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Fluctuating temperatures influence the susceptibility of pest insects to biological control agents

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Abstract

Despite the fact that temperatures fluctuate on a daily basis in the field, the effect of fluctuating temperature on the susceptibility of pest insects to agricultural management tactics are lacking. We thus tested how the development of Spodoptera littoralis and Heliothis virescens (Lepidoptera: Noctuidae) is influenced by exposure to an insecticidal genetically engineered pulverized powder of, Bollgard II cotton producing the Bt proteins Cry1Ac and Cry2Ab, or an entomopathogenic fungus (Beauveria bassiana) under fluctuating temperatures in comparison with constant temperature. When temperature fluctuated symmetrically around 25 °C either in small range (± 5 °C) or in a large range (± 10 °C) on daily basis, development of both lepidopteran species was positively or not influenced in absence of additional stressors. Both species were affected by Bt-cotton when added at low concentrations to the artificial diet, but their reaction to Bt-cotton did not differ between fluctuating temperatures compared to a constant 25 °C. When H. virescens larvae were dipped into spore suspension of B. bassiana, all larvae reared at constant 25 °C died before pupation, while no detrimental effect of the fungus was visible in the fluctuating temperature regimes. In contrast, S. littoralis was not affected by the fungus in any treatment. Since fungal growth was reduced at fluctuating temperatures, this might have affected the infection rate in H. virescens. The results of this study indicate that fluctuating, compared to constant temperatures, can influence the susceptibility of pest insects to biological control agents, while temperature regimes seem to be less important for the efficacy of insecticidal genetically engineered crops.

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  • 26 June 2020

    In the original publication of this article, the complete author affiliations were incorrect. The correct affiliations are provided in this correction.

References

  • Acuna-Jimenez M, Rosas-Garcia NM, Lopez-Meyer M, Saínz-Hernandez JC, Mundo-Ocampo M, García-Gutierrez C (2015) Pathogenicity of micro encapsulated insecticide from Beauveria bassiana and Metarhizium anisopliae against tobacco budworm, Heliothis virescens (Fabricius). Southwest Entomol 40:531–538

    Google Scholar 

  • Atkinson NJ, Urwin PE (2012) The interaction of plant biotic and abiotic stresses: from genes to the field. J Exp Bot 63:3523–3543

    CAS  PubMed  Google Scholar 

  • Auad AM, Silva SEB, Santos JC, Vieira TM (2015) Impact of fluctuating and constant temperatures on key life history parameters of Siphaflava (Hemiptera: Aphididae). Fla Entomol 98:424–429

    Google Scholar 

  • Bahar MDH, Juliana J, SorokaI DLM (2012) Constant versus fluctuating temperatures in the interactions between Plutella xylostella (Lepidoptera: Plutellidae) and its larval parasitoid Diadegmainsulare (Hymenoptera: Ichneumonidae). Environ Entomol 41:1653–1661

    PubMed  Google Scholar 

  • Beck SD (1983) Insect thermoperiodism. Annu Rev Entomol 28:91–108

    Google Scholar 

  • Boller EF, Avilla J, Joerg E, Malavolta C, Wijnands FG, Esbjerg P (2004) Integrated Production–principles and technical guidelines, 3rd Edn, IOBC-WPRS Bulletin, vol 27(2)

  • Brakefield PM, Kesbeke F (1997) Genotype–environment interactions for insect growth in constant and fluctuating temperature regimes. Proc R Soc 264:717–723

    Google Scholar 

  • Butler GD, Hamilton AG, Proshold FI (1979) Developmental times of Heliothis virescens and H. subflexa in relation to constant temperature. Ann Entomol Soc Am 72:263–266

    Google Scholar 

  • Cao Y, Yang H, Li J, Zhang G, Wang Y, Li C, Gao Y (2019) Population development of Frankliniella occidentalis and Thrips hawaiiensis in constant and fluctuating temperatures. J Appl Entmol 143:49–57

