Skip to main content
SpringerLink
Log in
Book cover

Ecology and Evolution of the Acari pp 231–249Cite as

Behaviour and indirect interactions in food webs of plant-inhabiting arthropods

  • Chapter

Part of the book series: Series Entomologica ((SENT,volume 55))

Abstract

With the increased use of biological control agents, artificial food webs are created in agricultural crops and the interactions among plants, herbivores and natural enemies change from simple tritrophic interactions to more complex food web interactions. Therefore, herbivore densities will not only be determined by direct predator—prey interactions and direct and indirect defence of plants against herbivores, but also by other direct and indirect interactions such as apparent competition, intraguild predation, resource competition, etc. Although these interactions have received considerable attention in theory and experiments, little is known about their impact on biological control. In this paper, we first present a review of indirect food web interactions in biological control systems. We propose to distinguish between numerical indirect interactions which are interactions where one species affects densities of another species through an effect on the numbers of an intermediate species, and functional indirect interactions defined as changes in the way that two species interact through the presence of a third species. It is argued that functional indirect interactions are important in food webs and deserve more attention. Subsequently, we discuss experimental results on interactions in an artificial food web consisting of pests and natural enemies on greenhouse cucumber. The two pest species are the twospotted spider mite Tetranychus urticae and the western flower thrips, Frankliniella occidentalis. Their natural enemies are the predatory mite Phytoseiulus persimilis, which is commonly used for spider mite control, and the predatory mites Neoseiulus cucumeris and Iphiseius degenerans and the predatory bug Orius laevigatus, all natural enemies of thrips. First, we analyse the possible interactions among these seven species and we continue by discussing how functional indirect interactions, particularly the behaviour of arthropods, may change the significance and impact of direct interactions and numerical indirect interactions. It was found that a simple food web of only four species already gives rise to some quite complicated combinations of interactions. Spider mites and thrips interact indirectly through resource competition, but thrips larvae are intraguild predators of spider mites. Some of the natural enemies used for control of the two herbivore species are also intraguild predators. Moreover, spider mites produce a web that is subsequently used by thrips to hide from their predators. We discuss these and other results obtained so far and we conclude with a discussion of the potential impact of functional indirect and direct interactions on food webs and their significance for biological control

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

Chapter
USD   29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD   259.00
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD   329.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD   329.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Learn about institutional subscriptions

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  • Abrams, P.A. 1984. Foraging time optimization and interactions in food webs. Am. Nat. 124: 80–96.

    Google Scholar 

  • Abrams, P.A. 1995. Implications of dynamically variable traits for identifying, classifying, and measuring direct and indirect effects in ecological communities. Am. Nat. 146: 112–134.

    Google Scholar 

  • Abrams, P.A. 1996. Dynamics and interactions in food webs with adaptive foragers. In: Food webs. Integration of patterns and dynamics, G.A. Polis and K.O. Winemiller (eds), pp. 149–159. Chapman & Hall, New York.

    Google Scholar 

  • Abrams, P.A. and Matsuda, H. 1996. Positive indirect effects between prey species that share predators. Ecology 77: 610–616.

    Article  Google Scholar 

  • Abrams, P.A., Menge, B.A., Mittelbach, G.G., Spiller, D.A. and Yodzis, P.A., 1996. The role of indirect effects in food webs. In: Food webs. Integration of patterns and dynamics, G.A. Polis and K.O. Winemiller (eds), pp. 371–395. Chapman & Hall, New York.

    Google Scholar 

  • Birch, M.C., Svihra, P., Paine, T.D. and Miller, J.C. 1980. Influence of chemically mediated behavior on host tree colonization by four cohabiting species of bark beetles. J. Chem. Ecol. 6: 395–414.

    Google Scholar 

  • Bonsall, M.B. and Hassell, M.P. 1997. Apparent competition structures ecological assemblages. Nature 388: 371–373.

