Skip to main content
SpringerLink
Log in

Integrating adverse effect analysis into environmental risk assessment for exotic generalist arthropod biological control agents: a three-tiered framework

  • Review
  • Published:
BioControl Aims and scope Submit manuscript

A Publisher Correction to this article was published on 18 January 2021

This article has been updated

Abstract

Environmental risk assessments (ERAs) are required before utilizing exotic arthropods for biological control (BC). Present ERAs focus on exposure analysis (host/prey range) and have resulted in approval of many specialist exotic biological control agents (BCA). In comparison to specialists, generalist arthropod BCAs (GABCAs) have been considered inherently risky and less used in classical biological control. To safely consider exotic GABCAs, an ERA must include methods for the analysis of potential effects. A panel of 47 experts from 14 countries discussed, in six online forums over 12 months, scientific criteria for an ERA for exotic GABCAs. Using four case studies, a three-tiered ERA comprising Scoping, Screening and Definitive Assessments was developed. The ERA is primarily based on expert consultation, with decision processes in each tier that lead to the approval of the petition or the subsequent tier. In the Scoping Assessment, likelihood of establishment (for augmentative BC), and potential effect(s) are qualitatively assessed. If risks are identified, the Screening Assessment is conducted, in which 19 categories of effects (adverse and beneficial) are quantified. If a risk exceeds the proposed risk threshold in any of these categories, the analysis moves to the Definitive Assessment to identify potential non-target species in the respective category(ies). When at least one potential non-target species is at significant risk, long-term and indirect ecosystem risks must be quantified with actual data or the petition for release can be dismissed or withdrawn. The proposed ERA should contribute to the development of safe pathways for the use of low risk GABCAs.

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
Fig. 4
Fig. 5

Similar content being viewed by others

Change history

  • 18 January 2021

    Due to typesetting errors, Table 5 was not displayed correctly in the initial online publication. The original online article has been corrected.

References

  • Andow DA, Lane CP, Olson DM (1995) Use of Trichogramma in maize-estimating environmental risks. In: Lynch JM, Hokkanen HH (eds) Benefits and risks of introducing biocontrol agents. Blackwell, London, pp 101–118

    Google Scholar 

  • Andreassen LD, Kuhlmann U, Mason PG, Holliday NJ (2009) Host range testing of a prospective classical biological control agent against cabbage maggot, Delia radicum, in Canada. Biol Control 48:210–220

    Google Scholar 

  • Arthurs S, McKenzie CL, Chen J, Doğramaci M, Brennan M, Houben K, Osborne L (2009) Evaluation of Neoseiulus cucumeris and Amblyseius swirskii (Acari: Phytoseiidae) as biological control agents of chilli thrips, Scirtothrips dorsalis (Thysanoptera: Thripidae) on pepper. Biol Control 49:91–96

    Google Scholar 

  • Barlow ND, Barratt BIP, Ferguson CM, Barron MC (2004) Using models to estimate parasitoid impacts on non-target host abundance. Environ Entomol 33:941–948

    Google Scholar 

  • Barratt BIP, Todd J, Malone LA (2016) Selecting non-target species for arthropod biological control agent host range testing: evaluation of a novel method. Biol Control 93:84–92

    Google Scholar 

  • Bigler F, Babendreier D, Kuhlmann U (2006) Environmental impact of invertebrates for biological control of arthropods: methods and risk assessment. CAB International, Wallingford

    Google Scholar 

  • Carmichael AC, Wharton RA, Clarke AR (2005) Opiine (Hymenoptera: Braconidae) parasitoids of tropical fruit flies (Diptera: Tephritidae) of the Australian and South Pacific region. Bull Entomol Res 95:545–569

    CAS  PubMed  Google Scholar 

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

    Google Scholar 

  • Cédola C, Polack A (2011) First record of Amblyseius swirskii (Acari: Phytoseiidae) from Argentina. Rev Soc Entomol Arg 70:375–378

