Skip to main content
Log in

Non-consumptive effects of Encarsia formosa on the reproduction and metabolism of the whitefly Bemisia tabaci

  • Published:
BioControl Aims and scope Submit manuscript

Abstract

The impact of predatory or parasitic natural enemies on their pest prey or hosts arises not only through consumption but also through non-consumptive effects. Multiple studies have investigated the impacts of non-consumptive effects from predators on the behaviour, development and metabolism of invertebrate pests. However, the non-consumptive effects from parasitoids on their insect hosts remain less well understood. Here, we investigated the non-consumptive effects of the parasitoid Encarsia formosa on the fecundity, longevity and metabolism of the whitefly Bemisia tabaci. Results showed that both the fecundity and longevity of whitefly females were significantly reduced when the whiteflies were threatened by Encarsia parasitoids during their nymphal stages. In addition, we tested three costly and potential physiological correlates that may contribute to the fecundity and longevity variation of B. tabaci under the non-consumptive effects: the relative expression level of vitellogenin and its receptor genes (Vg and Vgr), relative expression level of stress proteins (Hsp70 and Hsp90) and the activities of the antioxidant enzymes superoxide dismutase (SOD), catalase (CAT) and peroxidase (POD). When B. tabaci 4th instar nymphs were threatened for 24 h by E. formosa the relative expression levels of Vg and Vgr were reduced, whereas Hsp70 and Hsp90 were significantly increased. SOD and CAT activities were distinctly up-regulated while POD activity was down-regulated. We propose that, in order to counteract the negative effects of non-consumption, whitefly nymphs need to adjust their performance by changing the expression of related metabolic genes in an energetic cost way, thus reducing the fecundity and longevity of female adults.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • Aebi H (1984) Catalase in vitro. Method Enzymol 105:121–126

    Article  CAS  Google Scholar 

  • Allo NM, Mekhlif AF (2019) Role of the predator Anisops sardea (hemiptera: notonectidae) in control mosquito Culex pipiens molestus (diptera: culicidae) population. Int. J. Mosquito Res. 6:46–50

    Google Scholar 

  • Beauchamp C, Fridovich I (1971) Superoxide dismutase: improved assays and an assay applicable to acrylamide gels. Anal Biochem 44:276–287

    Article  CAS  PubMed  Google Scholar 

  • Benard MF (2004) Predator-induced phenotypic plasticity in organisms with complex life histories. Annu Rev Ecol Evol Syst 35(1):651–673

    Article  Google Scholar 

  • Boisclair J, Brueren GJ, van Lenteren JC (1990) Can Bemisia tabaci be controlled with Encarsia formosa? SROP/WPRS Bull 5:32–35

    Google Scholar 

  • Chen W, Hasegawa DK, Kaur N, Kliot A, Pinheiro PV, Luan J, Stensmyr MC, Zheng Y, Liu W, Sun H, Xu Y, Luo Y, Kruse A, Yang X, Kontsedalov S, Lebedev G, Fisher TW, Nelson DR, Hunter WB, Brown JK, Jander G, Cilia M, Douglas AE, Ghanim M, Simmons AM, Wintermantel WM, Ling KS, Fei Z (2016) The draft genome of whitefly Bemisia tabaci MEAM1, a global crop pest, provides novel insights into virus transmission, host adaptation, and insecticide resistance. BMC Biol 14:110

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Corona M, Velarde RA, Remolina S, Moran-Lauter A, Wang Y, Hughes KA, Robinson GE (2007) Vitellogenin, juvenile hormone, insulin signaling, and queen honey bee longevity. PNAS 104(17):7128–7133

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Díaz F, Orobio RF, Chavarriaga P, Toro-Perea N (2015) Differential expression patterns among heat-shock protein genes and thermal responses in the whitefly Bemisia tabaci (MEAM 1). J Therm Biol 52:199–207

    Article  CAS  PubMed  Google Scholar 

  • Ebrahim SA, Dweck HK, Stokl J, Hofferberth JE, Trona F, Weniger K, Rybak J, Seki Y, Stensmyr MC, Sachse S, Hansson BS, Knaden M (2015) Drosophila avoids parasitoids by sensing their semiochemicals via a dedicated olfactory circuit. PLoS Biol 13(12):e1002318