    Article  CAS  Google Scholar 

  • Briggs, C.J. 1993. Competition among parasitoid species on a stage-structured host and its effect on host suppression. Am. Nat. 141: 372–397.

    Google Scholar 

  • Bredsgaard, H.F. and Enkegaard, A. 1995. Interactions among polyphagous anthocorid bugs used for thrips control and other beneficials in multi-species biological pest management systems. Med. Fac. Landbouww. Univ. Gent 60: 893–900.

    Google Scholar 

  • Chivers, D.P., Brown, G.E. and Smith R.J.F. 1996. The evolution of chemical alarm signals: attracting predators benefits alarm signal senders. Am. Nat. 148: 649–659.

    Google Scholar 

  • Cloutier, C. and Johnson, S.G. 1993. Predation by Orius tristicolor (Hemiptera, Anthocoridae) on Phytoseiulus persimilis ( Acarina, Phytoseiidae) - testing for compatibility between biocontrol agents. Environ. Entomol. 22: 477–482.

    Google Scholar 

  • Collyer, E. 1964. The effect of an alternative food supply on the relationship between two Typhlodromus species and Panonychus ulmi (Koch) (Acarina). Entomol. Exp. Appl. 7: 120–124.

    Google Scholar 

  • Dicke, M. 1994. Local and systemic production of volatile herbivore-induced terpenoids: their role in plant-carnivore mutualism. J. Plant Physiol. 143: 465–472.

    Article  CAS  Google Scholar 

  • Dicke, M. 1998. Evolution of induced indirect defense of plants. In: Evolution of induced defenses, C.D. Harvell and R. Tollrian (eds). Princeton University Press, in press.

    Google Scholar 

  • Dicke, M. and Sabelis, M.W. 1988. How plants obtain predatory mites as bodyguards. Neth. J. Zool. 38: 148–165.

    Google Scholar 

  • Dicke, M., Van Beek, T.A., Posthumus, M.A., Ben Dom, N., Van Bokhoven, H. and De Groot, E. 1990a. Isolation and identification of volatile kairomone that affects acarine predator-prey interactions. J. Chem. Ecol. 16: 381–396.

    Google Scholar 

  • Dicke, M., Van der Maas, K.J., Takabajashi, J. and Vet, L.E.M. 1990b. Learning affects response to volatile allelochemicals by predatory mites. Proc. Exp. Appl. Entomol. 1: 31–36.

    Google Scholar 

  • Dicke, M., Van Baarlen, P., Wessels, R. and Dijkman, H. 1993. Herbivory induces systemic production of plant volatiles that attract predators of the herbivore - extraction of endogenous elicitor. J. Chem. Ecol. 19: 581–599.

    Google Scholar 

  • Dicke, M., Takabayashi, J., Posthumus, M.A., Schütte, C. and Krips, O.E. 1998. Plant-phytoseiid interactions mediated by herbivore-induced plant volatiles: variation in production of cues and in responses of predatory mites. Exp. Appl. Acarol. 22: 311–333.

    Google Scholar 

  • Behaviour and indirect interactions in food Dill, L.M. 1987. Animal decision making and its ecological consequences: the future of aquatic ecology and behaviour. Can. J. Zool. 65: 803–811.

    Google Scholar 

  • Drukker, B., Scutareanu, P. and Sabelis, M.W. 1995. Do anthocorid predators respond to synomones from Psylla-infested pear trees under field conditions? Entomol. Exp. Appl. 77: 193–203.

    Google Scholar 

  • Ehler, L.E. 1996. Structure and impact of natural enemy guilds in biological control of insect pests. In: Food webs. Integration of patterns and dynamics, G.A. Polis and K.O. Winemiller (eds), pp. 337–342. Chapman & Hall, New York.

    Google Scholar 

  • English-Loeb, G.M., Karban, R. and Hougen-Eitzman, D. 1993. Direct and indirect competition between spider mites feeding on grapes. Ecol. Appl. 3: 699–707.