    Google Scholar 

  • Cock MJW, Murphy ST, Kairo MTK, Thompson E, Murphy RJ, Francis AW (2016) Trends in the classical biological control of insect pests by insects: an update of the BIOCAT database. BioControl 61:349–363

    CAS  Google Scholar 

  • EPA (New Zealand) (2013) Application to import for release or to release from containment new organisms, Macrolophus pygmaeus, application APP201254, 2013 November 20. https://www.epa.govt.nz/assets/FileAPI/hsno-ar/APP201254/APP201254-EPA-BCA-application-Macrolophus-2013-FINAL.pdf. Accessed 6 Feb 2019

  • EPA (New Zealand) (2014) EPA decision for application APP201254, 2014 April 17. https://www.epa.govt.nz/assets/FileAPI/hsno-ar/APP201254/APP201254-APP201254-Decision-FINAL-2014-04-17.pdf. Accessed 6 Feb 2019

  • EPPO (European and Mediterranean Plant Protection Organization) (2018) PM 6/04 (1) decision-support scheme for import and release of biological control agents of plant pests. EPPO Bull 48:352–367

    Google Scholar 

  • EPPO (2020) PM 6/3(4) List of biological control agents widely used in the EPPO region—2020 version. https://www.eppo.int/media/uploaded_images/RESOURCES/eppo_standards/pm6/pm6-03-2020-en.pdf. Accessed 12 Sept 2020

  • Harris HJ, Wegner RB, Harris VA, Devault DS (1994) A method for assessing environmental risk: a case study of Green Bay, Lake Michigan, USA. Environ Manag 18:295–306

    Google Scholar 

  • Holler TC, Gerónimo F, Sivinski J, Gonzalez JC, Stewart J (1996) Mediterranean fruit fly parasitoid aerial release test in Guatemala. In: 2º WGFFWH meeting, Viña del Mar, Chile, pp 74–75

  • Hopper KR (2001) Research needs concerning non-target impacts of biological control introductions. In: Wajnberg E, Scott JK, Quimby PC (eds) Evaluating indirect ecological effects of biological control. CAB International, Wallingford, pp 39–56

    Google Scholar 

  • Kade N, Gueye-Ndiaye A, Duverney C, Moraes GJ (2011) Phytoseiid mites (Acari: Phytoseiidae) from Senegal. Acarologia 51:133–138

    Google Scholar 

  • Kuhlmann U, Schaffner U, Mason PG (2006) Selection of non-target species for host specificity testing of entomophagous biological control agents. In: Second international symposium on biological control of arthropods, Davos, Switzerland, pp 12–16

  • Kynn M (2008) The ‘heuristics and biases’ bias in expert elicitation. J R Stat Soc A 171:239–264

    Google Scholar 

  • Le Hesran S, Ras E, Wajnberg E, Beukeboom L (2019) Next generation biological control—an introduction. Entomol Exp Appl 167:579–583

    Google Scholar 

  • Lynch LD, Hokkanen HMT, Babendreier D, Bigler F, Burgio G, Gao ZH, Kuske S, Loomans A, Menzler-Hokkanen I, Thomas MB, Tommasini G, Waage JK, van Lenteren JC, Zeng QQ (2001) Insect biological control and non-target effects: a European perspective. In: Wajnberg E, Scott JK, Quimby PC (eds) Evaluating indirect ecological effects of biological control. CAB International, Wallingford, pp 99–125

    Google Scholar 

  • McGrath Z, MacDonald F, Walker G, Ward D (2020) A framework for predicting competition between native and exotic hymenopteran parasitoids of lepidopteran larvae using taxonomic collections and species level traits. BioControl. https://doi.org/10.1007/s10526-020-10025-y

    Article  Google Scholar 

  • McMurtry JA, De Moraes GJ, Sourassou NF (2013) Revision of the lifestyles of phytoseiid mites (Acari: Phytoseiidae) and implications for biological control strategies. Syst Appl Acarol 18:297–320

