Skip to main content
SpringerLink
Log in

Apparent competition between major pests reduces pest population densities on tomato crop, but not yield loss

  • Original Paper
  • Published:
Journal of Pest Science Aims and scope Submit manuscript

An Erratum to this article was published on 23 October 2015

Abstract

Increased pest control by generalist predators has been successfully achieved in several cases by promoting apparent competition, which is the reciprocal negative interactions between prey mediated by their shared predator. However, the presence of alternative prey does not always result in an improved control of the target pest species, due to the complexity and specificity of biotic interactions. To increase the effectiveness of IPM programs, a fine understanding of the interactions among co-occurring pest species and their biocontrol agents is necessary. We tested the occurrence of apparent competition between the major tomato pests Tuta absoluta and Bemisia tabaci when preyed on by a generalist mirid bug Macrolophus pygmaeus, by monitoring pest and predator population dynamics in a greenhouse experiment. We also measured the cascading effect of the shared predator on plant and fruit damage due to pests. We observed higher predator population growth and reduced population densities of both prey in treatments with two prey, as compared to treatments with one prey, showing that apparent competition occurred. Plant and fruit damage caused by B. tabaci was reduced in the presence of T. absoluta, but damage due to T. absoluta, which accounted for the major part, was not reduced in the presence of B. tabaci, resulting in similar levels of total damage when pests co-occurred. This study demonstrates that, even if promoting apparent competition leads to actual reduction in pest densities, yield loss may not be reduced when this strategy is applied to major pests such as T. absoluta.

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

Similar content being viewed by others

References

  • Abrams PA, Matsuda H (1996) Positive indirect effects between prey species that share predators. Ecology 77:610–616

    Article  Google Scholar 

  • Abrams PA, Holt RD, Roth JD (1998) Apparent competition or apparent mutualism? Shared predation when populations cycle. Ecology 79:201–212

    Article  Google Scholar 

  • Bompard A, Jaworski CC, Bearez P, Desneux N (2013) Sharing a predator: can an invasive alien pest affect the predation on a local pest? Popul Ecol 55:433–440

    Article  Google Scholar 

  • Brassil CE (2006) Can environmental variation generate positive indirect effects in a model of shared predation? Am Nat 167:43–54

    Article  PubMed  Google Scholar 

  • Calvo F, Bolckmans K, Belda J (2011) Control of Bemisia tabaci and Frankliniella occidentalis in cucumber by Amblyseius swirskii. Biocontrol 56:185–192

    Article  Google Scholar 

  • Cardinale BJ, Harvey CT, Gross K, Ives AR (2003) Biodiversity and biocontrol: emergent impacts of a multi-enemy assemblage on pest suppression and crop yield in an agroecosystem. Ecol Lett 6:857–865

    Article  Google Scholar 

  • Castané C, Arno J, Gabarra R, Alomar O (2011) Plant damage to vegetable crops by zoophytophagous mirid predators. Biol Control 59:22–29

    Article  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:e48068

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Chailleux A, Bearez P, Pizzol J, Amiens-Desneux E, Ramirez-Romero R, Desneux N (2013) Potential for combined use of parasitoids and generalist predators for biological control of the key invasive tomato pest Tuta absoluta. J Pest Sci 86:533–541

    Article  Google Scholar 

  • Chailleux A, Mohl E, Teixeira A, Messelink G, Desneux N (2014) Natural enemy-mediated indirect interactions among prey species: current theories and potential for enhancing biocontrol services in agro-ecosystems. Pest Manag Sci 70:1769–1779

    Article  CAS  PubMed  Google Scholar 

  • Chaneton EJ, Bonsall MB (2000) Enemy-mediated apparent competition: empirical patterns and the evidence. Oikos 88:380–394

    Article  Google Scholar 

  • Costamagna AC, Landis DA, Difonzo CD (2007) Suppression of soybean aphid by generalist predators results in a trophic cascade in soybeans. Ecol Appl 17:441–451

    Article  PubMed  Google Scholar 

  • Dangremond EM, Pardini EA, Knight TM (2000) Apparent competition with an invasive plant hastens the extinction of an endangered lupine. Ecology 91:2261–2271

    Article  Google Scholar 

  • Desneux N, O’Neil RJ (2008) Potential of an alternative prey to disrupt predation of the generalist predator, Orius insidiosus, on the pest aphid, Aphis glycines, via short-term indirect interactions. Bull Entomol Res 98:631–639