    Google Scholar 

  • Evans, E.W. 1991. Intra versus interspecific interations of ladybeetles ( Coleoptera: Coccinellidae) attacking aphids. Oecologia 87: 401–408.

    Google Scholar 

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

    Google Scholar 

  • Faeth, S.H. 1991. Variable induced responses: direct and indirect effects on oak folivores. In: Phytochemical induction by herbivores, D.W. Tallamy and M.J. Raupp, (eds), pp. 293–323. Wiley, New York.

    Google Scholar 

  • Ferguson, K.I. and Stiling, P. 1996. Non additive effects of multiple natural enemies on aphid populations. Oecologia 108: 375–379.

    Google Scholar 

  • Force, D.C. 1974. Ecology of insect host-parasitoid communities. Science 184: 624–632.

    Article  PubMed  CAS  Google Scholar 

  • Haukioja, E. 1990. Induction of defenses in trees. Annu. Rev. Entomol. 36: 25–42.

    Google Scholar 

  • Hochberg, M.E. 1996. Consequences for host population levels of increasing natural enemy species richness in classical biological control. Am. Nat. 147: 307–318.

    Google Scholar 

  • Holt R.D. 1977. Predation apparent competition and the structure of prey communities. Theor. Popul. Biol. 12: 197–229.

    Article  PubMed  CAS  Google Scholar 

  • Holt R.D. 1984. Spatial heterogeneity: indirect interactions and the coexistence of prey species. Am. Nat. 124: 377–406.

    Article  Google Scholar 

  • Holt, R.D. 1997. Community modules. In: Multitrophic interactions in terrestrial systems, A.C. Gange and V.K. Brown (eds), pp. 333–350. Blackwell, London.

    Google Scholar 

  • Holt R.D. and Kotler B.P. 1987. Short-term apparent competition. Am. Nat. 130: 412–430.

    Article  Google Scholar 

  • Holt, R.D. and Lawton, J.H. 1993. Apparent competition and enemy-free space in insect host-parasitoid communities. Am. Nat. 142: 623–645.

    Google Scholar 

  • Holt, R.D. and Lawton, J.H. 1994. The ecological consequences of shared natural enemies. Annu. Rev. Ecol. Syst. 25: 495–520.

    Google Scholar 

  • Holt, R.D. and Polis, G.A. 1997. A theoretical framework for intraguild predation. Am. Nat. 149: 745764.

    Google Scholar 

  • Hougen-Eitzman, D. and Karban, R. 1995. Mechanisms of interspecific competition that result in successful control of Pacific mites following inoculations of Willamette mites on grapevines. Oecologia 103: 157–161.

    Article  Google Scholar 

  • Janssen, A., Van Alphen, J.J.M., Sabelis, M.W. and Bakker, K. 1995a. Odour-mediated avoidance of competition in Drosophila parasitoids: the ghost of competition. Oikos 73: 356–366.

    Article  Google Scholar 

  • Janssen, A., Van Alphen, J.J.M., Sabelis, M.W. and Bakker, K. 1995b. Specificity of odour mediated avoidance of competition in Drosophila parasitoids. Be-hay. Ecol. Sociobiol. 36: 229–235.

    Google Scholar 

  • Janssen, A., Bruin, J., Jacobs, G., Schraag, R. and Sabelis, M.W. 1997. Predators use odours to avoid prey patches with conspecifics. J. Animal Ecol. 66: 223–232.

    Article  Google Scholar 

  • Kakehashi, N., Suzuki, Y. and Iwasa, Y. 1984. Niche overlap of parasitoids in host-parasitoid systems: its consequence to single versus multiple introduction controversy in biological control. J. Appl. Ecol. 21: 115–131.

    Google Scholar 

  • Karban, R. and Myers, J.H. 1989. Induced plant responses to herbivory. Annu. Rev. Ecol. Syst. 20: 331–348.

    Google Scholar 

  • Karban, R. and Niiho, C. 1995. Induced resistance and susceptibility to herbivory: plant memory and altered plant development. Ecology 76: 1220–1225.

