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Biological and physiological response of a tropical parasitoid, Tetrastichus brontispae (Ferriere) following exposure to low temperature

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Abstract

Tetrastichus brontispae Ferrière (Hymenoptera: Eulophidae) is an important natural enemy of the coconut leaf beetle Brontispa longissima (Gestro), a serious invasive pest on palm plants. Exposure to low temperature (2 °C) for 4, 24 and 48 h had an adverse effect on biological performance (survival, parasitism rate) of T. brontispae with immature parasitoids (eggs, larvae, and pupae) being more sensitive to low temperature than adults. Exposure to 2 °C for 24 h reduced the water content and increased the concentration of glycerol and trehalose, and activity of superoxidae in T. brontispae adults. Analysis of suppression subtractive hybridization indicated the integrative controlling and transcriptome regulation of the networks in the cold stress response of T. brontispae. Our study suggests that the allocation of energy reserves to either prevent or repair cold-induced damage may consume resources that could otherwise be invested in reproduction and consequently its ability to exert control on B. longissima.

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References

  • Andreadis SS, Vryzas Z, Papadopoulou-mourkidou E, Savopoulou-soultani M (2008) Age-dependent changes in tolerance to cold and accumulation of cryoprotectants in overwintering and non-overwintering larvae of European corn borer Ostrinia nubilalis. Physiol Entomol 33:365–371

    Article  Google Scholar 

  • Ayvaz A, Karasu E, Karabörklü S, Tunçbilek AŞ (2008) Effects of cold storage, rearing temperature, parasitoid age and irradiation on the performance of Trichogramma evanescens Westwood (Hymenoptera: Trichogrammatidae). J Stored Prod Res 44:232–240

    Article  Google Scholar 

  • Bayram A, Ozcan H, Kornosor S (2005) Effect of cold storage on the performance of Telenomus busseolae Gahan (Hymenoptera: Scelionidae), an egg parasitoid of Sesamia nonagrioides (Lefebvre) (Lepidoptera: Noctuidae). Biol Control 35:68–77

    Article  Google Scholar 

  • Bowler K, Terblanche JS (2008) Insect thermal tolerance: what is the role of ontogeny, ageing and senescence? Biol Rev 83:339–355

    Article  PubMed  Google Scholar 

  • Carrillo M, Heimpel G, Moon R, Cannon C, Hutchison W (2005) Cold hardiness of Habrobracon hebetor (Say) (Hymenoptera: Braconidae), a parasitoid of pyralid moths. J Insect Physiol 51:759–768

    Article  CAS  PubMed  Google Scholar 

  • Chamoun R, Samsatly J, Pakala SB, Cubeta MA, Jabaji S (2015) Suppression subtractive hybridization and comparative expression of a pore-forming toxin and glycosyl hydrolase genes in Rhizoctonia solani during potato sprout infection. Mol Genet Genom 290:877–900

    Article  CAS  Google Scholar 

  • Chen C-P, Lee RE Jr, Denlinger DL (1990) A comparison of the responses of tropical and temperate flies (Diptera: Sarcophagidae) to cold and heat stress. J Comp Physiol B 160:543–547

    Article  Google Scholar 

  • Chen W-L, Leopold RA, Boetel MA (2008a) Cold storage of adult Gonatocerus ashmeadi (Hymenoptera: Mymaridae) and effects on maternal and progeny fitness. J Econ Entomol 101:1760–1770

    Article  PubMed  Google Scholar 

  • Chen W-L, Leopold RA, Harris MO (2008b) Cold storage effects on maternal and progeny quality of Gonatocerus ashmeadi Girault (Hymenoptera: Mymaridae). Biol Control 46:122–132

    Article  Google Scholar 

  • Chen Q, Peng Z, Xu C, Tang C, Lu B, Jin Q, Wen H, Wan F (2010) Biological assessment of Tetrastichus brontispae, a pupal parasitoid of coconut leaf beetle Brontispa longissima. Biocontrol Sci Technol 20:283–295

    Article  CAS  Google Scholar 

  • Cheng MY, Hartl F, Martin J, Pollock RA, Kalousek F, Neupert W, Hallberg EM, Hallberg RL, Horwich AL (1989) Mitochondrial heat-shock protein hsp60 is essential for assembly of proteins imported into yeast mitochondria. Nature 337:585–674

