Skip to main content
SpringerLink
Log in

Integrative Systematics and Adaptations of Natural Enemies to Their Hosts

  • Chapter
  • First Online:
Extended Biocontrol

  • 584 Accesses

Abstract

The beneficial macroorganisms that can be used for plant protection are extremely diverse and often very difficult to identify. This taxonomic diversity is accompanied by extremely varied adaptations that ultimately have a major impact on the effectiveness of biological control strategies. As a result, being able to initially identify these species and continue to do so reliably are major challenges. Inaccurate characterization of natural enemies during the research and development phase or during field applications leads indeed to suboptimal or even failed pest regulation. In this chapter, we begin with an overview of the taxonomic diversity of macroorganisms and illustrate the range of antagonistic interactions with their target pests. We then present integrative systematics, a discipline that combines various approaches (such as morphological study, which includes genitalia, DNA sequencing and especially barcoding, etc.). This discipline is now key to identifying and understanding interactions between species. Finally, we look at three cross-cutting themes from an eco-evolutionary perspective: ecological specialization, behavioural adaptations (host/prey location) and diversity of symbionts in natural enemies.

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

Access this chapter

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 149.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 199.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 199.99
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

Institutional subscriptions

References

  • Aberlenc, H.-P. 2011. Une coccinelle mycétophage. In La faune auxiliaire des vignobles de France, ed. G. Sentenac, 152. Paris: Éditions France agricole.

    Google Scholar 

  • Al Khatib, F., L. Fusu, A. Cruaud, G. Gibson, N. Borowiec, J.-Y. Rasplus, N. Ris, and G. Delvare. 2014. An integrative approach to species discrimination in the Eupelmus urozonus complex (Hymenoptera, Eupelmidae), with the description of 11 new species from the Western Palaearctic. Systematic Entomology 39 (4): 806–862.

    Article  Google Scholar 

  • Al Khatib, F., A. Cruaud, L. Fusu, G. Genson, J.-Y. Rasplus, N. Ris, and G. Delvare. 2016. Multilocus phylogeny and ecological differentiation of the “Eupelmus urozonus species group” (Hymenoptera, Eupelmidae) in the West-Palaearctic. BMC Evolutionary Biology 16 (13): 1–20.

    Google Scholar 

  • Alberdi, A., O. Aizpurua, K. Bohmann, S. Gopalakrishnan, C. Lynggaard, M. Nielsen, and M.T.P. Gilbert. 2019. Promises and pitfalls of using high-throughput sequencing for diet analysis. Molecular Ecology Resources 19 (2): 327–348.

    Article  PubMed  Google Scholar 

  • Arthemis. 2021. The Arthemis database. https://arthemisdb.supagro.inra.fr/. Date of access 8 June 2021.

  • Benvenuto, C., E. Tabone, E. Vercken, N. Sorbier, E. Colombel, S. Warot, X. Fauvergue, and N. Ris. 2012. Intraspecific variability in the parasitoid wasp Trichogramma chilonis: Can we predict the outcome of hybridization? Evolutionary Applications 5 (5): 498–510.

    Article  PubMed  PubMed Central  Google Scholar 

  • Bout, A., J. Lambion, B. Quaglietti, Scotta M. Ion, I. Ruiz, I. Le Goff, N. Ris, and J.-C. Streito. 2019. M. pygmaeus, une punaise auxiliaire pleine de ressources. Phytoma 724: 41–44.

    Google Scholar 

  • Buhay, J.E. 2009. “COI-like” sequences are becoming problematic in molecular systematic and DNA barcoding studies. Journal of Crustacean Biology 29 (1): 96–110.

    Article  Google Scholar 

  • Burnell, A.M., and P.S. Stock. 2000. Heterorhabditis, Steinernema and their bacterial symbionts – Lethal pathogens of insects. Nematology 2 (1): 31–42.

    Article  Google Scholar 

  • Carletto, J., E. Lombaert, P. Chavigny, T. Brévault, L. Lapchin, and F. Vanlerberghe-Masutti. 2009. Ecological specialization of the aphid Aphis gossypii Glover on cultivated host plants. Molecular Ecology 18 (10): 2198–2212.

    Article  CAS  PubMed  Google Scholar 

  • Carroll, D.P., and S.C. Hoyt. 1984. Augmentation of European earwigs (Dermaptera: Forficulidae) for biological control of apple aphid (Homoptera: Aphididae) in an apple orchard. Journal of Economic Entomology 77 (3): 738–740.