    Google Scholar 

  • Colinet H, Sinclair BJ, Vernon P, Renault D (2015) Insects in fluctuating thermal environments. Annu Rev Entomol 60:123–140

    CAS  PubMed  Google Scholar 

  • De Luis R, Lavilla M, Sánchez L, Calvo M, Pérez MD (2009) Immunochemical detection of Cry1A(b) protein in model processed foods made with transgenic maize. Eur Food Res Technol 229:15–19

    CAS  Google Scholar 

  • Eisenring M, Romeis J, Naranjo SE, Meissle M (2017) Multitrophic Cry-protein flow in a dual-gene Bt-cotton field. Agric Ecosyst Environ 247:283–289

    CAS  Google Scholar 

  • El-Malki KG (2000) Thermal requirements and prediction models of cotton leafworm Spodoptera littoralis (Boisd). In: Proceedings of the Beltwide Cotton Conference, 4–8 January 2000, San Antonio Texas, United States 2, pp 1019–1021

  • Fargues J, Maniania NK, Delmas JC, Smith N (1992) Influence of temperature on in vitro growth of entomopathogenic hyphomycetes [Beauveria brongniartii, Metarhizium flavoviride, Nomuraearileyi, Paecilomyces]. Agron 12:557–564

    Google Scholar 

  • Feng Y, Ling L, Fan H, Liu Y, Tan F, Shu Y, Wang J (2011) Effects of temperature, water content and pH on degradation of Cry1Ab protein released from Bt corn straw in soil. Soil Biol Biochem 43:1600–1606

    CAS  Google Scholar 

  • Fischer K, Kolzow N, Holtje H, Karl I (2011) Assay conditions in laboratory experiments: is the use of constant rather than fluctuating temperatures justified when investigating temperature-induced plasticity? Oecologia 166:23–33

    PubMed  Google Scholar 

  • Greenplate JT, Mullins JW, Penn SR, Dahm A, Reich BJ, Osborn JA, Rahn PR, Ruschke L, Shappley ZW (2003) Partial characterization of cotton plants expressing two toxin proteins from Bacillus thuringiensis: relative toxin contribution, toxin interaction, and resistance management. J Appl Entomol 127:340–347

    CAS  Google Scholar 

  • Hagenbucher S, Eisenring M, Meissle M, Romeis J (2017) Interaction of transgenic and natural insect resistance mechanisms against Spodoptera littoralis in cotton. Pest Manag Sci 73:1670–1678

    CAS  PubMed  Google Scholar 

  • Haller S, Romeis J, Meissle M (2017) Effects of purified or plant-produced Cry proteins on Drosophila melanogaster (Diptera: Drosophilidae) larvae. Sci Rep 7:11172

    PubMed  PubMed Central  Google Scholar 

  • Hallsworth JE, Magan N (1999) Water and temperature relations of growth of the entomogenous fungi Beauveria bassiana, Metarhizium anisopliae, and Paecilomycesfarinosus. J Invertebr Pathol 74:261–266

    CAS  PubMed  Google Scholar 

  • Inglis GD, Duke GM, Kawchuk LM, Goettel MS (1999) Influence of oscillating temperatures on the competitive infection and colonization of the migratory grasshopper by Beauveria bassiana and Metarhizium flavoviride. Biol Control 14:111–120

    Google Scholar 

  • Inglis GD, Goettel MS, Butt TM, Strasser H (2001) Use of hyphomycetous fungi for managing insect pests. In: Magan N, Butt TM, Jackson C (eds) Fungi as Biocontrol Agents. CABI Publishers, Wallingford, pp 23–69. https://doi.org/10.1046/j.1365-3059.2002.07351.x

    Chapter  Google Scholar 

  • Karimi-Malati A, Fathipour Y, Talebi AA, Bazoubandi M (2014) Life table parameters and survivorship of Spodoptera exigua (Lepidoptera: Noctuidae) at constant temperatures. Environ Entomol 43:795–803

