Skip to main content
SpringerLink
Log in

Density-dependent dispersal in biological control agents: a reflexion on the side-effects of mass-rearing conditions

  • Published:
BioControl Aims and scope Submit manuscript

Abstract

High-density rearing conditions for the mass-production of biological control agents are known to affect individual quality and performance. However, complex phenotypic traits like dispersal behaviour and their response to rearing conditions are rarely investigated, although they are likely to affect directly biocontrol efficiency in the field. In this study, we develop an original experimental design to evaluate two complementary components of dispersal behaviour in Trichogramma. Then, we investigate how these components respond to variations in rearing density, and their correlation with traits related to parasitoid fitness. We find that under high-density conditions, a large proportion of individuals display reduced mobility and fecundity, indicative of a lower-quality phenotype. These interactive effects between dispersal performance and individual fitness highlight the need to develop integrative experimental designs to easily quantify complex phenotypic traits related to the field performance of biological control agents.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Bean DW, Dudley TL, Keller JC (2007) Seasonal timing of diapause induction limits the effective range of Diorhabda elongata deserticola (Coleoptera: Chrysomelidae) as a biological control agent for tamarisk (Tamarix spp.). Environ Entomol 36:15–25

    Article  PubMed  Google Scholar 

  • Bellamy DE, Asplen MK, Byrne DN (2004) Impact of Eretmocerus eremicus (Hymenoptera: Aphelinidae) on open-field Bemisia tabaci (Hemiptera: Aleyrodidae) populations. Biol Control 29:227–234

    Article  Google Scholar 

  • Bigler F (1994) Quality control in Trichogramma production. In: Wajnberg E, Hassan SA (eds) Biological control with egg parasitoids. CABI, Wallingford, pp 93–111

    Google Scholar 

  • Boivin G (2010) Phenotypic plasticity and fitness in egg parasitoids. Neotrop Entomol 39:457–463

    Article  PubMed  Google Scholar 

  • Boivin G, Fauvergue X, Wajnberg E (2004) Optimal patch residence time in egg parasitoids: innate versus learned estimate of patch quality. Oecologia 138:640–647

    Article  PubMed  Google Scholar 

  • Bowler DE, Benton TG (2005) Causes and consequences of animal dispersal strategies: relating individual behaviour to spatial dynamics. Biol Rev 80:205–225

    Article  PubMed  Google Scholar 

  • Chailleux A, Desneux N, Seguret J, Do Thi Khanh H, Maignet P, Tabone E (2012) Assessing European egg parasitoids as a mean of controlling the invasive South American tomato pinworm Tuta absoluta. PLoS ONE 7(10):e48068

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Chaput-Bardy A, Grégoire A, Baguette M, Pagano A, Secondi J (2010) Condition and phenotype-dependent dispersal in a damselfly, Calopteryx splendens. PLoS ONE 5(5):e10694

    Article  PubMed  PubMed Central  Google Scholar 

  • Cicero L, Sivinski J, Rull J, Aluja M (2011) Effect of larval host food substrate on egg load dynamics, egg size and adult female size in four species of braconid fruit fly (Diptera: Tephritidae) parasitoids. J Insect Physiol 57:1471–1479

    Article  PubMed  CAS  Google Scholar 

  • Clobert J, Danchin E, Dhondt AA, Nichols JD (2001) Dispersal. Oxford University Press, Oxford

    Google Scholar 

  • Collier T, van Steenwyk R (2004) A critical evaluation of augmentative biological control. Biol Control 31:245–256

    Article  Google Scholar 

  • Coupland J, Baker G (2009) Search for biological control agents of invasive Mediterranean snails. In: Vincent C, Goettel MS, Lazarovits G (eds) Biological control: a global perspective. CABI, Wallingford, pp 7–12

    Google Scholar 

  • Davis JM, Stamps JA (2004) The effect of natal experience on habitat preferences. Trends Ecol Evol 19:411–416

    Article  PubMed  Google Scholar 

  • Dutton A, Bigler F (1995) Flight activity assessment of the egg parasitoid Trichogramma brassicae (Hym.: Trichogrammatidae) in laboratory and field conditions. Entomophaga 40:223–233

    Article  Google Scholar 

  • Fournier F, Boivin G (2000) Comparative dispersal of Trichogramma evanescens and Trichogramma pretiosum (Hymenoptera: Trichogrammatidae) in relation to environmental conditions. Environ Entomol 29:55–63

    Article  Google Scholar 

  • Fusco G, Minelli A (2010) Phenotypic plasticity in development and evolution: facts and concepts. Philos Trans R Soc Lond B Biol Sci 365:547–556