    Article  Google Scholar 

  • Cassis, G., and R.T. Schuh. 2012. Systematics, biodiversity, biogeography, and host associations of the Miridae (Insecta: Hemiptera: Heteroptera: Cimicomorpha). Annual Review of Entomology 57: 377–404.

    Article  CAS  PubMed  Google Scholar 

  • Castañé, C., J. Arnó, R. Gabarra, and O. Alomar. 2011. Plant damage to vegetable crops by zoophytophagous mirid predators. Biological Control 59 (1): 22–29.

    Article  Google Scholar 

  • Cheng, H.K., J.H. Zhao, M. Xie, S.X. Wei, X.P. Song, and J.Z. Wang. 1992. Tests on the effect of releasing Aphidoletes aphidimyza (Dip.: Cecidomyiidae) to control the aphid, Myzus persicae, in greenhouses and plastic tunnels. Chinese Journal of Biological Control 8 (3): 97–100.

    Google Scholar 

  • Collins, R.A., and R.H. Cruickshank. 2013. The seven deadly sins of DNA barcoding. Molecular Ecology Resources 13 (6): 969–975.

    CAS  PubMed  Google Scholar 

  • Daane, K.M., G.Y. Yokota, Y. Zheng, and K.S. Hagen. 1996. Inundative release of common green lacewings (Neuroptera: Chrysopidae) to suppress Erythroneura variabilis and E. elegantula (Homoptera: Cicadellidae) in vineyards. Environmental Entomology 25 (1): 1224–1234.

    Article  Google Scholar 

  • Dayrat, B. 2005. Towards integrative taxonomy. Biological Journal of the Linnean Society 85 (3): 407–415.

    Article  Google Scholar 

  • De Barro, P.J. 2005. Genetic structure of the whitefly Bemisia tabaci in the Asia-Pacific region revealed using microsatellite markers. Molecular Ecology 14 (12): 3695–3718.

    Article  CAS  PubMed  Google Scholar 

  • De Boer, J.G., and M. Dicke. 2006. Olfactory learning by predatory arthropods. Animal Biology 56: 143–155.

    Article  Google Scholar 

  • de Lange, E.S., K. Farnier, B. Gaudillat, and T.C.J. Turlings. 2016. Comparing the attraction of two parasitoids to herbivore-induced volatiles of maize and its wild ancestors, the teosintes. Chemoecology 26 (1): 33–44.

    Article  CAS  Google Scholar 

  • Delfosse, E. 2015. Addendum sur les Arachnides, les Myriapodes et les insectes de France et du monde (Arthropoda). Le bulletin d’Arthropoda 48: 5–22.

    Google Scholar 

  • Delvare, G. 2011. Les principaux auxiliaires en viticulture : description, écologie, biologie. Parasitoïdes. In La faune auxiliaire des vignobles de France, ed. G. Sentenac, 107–151. Paris: Éditions France agricole.

    Google Scholar 

  • Drezen, J.-M., G. Chevignon, F. Louis, and E. Huguet. 2014. Origin and evolution of symbiotic viruses associated with parasitoid wasps. Current Opinion in Insect Science 6: 35–43.

    Article  PubMed  Google Scholar 

  • Dukas, R. 2008. Evolutionary biology of insect learning. Annual Review of Entomology 53: 145–160.

    Article  CAS  PubMed  Google Scholar 

  • Duron, O., D. Bouchon, S. Boutin, L. Bellamy, L. Zhou, J. Engelstädter, and G.D. Hurst. 2008. The diversity of reproductive parasites among arthropods: Wolbachia do not walk alone. BMC Biology 6: 1–12.

    Article  CAS  Google Scholar 

  • Enigl, M., and P. Schausberger. 2007. Incidence of the endosymbionts Wolbachia, Cardinium and Spiroplasma in phytoseiid mites and associated prey. Experimental and Applied Acarology 42 (2): 75–85.

    Article  PubMed  Google Scholar 

  • Feener, D.H., Jr., and B.V. Brown. 1997. Diptera as parasitoids. Annual Review of Entomology 42: 73–97.

    Article  CAS  PubMed  Google Scholar 

  • Foottit, R.G., and P.H. Adler. 2017. Insect Biodiversity: Science and Society. Vol. I and II. Hoboken: Wiley Blackwell.

    Book  Google Scholar 

  • Forst, S., B. Dowds, N. Boemare, and E. Stackebrandt. 1997. Xenorhabdus and Photorhabdus spp.: Bugs that kill bugs. Annual Review of Microbiology 51: 47–72.

