Skip to main content
Log in

Chronic, predator-induced stress alters development and reproductive performance of the cotton bollworm, Helicoverpa armigera

  • Published:
BioControl Aims and scope Submit manuscript

Abstract

Predators can significantly impact potential prey without consuming them, generating potential ramifications for biological control. In this study, we examined the cumulative impacts of adult Harmonia axyridis Pallas (Coleoptera: Coccinellidae) on development and reproduction of Helicoverpa armigera Hübner (Lepidoptera: Noctuidae), over three generations. Development became faster in each of the three generations and pupae became heavier than controls, although survival declined in the third generation. Predator stress increased wing deformations in the first generation, but not thereafter, and female fecundity became higher than controls in the third generation. We concluded that predator stress increased larval consumption to eventually result in both faster development and larger adult size when food was abundant. The results demonstrated that H. armigera could respond to exposure from a non-consumptive predator by shifting aspects of developmental timing and increasing reproductive effort, with both individual- and population-level consequences. The adaptive significances of these changes are discussed. This study advances our understanding of the potential for non-lethal predators to impact prey life histories.

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

Similar content being viewed by others

References

  • Ball SL, Baker RL (1996) Predator-induced life history changes: antipredator behavior costs or facultative life history shifts? Ecology 77:1116–1124

    Article  Google Scholar 

  • Beckerman AP, Wieski K, Baird DJ (2007) Behavioural versus physiological mediation of life history under predation risk. Oecologia 152:335–343

    Article  PubMed  Google Scholar 

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

    Article  Google Scholar 

  • Benard MF, Fordyce JA (2003) Are induced defenses costly? Consequences of predator-induced defenses in western toads, Bufo boreas. Ecology 84:68–78

    Article  Google Scholar 

  • Brodin T, Johansson F (2002) Effects of predator-induced thinning and activity changes on life history in a damselfly. Oecologia 132:316–322

    Article  Google Scholar 

  • Brodin T, Mikolajewski DJ, Johansson F (2006) Behavioural and life history effects of predator diet cues during ontogeny in damselfly larvae. Oecologia 148:162–169

    Article  PubMed  Google Scholar 

  • Evans EW (2009) Lady beetles as predators of insects other than Hemiptera. Biol Control 51:255–267

    Article  Google Scholar 

  • Fox CW, Czesak ME (2000) Evolutionary ecology of progeny size in arthropods. Annu Rev Entomol 45:341–369

    Article  CAS  PubMed  Google Scholar 

  • Hammill E, Rogers A, Beckerman AP (2008) Costs, benefits and the evolution of inducible defences: a case study with Daphnia pulex. J Evol Biol 21:705–715

    Article  CAS  PubMed  Google Scholar 

  • Hawlena D, Schmitz OJ (2010a) Physiological stress as a fundamental mechanism linking predation to ecosystem functioning. Am Nat 176:537–556

    Article  PubMed  Google Scholar 

  • Hawlena D, Schmitz OJ (2010b) Herbivore physiological response to predation risk and implications for ecosystem nutrient dynamics. Proc Natl Acad Sci USA 107:15503–15507

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Hechtel LJ, Juliano SA (1997) Effects of a predator on prey metamorphosis: plastic responses of prey or selective mortality? Ecology 78:838–851

    Article  Google Scholar 

  • Huhta A, Muotka T, Tikkanen P (2000) Nocturnal drift of mayfly nymphs as a post-contact antipredator mechanism. Freshw Biol 45:33–42

    Article  Google Scholar 

  • Kimbro DL (2012) Tidal regime dictates the cascading consumptive and nonconsumptive effects of multiple predators on a marsh plant. Ecology 93:334–344

    Article  PubMed  Google Scholar 

  • Koch RL (2003) The multicolored Asian lady beetle, Harmonia axyridis: a review of its biology, uses in biological control, and non-target impacts. J Insect Sci 3:32