    Article  Google Scholar 

  • Karban, R., Hougen-Eitzmann, D. and English-Loeb, G. 1994. Predator-mediated apparent competition between two herbivores that feed on grapevines. Oecologia 97: 508–511.

    Article  Google Scholar 

  • Karban, R., English-Loeb, G. and Hougen-Eitzman, D. 1997. Mite vaccinations for sustainable management of spider mites in vineyards. Ecol. Appl. 7: 183193.

    Google Scholar 

  • Kindlman, P. and Rûzicka, Z. 1992. Possible consequences of a specific interaction between predators and parasites of aphids. Ecol. Model. 61: 253–365.

    Google Scholar 

  • Lewis, W.J. and Takasu, K. 1990. Use of learned odours by a parasitic wasp in accordance with host and food needs. Nature 348: 635–636.

    Article  Google Scholar 

  • Liepert, C. and Dettner, K. 1993. Recognition of aphid parasitoids by honeydew-collecting ants: the role of cuticular lipids in a chemical mimicry system. J. Chem. Ecol. 19: 2143–2153.

    Google Scholar 

  • Lima, S.L. and Dill, L.M. 1990. Behavioral decisions made under the risk of predation: a review and prospectus. Can. J. Zool. 68: 619–640.

    Google Scholar 

  • Masters, G.J. and Brown, V.K. 1997. Host-plant mediated interactions between spatially separated herbivores: effects on community structure. In: Multitrophic interactions in terrestrial systems, A.C. Gange and V.K. Brow (eds), pp. 217–237. Blackwell, London.

    Google Scholar 

  • Matsuda, H., Abrams, P.A. and Hori, H. 1993. The effect of adaptive anti-predator behavior on exploitative competition and mutualism between predators. Oikos 68: 549–559.

    Article  Google Scholar 

  • Menge, B.A. 1997. Detection of direct versus indirect effects: were the experiments long enough ? Am. Nat. 149: 801–823.

    Article  PubMed  CAS  Google Scholar 

  • Miller, T.E. and Kerfoot, W.C. 1987. Redefining indirect effects. In: Predation: direct and indirect impacts on aquatic communities, W.C. Kerfoot and A. Sih (eds), pp. 33–37. University Press of New England, Hanover.

    Google Scholar 

  • Milne, M. and Walter, G.H. 1997. The significance of prey in the diet of the phytophagous thrips, Frankliniella schultzei. Ecol. Entomol. 22: 74–81.

    Google Scholar 

  • Moran, M.D. and Hurd, L.E. 1994. Short-term responses to elevated predator densities: noncompetitive intraguild interactions and behavior. Oecologia 98: 269–273.

    Article  Google Scholar 

  • Moran, M.D., Rooney, T.P. and Hurd, L.E. 1996. Top down cascade from a bitrophic predator in an old field community. Ecology 77: 2219–2227.

    Article  Google Scholar 

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

    Google Scholar 

  • Pallini, A., Janssen, A. and Sabelis, M.W. 1997. Odour-mediated responses of phytophagous mites to con-specific and heterospecific competitors. Oecologia 110: 179–185.

    Article  Google Scholar 

  • Pallini, A., Janssen, A. and Sabelis, M.W. 1999. Do western flower thrips avoid plants infested with spider mtes? Interactions between potential competitors. In: J. Bruin, L.P.S. van der Geest and M.W. Sabelis (eds), Ecology and Evolution of the Acari. Kluwer Academic Publishers, Dordrecht, pp. 375380.

    Google Scholar 

  • Peacor, S.D. and Werner, E.E. 1997. Trait-mediated indirect interactions in a simple aquatic food web. Ecology 78: 1146–1156.

    Article  Google Scholar 

  • Poland, T.M. and Borden, J.H. 1994. Semiochemicalbased communication in interspecific interactions between Ips pipi (Say) and Pityogenes knechteli (Swaine) ( Coleoptera, Scolytidae) in lodgepole pine. Can. Entomol. 126: 269–276.