    Google Scholar 

  • Messing R, Roitberg B, Brodeur J (2006) Measuring and predicting indirect impacts of biological control: competition, displacement and secondary interactions. In: Bigler F, Babendreier D, Kuhlmann U (eds) Environmental impact of invertebrates for biological control of arthropods: methods and risk assessment. CAB International, Wallingford, pp 64–77

    Google Scholar 

  • Mitchell R, Agle B, Wood D (1997) Toward a theory of stakeholder identification and salience: defining the principle of who and what really counts. Acad Manag Rev 22:853–886

    Google Scholar 

  • Morgan MG (2014) Use (and abuse) of expert elicitation in support of decision making for public policy. PNAS 111:7176–7184

    CAS  PubMed  Google Scholar 

  • NAPPO (2015) RSPM 12 Guidelines for petition for first release of non-indigenous entomophagous biological control agents. The Secretariat of the North American Plant Protection Organization, Ottawa, p 14

    Google Scholar 

  • Nechols JR, Kauffman WC, Schaefer PW (1992) Significance of host specificity in classical biological control. In: Kauffman WC, Nechols JR (eds) Selection criteria and ecological consequences of importing natural enemies. Thomas Say Publications in Entomology, Entomological Society of America, Lanham, pp 41–52

    Google Scholar 

  • O'Hagan A (2005) Research in elicitation. Department of Probability and Statistics, School of Mathematics, University of Sheffield, Sheffield

    Google Scholar 

  • Olckers T (2003) Assessing the risks associated with the release of a flowerbud weevil, Anthonomus santacruzi, against the invasive tree Solanum mauritianum in South Africa. Biol Control 28:302–312

    Google Scholar 

  • Ovruski S, Aluja M, Sivinski J, Wharton R (2000) Hymenopteran parasitoids on fruit-infesting Tephritidae (Diptera) in Latin America and the southern United States: diversity, distribution, taxonomic status and their use in fruit fly biological control. J Integr Pest Manag 5:81–107

    Google Scholar 

  • Paula DP, Linard B, Platt AC, Srivathsan A, Timmermans MJTN, Sujii ER, Pires CSS, Souza LM, Andow DA, Vogler AP (2016) Uncovering trophic interactions in arthropod predators through DNA shotgun-sequencing of gut contents. PLoS ONE 11(9):e0161841

    PubMed  PubMed Central  Google Scholar 

  • Pedrycz W, Gomide F (2007) Fuzzy systems engineering: toward human-centric computing. Wiley, New York

    Google Scholar 

  • Petit JN, Hoddle MS, Grandgirard J, Roderick GK, Davies N (2009) Successful spread of a biocontrol agent reveals a biosecurity failure: elucidating long distance invasion pathways for Gonatocerus ashmeadi in French Polynesia. BioControl 54:485–495

    Google Scholar 

  • Puccia CJ, Levins R (2013) Qualitative modeling of complex systems: an introduction to loop analysis and time averaging. Harvard University Press, Cambridge

    Google Scholar 

  • Rahman MM (2016) Multiplication and division of triangular fuzzy numbers. DIU J Sci Technol 11(2):49–53

    Google Scholar 

  • Rousse P, Harris EJ, Quilici S (2005) Fopius arisanus, an egg-pupal parasitoid of Tephritidae—an overview. Biocontrol News Info 26:59–69

