Skip to main content
Log in

Environmental risk assessment of the egg parasitoid Anaphes inexpectatus for classical biological control of the Eucalyptus snout beetle, Gonipterus platensis

  • Published:
BioControl Aims and scope Submit manuscript

Abstract

Classical biological control is a valuable tool against invasive pests, but concerns about non-target effects requires risk assessment studies. Potential non-target effects of Anaphes inexpectatus Huber and Prinsloo (Hymenoptera: Mymaridae) were assessed for a classical biological control programme against the Eucalyptus snout beetle, Gonipterus platensis (Marelli) (Coleoptera: Curculionidae). No-choice tests were conducted with 17 non-target species to assess host specificity, including 11 curculionids. In behavioural observations, A. inexpectatus showed no interest in any of the non-target species, but two weevil species were parasitised within five days of exposure, although at significantly lower rates than G. platensis. In choice tests, only one non-target, Hypera postica (Gyllenhal) (Coleoptera: Curculionidae), was parasitised, at a rate of 0.6%, while 50.0% of G. platensis eggs were parasitised. Based on the host specificity test results and the potential host fauna found in the target area, the likelihood of non-target effects resulting from the release of A. inexpectatus is considered to be negligible.

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

Access this article

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

Instant access to the full article PDF.

Similar content being viewed by others

References

  • Alonso-Zarazaga MA (2013a) Curculionidae. Fauna Europaea. v2.6.2. http://www.faunaeur.org. Cited 21 Nov 2016

  • Alonso-Zarazaga MA (2013b) New nomenclatural and taxonomic acts, and comments—Curculionidae: Entiminae: Gonipterini. In: Löbl I, Smetana A (eds) Catalogue of palaearctic coleoptera, vol 8. Curculionoidea II. Brill, Leiden, p 69

    Google Scholar 

  • Babendreier D, Bigler F, Kuhlmann U (2005) Methods used to assess non-target effects of invertebrate biological control agents of arthropod pests. BioControl 50:821–870

    Article  Google Scholar 

  • Barratt BIP (2011) Assessing safety of biological control introductions. CABI reviews. Perspect Agric Vet Sci Nutr Nat Resour 6:1–12

    Google Scholar 

  • Barratt BIP, Howarth F, Withers T, Kean J, Ridley G (2010) Progress in risk assessment for classical biological control. Biol Control 52:245–254

    Article  Google Scholar 

  • Barratt BIP, Oberprieler RG, Barton DM, Mouna M, Stevens M, Alonso-Zarazaga MA, Vink CJ, Ferguson CM (2012) Could research in the native range, and non-target host range in Australia, have helped predict host range of the parasitoid Microctonus aethiopoides Loan (Hymenoptera: Braconidae), a biological control agent introduced for Sitona discoideus Gyllenhal (Coleoptera: Curculionidae) in New Zealand? BioControl 57:735–750

    Article  Google Scholar 

  • Browne BL, Withers TM (2002) Time-dependent changes in the host-acceptance threshold of insects: implications for host specificity testing of candidate biological control agents. Biocontrol Sci Technol 12:677–693

    Article  Google Scholar 

  • Cordero-Rivera A, Santolamazza-Carbone S, Andrés JA (1999) Life cycle and biological control of the Eucalyptus snout beetle (Coleoptera, Curculionidae) by Anaphes nitens (Hymenoptera, Mymaridae) in north-west Spain. Agric For Entomol 1:103–109

    Article  Google Scholar 

  • Council of the European Communities (1992) Council Directive 92/43/EEC of 21 May 1992 on the conservation of natural habitats and of wild fauna and flora. Off J Eur Commun 35:7–50

    Google Scholar 

  • Davies AP, Takashino K, Watanabe M, Miura K (2009) Parental genetic traits in offspring from inter-specific crosses between introduced and indigenous Diadegma Foerster (Hymenoptera: Ichneumonidae): possible effects on conservation genetics. Appl Entomol Zool 44:535–541