    Article  CAS  PubMed  Google Scholar 

  • Gagné, R.J., and M. Jaschhof. 2017. A Catalog of Cecidomyiidae (Diptera) of the World. 4th ed. Digital [Online].

    Google Scholar 

  • Gardiner, M.M., D.A. Landis, C. Gratton, N. Schmidt, M. O’Neal, E. Mueller, J. Chacon, and G.E. Heimpel. 2010. Landscape composition influences the activity density of Carabidae and Arachnida in soybean fields. Biological Control 55 (1): 11–19.

    Article  Google Scholar 

  • Gargominy, O., S. Tercerie, C. Régnier, T. Ramage, P. Dupont, P. Daszkiewicz, and L. Poncet. 2018. TAXREF v12, référentiel taxonomique pour la France : méthodologie, mise en oeuvre et diffusion, Rapport Patrinat 2018-117. Paris: Muséum national d’histoire naturelle.

    Google Scholar 

  • Giorgi, J.A., N.J. Vandenberg, J.V. McHugh, J.A. Forrester, S.A. Ślipiński, K.B. Miller, L.R. Shapiro, and M.F. Whiting. 2009. The evolution of food preferences in Coccinellidae. Biological Control 51 (2): 215–231.

    Article  Google Scholar 

  • Giunti, G., A. Canale, R.H. Messing, E. Donati, C. Stefanini, J.P. Michaud, and G. Benelli. 2015. Parasitoid learning: Current knowledge and implications for biological control. Biological Control 90: 208–219.

    Article  Google Scholar 

  • Godfray, H.C.J. 1994. Parasitoids: Behavioral and Evolutionary Ecology. Princeton: Princeton University Press.

    Book  Google Scholar 

  • Hebert, P.D.N., and T.R. Gregory. 2005. The promise of DNA barcoding for taxonomy. Systematic Biology 54 (5): 852–859.

    Article  PubMed  Google Scholar 

  • Heimpel, G.E., and T.R. Collier. 1996. The evolution of host-feeding behaviour in insect parasitoids. Biological Reviews 71 (3): 373–400.

    Article  Google Scholar 

  • Henry, C.S., S.J. Brooks, J.B. Johnson, and P. Duelli. 1999. Revised concept of Chrysoperla mediterranea (Hölzel), a green lacewing associated with conifers: Courtship songs across 2800 kilometres of Europe (Neuroptera: Chrysopidae). Systematic Entomology 24 (4): 335–350.

    Article  Google Scholar 

  • Heraty, J. 2017. Parasitoid biodiversity and insect pest management. In Insect Biodiversity: Science and Society, ed. R.G. Foottit and P.H. Adler, vol. I, 603–626. Hoboken: Wiley Blackwell.

    Chapter  Google Scholar 

  • Herniou, E.A., E. Huguet, J. Thézé, A. Bézier, G. Periquet, and J.-M. Drezen. 2013. When parasitic wasps hijacked viruses: Genomic and functional evolution of polydnaviruses. Philosophical Transactions of the Royal Society, B: Biological Sciences 368 (1626): 20130051.

    Article  CAS  PubMed Central  Google Scholar 

  • Hilgenboecker, K., P. Hammerstein, P. Schlattmann, A. Telschow, and J.H. Werren. 2008. How many species are infected with Wolbachia? A statistical analysis of current data. FEMS Microbiology Letters 281 (2): 215–220.

    Article  CAS  PubMed  Google Scholar 

  • Jervis, M.A., and N.A.C. Kidd. 1986. Host-feeding strategies in Hymenoptera parasitoids. Biological Reviews 61 (4): 395–434.

    Article  Google Scholar 

  • Kreiter, S. 2011. Les principaux auxiliaires en viticulture : description, écologie, biologie. Prédateurs. In La faune auxiliaire des vignobles de France, ed. G. Sentenac, 52–106. Paris: Éditions France agricole.

    Google Scholar 

  • Kuznetsov, V.N. 1999. Employment of Coccinellidae in biological control of plant pests. In Research Progress in Plant Protection and Plant Nutrition, 219–227. Beijing: China Agriculture Press.

    Google Scholar 

  • Lattin, J.D. 1999. Bionomics of the Anthocoridae. Annual Review of Entomology 44: 207–231.

    Article  CAS  PubMed  Google Scholar 

  • Lewis, E.E., J. Campbell, C. Griffin, H. Kaya, and A. Peters. 2006. Behavioral ecology of entomopathogenic nematodes. Biological Control 38 (1): 66–79.