    Google Scholar 

  • Roy HE, Brown PM, Adriaens T, Berkvens N, Borges I, Clusella-Trullas S, Comont RF, De Clercq P, Eschen R, Estoup A, Evans EW, Facon B, Gardiner MM, Gil A, Grez AA, Guillemaud T, Haelewaters D, Herz A, Honek A, Howe AG, Hui C, Hutchison WD, Kenis M, Koch RL, Kulfan J, Handley LL, Lombaert E, Loomans A, Losey J, Lukashuk AO, Maes D, Magro A, Murray KM, Martin GS, Martinkova Z, Minnaar IA, Nedved O, Orlova-Bienkowskaja MJ, Osawa N, Rabitsch W, Ravn HP, Rondoni G, Rorke SL, Ryndevich SK, Saethre M-G, Sloggett JJ, Soares AO, Stals R, Tinsley MC, Vandereycken A, van Wielink P, Viglášová S, Zach P, Zakharov IA, Zaviezo T, Zhao Z (2016) The harlequin ladybird, Harmonia axyridis: global perspectives on invasion history and ecology. Biol Invasions 18:997–1044

    Google Scholar 

  • Sackman H (1974) Delphi assessment: expert opinion, forecasting, and group process (no. RAND-R-1283-PR). Rand Corp, Santa Monica

    Google Scholar 

  • Sands DPA, van Driesche RG (2004) Using the scientific literature to estimate the host range of a biological control agent. In: van Driesche RG, Sands DPA (eds) Assessing host ranges of parasitoids and predators used for classical biological control: a guide to best practice. Forest Health Technology Enterprise Team, Forest Service, USDA, Morgantown, pp 15–23

    Google Scholar 

  • Sato Y, Mochizuki A (2011) Risk assessment of non-target effects caused by releasing two exotic phytoseiid mites in Japan: can an indigenous phytoseiid mite become IG prey? Exp Appl Acarol 54:319–329

    PubMed  Google Scholar 

  • Snyder WE, Evans EW (2006) Ecological effects of invasive arthropod generalist predators. Annu Rev Ecol Evol Syst 37:95–122

    Google Scholar 

  • Stahl J, Tortorici F, Pontini M, Bon M-C, Hoelmer K, Marazzi C, Tavella L, Haye T (2019) First discovery of adventive populations of Trissolcus japonicus in Europe. J Pest Sci 92:371–379

    Google Scholar 

  • Todd JH, Barratt BIP, Tooman L, Beggs JR, Malone LA (2015) Selecting non-target species for risk assessment of entomophagous biological control agents: evaluation of the PRONTI decision-support tool. Biol Control 80:77–88

    Google Scholar 

  • van Lenteren JC, Babendreier D, Bigler F, Burgio G, Hokkanen HMT, Kuske S, Loomans AJM, Menzler-Hokkanen I, van Rijn PCJ, Thomas MB, Tommasini MG, Zeng QQ (2003) Environmental risk assessment of exotic natural enemies used in inundative biological control. BioControl 48:3–38

    Google Scholar 

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

    PubMed  Google Scholar 

  • van Lenteren JC (2012) The state of commercial augmentative biological control: plenty of natural enemies, but a frustrating lack of uptake. BioControl 57:1–20

    Google Scholar 

  • van Lenteren JC, Bolckmans K, Köhl J, Ravensberg WJ, Urbaneja A (2018) Biological control using invertebrates and microorganisms: plenty of new opportunities. BioControl 63:39–59

    Google Scholar 

  • van Lenteren JC, Bueno VH, Colmenarez YC, Luna MG (2020) Biological control in Latin America and the Caribbean: its rich history and bright future. CAB International, Wallingford, p 522

    Google Scholar 

  • Vanderhoeven S, Branquart E, Casaer J, Dhondt B, Hulme PE, Shwartz A, Strubbe D, Turbé A, Verreycken H, Adriaens T (2017) Beyond protocols: improving the reliability of expert-based risk analysis underpinning invasive species policies. Biol Invasions 19:2507–2517

    Google Scholar 

  • Vargas RI, Stark JD, Uchida GK, Purcell M (1993) Opiine parasitoids (Hymenoptera: Braconidae) of Oriental fruit fly (Diptera: Tephritidae) on Kauai Island, Hawaii: Islandwide relative abundance and parasitism rates in wild and orchard guava habitats. Environ Entomol 22:246–253

