 27: 251-259.
Go to original source... - Wang Y., Guo J.J., Chen J.H. & Ji Q.E. 2013: The changes of the activity of four enzymes in larvae of Bactrocera dorsalis (Hendel) parasitized by Diachasmimorpha longicaudata. - Chin. J. Trop. Crops 34: 335-338.
- Wharton R.A. & Gilstrap F.E. 1983: Key to and status of opiine braconid (Hymenoptera) parasitoids used in biological control of Ceratitis and Dacus s. l. (Diptera: Tephritidae). - Ann. Entomol. Soc. Am. 76: 721-742.
Go to original source... - Wong T.T.Y., Ramadan M.M., Anderson T.E. & Leppla N.C. (eds) 1992: Mass Rearing Biology of Larval Parasitoids (Hymenoptera: Braconidae) of Tephritid Fruit Flies in Hawaii. Advances in Insect Rearing for Research and Pest Management. Westview Press, Boulder, CO, pp. 405-476.
Go to original source... - Yang L.H., Huang H. & Wang J.J. 2010: Antioxidant responses of citrus red mite, Panonychus citri (McGregor) (Acari: Tetranychidae), exposed to thermal stress (Acari: Tetranychidae). - J. Insect Physiol. 56: 1871-1876.
Go to original source... - Yang J.Q., Cai P.M., Chen J., Zhang H.H., Wang C., Xiang H.J., Wu J., Yang Y.C., Chen J.H., Ji Q.E. & Song D.B. 2018: Interspecific competition between Fopius arisanus and Psyttalia incisi (Hymenoptera: Braconidae), parasitoids of Bactrocera dorsalis (Diptera: Tephritidae). - Biol. Control 121: 183-189.
Go to original source... - Zar J.H. 1984: Biostatistical Analysis. Englewood Cliffs, Prentice-Hall, NJ, 718 pp.
- Zhang R.M., He S.Y. & Chen J.H. 2014: Monitoring of Bactrocera dorsalis (Diptera: Tephritidae) resistance to Cyantraniliprole in the south of China. - J. Econ. Entomol. 107: 1233-1238.
Go to original source...
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