    Article  Google Scholar 

  • Colinet H, Boivin G (2011) Insect parasitoids cold storage: a comprehensive review of factors of variability and consequences. Biol Control 58:83–95

    Article  Google Scholar 

  • Colinet H, Hoffmann AA (2012) Comparing phenotypic effects and molecular correlates of developmental, gradual and rapid cold acclimation responses in Drosophila melanogaster. Funct Ecol 26:84–93

    Article  Google Scholar 

  • Colinet H, Muratori F, Hance T (2010) Cold-induced expression of diapause in Praon volucre: fitness cost and morpho-physiological characterization. Physiol Entomol 35:301–307

    Article  Google Scholar 

  • Daane KM, Malakar-Kuenen RD, Walton VM (2004) Temperature-dependent development of Anagyrus pseudococci (Hymenoptera: Encyrtidae) as a parasitoid of the vine mealybug, Planococcus ficus (Homoptera: Pseudococcidae). Biol Control 31:123–132

    Article  Google Scholar 

  • De Bach P (1943) The effect of low storage temperature on reproduction in certain parasitic Hymenoptera. Pan-Pac Entomol 19:112–119

    Google Scholar 

  • Denlinger DL, Lee RE Jr (2010) Low temperature biology of insects. Cambridge University Press, Cambridge

    Book  Google Scholar 

  • Diatchenko L, Lau YL, Campbell A, Chenchik A, Moqadam F, Huang B, Lukyanov S, Lukyanov KA, Gurskaya NG, Siebert PD (1996) Suppression subtractive hybridization: a method for generating differentially regulated or tissue-specific cDNA probes and libraries. Proc Natl Acad Sci USA 93:6025–6030

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dubovskiy I, Martemyanov V, Vorontsova Y, Rantala M, Gryzanova E, Glupov 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

    CAS  Google Scholar 

  • Dunning LT, Dennis AB, Park D, Sinclair BJ, Newcomb RD, Buckley TR (2013) Identification of cold-responsive genes in a New Zealand alpine stick insect using RNA-Seq. Comp Biochem Phys D 8:24–31

    CAS  Google Scholar 

  • Feder ME, Hofmann GE (1999) Heat-shock proteins, molecular chaperones, and the stress response: evolutionary and ecological physiology. Annu Rev Physiol 61:243–282

    Article  CAS  PubMed  Google Scholar 

  • Felton GW, Summers CB (1995) Antioxidant systems in insects. Arch Insect Biochem 29:187–197

    Article  CAS  Google Scholar 

  • Garcia PV, Pereira N, Oliveira LM (2009) Side-effects of organic and synthetic pesticides on cold-stored diapausing prepupae of Trichogramma cordubensis. BioControl 54:451–458

    Article  CAS  Google Scholar 

  • Hance T, van Baaren J, Vernon P, Boivin G (2006) Impact of extreme temperatures on parasitoids in a climate change perspective. Annu Rev Entomol 52:107–126

    Article  CAS  Google Scholar 

  • Hanson AA, Venette RC, Lelito JP (2013) Cold tolerance of Chinese emerald ash borer parasitoids: Spathius agrili Yang (Hymenoptera: Braconidae), Tetrastichus planipennisi Yang (Hymenoptera: Eulophidae), and Oobius agrili Zhang and Huang (Hymenoptera: Encyrtidae). Biol Control 67:516–529

    Article  Google Scholar 

  • Huang LH, Kang L (2007) Cloning and interspecific altered expression of heat shock protein genes in two leafminer species in response to thermal stress. Insect Biochem Mol Biol 16:491–500

    Article  Google Scholar 

  • Jagdale GB, Grewal PS, Salminen SO (2005) Both heat-shock and cold-shock influence trehalose metabolism in an entomopathogenic nematode. J Parasitol 91:988–994

    Article  CAS  PubMed  Google Scholar 

  • Jalali S, Singh S (1992) Differential response of four Trichogramma species to low temperatures for short term storage. Entomophaga 37:159–165

    Article  Google Scholar 

  • Kim BG, Shim JK, Kim DW, Kwon YJ, Lee KY (2008) Tissue-specific variation of heat shock protein gene expression in relation to diapause in the bumblebee Bombus terrestris. Entomol Res 38:10–16

