, Volume 61, Issue 4, pp 365–377 | Cite as

Laboratory odour-specificity testing of Cotesia urabae to assess potential risks to non-target species

  • Gonzalo A. Avila
  • Toni M. Withers
  • Gregory I. Holwell


The larval parasitoid Cotesia urabae Austin and Allen (Hymenoptera: Braconidae) is known to be attracted to odours of its target host Uraba lugens Walker (Lepidoptera: Nolidae), host plant (Eucalyptus species), and target plant-host complex. Cotesia urabae females were tested in both a Y-tube and four-arm olfactometer to further investigate these attractions as well as their attraction to three non-target Lepidoptera (two in the family Erebidae and one in the family Geometridae), and their corresponding host plants and plant-host complexes. In a Y-tube olfactometer, wasps were attracted to the odours of the non-target Erebidae larvae when tested on their own and when feeding on their host plants, but not to their non-target host plants alone, suggesting some rare circumstances in the field these non-targets could be attacked by C. urabae. The multiple-comparison bioassay conducted in a four-arm olfactometer indicates that target plant-host complex odours invariably produced the strongest attraction compared with any other of the non-target plant-host complex odours tested. Cotesia urabae females that were given prior exposure and the opportunity to oviposit within either non-target species were not subsequently more attracted to the Erebidae odours, suggesting that associative learning is unlikely to increase non-target attack. Such olfactometer assays could be a very useful addition to the host specificity testing methods able to be conducted within quarantine facilities, prior to the release of candidate biological control agents. We urge other biocontrol scientists to undertake similar assays to assist with non-target risk assessments.


Braconidae Endoparasitoid Olfactometer Ecological host range Host specificity testing Infochemicals 



Thanks to Maria Saavedra and Nicky Kerr who assisted with the rearing of the Cotesia urabae colony, and also to Anne Barrington (Plant and Food Research) and Lindsay McIntyre for supplying non-target species larvae for this research project. This work was partly funded by Scion as part of the Better Border Biosecurity (B3) ( research collaboration.