    Article  CAS  Google Scholar 

  • De Clercq P, Mason PG, Babendreier D (2011) Benefits and risks of exotic biological control agents. BioControl 56:681–698

    Article  Google Scholar 

  • Fatouros NE, Dicke M, Mumm R, Meiners T, Hilker M (2008) Foraging behavior of egg parasitoids exploiting chemical information. Behav Ecol 19:677–689

    Article  Google Scholar 

  • Froud KJ, Stevens PS (2004) Estimating the host range of a thrips parasitoid. In: van Driesche RG, Reardon R (eds) Assessing host ranges for parasitoids and predators used for classical biological control: a guide to best practice. US Dep Agric For Health Technol Enterp Team, Morgantown, pp 90–102

    Google Scholar 

  • Gilbert LE, Morrison LW (1997) Patterns of host specificity in Pseudacteon parasitoid flies (Diptera: Phoridae) that attack Solenopsis fire ants (Hymenoptera: Formicidae). Environ Entomol 26:1149–1154

    Article  Google Scholar 

  • Gillett CP, Crampton-Platt A, Timmermans MJ, Jordal B, Emerson BC, Vogler AP (2014) Bulk de novo mitogenome assembly from pooled total DNA elucidates the phylogeny of weevils (Coleoptera: Curculionoidea). Mol Biol Evol 31:2223–2237

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gunter NL, Oberprieler RG, Cameron SL (2016) Molecular phylogenetics of Australian weevils (Coleoptera: Curculionoidea): exploring relationships in a hyperdiverse lineage through comparison of independent analyses. Austral Entomol 55:217–233

    Article  Google Scholar 

  • Hajek AE, Hurley BP, Kenis M, Garnas JR, Bush SJ, Wingfield MJ, van Lenteren JC, Cock MJ (2016) Exotic biological control agents: a solution or contribution to arthropod invasions? Biol Invasions 18:953–969

    Article  Google Scholar 

  • Haran J, Timmermans MJ, Vogler AP (2013) Mitogenome sequences stabilize the phylogenetics of weevils (Curculionoidea) and establish the monophyly of larval ectophagy. Mol Phylogenet Evol 67:156–166

    Article  PubMed  Google Scholar 

  • Haye T, Goulet H, Mason P, Kuhlmann U (2005) Does fundamental host range match ecological host range? A retrospective case study of a Lygus plant bug parasitoid. Biol Control 35:55–67

    Article  Google Scholar 

  • Hopper KR, Britch SC, Wajnberg E (2006) Risks of interbreeding between species used in biological control and native species, and methods for evaluating their occurrence and impact. In: Bigler F, Babendreier D, Kuhlmann U (eds) Environmental impact of invertebrates for biological control of arthropods: methods and risk assessment. CABI, Wallingford, pp 78–97

    Chapter  Google Scholar 

  • Huber JT (1986) Systematics, biology, and hosts of the Mymaridae and Mymarommatidae (Insecta: Hymenoptera). Entomography 4:185–243

    Google Scholar 

  • Huber JT, Prinsloo GL (1990) Redescription of Anaphes nitens (Girault) and description of two new species of Anaphes Haliday (Hymenoptera: Mymaridae), parasites of Gonipterus scutellatus Gyllenhal (Coleoptera: Curculionidae) in Tasmania. Austr J Entomol 29:333–341

    Article  Google Scholar 

  • Kenis M, Branco M (2010) Impact of alien terrestrial arthropods in Europe. BioRisk 4:51–71

    Article  Google Scholar 

  • Krugner R, Johnson MW, Groves RL, Morse JG (2008) Host specificity of Anagrus epos: a potential biological control agent of Homalodisca vitripennis. BioControl 53:439–449

    Article  Google Scholar 

  • Kuhlmann U, Schaffner U, Mason PG (2006) Selection of non-target species for host specificity testing. In: Bigler F, Babendreier D, Kuhlmann U (eds) Environmental impact of invertebrates for biological control of arthropods: methods and risk assessment. CABI, Wallingford, pp 15–37