    Article  Google Scholar 

  • Langer A, Hance T (2000) Overwintering strategies and cold hardiness of two aphid parasitoid species (Hymenoptera: Braconidae: Aphidiinae). J Insect Physiol 46:671–676

    Article  CAS  PubMed  Google Scholar 

  • Levie A, Vernon P, Hance T (2005) Consequences of acclimation on survival and reproductive capacities of cold-stored mummies of Aphidius rhopalosiphi (Hymenoptera: Aphidiinae). J Econ Entomol 98:704–708

    Article  CAS  PubMed  Google Scholar 

  • Li A, Denlinger D (2008) Rapid cold hardening elicits changes in brain protein profiles of the flesh fly, Sarcophaga crassipalpis. Insect Mol Biol 17:565–572

    Article  PubMed  Google Scholar 

  • Lopez-Martinez G, Elnitsky MA, Benoit JB, Lee RE, Denlinger DL (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

    Article  CAS  PubMed  Google Scholar 

  • Lovelock J (1954) The protective action of neutral solutes against haemolysis by freezing and thawing. Biochem J 56:265–270

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lu B, Peng Z, Xu C, Tang C, Fu Y, Wan F (2005) Biological characteristics of Tetrastichus brontispae Ferriere (Hymenoptera: Eulophidae), a parasitoid of Brontispa longissima (Gestro) (Coleoptera: Hispidae). Acta Entomol Sin 49:643–649

    Google Scholar 

  • Lu B, Jin Q, Wen H, Du Y, Peng Z (2012) Current status of Brontispa longissima outbreaks and control. Chin J Appl Entomol 6:1708–1715

    Google Scholar 

  • Lu B, Zhu W, Bellis G, Jin Q, Wen H, Feng Y, Peng Z (2014) Factors affecting the parasitism rate and the number and sex ratio of offspring of Asecodes hispinarum Bouček (Hymenoptera: Eulophidae), a biological control agent of Brontispa longissima (Gestro)(Coleoptera: Chrysomelidae). Biocontrol Sci Technol 24:270–278

    Article  Google Scholar 

  • Miao H, Ye Z, Hu G, Qin Y (2015) Comparative transcript profiling of gene expression between self-incompatible and self-compatible mandarins by suppression subtractive hybridization and cDNA microarray. Mol Breed 35:1–15

    Article  CAS  Google Scholar 

  • Michaud MR, Denlinger DL (2007) Shifts in the carbohydrate, polyol, and amino acid pools during rapid cold-hardening and diapause-associated cold-hardening in flesh flies (Sarcophaga crassipalpis): a metabolomic comparison. J Comp Physiol B 177:753–763

    Article  CAS  PubMed  Google Scholar 

  • Overgaard J, Malmendal A, Sørensen JG, Bundy JG, Loeschcke V, Nielsen NC, Holmstrup M (2007) Metabolomic profiling of rapid cold hardening and cold shock in Drosophila melanogaster. J Insect Physiol 53:1218–1232

    Article  CAS  PubMed  Google Scholar 

  • Qin W, Neal S, Robertson R, Westwood J, Walker V (2005) Cold hardening and transcriptional change in Drosophila melanogaster. Insect Mol Biol 14:607–613

    Article  CAS  PubMed  Google Scholar 

  • Riddick E (2001) Effect of cold storage on emergence, longevity, fertility, and survival of Cotesia marginiventris (Hymenoptera: Braconidae). J Entomol Sci 36:366–379

    Google Scholar 

  • Rivers DB, Lee RE, Denlinger DL (2000) Cold hardiness of the fly pupal parasitoid Nasonia vitripennis is enhanced by its host Sarcophaga crassipalpis. J Insect Physiol 46:99–106

    Article  CAS  PubMed  Google Scholar 

  • Roitberg B, Boivin G, Vet LEM (2001) Fitness, parasitoids, and biological control: an opinion. Can Entomol 133:429–438

    Article  Google Scholar 

  • Rundle BJ, Thomson LJ, Hoffmann AA (2004) Effects of cold storage on field and laboratory performance of Trichogramma carverae (Hymenoptera: Trichogrammatidae) and the response of three Trichogramma spp. (T. carverae, T. nr. brassicae, and T. funiculatum) to cold. J Econ Entomol 97:213–221