    Article  Google Scholar 

  • Lis, J.A., B. Lis, and D.J. Ziaja. 2016. In BOLD we trust? A commentary on the reliability of specimen identification for DNA barcoding: A case study on burrower bugs (Hemiptera: Heteroptera: Cydnidae). Zootaxa 4114 (1): 83–86.

    Article  PubMed  Google Scholar 

  • Martinez, M. 2020. Ordre des Diptera (Diptères): 959–1152 (Vol. 1) and 528–82 (Vol. 2). In Les Insectes du Monde. Biodiversité. Classification. Clés de détermination des familles, ed. H.-P. Aberlenc. Versailles: Montpellier & Plaissan, Quae & MUSEO Éditions.

    Google Scholar 

  • Mayr, E. 1942. Systematics and the Origin of Species. New York: Columbia University Press.

    Google Scholar 

  • McMurtry, J.A., G.J. De Moraes, and N.F. Sourassou. 2013. Revision of the lifestyles of phytoseiid mites (Acari: Phytoseiidae) and implications for biological control strategies. Systematic and Applied Acarology 18 (4): 297–320.

    Article  Google Scholar 

  • Miñarro, A., and T. Dapena. 2003. Effects of groundcover management on ground beetles (Coleoptera: Carabidae) in an apple orchard. Applied Soil Ecology 23 (2): 111–117.

    Article  Google Scholar 

  • Mound, L.A. 2005. Thysanoptera: Diversity and interactions. Annual Review of Entomology 50: 247–269.

    Article  CAS  PubMed  Google Scholar 

  • Parolin, P., Scotta M. Ion, and C. Bresch. 2014. Biology of Dittrichia viscosa, a Mediterranean ruderal plant: A review. Phyton 83 (2): 251–262.

    Google Scholar 

  • Pineda, A., and M.A. Marcos-García. 2008. Introducing barley as aphid reservoir in sweet-pepper greenhouses: Effects on native and released hoverflies (Diptera: Syrphidae). European Journal of Entomology 105 (3): 531–535.

    Article  Google Scholar 

  • Quicke, D.L.J. 1997. Parasitic Wasps. London: Chapman and Hall.

    Google Scholar 

  • Ris, N., M. Ion-Scotta, Khatib F. Al, J. Lambion, F. Warlop, and A. Bout. 2014. Biodiversités « utile » et « nuisible » dans les agrosystèmes : importance pour la lutte biologique par conservation. Mémoires de la Société entomologique de France 9: 35–43.

    Google Scholar 

  • Robert, C., S. Bothorel, S. Luce, A. Lauvernay, M. Leflon, G. Delvare, J.-C. Streito, E. Pierre, P. Cruaud, M. Ollivier, G. Genson, A. Cruaud, and J.-Y. Rasplus. 2019. COLEOTOOL : développement d’outils moléculaires en vue d’identifier les principaux charançons ravageurs du colza et leurs auxiliaires parasitoïdes. Innovations agronomiques 71: 181–200.

    Google Scholar 

  • Sentenac, G. 2011. La faune auxiliaire des vignobles de France. Paris: Éditions France agricole.

    Google Scholar 

  • Shapiro-Ilan, D.I., D.H. Gouge, S.J. Piggott, and J.P. Fife. 2006. Application technology and environmental considerations for use of entomopathogenic nematodes in biological control. Biological Control 38 (1): 124–133.

    Article  Google Scholar 

  • Skuhravá, M., V. Skuhravý, P. Dauphin, and R. Coutin. 2005. Gall midges of France : Les cécidomyies de France (Diptera : Cecidomyiidae). Vol. 5. Bordeaux: Société linnéenne de Bordeaux, Coll. Mémoires de la Société linnéenne de Bordeaux.

    Google Scholar 

  • Steidle, J.L.M., and J.J.A. van Loon. 2003. Dietary specialization and infochemical use in carnivorous arthropods: Testing a concept. Entomologia Experimentalis et Applicata 108 (3): 133–148.

    Article  Google Scholar 

  • Stireman, J.O., III. 2002. Host location and selection cues in a generalist tachinid parasitoid. Entomologia Experimentalis et Applicata 103 (1): 23–34.

    Article  CAS  Google Scholar 

  • Stireman, J.O., III, J.E. O’Hara, and D.M. Wood. 2006. Tachinidae: Evolution, behavior, and ecology. Annual Review of Entomology 51: 525–555.