    Article  CAS  PubMed  Google Scholar 

  • Desneux N, O’neil RJ, Yoo HJS (2006) Suppression of population growth of the soybean aphid, Aphis glycines Matsumura, by predators: the identification of a key predator and the effects of prey dispersion, predator abundance, and temperature. Environ Entomol 35:1342–1349

    Article  Google Scholar 

  • Desneux N, Wajnberg E, Wyckhuys K, Burgio G, Arpaia S, Narvaez-Vasquez C, Gonzalez-Cabrera J, Catalan Ruescas D, Tabone E, Frandon J, Pizzol J, Poncet C, Cabello T, Urbaneja A (2010) Biological invasion of European tomato crops by Tuta absoluta: ecology, geographic expansion and prospects for biological control. J Pest Sci 83:197–215

    Article  Google Scholar 

  • Desneux N, Luna M, Guillemaud T, Urbaneja A (2011) The invasive South American tomato pinworm, Tuta absoluta, continues to spread in Afro-Eurasia and beyond: the new threat to tomato world production. J Pest Sci 84:403–408

    Article  Google Scholar 

  • Doutt RL, Nakata J (1973) The Rubus leafhopper and its egg parasitoid: an endemic biotic system useful in grape-pest management. Environ Entomol 2:381–386

    Article  Google Scholar 

  • Eubanks MD, Denno RF (2000) Health food versus fast food: the effects of prey quality and mobility on prey selection by a generalist predator and indirect interactions among prey species. Ecol Entomol 25:140–146

    Article  Google Scholar 

  • Evans EW, England S (1996) Indirect interactions in biological control of insects: pests and natural enemies in alfalfa. Ecol Appl 6:920–930

    Article  Google Scholar 

  • Evans EW, Toler TR (2007) Aggregation of polyphagous predators in response to multiple prey: ladybirds (Coleoptera: Coccinellidae) foraging in alfalfa. Popul Ecol 49:29–36

    Article  Google Scholar 

  • Evans EW, Stevenson AT, Richards DR (1999) Essential versus alternative foods of insect predators: benefits of a mixed diet. Oecologia 121:107–112

    Article  Google Scholar 

  • Fauvel G, Malausa J, Kaspar B (1987) Etude en laboratoire des principales caractéristiques biologiques de Macrolophus caliginosus (Heteroptera: Miridae). Entomophaga 32:529–543

    Article  Google Scholar 

  • Foglar H, Malausa J, Wajnberg E (1990) The functional-response and preference of Macrolophus caliginosus [Heteroptera: Miridae] for two of its prey Myzus persicae and Tetranychus urticae. Entomophaga 35:65–474

    Article  Google Scholar 

  • Hamdan AJS (2006) Functional and numerical responses of the predatory bug Macrolophus caliginosus Wagner fed on different densities of eggs of the greenhouse whitefly, Trialeurodes vaporariorum (Westwood). J Biol Res 6:147–154

    Google Scholar 

  • Harmon J, Andow DA (2004) Indirect effects between shared prey: predictions for biological control. Biocontrol 49:605–626

    Article  Google Scholar 

  • Harwood JD, Desneux N, Yoo HJS, Rowley DL, Greenstone MH, Obrycki JJ, O’Neil RJ (2007) Tracking the role of alternative prey in soybean aphid predation by Orius insidiosus: a molecular approach. Mol Ecol 16:4390–4400

    Article  CAS  PubMed  Google Scholar 

  • Holt RD (1977) Predation, apparent competition, and the structure of prey communities. Theor Popul Biol 12:197–229

    Article  CAS  PubMed  Google Scholar 

  • Holt RD, Kotler BP (1987) Short-term apparent competition. Am Nat 130:412–430

    Article  Google Scholar 

  • Holt RD, Lawton JH (1994) The ecological consequences of shared natural enemies. Annu Rev Ecol Syst 25:495–520

    Article  Google Scholar 

  • Huang N, Enkegaard A, Osborne LS, Ramakers PMJ, Messelink GJ, Pijnakker J, Murphy G (2011) The banker plant method in biological control. CRC Crit Rev Plant Sci 30:259–278

    Article  Google Scholar 

  • Jaworski CC, Bompard A, Genies L, Amiens-Desneux E, Desneux N (2013) Preference and prey switching in a generalist predator attacking local and invasive alien pests. PLoS One 8:e82231