    Article  PubMed  PubMed Central  Google Scholar 

  • González PI, Montoya P, Perez-Lachaud G, Cancino J, Liedo P (2007) Superparasitism in mass reared Diachasmimorpha longicaudata (Ashmead) (Hymenoptera: Braconidae), a parasitoid of fruit flies (Diptera: Tephritidae). Biol Control 40:320–326

    Article  Google Scholar 

  • Greatti M, Zandigiacomo P (1995) Postrelease dispersal of Trichogramma brassicae Bezdenko in corn fields. J Appl Entomol 119:671–675

    Article  Google Scholar 

  • Gross MR (1996) Alternative reproductive strategies and tactics: diversity within sexes. Trends Ecol Evol 11:92–98

    Article  PubMed  CAS  Google Scholar 

  • Harrison RG (1980) Dispersal polymorphisms in insects. Annu Rev Ecol Syst 11:95–118

    Article  Google Scholar 

  • Harvey JA (2005) Factors affecting the evolution of development strategies in parasitoid wasps: the importance of functional constraints and incorporating complexity. Entomol Exp Appl 117:1–13

    Article  Google Scholar 

  • Hassell MP, May RM (1988) Spatial heterogeneity and the dynamics of parasitoid-host systems. Ann Zool Fennici 25:55–61

    Google Scholar 

  • Heilmann LJ, DeVault JD, Leopold RL, Narang SK (1994) Improvement of natural enemies for biological control: a genetic engineering approach. In: Narang SK, Bartlett AC, Faust RM (eds) Applications of genetics to arthropods of biological control significance. CRC Press, Boca Raton, pp 167–189

    Google Scholar 

  • Heimpel GE, Asplen MK (2011) A ‘Goldilocks’ hypothesis for dispersal of biological control agents. BioControl 56:441–450

    Article  Google Scholar 

  • Hendricks DE (1967) Effect of wind on dispersal of Trichogramma semifumatum. J Econ Entomol 60:1367–1373

    Article  Google Scholar 

  • Hirzel AH, Nisbet RM, Murdoch WW (2007) Host-parasitoid spatial dynamics in heterogeneous landscapes. Oikos 116:2082–2096

    Article  Google Scholar 

  • Hopper KR, Roush RT, Powell W (1993) Management of genetics of biological-control introductions. Annu Rev Entomol 38:27–51

    Article  Google Scholar 

  • Huigens ME, Woelke JB, Pashalidou FG, Bukovinszky T, Smid HM, Fatouros NE (2010) Chemical espionage on species-specific butterfly anti-aphrodisiacs by hitchhiking Trichogramma wasps. Behav Ecol 21:470–478

    Article  Google Scholar 

  • Ims RA, Hjermann DO (2001) Condition-dependent dispersal. In: Clobert J, Danchin E, Dhondt AA, Nichols JD (eds) dispersal. Oxford University Press, Oxford, pp 203–216

    Google Scholar 

  • Kölliker-Ott UM, Bigler F, Hoffmann AA (2004) Field dispersal and host location of Trichogramma brassicae is influenced by wing size but not wing shape. Biol Control 31:1–10

    Article  Google Scholar 

  • Kruidhof HM, Pashalidou FG, Fatouros NE, Figueroa IA, Vet LEM, Smid HM, Huigens ME (2012) Reward value determines memory consolidation in parasitic wasps. PLoS ONE 7(8):e39615

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Lewis JW, Vet LEM, Tumlinson JH, van Lenteren JC, Papaj DR (2003) Variations in natural-enemy foraging behaviour: essential element of a sound biological control theory. In: van Lenteren JC (ed) Quality control and production of biological control agents: theory and testing procedures. CABI, Wallingford, pp 41–58

    Chapter  Google Scholar 

  • Luczynski A, Nyrop JP, Shi A (2007) Influence of cold storage on pupal development and mortality during storage and on post-storage performance of Encarsia formosa and Eretmocerus eremicus (Hymenoptera: Aphelinidae). Biol Control 40:107–117

    Article  Google Scholar 

  • Matthysen E (2005) Density-dependent dispersal in birds and mammals. Ecography 28:403–416

    Article  Google Scholar 

  • Mawela KV, Kfir R, Krueger K (2013) Effect of temperature and host species on parasitism, development time and sex ratio of the egg parasitoid Trichogrammatoidea lutea Girault (Hymenoptera: Trichogrammatidae). Biol Control 64:211–216

    Article  Google Scholar 

  • McDougall SJ, Mills NJ (1997) Dispersal of Trichogramma platneri Nagarkatti (Hym., Trichogrammatidae) from point-source releases in an apple orchard in California. J Appl Entomol 121:205–209

    Article  Google Scholar 

  • Mousseau TA, Fox CW (1998) The adaptive significance of maternal effects. Trends Ecol Evol 13:403–407