    Article  CAS  PubMed  Google Scholar 

  • Stouthamer, R., R.F. Luck, J.D. Pinto, G.R. Platner, and B. Stephens. 1996. Non-reciprocal cross-incompatibility in Trichogramma deion. Entomologia Experimentalis et Applicata 80 (3): 481–489.

    Article  Google Scholar 

  • Stouthamer, R., J.A.J. Breeuwer, and G.D.D. Hurst. 1999. Wolbachia pipientis: Microbial manipulator of arthropod reproduction. Annual Review of Microbiology 53: 71–102.

    Article  CAS  PubMed  Google Scholar 

  • Stouthamer, R., P. Jochemsen, G.R. Platner, and J.D. Pinto. 2000. Crossing incompatibility between Trichogramma minutum and T. platneri (Hymenoptera: Trichogrammatidae): Implications for application in biological control. Environmental Entomology 29 (4): 832–837.

    Article  Google Scholar 

  • Stuart, R.J., F.E. El-Borai, and L.W. Duncan. 2008. From augmentation to conservation of entomopathogenic nematodes: Trophic cascades, habitat manipulation and enhanced biological control of Diaprepes abbreviatus root weevils in Florida citrus groves. Journal of Nematology 40 (2): 73–84.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Turlings, T.C.J., and M. Erb. 2018. Tritrophic interactions mediated by herbivore-induced plant volatiles: Mechanisms, ecological relevance, and application potential. Annual Review of Entomology 63: 433–452.

    Article  CAS  PubMed  Google Scholar 

  • Vavre, F., C. Girin, and M. Boulétreau. 1999. Phylogenetic status of a fecundity-enhancing Wolbachia that does not induce thelytoky in Trichogramma. Insect Molecular Biology 8 (1): 67–72.

    Article  CAS  PubMed  Google Scholar 

  • Vet, L.E.M., and M. Dicke. 1992. Ecology of infochemical use by natural enemies in a tritrophic context. Annual Review of Entomology 37: 141–172.

    Article  Google Scholar 

  • Werren, J.H. 1997. Biology of Wolbachia. Annual Review of Entomology 42: 587–609.

    Article  CAS  PubMed  Google Scholar 

  • Wilson, J.-J., K.-W. Sing, R.M. Floyd, and P.D.N. Hebert. 2017. DNA barcodes and insect biodiversity. In Insect Biodiversity: Science and Society, ed. R.G. Foottit and P.H. Adler, vol. I, 572–592. Hoboken: Wiley Blackwell.

    Google Scholar 

Download references

Author information

Authors and Affiliations

  1. ISA. INRAE, CNRS, UCA, Sophia Antipolis, France

    Nicolas Ris

  2. CBGP. INRAE, Univ Montpellier, Montpellier SupAgro, CIRAD, IRD, Montpellier, France

    Éric Pierre & Jean-Claude Streito

Authors
  1. Nicolas Ris
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Éric Pierre
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Jean-Claude Streito
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Jean-Claude Streito .

Editor information

Editors and Affiliations

  1. ISA. INRAE, CNRS, UCA, Sophia Antipolis, France

    Xavier Fauvergue

  2. SAVE. INRAE, Bordeaux Sciences Agro, ISVV, Villenave d’Ornon, France

    Adrien Rusch

  3. IRHS. Univ Angers, Institut Agro, INRAE, SFR QUASAV, Angers, France

    Matthieu Barret

  4. Pathologie Végétale. INRAE, Montfavet, France

    Marc Bardin

  5. iEES-Paris. INRAE, CNRS, IRD, Sorbonne Univ, Univ Paris, Univ Paris Est Créteil, Versailles, France

    Emmanuelle Jacquin-Joly

  6. ISA. INRAE, CNRS, UCA, Sophia Antipolis, France

    Thibaut Malausa

  7. SPE. INRAE, Sophia Antipolis, France

    Christian Lannou

Rights and permissions

Reprints and permissions

Copyright information

© 2022 The Author(s), under exclusive license to Springer Nature B.V.

About this chapter

Check for updates. Verify currency and authenticity via CrossMark

Cite this chapter

Ris, N., Pierre, É., Streito, JC. (2022). Integrative Systematics and Adaptations of Natural Enemies to Their Hosts. In: Fauvergue, X., et al. Extended Biocontrol. Springer, Dordrecht. https://doi.org/10.1007/978-94-024-2150-7_1

Download citation

Publish with us

Policies and ethics

Search

Navigation