    Chapter  Google Scholar 

  • Leschen RAB, Beutel RG (2014) Handbook of zoology, Arthropoda: Insecta. Coleoptera, Beetles. Volume 3: Morphology and systematics (Phytophaga). Walter de Gruyter, Berlin/Boston

  • Löbl I, Smetana A (2013) Catalogue of palaearctic coleoptera, vol 8. Curculionoidea II. Brill, Leiden

    Google Scholar 

  • Loch A (2008) Parasitism of the Eucalyptus weevil, Gonipterus scutellatus Gyllenhal, by the egg parasitoid, Anaphes nitens Girault, in Eucalyptus globulus plantations in southwestern Australia. Biol Control 47:1–7

    Article  Google Scholar 

  • Louda SM, Pemberton R, Johnson M, Follett P (2003) Nontarget effects—the Achilles’ heel of biological control? Retrospective analyses to reduce risk associated with biocontrol introductions. Annu Rev Entomol 48:365–396

    Article  CAS  PubMed  Google Scholar 

  • Manrique V, Jones WA, Williams LH, Bernal JS (2005) Olfactory responses of Anaphes iole (Hymenoptera: Mymaridae) to volatile signals derived from host habitats. J Insect Behav 18:89–104

    Article  Google Scholar 

  • Mapondera TS, Burgess T, Matsuki M, Oberprieler RG (2012) Identification and molecular phylogenetics of the cryptic species of the Gonipterus scutellatus complex (Coleoptera: Curculionidae: Gonipterini). Austr J Entomol 51:175–188

    Article  Google Scholar 

  • McCoy ED, Frank J (2010) How should the risk associated with the introduction of biological control agents be estimated? Agric For Entomol 12:1–8

    Article  Google Scholar 

  • McKenna DD, Sequeira AS, Marvaldi AE, Farrell BD (2009) Temporal lags and overlap in the diversification of weevils and flowering plants. Proc Natl Acad Sci 106:7083–7088

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Murray TJ, Withers TM, Mansfield S (2010) Choice versus no-choice test interpretation and the role of biology and behavior in parasitoid host specificity tests. Biol Control 52:153–159

    Article  Google Scholar 

  • Oberprieler RG (2010) A reclassification of the weevil subfamily Cyclominae (Coleoptera: Curculionidae). Zootaxa 2515:1–35

    Google Scholar 

  • Oberprieler RG, Caldara R, Skuhrovec J (2014). Bagoini Thomson, 1859; Gonipterini Lacordaire, 1863; Hyperini Marseul, 1863. In: Leschen RAB, Beutel RG (eds) Handbook of Zoology, Arthropoda: Insecta. Coleoptera, Beetles. Volume 3: Morphology and systematics (Phytophaga). Walter de Gruyter, Berlin/Boston, pp 452–476

  • Paine TD, Millar JG, Hanks LM, Gould J, Wang Q, Daane K, Dahlsten DL, Mcpherson EG (2015) Cost-benefit analysis for biological control programs that targeted insect pests of eucalypts in urban landscapes of California. J Econ Entomol 108:2497–2504

    Article  CAS  PubMed  Google Scholar 

  • Reis AR, Ferreira L, Tomé M, Araújo C, Branco M (2012) Efficiency of biological control of Gonipterus platensis (Coleoptera: Curculionidae) by Anaphes nitens (Hymenoptera: Mymaridae) in cold areas of the Iberian Peninsula: implications for defoliation and wood production in Eucalyptus globulus. For Ecol Manag 270:216–222

    Article  Google Scholar 

  • Sands DPA, van Driesche RG (2000) Evaluating the host range of agents for biological control of arthropods: rationale, methodology and interpretation. In: van Driesche RG, Heard TA, McClay AS, Reardon R (eds) Proceedings: host-specificity testing of exotic arthropod biological control agents: the biological basis for improvement in safety. USDA Forest Service, Morgantown, pp 69–83