  • Nunney L (2003) Managing captive populations for release: a population-genetic perspective. In: van Lenteren JC (ed) Quality control and production of biological control agents: theory and testing procedures. CABI, Wallingford, pp 73–88

    Chapter  Google Scholar 

  • Pereira R, Silva N, Quintal C, Abreu R, Andrade J, Dantas L (2007) Effect of acclimation to outdoor conditions on the sexual performance of mass-produced medflies (Diptera: Tephritidae). Fla Entomol 90:171–174

    Article  Google Scholar 

  • Pigliucci M, Preston K (2004) Phenotypic integration: studying the ecology and evolution of complex phenotypes. Oxford University Press, Oxford

    Google Scholar 

  • Pigliucci M, Murren CJ, Schlichting CD (2006) Phenotypic plasticity and evolution by genetic assimilation. J Exp Biol 209:2362–2367

    Article  PubMed  Google Scholar 

  • Pineda A, Marcos-García M (2008) Evaluation of several strategies to increase the residence time of Episyrphus balteatus (Diptera, Syrphidae) releases in sweet pepper greenhouses. Ann Appl Biol 152:271–276

    Article  Google Scholar 

  • Quicke DLJ (1997) Parasitic wasps. Chapman and Hall, London

    Google Scholar 

  • Rietdorf K, Steidle JLM (2002) Was Hopkins right? Influence of larval and early adult experience on the olfactory response in the granary weevil Sitophilus granarius (Coleoptera, Curculionidae). Physiol Entomol 27:223–227

    Article  Google Scholar 

  • Rodrigues AMM, Johnstone RA (2014) Evolution of positive and negative density-dependent dispersal. Proc R Soc Lond B Biol Sci 281:20141226

    Article  Google Scholar 

  • Roff DA, Fairbairn DJ (2001) The genetic basis of dispersal and migration, and its consequences for correlated traits. In: Clobert J, Nichols JD, Danchin E, Dhondt AA (eds) dispersal. Oxford University Press, Oxford, pp 191–202

    Google Scholar 

  • Ronce O (2007) How does it feel to be like a rolling stone? Ten questions about dispersal evolution. Annu Rev Ecol Evol Syst 38:231–253

    Article  Google Scholar 

  • Rosenheim JA, Hoy MA (1988) Genetic improvement of a parasitoid biological control agent: artificial selection for insecticide resistance in Aphytis melinus (Hymenoptera: Aphelinidae). J Econ Entomol 81:1539–1550

    Article  CAS  Google Scholar 

  • Ruberson JR, Nechols JR, Tauber MJ (1999) Biological control of arthropod pests. In: Ruberson JR (ed) Handbook of pest management. Marcel Dekker, New York, pp 417–448

    Google Scholar 

  • Russell TL, Lwetoijera DW, Knols BGJ, Takken W, Killeen GF, Ferguson HM (2011) Linking individual phenotype to density-dependent population growth: the influence of body size on the population dynamics of malaria vectors. Proc R Soc Lond B Biol Sci 278:3142–3151

    Article  Google Scholar 

  • Schöller M (2010) Prospects for biological control of stored-product pests. Julius-Kühn-Arch 429:25–31

    Google Scholar 

  • Shingleton AW, Frankino WA, Flatt T, Nijhout HF, Emlen DJ (2007) Size and shape: the developmental regulation of static allometry in insects. BioEssays News Rev Mol Cell Dev Biol 29:536–548

    Article  Google Scholar 

  • Silva IMMS, van Meer MMM, Roskam MM, Hoogenboom A, Gort G, Stouthamer R (2000) Biological control potential of Wolbachia-infected versus uninfected wasps: laboratory and greenhouse evaluation of Trichogramma cordubensis and T. deion strains. Biocontrol Sci Technol 10:223–238

    Article  Google Scholar 

  • Smith SM (1996) Biological control with Trichogramma: advances, successes, and potential of their use. Annu Rev Entomol 41:375–406

    Article  PubMed  CAS  Google Scholar 

  • Stouthamer R (2003) The use of unisexual wasps in biological control. In: van Lenteren JC (ed) Quality control and production of biological control agents: theory and testing procedures. CABI, Wallingford, pp 93–114

    Chapter  Google Scholar 

  • Tabone E, Bardon C, Desneux N, Wajnberg E (2010) Parasitism of different Trichogramma species and strains on Plutella xylostella L. on greenhouse cauliflower. J Pest Sci 83:251–256

    Article  Google Scholar 

  • Tormos J, Asís J, Sabater-Muñoz B, Baños L, Gayubo SF, Beitia F (2012) Superparasitism in laboratory rearing of Spalangia cameroni (Hymenoptera: Pteromalidae), a parasitoid of medfly (Diptera: Tephritidae). Bull Entomol Res 102:51–61