    Google Scholar 

  • Polis, G.A. and Strong, D.R. 1996. Food web complexity and community dynamics. Am. Nat. 147: 813846.

    Google Scholar 

  • Polis, G.A., Myers, C.A. and Holt, R.D. 1989. The ecology and evolution of intraguild predation: potential competitors that eat each other. Annu. Rev. Ecol. Syst. 20: 297–330.

    Google Scholar 

  • Ramakers, P.M.J. 1990. Manipulation of phytoseiid thrips predators in the absence of thrips. SROP/WPRS Bull. 13 (5): 169–172.

    Google Scholar 

  • Rosenheim, J.A., Kaya, H.K., Ehler, L.E., Marois, J.J. and Jaffee, B.A. 1995. Intraguild predation among biological-control agents: theory and evidence. Biol. Control 5: 303–335.

    Google Scholar 

  • Ruxton, G.D. 1995. Short term refuge use and stability of predator-prey models. Theor. Popul. Biol. 47: 117.

    Google Scholar 

  • Sabelis, M.W. and Bakker, F.M. 1992. How predatory mites cope with the web of their tetranychid prey: a functional view on dorsal chaetotaxy in the Phytoseiidae. Exp. Appl. Acarol. 16: 203–225.

    Google Scholar 

  • Sabelis M.W. and Dicke M. 1985. Long range dispersal and searching behaviour. In: Spider mites: their biology, natural enemies and control, Vol. 1B, W. Helle and M.W. Sabelis (eds), pp. 141–160. Elsevier, Amsterdam.

    Google Scholar 

  • Sabelis, M.W. and Van de Baan, H.E. 1983. Location of distant spider mite colonies by phytoseiid predators: demonstration of specific kairomones emitted by Tetranychus urticae and Panonychus ulmi. Entomol. Exp. Appl. 33: 303–314.

    Google Scholar 

  • Sabelis, M.W. and Van der Weel, J.J. 1993. Anemotactic responses of the predatory mite, Phytoseiulus per-similis Athias-Henriot, and their role in prey finding. Exp. Appl. Acarol. 17: 521–529.

    Google Scholar 

  • Sabelis, M.W. and Van Rijn, P.C.J. 1996. Eriophyoid mites as alternative prey. In: Eriophyoid mites: their biology, natural enemies and control, E.E. Linguist, M.W. Sabelis and J. Bruin (eds), pp. 757–764. Elsevier, Amsterdam.

    Chapter  Google Scholar 

  • Sabelis, M.W. and Van Rijn, P.C.J. 1997. Predation by insects and mites. In: Thrips as crop pests, T. Lewis (ed.), pp. 259–354. CAB International, Oxon.

    Google Scholar 

  • Sabelis, M.W., Van Baalen, M., Bruin, J., Egas, M., Jansen, V.A.A., Janssen, A. and Pels, B. 1998. The evolution of overexploitation and mutualism in plantherbivore-predator interactions and its impact on population dynamics. In Theoretical approaches to biological control, B.A. Hawkins and H.V. Cornell (eds), pp. 259–282. Cambridge University Press.

    Google Scholar 

  • Schmitz, O.J., Beckerman, A.P. and O’Brien, K.M. 1997. Behaviorally mediated trophic cascades: effects of predation risk on food web interactions. Ecology 78: 1388–1399.

    Article  Google Scholar 

  • Strong, D.A. 1992. Are trophic cascades all wet? Differentiation and donor-control in speciose ecosystems. Ecology 73: 747–754.

    Article  Google Scholar 

  • Trichilo, P.J. and Leigh, T.F. 1986. Predation on spider mite eggs by the Western Flower Thrips, Frankliniella occidentalis ( Thysanoptera: Thripidae), an opportunist in a cotton agroecosystem. Environ. Entomol. 15: 821–825.