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Eilenberg J, Hajek A, Lomer C (2001) Suggestions for unifying the terminology in biological control. BioControl 46:387–400

    Article  Google Scholar 

  • Fill A, Long EY, Finke DL (2012) Non-consumptive effects of a natural enemy on a non-prey herbivore population. Ecol Entomol 37:43–50

    Article  Google Scholar 

  • Gerling D (1966) Biological studies on Encarsia formosa (hymenoptera: aphelinidae). Ann Entomol Soc Am 59:142–143

    Article  Google Scholar 

  • Hawkins BA, Cornell HV, Hochberg ME (1997) Predators, parasitoids, and pathogens as mortality agents in phytophagous insect populations. Ecology 78:2145–2152

    Article  Google Scholar 

  • Hawlena D, Kress H, Dufresne ER, Schmitz OJ (2010) Grasshoppers alter jumping biomechanics to enhance escape performance under chronic risk of spider predation. Funct Ecol 25(1):279–288

    Article  Google Scholar 

  • He Z, Liu Y, Wang L, Guo Q, Ali S, Chen XS, Qiu BL (2018) Risk assessment of two insecticides on Encarsia formosa, parasitoid of whitefly Bemisia tabaci. Insects 9(3):116

    Article  PubMed Central  Google Scholar 

  • Hermann SL, Landis DA (2017) Scaling up our understanding of non-consumptive effects in insect systems. Curr Opin Insect Sci 20:54–60

    Article  PubMed  Google Scholar 

  • Huo Y, Chen XY, Fang RX, Zhang LL (2018) Study on the production of vitellogenin and its non-nutritional functions. Biotechnol Bull 34:66–73

    Google Scholar 

  • Ingerslew KS, Finke DL (2017) Mechanisms underlying the nonconsumptive effects of parasitoid wasps on aphids. Environ Entomol 46:75–83

    CAS  PubMed  Google Scholar 

  • Jia FX, Dou W, Hu F, Wang JJ (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

    Article  CAS  Google Scholar 

  • Krishnan N, Kodrı´k D (2006) Antioxidant enzymes in Spodoptera littoralis (boisduval): are they enhanced to protect gut tissues during oxidative stress. J Insect Physiol 52:11–20

    Article  CAS  PubMed  Google Scholar 

  • Li C, Wang Y, Wang G, Chen Y, Guo J, Pan C, Liu E, Ling Q (2019) Physicochemical changes in liver and Hsc70 expression in pikeperch Sander lucioperca under heat stress. Ecotoxicol Environ Saf 181:130–137

    Article  CAS  PubMed  Google Scholar 

  • Liu X, Zhang Y, Xie W, Wu Q, Wang S (2016) The suitability of biotypes Q and B of Bemisia tabaci (gennadius) (Hemiptera: Aleyrodidae) at different nymphal instars as hosts for Encarsia formosa Gahan (Hymenoptera: Aphelinidae). PeerJ 4:e1863

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Luan JB, Wang YL, Wang J, Wang XW, Liu SS (2013) Detoxification activity and energy cost is attenuated in whiteflies feeding on tomato yellow leaf curl China virus-infected tobacco plants. Insect Mol Biol 22:597–607

    Article  CAS  PubMed  Google Scholar 

  • Luttbeg B, Kerby JL (2005) Are scared prey as good as dead? Trends Ecol Evol 20:416–418

    Article  PubMed  Google Scholar 

  • Michael CM, Andrew S, Jay AR (2020) Bugs scaring bugs: enemy-risk effects in biological control systems. Ecol Lett 23:1693–1714

    Article  Google Scholar 

  • Moll RJ, Redilla KM, Mudumba T, Muneza AB, Gray SM, Abade L, Hayward MW, Millspaugh JJ, Montgomery RA (2017) The many faces of fear: a synthesis of the methodological variation in characterizing predation risk. J Anim Ecol 86(4):749–765

    Article  PubMed  Google Scholar 

  • Mondor EB, Roitberg BD (2002) Pea aphid, Acyrthosiphon pisum, cornicle ontogeny as an adaptation to differential predation risk. Can J Zool 80:2131–2136