    Article  PubMed  CAS  Google Scholar 

  • van Baaren J, Nénon J-P, Boivin G (1995) Comparison of oviposition behavior of a solitary and a gregarious parasitoid (Hymenoptera: Mymaridae). J Insect Behav 8:671–686

    Article  Google Scholar 

  • van Lenteren JC (2003) Need for quality control of mass-produced biological control agents. In: van Lenteren JC (ed) Quality control and production of biological control agents: theory and testing procedures. CABI, Wallingford, pp 1–18

    Chapter  Google Scholar 

  • van Lenteren JC, Hale A, Klapwijk JN, van Schelt J, Steinberg S (2003) Guidelines for quality control of commercially produced natural enemies. In: van Lenteren JC (ed) Quality control and production of biological control agents: theory and testing procedures. CABI, Wallingford, pp 265–304

    Chapter  Google Scholar 

  • Vercken E, Vincent F, Mailleret L, Ris N, Tabone E, Fauvergue X (2013) Time-lag in extinction dynamics in experimental populations: evidence for a genetic Allee effect? J Anim Ecol 82:621–631

    Article  PubMed  PubMed Central  Google Scholar 

  • Vercken E, Fauvergue X, Ris N, Crochard D, Mailleret L (2015) Temporal autocorrelation in host density increases establishment success of parasitoids in an experimental system. Ecol Evol 5:2684–2693

    Article  PubMed  PubMed Central  Google Scholar 

  • Vet LEM, Lewis WJ, Papaj DR, van Lenteren JC (2003) A variable-response model for parasitoid foraging behaviour. In: van Lenteren JC (ed) Quality control and production of biological control agents: theory and testing procedures. CABI, Wallingford, pp 25–40

    Chapter  Google Scholar 

  • Wajnberg E, Fauvergue X, Pons O (2000) Patch leaving decision rules and the Marginal Value Theorem: an experimental analysis and a simulation model. Behav Ecol 11:577–586

    Article  Google Scholar 

  • Whitman DW, Agrawal AA (2009) What is phenotypic plasticity and why is it important? In: Whitman DW, Ananthakrishnan TN (eds) Phenotypic plasticity of insects: mechanisms and consequences. Science Publishers, Enfield, pp 1–64

    Chapter  Google Scholar 

  • Wright MG, Hoffmann MP, Chenus SA, Gardner J (2001) Dispersal behavior of Trichogramma ostriniae (Hymenoptera: Trichogrammatidae) in sweet corn fields: implications for augmentative releases against Ostrinia nubilalis (Lepidoptera: Crambidae). Biol Control 22:29–37

    Article  Google Scholar 

  • Wylie HG (1965) Effects of superparasitism on Nasonia vitripennis (Walk.) (Hymenoptera: Pteromalidae). Can Entomol 97:326–331

    Article  Google Scholar 

  • Yu DSK, Laing JE, Hagley AC (1984) Dispersal of Trichogramma spp. (Hymenoptera: Trichogrammatidae) in an apple orchard after inundative releases. Environ Entomol 13:371–374

    Article  Google Scholar 

  • Zera AJ, Denno RF (1997) Physiology and ecology of dispersal polymorphism in insects. Annu Rev Entomol 42:207–230

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

This work was supported by the Department Santé des Plantes et Environnement from the INRA (SPE Grant 2011_1301_13) and by the French Ministry of Agriculture (projet Casdar TutaPI 2011–2014). We thank Ludovic Mailleret and Vincent Calcagno for helpful comments on the study design.

Author information

Authors and Affiliations

  1. INRA, UMR 1355 Institut Sophia Agrobiotech, 06900, Sophia Antipolis, France

    Antoine Zboralski, Marine Vilarelle & Elodie Vercken

  2. Université Nice Sophia Antipolis, UMR 7254 Institut Sophia Agrobiotech, 06900, Sophia Antipolis, France

    Antoine Zboralski, Marine Vilarelle & Elodie Vercken

  3. CNRS, UMR 7254 Institut Sophia Agrobiotech, 06900, Sophia Antipolis, France

    Antoine Zboralski, Marine Vilarelle & Elodie Vercken

  4. INRA, UEFM Laboratoire BioContrôle, 06160, Antibes, France

    Antoine Zboralski, Etty Colombel & Elisabeth Tabone

Authors
  1. Antoine Zboralski
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Marine Vilarelle
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Etty Colombel
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Elisabeth Tabone
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Elodie Vercken
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Elodie Vercken.

Additional information

Handling Editor: Stefano Colazza.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Zboralski, A., Vilarelle, M., Colombel, E. et al. Density-dependent dispersal in biological control agents: a reflexion on the side-effects of mass-rearing conditions. BioControl 61, 13–22 (2016). https://doi.org/10.1007/s10526-015-9696-x

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10526-015-9696-x

Keywords

Search

Navigation