  1. Agelopoulos N, Keller M (1994) Plant- natural enemy association in tritrophic system, Cotesia rubeculaPieris rapaeBrassicaceae (Cruciferae). III: collection and identification of plant and frass volatiles. J Chem Ecol 20:1955–1967CrossRefPubMedGoogle Scholar
  2. Allen GR (1990) Uraba lugens Walker (Lepidoptera: Noctuidae): Larval survival and parasitoid biology in the field in South Australia. J Aust Entomol Soc 29:301–312CrossRefGoogle Scholar
  3. Avila GA, Berndt LA, Holwell GI (2013) First releases and monitoring of the biological control agent Cotesia urabae Austin and Allen (Hymenoptera: Braconidae). N Z Entomol 36:65–72CrossRefGoogle Scholar
  4. Avila GA, Withers TM, Holwell GI (2016) Olfactory cues used in host-habitat location and host location by the parasitoid Cotesia urabae (Hymenoptera: Braconidae). Entomol Exp Appl. doi: 10.1111/eea.12393 Google Scholar
  5. Avila GA, Withers TM, Holwell GI (2015) Host testing of the parasitoid Cotesia urabae (Austin & Allen, 1989) (Hymenoptera: Braconidae) to assess the risk posed to the New Zealand nolid moth Celama parvitis (Howes, 1917) (Lepidoptera: Nolidae): do host deprivation and experience influence acceptance of non-target hosts? Aust Entomol 54:270–277CrossRefGoogle Scholar
  6. Bai S-X, Wang Z-Y, He K-L, Im D-J (2011) Olfactory response of Trichogramma ostriniae (Hymenoptera: Trichogrammatidae) to volatiles emitted by mungbean plants. Agric Sci China 10:560–565CrossRefGoogle Scholar
  7. Berndt L, Brockerhoff EG, Jactel H, Weiss T, Beaton J (2004) Biology and rearing of Pseudocoremia suavis, an endemic looper (Lepidoptera: Geometridae) with a history of outbreaks on exotic conifers. N Z Entomol 27:73–82CrossRefGoogle Scholar
  8. Berndt LA, Allen GR (2010) Biology and pest status of Uraba lugens Walker (Lepidoptera: Nolidae) in Australia and New Zealand. Aust J Entomol 49:268–277CrossRefGoogle Scholar
  9. Berndt LA, Sharpe A, Withers TM, Kimberley M, Gresham B (2010) Evaluation & review report for the release of Cotesia urabae for the biological control of gum leaf skeletoniser. Application ER-AF-NOR-1-2 09/05. Appendix 2: risks to non-target species from potential biological control agent Cotesia urabae against Uraba lugens in New Zealand. Accessed 05 Sept 2015
  10. Berndt LA, Mansfield S, Withers TM (2007) A method for host range testing of a biological control agent for Uraba lugens. N Z Plant Prot 60:286–290Google Scholar
  11. Berndt LA, Withers TM, Mansfield S, Hoare RJB (2009) Non-target species selection for host range testing of Cotesia urabae. N Z Plant Prot 62:168–173Google Scholar
  12. Berry JA, Walker GP (2004) Meteorus pulchricornis (Wesmael) (Hymenoptera: Braconidae: Euphorinae): An exotic polyphagous parasitoid in New Zealand. N Z J Zool 31:33–44CrossRefGoogle Scholar
  13. Cameron E (1935) A study of the natural control of ragwort (Senecio jacobaea L.). J Ecol 23:265–322CrossRefGoogle Scholar
  14. Cameron PJ, Walker GP (1997) Host specificity of Cotesia rubecula and Cotesia plutellae, parasitoids of white butterfly and diamondback moth. In: Proceedings of the 50th New Zealand plant protection conference, Lincoln University, Canterbury, New Zealand, pp 236–241Google Scholar
  15. Cameron PJ, Walker GP, Keller MA (1997) Clearwater JR Host specificity assessments of Cotesia plutellae, a parasitoid of diamondback moth. In: Sivapragasam A, Loke WH, Hussan AK, Lim GS (eds) The management of diamondback moth and other crucifer pests: Proceedings of the third international workshop. Kuala Lumpur, Malaysia, pp 85–89Google Scholar
  16. Chinwada P, Schulthess F, Overholt W, Jowah P, Omwega C (2008) Release and establishment of Cotesia flavipes for biological control of maize stemborers in Zimbabwe. Phytoparasitica 36:160–167CrossRefGoogle Scholar
  17. Conover WJ (1999) Practical nonparametric statistics, 3rd edn. Wiley, New YorkGoogle Scholar
  18. Conti E, Salerno G, Bin F, Bradleigh Vinson S (2004) The role of host semiochemicals in parasitoid specificity: a case study with Trissolcus brochymenae and Trissolcus simoni on pentatomid bugs. Biol Control 29:435–444CrossRefGoogle Scholar
  19. Cugala D, Overholt W, Santos L, Giga D (2001) Release of Cotesia flavipes Cameron for biological control of cereal stemborers in two ecological zones in Mozambique. Insect Sci Appl 21:303–310Google Scholar