    Google Scholar 

  • Turlings, T.C.J., Tumlinson, J.H. and Lewis, W.J. 1990. Exploitation of herbivore-induced plant odors by host-seeking parasitic wasps. Science 250: 1251 1253.

    Google Scholar 

  • Turlings, T.C.J., Loughrin, J.H., McCall, P.J., Röse, U., Lewis, W.J. and Tumlinson, J.H. 1995. How caterpillar-damaged plants protect themselves by attracting parasitic wasps. Proc. Natl Acad. Sci. USA 92: 4169–4174.

    Google Scholar 

  • Van Rijn, P.C.J. and Sabelis, M.W. 1990. Pollen availability and its effect on the maintenance of populations of Amblyseius cucumeris, a predator of thrips. Meded. Fac. Landbouww. Rijksuniv. Gent 55: 335341.

    Google Scholar 

  • Van Rijn, P.C.J. and Sabelis, M.W. in press. Should plants provide food for predators when it also benefits the herbivores? The effects of pollen on a thrips-predatory mite system. In: Acarology IX, Symposia R. Mitchell, D.J. Horn, G.R. Needham and W.C. Welbourn (eds). Ohio Biological Survey, Columbus, OH, in press.

    Google Scholar 

  • Völkl, W. 1992. Aphids or their parasitoids: who actually benefits from ant-attendance? J. Anim. Ecol. 61: 273–281.

    Google Scholar 

  • Walter, D.E. and O’Dowd, D.J. 1992. Leaves with domatia have more mites. Ecology 73: 1514–1518.

    Article  Google Scholar 

  • Wittmann, E.J. and Leather, S.R. 1997. Compatibility of Orius laevigatus Fieber (Hemiptera: Anthocoridae) with Neoseiulus (Amblyseius) cucumeris Oudemans (Acari: Phytoseiidae) and Jphiseius (Amblyseius) degenerans Berlese (Acari, Phytoseiidae) in the biocontrol of Frankliniella occidentalis Pergande ( Thysanoptera: Thripidae). Exp. Appl. Acarol. 21: 523–538.

    Google Scholar 

  • Wootton, J.T. 1994. The nature and consequences of indirect effects in ecological communities. Annu. Rev. Ecol. Syst. 25: 443–466.

    Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Institute of Systematics and Population Biology, University of Amsterdam, Kruislaan 320, 1098 SM, Amsterdam, The Netherlands

    Arne Janssen & Maurice W. Sabelis

  2. Federal University of Viçosa, Minas Gerais, Brasil

    Angelo Pallini

  3. Agricultural Research Institute of Minas Gerais (EPAMIG), Brasil

    Madelaine Venzon

Authors
  1. Arne Janssen
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Angelo Pallini
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Madelaine Venzon
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Maurice W. Sabelis
    View author publications

    You can also search for this author in PubMed Google Scholar

Editor information

Editors and Affiliations

  1. Section Population Biology, University of Amsterdam, The Netherlands

    Jan Bruin , L. P. S. van der Geest  & M. W. Sabelis ,  & 

Rights and permissions

Reprints and permissions

Copyright information

© 1999 Springer Science+Business Media Dordrecht

About this chapter

Cite this chapter

Janssen, A., Pallini, A., Venzon, M., Sabelis, M.W. (1999). Behaviour and indirect interactions in food webs of plant-inhabiting arthropods. In: Bruin, J., van der Geest, L.P.S., Sabelis, M.W. (eds) Ecology and Evolution of the Acari. Series Entomologica, vol 55. Springer, Dordrecht. https://doi.org/10.1007/978-94-017-1343-6_16

Download citation

  • DOI: https://doi.org/10.1007/978-94-017-1343-6_16

  • Publisher Name: Springer, Dordrecht

  • Print ISBN: 978-90-481-5200-1

  • Online ISBN: 978-94-017-1343-6

  • eBook Packages: Springer Book Archive

Publish with us

Policies and ethics

Search

Navigation