    Article  Google Scholar 

  • Nelson EH (2007) Predator avoidance behavior in the pea aphid: costs, frequency, and population consequences. Oecologia 151:22–32

    Article  PubMed  Google Scholar 

  • Peacor SD, Barton BT, Kimbro DL, Sih A, Sheriff MJ (2020) A framework and standardized terminology to facilitate the study of predation-risk effects. Ecology 101:e03152

    Article  PubMed  Google Scholar 

  • Peckarsky BL, Abrams PA, Bolnick DI, Dill LM, Grabowski JH, Luttbeg B, Orrock JL, Peacor SD, Preisser EL, Schmitz OJ, Trussell GC (2008) Revisiting the classics considering nonconsumptive effects in textbook examples of predator–prey interactions. Ecology 89:2416–2425

    Article  PubMed  Google Scholar 

  • Preisser EL, Bolnick DI, Benard MF (2005) Scared to death? The effects of intimidation and consumption in predator–prey interactions. Ecology 86(2):501–509

    Article  Google Scholar 

  • Qiu BL, Susan AC, Ren SX, Ali MI, Xu CX, Brown JK (2007a) Phylogenetic relationship of native and introduced Bemisia tabaci (Homoptera: Aleyrodidae) from China and India based on mtCOI DNA sequencing and host plant comparisons. Prog Nat Sci 17(6):645–654

    Article  CAS  Google Scholar 

  • Qiu BL, De Barro PJ, He YR, Ren SX (2007b) Suitability of Bemisia tabaci (Hemiptera: Aleyrodidae) instars for the parasitization by Encarsia bimaculata and Eretmocerus sp nr. furuhashii (Hymenoptera: Aphelinidae) on glabrous and hirsute host plants. Biocontrol Sci Technol 17:823–839

    Article  Google Scholar 

  • Richter K, Haslbeck M, Buchner J (2010) The heat shock response: life on the verge of death. Mol Cell 40:253–266

    Article  CAS  PubMed  Google Scholar 

  • Rosenheim JA (1998) Higher-order predators and the regulation of insect herbivore populations. Annu Rev Entomol 43:421–447

    Article  CAS  PubMed  Google Scholar 

  • Ryter SW, Kim HP, Hoetzel A, Park JW, Nakahira K, Wang X, Choi AMK (2007) Mechanisms of cell death in oxidative stress. Antioxid Redox Signal 9(1):49–89

    Article  CAS  PubMed  Google Scholar 

  • Schmitz OJ (1997) Direct and indirect effects of predation and predation risk in old-field interaction webs. Am Nat 151:327–342

    Article  Google Scholar 

  • Sheriff MJ, Thaler JS (2014) Ecophysiological effects of predation risk; an integration across disciplines. Oecologia 176:607–611

    Article  PubMed  Google Scholar 

  • Slos S, Stoks R (2008) Predation risk induces stress proteins and reduces antioxidant defense. Funct Ecol 22(4):637–642

    Article  Google Scholar 

  • Slos S, Meester LD, Stoks R (2009a) Food level and sex shape predator-induced physiological stress: immune defence and antioxidant defence. Oecologia 161(3):461–467

    Article  PubMed  Google Scholar 

  • Slos S, Meester LD, Stoks R (2009b) Behavioural activity levels and expression of stress proteins under predation risk in two damselfly species. Ecol Entomol 34:297–303

    Article  Google Scholar 

  • Snyder WE, Ives AR (2001) Generalist predators disrupt biological control by a specialist parasitoid. Ecology 82:705–716

    Article  Google Scholar 

  • Stoks R, Block MD, McPeek MA (2005) Alternative growth and energy storage responses to mortality threats in damselflies. Ecol Lett 8(12):1307–1316

    Article  Google Scholar 

  • Tahir M, Hamza A, Khalid N, Khan AA, Shahzad U (2017) Indirect effect of spiders on herbivory of insects: a review. J Entomol Zool Stud 5(4):753–757

    Google Scholar 

  • Thaler JS, McArt SH, Kaplan I (2012) Compensatory mechanisms for ameliorating the fundamental trade-off between predator avoidance and foraging. PNAS 109(30):12075–12080