    Google Scholar 

  • Tribe GD (2003) Biological control of defoliating, and phloem-or wood-feeding insects in commercial forestry in southern Africa. In: Neuenschwander P, Borgemeister C, Langewald J (eds) Biological control in IPM systems in Africa. CABI, Wallingford, pp 113–129

    Google Scholar 

  • Valente C, Gonçalves CI, Reis AR, Branco M (2017) Pre-selection and biological potential of the egg parasitoid Anaphes inexpectatus for the control of the Eucalyptus snout beetle, Gonipterus platensis. J Pest Sci. doi:10.1007/s10340-017-0839-y

  • van Driesche RGV, Murray TJ (2004) Overview of testing schemes and designs used to estimate host ranges. In: van Driesche RG, Reardon R (eds) Assessing host ranges for parasitoids and predators used for classical biological control: a guide to best practice. US Dep Agric For Health Technol Enterp Team, Morgantown, pp 68–89

    Google Scholar 

  • van Lenteren JC, Loomans AJM (2006) Environmental risk assessment: methods for comprehensive evaluation and quick scan. In: Bigler F, Babendreier D, Kuhlmann U (eds) Environmental impact of invertebrates for biological control of arthropods: methods and risk assessment. CABI, Wallingford, pp 254–272

    Chapter  Google Scholar 

  • van Lenteren JC, Bale J, Bigler F, Hokkanen HMT, Loomans AJM (2006a) Assessing risks of releasing exotic biological control agents of arthropod pests. Annu Rev Entomol 51:609–634

    Article  PubMed  Google Scholar 

  • van Lenteren JC, Cock MJW, Hoffmeister TS, Sands DPA (2006b) Host specificity in arthropod biological control, methods for testing and interpretation of the data. In: Bigler F, Babendreier D, Kuhlmann U (eds) Environmental impact of invertebrates for biological control of arthropods: methods and risk assessment. CABI, Wallingford, pp 38–63

    Chapter  Google Scholar 

  • Verdú JR, Numa C, Galante E (2011) Atlas y libro rojo de los invertebrados amenazados de España (especies vulnerables). Dirección General de Medio Natural y Política Forestal, Ministerio de Medio Ambiente, Medio Rural y Marino, Madrid

  • Wingfield MJ, Brockerhoff EG, Wingfield B, Slippers B (2015) Planted forest health: the need for a global strategy. Science 349:832–836

    Article  CAS  PubMed  Google Scholar 

  • Yara K, Sasawaki T, Kunimi Y (2010) Hybridization between introduced Torymus sinensis (Hymenoptera: Torymidae) and indigenous T. beneficus (late-spring strain), parasitoids of the Asian chestnut gall wasp Dryocosmus kuriphilus (Hymenoptera: Cynipidae). Biol Control 54:14–18

    Article  CAS  Google Scholar 

Download references

Acknowledgements

The authors wish to thank Rolf Oberprieler (CSIRO Ecosystem Sciences, Australia) and Brett Hurley (FABI, University of Pretoria, South Africa) for their useful suggestions on non-target species selection, and John Huber (Agriculture and Agri-Food, Canada) for kindly confirming the identity of parasitoids. We are grateful to Matthias Schöller (Humboldt University of Berlin, Germany) for providing C. rufipes eggs and to Koppert Biological Systems (The Netherlands) for providing C. carnea eggs. We would also like to thank two anonymous reviewers for valuable comments on the manuscript.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Carlos Valente.

Additional information

Handling Editor: Dirk Babendreier.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Valente, C., Afonso, C., Gonçalves, C.I. et al. Environmental risk assessment of the egg parasitoid Anaphes inexpectatus for classical biological control of the Eucalyptus snout beetle, Gonipterus platensis . BioControl 62, 457–468 (2017). https://doi.org/10.1007/s10526-017-9809-9

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10526-017-9809-9

Keywords

Navigation