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Kunert G, Otto S, Roese USR, Gershenzon J, Weisser WW (2005) Alarm pheromone mediates production of winged dispersal morphs in aphids. Ecol Lett 8:596–603

    Article  Google Scholar 

  • Li YP, Ge F (2010) Effect of prey stress from Propy lea japonica on development and fecundity of Drosophila melanogaster in successive three generations. Chin Bull Entomol 47:139–145

    Google Scholar 

  • Mangel M, Stamps J (2001) Trade-offs between growth and mortality and the maintenance of individual variation in growth. Evol Ecol Res 3:583–593

    Google Scholar 

  • Matassa CM, Trussell GC (2011) Landscape of fear influences the relative importance of consumptive and nonconsumptive predator effects. Ecology 92:2258–2266

    Article  PubMed  Google Scholar 

  • McCauley SJ, Davis CJ, Werner EE (2008) Predator induction of spine length in larval Leucorrhinia intacta (Odonata). Evol Ecol Res 10:435–447

    Google Scholar 

  • McCauley SJ, Rowe L, Fortin MJ (2011) The deadly effects of “nonlethal” predators. Ecology 92:2043–2048

    Article  PubMed  Google Scholar 

  • McCollum SA, Buskirk JV (1996) Costs and benefits of a predator-induced polyphenism in the gray treefrog Hyla chrysoscelis. Evolution 50:583–593

    Article  Google Scholar 

  • McPeek MA (2004) The growth/predation risk trade-off: so what is the mechanism? Am Nat 163:E88–E111

    Article  PubMed  Google Scholar 

  • McPeek MA, Grace M, Richardson JML (2001) Physiological and behavioral responses to predators shape the growth/predation risk trade-off in damselflies. Ecology 82:1535–1545

    Article  Google Scholar 

  • Michaud JP, Olsen LE (2004) Suitability of Asian citrus psyllid, Diaphorina citri, as prey for ladybeetles. BioControl 49:417–431

    Article  Google Scholar 

  • Nelson EH, Matthews CE, Rosenheim JA (2004) Predators reduce prey population growth by inducing changes in prey behaviour. Ecology 85:1853–1858

    Article  Google Scholar 

  • Orizaola G, Dahl E, Laurila A (2012) Reversibility of predator-induced plasticity and its effect at a life-history switch point. Oikos 121:44–52

    Article  Google Scholar 

  • Pangle KL, Peacor SD, Johannsson OE (2007) Large nonlethal effects of an invasive invertebrate predator on zooplankton population growth rate. Ecology 88:402–412

    Article  PubMed  Google Scholar 

  • Peacor SD (2002) Positive effect of predators on prey growth rate through induced modifications of prey behaviour. Ecol Lett 5:77–85

    Article  Google Scholar 

  • Peacor SD, Werner EE (1997) Trait-mediated indirect interactions in a simple aquatic food web. Ecology 78:1146–1156

    Article  Google Scholar 

  • Peacor SD, Peckarsky BL, Trussell GC, Vonesh JR (2013) Costs of predator-induced phenotypic plasticity: a graphical model for predicting the contribution of nonconsumptive and consumptive effects of predators on prey. Oecologia 171:1–10

    Article  PubMed  Google Scholar 

  • Peckarsky BL, Taylor BW, McIntosh AR, McPeek MA, Lytle DA (2001) Variation in mayfly size at metamorphosis as a developmental response to risk of predation. Ecology 82:740–757

    Article  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 non-consumptive effects in textbook examples of predator–prey interactions. Ecology 89:2416–2425

    Article  PubMed  Google Scholar 

  • Pimentel C, Santos M, Ferreira C, Nilsson JA (2012) Temperature, size, reproductive allocation, and life-history evolution in a gregarious caterpillar. Biol J Linn Soc 105:340–349