    Article  PubMed  Google Scholar 

  • Sonoda S, Fukumoto K, Izumi Y, Yoshida H, Tsumuki H (2006) Cloning of heat shock protein genes (hsp90 and hsc70) and their expression during larval diapause and cold tolerance acquisition in the rice stem borer, Chilo suppressalis Walker. Arch Insect Biochem Physiol 63:36–47

    Article  CAS  PubMed  Google Scholar 

  • Thompson SN (2003) Trehalose—the insect ‘blood’sugar. Adv Insect Physiol 31:205–285

    Article  CAS  Google Scholar 

  • Tullett A, Hart A, Worland M, Bale J (2004) Assessing the effects of low temperature on the establishment potential in Britain of the non-native biological control agent Eretmocerus eremicus. Physiol Entomol 29:363–371

    Article  Google Scholar 

  • Vesala L, Salminen T, Laiho A, Hoikkala A, Kankare M (2012) Cold tolerance and cold-induced modulation of gene expression in two Drosophila virilis group species with different distributions. Insect Mol Biol 21:107–118

    Article  CAS  PubMed  Google Scholar 

  • Waterhouse DF, Norris KR (1987) Biological control: Pacific prospects. Inkata Press, Melbourne

    Google Scholar 

  • Yan S-P, Zhang Q-Y, Tang Z-C, Su W-A, Sun W-N (2006) Comparative proteomic analysis provides new insights into chilling stress responses in rice. Mol Cell Proteom 5:484–496

    Article  CAS  Google Scholar 

  • Yang L-H, Huang H, Wang J-J (2010) Antioxidant responses of citrus red mite, Panonychus citri (McGregor) (Acari: Tetranychidae), exposed to thermal stress. J Insect Physiol 56:1871–1876

    Article  CAS  PubMed  Google Scholar 

  • Yocum GD, Žďárek J, Joplin KH, Lee RE, Smith DC, Manter KD, Denlinger DL (1994) Alteration of the eclosion rhythm and eclosion behavior in the flesh fly, Sarcophaga crassipalpis, by low and high temperature stress. J Insect Physiol 40:13–21

    Article  Google Scholar 

  • Zamani AA, Talebi A, Fathipour Y, Baniameri V (2007) Effect of temperature on life history of Aphidius colemani and Aphidius matricariae (Hymenoptera: Braconidae), two parasitoids of Aphis gossypii and Myzus persicae (Homoptera: Aphididae). Environ Entomol 36:263–271

    Article  PubMed  Google Scholar 

  • Zera AJ, Harshman LG (2001) The physiology of life history trade-offs in animals. Annu Rev Ecol Evol Syst 32:95–126

    Article  Google Scholar 

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Acknowledgments

The authors gratefully acknowledge the NSF of China (31101496), the NSF of Hainan (312036), the International Cooperation Projects of China (KY201301025 and KJHZ2015-01) for financial support.

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Authors and Affiliations

  1. Key Laboratory of Integrated Pest Management on Tropical Crops, Ministry of Agriculture China, Environment and Plant Protection Institute, Chinese Academy of Tropical Agricultural Sciences, Haikou, 571101, Hainan Province, China

    Baoqian Lu, Qi-an Jin, Zhengqiang Peng & Haibo Wen

  2. Forest Quarantine Station of Danzhou, Danzhou, 571737, Hainan, China

    Zhenzheng Tang

  3. Charles Darwin University, Darwin, NT, 0810, Australia

    Glenn A. Bellis

  4. Department of Plant and Environmental Protection Sciences, College of Tropical Agriculture and Human Resources, University of Hawaii at Manoa, Honolulu, HI, 96833, USA

    Mark G. Wright

  5. College of Environment and Plant Protection, Hainan University, Haikou, 570228, Hainan Province, China

    Jie Wan & Yiqiong Li

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  1. Baoqian Lu
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  2. Zhenzheng Tang
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  3. Glenn A. Bellis
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Correspondence to Zhengqiang Peng.

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Lu, B., Tang, Z., Bellis, G.A. et al. Biological and physiological response of a tropical parasitoid, Tetrastichus brontispae (Ferriere) following exposure to low temperature. BioControl 61, 649–659 (2016). https://doi.org/10.1007/s10526-016-9757-9

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  • DOI: https://doi.org/10.1007/s10526-016-9757-9

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