    Google Scholar 

  • Vargas RI, Leblanc L, Putoa R, Eitam A (2007) Impact of introduction of Bactrocera dorsalis (Diptera: Tephritidae) and classical biological control releases of Fopius arisanus (Hymenoptera: Braconidae) on economically important fruit flies in French Polynesia. J Econ Entomol 100:670–679

    PubMed  Google Scholar 

  • Wang XG, Bokonon-Ganta AH, Ramadan MM, Messing RH (2004) Egg-larval opiine parasitoids (Hym., Braconidae) of tephritid fruit fly pests do not attack the flowerhead-feeder Trupanea dubautiae (Dipt., Tephritidae). J Appl Entomol 12:716–722

    Google Scholar 

  • Waterhouse DF (1993) Pest fruit flies in the Oceanic Pacific. In: Waterhouse DF (ed) Biological control: Pacific prospects—supplement 2. Australian Centre for International Agricultural Research, Canberra, pp 4–47

    Google Scholar 

  • Wyckhuys KA, Lu Y, Morales H, Vazquez LL, Legaspi JC, Eliopoulos PA, Hernandez LM (2013) Current status and potential of conservation biological control for agriculture in the developing world. Biol Control 65:152–167

    Google Scholar 

Download references

Acknowledgements

We are grateful for all the experts and stakeholders worldwide who contributed to this work. We thank Embrapa (grant number SEG 12.13.12.005.00.00), USDA (NIFA grant 2019-67013-29406) and the New Zealand Better Border Biosecurity Research Collaboration for their financial support.

Author information

Author notes

  1. Débora. P. Paula and David A. Andow contributed equally to the study.

Authors and Affiliations

  1. Department of Biological Control, Embrapa Genetic Resources and Biotechnology, Brasília, DF, 70770-901, Brazil

    Débora P. Paula, Eliana M. G. Fontes & Carmen S. S. Pires

  2. Department of Entomology, University of Minnesota, 219 Hodson Hall, St. Paul, MN, 55108, USA

    David A. Andow

  3. AgResearch, Invermay Research Centre, PB 50034, Mosgiel, New Zealand

    Barbara I. P. Barratt

  4. Better Border Biosecurity, Wellington, New Zealand

    Barbara I. P. Barratt & Jacqui H. Todd

  5. Pests, Pathogens and Biocontrol Permitting, Plant Health Programs, USDA APHIS PPQ, 4700 River Road, Unit 133, Riverdale, MD, 20737, USA

    Robert S. Pfannenstiel

  6. AgResearch, Ruakura Research Centre, PB, 3123, Hamilton, New Zealand

    Philippa J. Gerard

  7. The New Zealand Institute for Plant and Food Research Limited, Private Bag 92169, Auckland, 1142, New Zealand

    Jacqui H. Todd

  8. Facultad Agronomía e Ing. Forestal, Pontificia Universidad Católica de Chile, Santiago, Chile

    Tania Zaviezo

  9. CEPAVE (CONICET - UNLP), Boulevard 120 entre 60 y 64, 1900, La Plata, Argentina

    Maria G. Luna & Claudia V. Cédola

  10. National Plant Protection Organization (NPPO), Netherlands Food and Consumer Product Safety Authority (NVWA), Geertjesweg 15, 6706 EA, Wageningen, The Netherlands

    Antoon J. M. Loomans

  11. Department of Geosciences and Natural Resource Management, University of Copenhagen, Rolighedsvej 23, 1958, Frederiksberg C, Denmark