    Article  Google Scholar 

  • Preisser EL, Bolnick DI (2008) The many faces of fear: comparing the pathways and impacts of nonconsumptive predator effects on prey populations. PLoS ONE 3:e2465

    Article  PubMed Central  PubMed  Google Scholar 

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

    Article  Google Scholar 

  • Qian SS (2009) Environmental and Ecological Statistics with R. CRC Press, Florida

    Google Scholar 

  • R Foundation for Statistical Computing (2015) A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna

    Google Scholar 

  • Relyea RA (2003) Predators come and go: the reversibility of predator-induced traits. Ecology 84:1840–1848

    Article  Google Scholar 

  • Roff DA (2001) Age and size at maturity. In: Fox CW, Roff DA, Fairbairn DJ (eds) Evolutionary ecology, concepts and case studies. Oxford University Press, New York, pp 99–112

    Google Scholar 

  • Sheriff MJ, Krebs CJ, Boonstra R (2009) The sensitive hare: sublethal effects of predator stress on reproduction in snowshoe hares. J Anim Ecol 78:1249–1258

    Article  PubMed  Google Scholar 

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

    Article  Google Scholar 

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

    Article  PubMed  Google Scholar 

  • SPSS (1998) SPSS 8.0 for windows. SPSS Inc., Prentice Hall, New Jersey

    Google Scholar 

  • Stoks R (2001) Food stress and predator-induced stress shape developmental performance in a damselfly. Oecologia 127:222–229

    Article  CAS  PubMed  Google Scholar 

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

    Article  Google Scholar 

  • Tay WT, Soria MF, Walsh T, Thomazoni D, Silvie P, Behere GT, Anderson C, Downes S (2013) A brave new world for an old world pest: Helicoverpa armigera (Lepidoptera: Noctuidae) in Brazil. PLoS ONE 8:e80134

    Article  PubMed Central  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 

  • Vonesh JR, Warkentin KM (2006) Opposite shifts in size at metamorphosis in response to larval and metamorph predators. Ecology 87:556–562

    Article  PubMed  Google Scholar 

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

    Article  Google Scholar 

  • Walzer A, Lepp N, Schausberger P (2015) Compensatory growth following transient intraguild predation risk in predatory mites. Oikos 124:603–609

    Article  PubMed Central  PubMed  Google Scholar 

  • Weber DC, Lundgren JG (2009) Assessing the trophic ecology of the Coccinellidae: their roles as predators and as prey. Biol Control 51:199–214

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Wu KJ (1980) The artificial diet of Helicoverpa armigera Hübner (Lepidoptera: Noctuidae). Chin Bull Entomol 17:36–37

    Google Scholar 

  • Wu KM, Mu W, Liang GM, Guo YY (2005) Regional reversion of insecticide resistance in Helicoverpa armigera (Lepidoptera: Noctuidae) is associated with the use of Bt cotton in northern China. Pest Manag Sci 61:491–498

    Article  CAS  PubMed  Google Scholar 

  • Yarro JG (1985) Effect of host plant on moulting in the African armyworm, Spodoptera exempta (Walker) (Lepidoptera: Noctuidae) at constant temperature and humidity conditions. Insect Sci Appl 6:171–175

    Google Scholar 

Download references

Acknowledgments

This research was funded by the National “Twelfth Five-Year” Plan for Science & Technology Support of China (2012BAD19B05). The authors thank the Beijing Academy of Agricultural and Forestry Sciences for allowing the collection of lady beetles in their experimental fields, Fan Zhang for technical assistance with predator rearing, and Qingpo Yang for help with data collection.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Xiaoxia Liu.

Additional information

Handling Editor: Marta Montserrat.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Xiong, X., Michaud, J.P., Li, Z. et al. Chronic, predator-induced stress alters development and reproductive performance of the cotton bollworm, Helicoverpa armigera . BioControl 60, 827–837 (2015). https://doi.org/10.1007/s10526-015-9689-9

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10526-015-9689-9

Keywords

Navigation