  20. Dicke M, Baarlen P, Wessels R, Dijkman H (1993) Herbivory induces systemic production of plant volatiles that attract predators of the herbivore: extraction of endogenous elicitor. J Chem Ecol 19:581–599CrossRefPubMedGoogle Scholar
  21. Drost YC, Carde RT (1992) Host switching in Brachymeria intermedia (Hymenoptera: Chalcididae), a pupal endoparasitoid of Lymantria dispar (Lepidoptera: Lymantriidae). Environ Entomol 21:760–766CrossRefGoogle Scholar
  22. El-Wakeil N, Farghaly H, Ragab Z (2010) Efficacy of inundative releases of Trichogramma evanescens in controlling Lobesia botrana in vineyards in Egypt. J Pest Sci 83:379CrossRefGoogle Scholar
  23. Godfray HCJ (1994) Parasitoids: behavioral and evolutionary ecology. Princeton University Press, PrincetonGoogle Scholar
  24. Jembere B, Ngi-Song AJ, Overholt W (2003) Olfactory responses of Cotesia flavipes (Hymenoptera: Braconidae) to target and non- target Lepidoptera and their host plants. Biol Control 28:360–367CrossRefGoogle Scholar
  25. Martin NA (2009) Plant-SyNZ™: an invertebrate herbivore biodiversity assessment tool. Landcare Research. Accessed 05 June 2015
  26. Munro VMW, Henderson IM (2002) Nontarget effect of entomophagous biocontrol: shared parasitism between native lepidopteran parasitoids and the biocontrol agent Trigonospila brevifacies (Diptera: Tachinidae) in forest habitats. Environ Entomol 31:388–396CrossRefGoogle Scholar
  27. Ngi-Song A, Overholt W, Njagi P, Dicke M, Ayertey J, Lwande W (1996) Volatile infochemicals used in host and host habitat location by Cotesia flavipes (Cameron) and Cotesia sesamiae (Cameron) (Hymenoptera: Braconidae), larval parasitoids of stemborers on graminae. J Chem Ecol 22:307–323CrossRefPubMedGoogle Scholar
  28. Ngi-Song AJ, Overholt WA (1997) Host location and acceptance by Cotesia flavipes Cameron and Cotesia sesamiae (Cameron) (Hymenoptera: Braconidae), parasitoids of african gramineous stemborers: role of frass and other host cues. Biol Control 9:136–142CrossRefGoogle Scholar
  29. Nordlund DA, Lewis WJ, Altieri MA (1988) Influence of plant produced allelochemicals on host-prey selection behavior of entomophagous insects. In: Barbosa P, Letourneau DK (eds) Novel aspects of insect-plant interaction. Wiley, New York, pp 65–90Google Scholar
  30. Obonyo M, Schulthess F, Le Ru B, van den Berg J, Silvain J-F, Calatayud P-A (2010) Importance of contact chemical cues in host recognition and acceptance by the braconid larval endoparasitoids Cotesia sesamiae and Cotesia flavipes. Biol Control 54:270–275CrossRefGoogle Scholar
  31. Orr DB, Garcia-Salazar C, Landis DA (2000) Trichogramma nontarget impacts: a method for biological control risk assessment. In: Follett PA, Duan JJ (eds) Nontarget effects of biological control. Kluwer Academic Publishers, Boston, pp 111–125CrossRefGoogle Scholar
  32. Perfecto I, Vet L (2003) Effect of a nonhost plant on the location behavior of two parasitoids: the tritrophic system of Cotesia spp. (Hymenoptera: Braconidae), Pieris rapae (Lepidoptera: Pieridae), and Brassica oleraceae. Environ Entomol 32:163–174CrossRefGoogle Scholar
  33. Péter A (2014) Solomon Coder (version beta 14.10.04): A simple solution and free solution for behavior coding. Accessed 09 Nov 2014
  34. Quinn GP, Keough MJ (2002) Experimental design and data analysis for biologists. Cambridge University Press, CambridgeCrossRefGoogle Scholar
  35. Romeis J, Shanower T, Zebitz C (1997) Volatile plant infochemicals mediate plant preference of Trichogramma chilonis. J Chem Ecol 23:2455–2465CrossRefGoogle Scholar
  36. Roux O, Gers C, Tene-Ghomsi J, Arvanitakis L, Bordat D, Legal L (2007) Chemical characterization of contact semiochemicals for host-recognition and host-acceptance by the specialist parasitoid Cotesia plutellae (Kurdjumov). Chemoecology 17:13–18CrossRefGoogle Scholar
  37. Rowbottom R, Allen G, Walker P, Berndt L (2013) Phenology, synchrony and host range of the Tasmanian population of Cotesia urabae introduced into New Zealand for the biocontrol of Uraba lugens. BioControl 58:625–633CrossRefGoogle Scholar
  38. Singh P, Mabbett F (1976) Note on the life history of the magpie moth, Nyctemera annulata (Lepidoptera: Arctiidae). N Z J Zool 3:277–278CrossRefGoogle Scholar