    Andy G. Howe

  12. Forest Industries Research Centre, University of the Sunshine Coast, GPO Box 267, Brisbane, QLD, 4001, Australia

    Andy G. Howe

  13. Department of Agriculture and Fisheries, GPO Box 267, Brisbane, QLD, 4001, Australia

    Michael D. Day

  14. Environmental Protection Authority, Level 10, 215 Lambton Quay, Wellington, 6011, New Zealand

    Clark Ehlers

  15. Department of Conservation, Private Bag 68908, Newton, Auckland, 1145, New Zealand

    Chris Green

  16. Division Bioenergy, Biorefinery and Green Chemistry, ENEA Research Centre Trisaia, S.S. 106 Jonica km 419.5, 75026, Rotondella, MT, Italy

    Salvatore Arpaia

  17. Center for Ecological Research (CER), Kyoto University, Hirano 2-509-3, Otsu, Shiga, 520-2113, Japan

    Eizi Yano

  18. Department of Agroecology, Aarhus University, Flakkebjerg Research Centre, Forsøgsvej 1, 4200, Slagelse, Denmark

    Gabor L. Lövei

  19. Laboratory of Ecological Information, Graduate School of Agriculture, Kyoto University, Kyoto, 606-8502, Japan

    Norihide Hinomoto

  20. Departamento de Ecologia, Universidade de Brasília (UnB), Campus Universitário Darcy Ribeiro, Brasília, DF, 70910-900, Brazil

    Pedro H. B. Togni

  21. Department of Entomology, Kansas State University, 123 Waters Hall, 1603 Old Claflin Place, Manhattan, KS, 66506, USA

    James R. Nechols

  22. Department of Entomology, Texas A&M University, TAMU 2475, College Station, TX, 77843-2475, USA

    Micky D. Eubanks

  23. Laboratory of Entomology, Department of Plant Sciences, Wageningen University and Research (WUR), PO Box 16, 6700 AA, Wageningen, The Netherlands

    Joop C. van Lenteren

Authors
  1. Débora P. Paula
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. David A. Andow
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Barbara I. P. Barratt
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Robert S. Pfannenstiel
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Philippa J. Gerard
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Jacqui H. Todd
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Tania Zaviezo
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Maria G. Luna
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Claudia V. Cédola
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. Antoon J. M. Loomans
    View author publications

    You can also search for this author in PubMed Google Scholar

  11. Andy G. Howe
    View author publications

    You can also search for this author in PubMed Google Scholar

  12. Michael D. Day
    View author publications

    You can also search for this author in PubMed Google Scholar

  13. Clark Ehlers
    View author publications

    You can also search for this author in PubMed Google Scholar

  14. Chris Green
    View author publications

    You can also search for this author in PubMed Google Scholar

  15. Salvatore Arpaia
    View author publications

    You can also search for this author in PubMed Google Scholar

  16. Eizi Yano
    View author publications

    You can also search for this author in PubMed Google Scholar

  17. Gabor L. Lövei
    View author publications

    You can also search for this author in PubMed Google Scholar

  18. Norihide Hinomoto
    View author publications

    You can also search for this author in PubMed Google Scholar

  19. Eliana M. G. Fontes
    View author publications

    You can also search for this author in PubMed Google Scholar

  20. Carmen S. S. Pires
    View author publications

    You can also search for this author in PubMed Google Scholar

  21. Pedro H. B. Togni
    View author publications

    You can also search for this author in PubMed Google Scholar

  22. James R. Nechols
    View author publications

    You can also search for this author in PubMed Google Scholar

  23. Micky D. Eubanks
    View author publications

    You can also search for this author in PubMed Google Scholar

  24. Joop C. van Lenteren
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Débora P. Paula.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Additional information

Handling Editor: Eric Wajnberg

The original online version of this article has been revised: Table 5 has been corrected.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary file1 (DOCX 202 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Paula, D.P., Andow, D.A., Barratt, B.I.P. et al. Integrating adverse effect analysis into environmental risk assessment for exotic generalist arthropod biological control agents: a three-tiered framework. BioControl 66, 113–139 (2021). https://doi.org/10.1007/s10526-020-10053-8

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10526-020-10053-8

Keywords

Search

Navigation