    PubMed  Google Scholar 

  • Keyser CA, Fernandes ÉK, Rangel DE, Roberts DW (2014) Heat-induced post-stress growth delay: a biological trait of many Metarhizium isolates reducing biocontrol efficacy? J Invertebr Pathol 120:67–73

    PubMed  Google Scholar 

  • Khadioli N, Tonnang ZEH, Ongamo G, AchiaT KipchirchirI, Kroschel J, Le Ru B (2014) Effect of temperature on the life history parameters of noctuid lepidopteran stem borers, Busseola fusca and Sesamia calamistis. Ann Appl Biol 165:373–386

    Google Scholar 

  • Kjærsgaard A, Pertoldi C, Loeschcke V, Blanckenhorn WU (2013) The effect of fluctuating temperatures during development on fitness-related traits of Scatophaga stercoraria (Diptera: Scathophagidae). Environ Entomol 42:1069–1078

    PubMed  Google Scholar 

  • Knight K, Head H, Rogers J (2013) Season-long expression of Cry1Ac and Cry2Ab proteins in Bollgard II cotton in Australia. Crop Prot 44:50–58

    CAS  Google Scholar 

  • Kryukov VY, Yaroslavtseva ON, Elisaphenko EA, Mitkovets PV, Lednev GR, Duisembekov BA, Zakian SM, Glupov VV (2012) Change in the temperature preferences of Beauveria bassiana sensu lato isolates in the latitude gradient of Siberia and Kazakhstan. Microbiology 81:453–459

    CAS  Google Scholar 

  • Lecuona RE, Rodriguez J, La Rossa FR (2005) Effect of constant and cyclical temperatures on the mortality of Triatoma infestans (Klug) (Hemiptera: Reduviidae) treated with Beauvaria bassiana (Bals.) Vuill. (Hyphomycetes). Neotrop Entomol 34:675–679

    Google Scholar 

  • Meissle M, Romeis J (2017) Transfer of Cry1Ac and Cry2Ab proteins from genetically engineered Bt cotton to herbivores and predators. Insect Sci 25:823–832

    PubMed  Google Scholar 

  • Milosavljević I, McCalla KA, Ratkowsky DA, Hoddle MS (2019) Effects of constant and fluctuating temperatures on development rates and longevity of Diaphorencyrtus aligarhensis (Hymenoptera: Encyrtidae). J Econ Entomol 112:1062–1072

    PubMed  Google Scholar 

  • Mironidis GK, Savopoulou-Soultani M (2008) Development, survivorship, and reproduction of Helicoverpa armigera (Lepidoptera: Noctuidae) under constant and alternating temperatures. Environ Entomol 37:16–28

    CAS  PubMed  Google Scholar 

  • Mittler R (2006) Abiotic stress, the field environment and stress combination. Trends Plant Sci 11:15–19

    CAS  PubMed  Google Scholar 

  • Mittler R, Blumwald E (2010) Genetic engineering for modern agriculture: challenges and perspectives. Annu Rev Plant Biol 61:443–462

    CAS  PubMed  Google Scholar 

  • Moghal MS, Schneider JC (1998) Effects of high temperature on development of Heliothis virescens (F.) on cotton fruiting structures in the laboratory. Southwest Entomol 23:123–126

    Google Scholar 

  • Müller E, Obermaier E (2012) Herbivore larval development at low spring time temperatures: the importance of short periods of heating in the field. Psyche 12:1–7

    Google Scholar 

  • Mwamburi LA, Laing MD, Miller RM (2015) Effect of surfactants and temperature on germination and vegetative growth of Beauveria bassiana. Braz J Microbiol 46:67–74

    CAS  PubMed  PubMed Central  Google Scholar 

  • Pineda A, Dicke M, Pieterse CMJ, Pozo MJ (2013) Beneficial microbes in a changing environment: are they always helping plants to deal with insects? Funct Ecol 27:574–586

    Google Scholar 

  • Ramegowdaa V, Senthil-Kumar M (2015) The interactive effects of simultaneous biotic and abiotic stresses on plants: Mechanistic understanding from drought and pathogen combination. J Plant Physiol 176:47–54