  39. Sullivan JJ, Winks CJ, Fowler SV (2008) Novel host associations and habitats for Senecio-specialist herbivorous insects in Auckland. N Z Ecol Soc 32:219–224Google Scholar
  40. Tumlinson JH, Lewis WJ, Vet LEM (1993) Parasitic wasps, chemically guided intelligent foragers. Sci Am 268:100–106CrossRefGoogle Scholar
  41. Turlings T, Tumlinson J, Eller F, Lewis W (1991) Larval-damaged plants: source of volatile synomones that guide the parasitoid Cotesia marginiventris to the micro-habitat of its hosts. Entomol Exp Appl 58:75–82CrossRefGoogle Scholar
  42. Turlings TC, Tumlinson JH (1992) Systemic release of chemical signals by herbivore-injured corn. PNAS 89:8399–8402CrossRefPubMedPubMedCentralGoogle Scholar
  43. Turlings TCJ, Tumlinson JH, Lewis WJ (1990) Exploitation of herbivore-induced plant odors by host-seeking parasitic wasps. Science 250:1251–1253CrossRefPubMedGoogle Scholar
  44. Turlings TCJ, Wackers FL (2004) Recruitment of predators and parasitoids by herbivore-injured plants. In: Cardé RT, Millar JG (eds) Advances in insect chemical ecology. Cambridge University Press, Cambridge, pp 21–75CrossRefGoogle Scholar
  45. Turlings TCJ, Wackers FL, Vet LEM, Lewis WJ, Tumlinson JH (1993) Learning of host-finding cues by hymenopterous parasitoids. In: Papaj DR, Lewis AC (eds) Insect learning: ecological and evolutionary perspectives, vol 3. Chapman & Hall, New York, pp 51–78CrossRefGoogle Scholar
  46. van Driesche R, Nunn C, Kreke N, Goldstein B, Benson J (2003) Laboratory and field host preferences of introduced Cotesia spp. parasitoids (Hymenoptera: Braconidae) between native and invasive Pieris butterflies. Biol Control 28:214–221CrossRefGoogle Scholar
  47. van Lenteren JC, Bale J, Bigler F, Hokkanen HMT, Loomans AJM (2006) Assessing risks of releasing exotic biological control agents of arthropod pests. Ann Rev Entomol 51:609–634CrossRefGoogle Scholar
  48. van Poecke RMP, Roosjen M, Pumarino L, Dicke M (2003) Attraction of the specialist parasitoid Cotesia rubecula to Arabidopsis thaliana infested by host or non-host herbivore species. Entomol Exp Appl 107:229–236CrossRefGoogle Scholar
  49. Vet LEM, Dicke M (1992) Ecology of infochemical use by natural enemies in a tritrophic context. Ann Rev Entomol 37:141–172CrossRefGoogle Scholar
  50. Vet LEM, van Lenteren JC, Heymans M, Meelis E (1983) An airflow olfactometer for measuring olfactory responses of hymenopterous parasitoids and other small insects. Physiol Entomol 8:97–106CrossRefGoogle Scholar
  51. Vet LEM, Lewis WJ, Carde RT (1995) Parasitoid foraging and learning. In: Carde RT, Bell WJ (eds) Chemical ecology of insects, vol 2. Chapman & Hall, New York, pp 65–101CrossRefGoogle Scholar
  52. Vet LEM, Wäckers FL, Dicke M (1991) How to hunt for hiding hosts: the reliability-detectability problem in foraging parasitoids. Neth J Zool 41:202–213CrossRefGoogle Scholar
  53. Vinson SB (1984) Parasitoid-host relationship. In: Bell WJ, Cardé RT (eds) Chemical ecology of insects. Chapman & Hall, London, pp 206–233Google Scholar
  54. Vinson SB (1998) The general host selection behavior of parasitoid Hymenoptera and a comparison of initial strategies utilized by larvaphagous and oophagous species. Biol Control 11:79–96CrossRefGoogle Scholar
  55. Xiaoyi W, Zhongqi Y (2008) Behavioral mechanisms of parasitic wasps for searching concealed insect hosts. Acta Ecol Sin 28:1257–1269CrossRefGoogle Scholar
  56. Yong T-H, Pitcher S, Gardner J, Hoffmann M (2007) Odor specificity testing in the assessment of efficacy and non-target risk for Trichogramma ostriniae (Hymenoptera: Trichogrammatidae). Biocontrol Sci Tech 17:135–153CrossRefGoogle Scholar
  57. Zahiri R, Kitching IJ, Lafontaine JD, Mutanen M, Kaila L, Holloway JD, Wahlberg N (2010) A new molecular phylogeny offers hope for a stable family level classification of the Noctuoidea (Lepidoptera). Zool Scr 40:158–173Google Scholar

Copyright information

© International Organization for Biological Control (IOBC) 2016

Authors and Affiliations

  • Gonzalo A. Avila
    • 1
    • 2
  • Toni M. Withers
    • 2
    • 3
  • Gregory I. Holwell
    • 1
  1. 1.School of Biological SciencesThe University of AucklandAucklandNew Zealand
  2. 2.Better Border Biosecurity, New Zealand
  3. 3.Scion (New Zealand Forest Research Institute)RotoruaNew Zealand

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