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Thaler JS, Contreras H, Davidowitz G (2014) Effects of predation risk and plant resistance on Manduca sexta caterpillar feeding behaviour and physiology. Ecol Entomol 39(2):210–216

    Article  Google Scholar 

  • Thomson RL, Tomas G, Forsman JT, Broggi J, Monkkonen M (2010) Predator proximity as a stressor in breeding flycatchers: mass loss, stress protein induction, and elevated provisioning. Ecology 91(6):1832–1840

    Article  PubMed  Google Scholar 

  • Valle D (1993) Vitellogenesis in insects and other groups: a review. Mem Inst Oswaldo Cruz 88:1–26

    Article  CAS  PubMed  Google Scholar 

  • van Uitregt VO, Hurst TP, Wilson RS (2012) Reduced size and starvation resistance in adult mosquitoes, Aedes notoscriptus, exposed to predation cues as larvae. J Anim Ecol 81:108–115

    Article  PubMed  Google Scholar 

  • Vetter JL, Steinberg MP, Nelson AI (1958) Enzyme assay, quantitative determination of peroxidase in sweet corn. J Agric Food Chem 6:39–41

    Article  CAS  Google Scholar 

  • Viggiani G (2000) The role of parasitic hymenoptera in integrated pest management in fruit orchards. Crop Prot 19:665–668

    Article  Google Scholar 

  • Walzer A, Schausberger P (2009) Non-consumptive effects of predatory mites on thrips and its host plant. Oikos 118(1):934–940

    Article  Google Scholar 

  • Wang Y, Oberley LW, Murhammer DW (2001) Antioxidant defense systems of two lipidopteran insect cell lines. Free Radic Biol Med 30(11):1254–1262

    Article  CAS  PubMed  Google Scholar 

  • Werner EE, Peacor SD (2003) A review of trait-mediated indirect interactions in ecological communities. Ecology 84(5):1083–1100

    Article  Google Scholar 

  • Xiong XF, Michaud JP, Li Z, Wu PX, Chu YN, Zhang QW, Liu XX (2015) Chronic, predator-induced stress alters development and reproductive performance of the cotton bollworm Helicoverpa armigera. BioControl 60(6):827–837

    Article  Google Scholar 

  • Zang LS, Liu TX, Zhang F, Shi SS, Wan FH (2011) Mating and host density affect host feeding and parasitism in two species of whitefly parasitoids. Insect Sci 18(1):78–83

    Article  Google Scholar 

  • Zhang SC, Wang SH, Li HY, Li L (2011) Vitellogenin, a multivalent sensor and an antimicrobial effector. Int J Biochem Cell Biol 43(3):303–305

    Article  CAS  PubMed  Google Scholar 

  • Zhou JC, Meng L, Li BP (2019) Non-reproductive effects of two parasitoid species on the oriental armyworm Mythimna separata on wheat and maize plants. BioControl 64:115–124

    Article  Google Scholar 

Download references

Acknowledgements

The work was funded by grants from The National Key Research and Development Program of China (Grant No. 2019YFD1002100). The authors also thank Dr Andrew G. S. Cuthbertson (York, UK) for his critical comments on an earlier manuscript.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Bao-Li Qiu.

Ethics declarations

Conflict of interest

On behalf of all authors, the corresponding author states that there is no conflict of interest.

Ethical approval

This article does not contain any studies with human or animals participants performed by any of the authors.

Additional information

Handling Editor: Stefano Colazzza

Supplementary Information

Below is the link to the electronic supplementary material.

10526_2021_10099_MOESM1_ESM.tif

Supplementary file1 (TIF 384 KB) Fig. S1 Visual diagram of the method used for non-consumptive effects on the fecundity and longevity of Bemisia tabaci

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Fan, ZY., Zhu, ZP., Peng, J. et al. Non-consumptive effects of Encarsia formosa on the reproduction and metabolism of the whitefly Bemisia tabaci. BioControl 66, 639–648 (2021). https://doi.org/10.1007/s10526-021-10099-2

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10526-021-10099-2

Keywords

Navigation