    Google Scholar 

  • Rana A, Khan SU, Ali S, Zia MA, Iqbal A, Ali GM, Tahir M (2015) Effect of temperature on Bt gene expression in candidate cotton lines of Pakistan. Am Eurasian J Toxicol Sci 7:26–33

    Google Scholar 

  • Régnière J, Powell J, Bentz B, Nealis V (2012) Effects of temperature on development, survival and reproduction of insects: Experimental design, data analysis and modeling. J Plant Physiol 58:634–647

    Google Scholar 

  • Resquín-Romero G, Garrido-Jurado I, Delso C, Ríos-Moreno A, Quesada-Moraga E (2016) Transient endophytic colonizations of plants improve the outcome of foliar applications of myco insecticides against chewing insects. J Invertebr Pathol 136:23–31

    PubMed  Google Scholar 

  • Shennan C (2008) Biotic interactions, ecological knowledge and agriculture. Phil Trans Royal Soc B 363:717–739

    Google Scholar 

  • Sivasupramanian S, Moar WJ, Ruschke LG, Osborn JA, Jiang C, Sebaugh JL, Brown GR, Shappley ZW, Oppenhuizen ME, Mullins JW, Greenplate JT (2008) Toxicity and characterization of cotton expressing Bacillus thuringiensis Cry1Ac and Cry2Ab2 proteins for control of lepidopteran pests. J Econ Entomol 101:546–554

    Google Scholar 

  • Strasser H, Forer A, Schinner F (1996) Development of media for theselective isolation and maintenance of virulence of Beauveria brongniartii. In: Proceedings of the 3rd international workshop on microbial control of soil dwelling pests, pp 125–130

  • Tabashnik BE, Brévault T, Carrière Y (2013) Insect resistance to Bt crops: lessons from the first billion acres. Nat Biotechnol 31:510–521

    CAS  PubMed  Google Scholar 

  • Teackle RE, Jensen JM (1985) Heliothis punctiger. In: Singh P, Moore RF (eds) Handbook of insect rearing, vol II. Elsevier, Amsterdam, pp 313–322

    Google Scholar 

  • Wieser W (1973) Effects of temperature on ectothermic organisms. Springer, Berlin

    Google Scholar 

  • Wu TH, Shiao SF, Okuyama T (2015) Development of insects under fluctuating temperature: a review and case study. J Appl Entomol 139:592–599

    Google Scholar 

  • Xing K, Ma CS, ZhaoHan FJC (2015) Effects of large temperature fluctuations on matching and subsequent development of the diamondback moth (Lepidoptera: Plutellidae). Florida Entomol 98:651–659

    Google Scholar 

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Acknowledgements

We acknowledge Monsanto for providing cotton seeds. This work was supported by a Swiss Government Excellence Scholarship (Ref. No. 2014.0884) granted to Muhammad Usman Ghazanfar.

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Authors and Affiliations

  1. Department of Plant Pathology, College of Agriculture, University of Sargodha, Sargodha, Pakistan

    Muhammad Usman Ghazanfar, Steffen Hagenbucher, Jörg Romeis & Michael Meissle

  2. Agroscope, Research Division Agroecology and Environment, Reckenholzstrasse 191, 8046, Zurich, Switzerland

    Muhammad Usman Ghazanfar

  3. Institute of Ecology and Evolution, University of Bern, Baltzerstrasse 6, 3012, Bern, Switzerland

    Muhammad Usman Ghazanfar & Jörg Romeis

  4. Agroscope, Research Division Plant Protection, Reckenholzstrasse 191, 8046, Zurich, Switzerland

    Giselher Grabenweger

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  1. Muhammad Usman Ghazanfar
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Correspondence to Muhammad Usman Ghazanfar.

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Ghazanfar, M.U., Hagenbucher, S., Romeis, J. et al. Fluctuating temperatures influence the susceptibility of pest insects to biological control agents. J Pest Sci 93, 1007–1018 (2020). https://doi.org/10.1007/s10340-020-01215-9

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