    Article  PubMed Central  PubMed  Google Scholar 

  • Jiao X, Xie W, Wang S, Wu Q, Zhou L, Pan H, Liu B, Zhang Y (2012) Host preference and nymph performance of B and Q putative species of Bemisia tabaci on three host plants. J Pest Sci 85:423–430

    Article  Google Scholar 

  • Karban R, Hougeneitzmann D, Englishloeb G (1994) Predator-mediated apparent competition between two herbivores that feed on grapevines. Oecologia 97:508–511

    Article  Google Scholar 

  • Kuusk AK, Ekbom B (2010) Lycosid spiders and alternative food: feeding behavior and implications for biological control. Biol Control 55:20–26

    Article  Google Scholar 

  • Liere H, Kim TN, Werling BP, Meehan TD, Landis DA, Gratton C (2015) Trophic cascades in agricultural landscapes: indirect effects of landscape composition on crop yield. Ecol Appl 25:652–661

    Article  PubMed  Google Scholar 

  • Lind J, Cresswell W (2005) Determining the fitness consequences of antipredation behavior. Behav Ecol 16:945–956

    Article  Google Scholar 

  • Liu CZ, Yan L, Li HR, Wang G (2006) Effects of predator-mediated apparent competition on the population dynamics of Tetranychus urticae on apples. Biocontrol 51:453–463

    Article  Google Scholar 

  • Lu Y, Wu K, Jiang Y, Guo Y, Desneux N (2012) Widespread adoption of Bt cotton and insecticide decrease promotes biocontrol services. Nature 487:362–365

    Article  CAS  PubMed  Google Scholar 

  • Messelink GJ, van Maanen R, van Steenpaal SE, Janssen A (2008) Biological control of thrips and whiteflies by a shared predator: two pests are better than one. Biol Control 44:372–379

    Article  Google Scholar 

  • Messelink GJ, Van Maanen R, Van Holstein-Saj R, Sabelis M, Janssen A (2010) Pest species diversity enhances control of spider mites and whiteflies by a generalist phytoseiid predator. Biocontrol 55:387–398

    Article  Google Scholar 

  • Molla O, Biondi A, Alonso-Valiente M, Urbaneja A (2013) A comparative life history study of two mirid bugs preying on Tuta absoluta and Ephestia kuehniella eggs on tomato crops: implications for biological control. Biocontrol 59:1–9

    Google Scholar 

  • Müller C, Godfray H (1997) Apparent competition between two aphid species. J Anim Ecol 66:57–64

    Article  Google Scholar 

  • Murdoch WW (1969) Switching in general predators: experiments on predator specificity and stability of prey populations. Ecol Monog 39:335–354

    Article  Google Scholar 

  • Murdoch WW, Briggs CJ, Nisbet RM (2003) Consumer resource dynamics. Princeton University Press, Princeton

    Google Scholar 

  • Nomikou M, Sabelis M, Janssen A (2010) Pollen subsidies promote whitefly control through the numerical response of predatory mites. Biocontrol 55:253–260

    Article  Google Scholar 

  • Oaten A, Murdoch WW (1975) Switching, functional response, and stability in predator-prey systems. Am Nat 109:299–318

    Article  Google Scholar 

  • Oliveira MRV, Henneberry TJ, Anderson P (2001) History, current status, and collaborative research projects for Bemisia tabaci. Crop Prot 20:709–723

    Article  Google Scholar 

  • Parrella G, Scassillo L, Giorgini M (2012) Evidence for a new genetic variant in the Bemisia tabaci species complex and the prevalence of the biotype Q in southern Italy. J Pest Sci 85:227–238

    Article  Google Scholar 

  • Perdikis D, Lykouressis D (2000) Effects of various items, host plants, and temperatures on the development and survival of Macrolophus pygmaeus Rambur (Hemiptera: Miridae). Biol Control 17:55–60

    Article  Google Scholar 

  • Prasad RP, Snyder WE (2006) Polyphagy complicates conservation biological control that targets generalist predators. J Appl Ecol 43:343–352

    Article  Google Scholar 

  • Saleh D, Laarif A, Clouet C, Gauthier N (2012) Spatial and host-plant partitioning between coexisting Bemisia tabaci cryptic species in Tunisia. Popul Ecol 54:261–274

    Article  Google Scholar 

  • Settle WH, Ariawan H, Astuti ET, Cahyana W, Hakim AL, Hindayana D, Lestari AS (1996) Managing tropical rice pests through conservation of generalist natural enemies and alternative prey. Ecology 77:1975–1988

    Article  Google Scholar 

  • Symondson WOC, Sunderland KD, Greenstone MH (2002) Can generalist predators be effective biocontrol agents? Annu Rev Entomol 47:561–594

    Article  CAS  PubMed  Google Scholar 

  • Tack AJM, Gripenberg S, Roslin T (2011) Can we predict indirect interactions from quantitative food webs? - An experimental approach. J Anim Ecol 80:108–118

    Article  PubMed  Google Scholar 

  • Urbaneja A, Monton H, Molla O (2009) Suitability of the tomato borer Tuta absoluta as prey for Macrolophus pygmaeus and Nesidiocoris tenuis. J Appl Entomol 133:292–296

    Article  Google Scholar 

  • Van Rijn PCJ, Van Houten YM, Sabelis MW (2002) How plants benefit from providing food to predators even when it is also edible to herbivores. Ecology 83:2664–2679

    Article  Google Scholar 

  • Van Veen FF, Morris RJ, Godfray HCJ (2006) Apparent competition, quantitative food webs, and the structure of phytophagous insect communities. Annu Rev Entomol 51:187–208

    Article  PubMed  Google Scholar 

  • Vandekerkhove B, De Clercq P (2010) Pollen as an alternative or supplementary food for the mirid predator Macrolophus pygmaeus. Biol Control 53:238–242

    Article  Google Scholar 

  • Wootton JT (1994) The nature and consequences of indirect effects in ecological communities. Annu Rev Ecol Syst 25:443–466

    Article  Google Scholar 

  • Zappalà L, Biondi A, Alma A, Al-Jboory I, Arnò J, Bayram A, Chailleux A, El-Arnaouty A, Gerling D, Guenaoui Y, Shaltiel-Harpaz L, Siscaro G, Stavrinides M, Tavella L, Vercher Aznar R, Urbaneja A, Desneux N (2013) Natural enemies of the South American moth, Tuta absoluta, in Europe, North Africa and Middle East, and their potential use in pest control strategies. J Pest Sci 86:635–647

    Article  Google Scholar 

Download references

Acknowledgments

We thank Emily Mohl and Anaïs Bompard for comments on the design of the study, Caroline Groiseau and Cécile Thomas for their assistance throughout the experiments, Jacques Frandon (Biotop) for providing part of the biological materials, and Ian Kaplan and Tim Oppenheim for helpful comments on the manuscript. This work was supported by funds from Plant Health and Environment and Environment and Agronomy Departments of INRA and from the French ministry of agriculture (CASDAR Project 10063 to ND).

Author contribution

ND, CJ, and PB conceived and designed the experiment. CJ, PB, and AC performed the experiment. CJ and ND analyzed the data. ND contributed reagents/materials/analysis tools. CJ, ND, and AC wrote the manuscript.

Author information

Authors and Affiliations

  1. Laboratoire Evolution et Diversité Biologique, CNRS, Université de Toulouse (UPS), ENFA, UMR5174, 118 route de Narbonne, 31062, Toulouse, France

    Coline C. Jaworski

  2. INRA (French National Institute for Agricultural Research), Univ. Nice Sophia Antipolis, CNRS, UMR 1355-7254, Institut Sophia Agrobiotech, 06903, Sophia Antipolis, France

    Coline C. Jaworski, Anaïs Chailleux, Philippe Bearez & Nicolas Desneux

  3. Cirad, UPR HortSys, 34398, Montpellier, France

    Anaïs Chailleux

Authors
  1. Coline C. Jaworski
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Anaïs Chailleux
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Philippe Bearez
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Nicolas Desneux
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding authors

Correspondence to Coline C. Jaworski or Nicolas Desneux.

Additional information

Communicated by M. Traugott.

Electronic supplementary material

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Jaworski, C.C., Chailleux, A., Bearez, P. et al. Apparent competition between major pests reduces pest population densities on tomato crop, but not yield loss. J Pest Sci 88, 793–803 (2015). https://doi.org/10.1007/s10340-015-0698-3

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10340-015-0698-3

Keywords

Search

Navigation