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Exotic generalist arthropod biological control agents: need to improve environmental risk assessment to ensure safe use

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Abstract

Exotic generalist arthropod biological control agents (GABCAs) have been historically marginalized in classical and augmentative biological control due to their broad diet breadth, but an increasing demand for a more sustainable pest control is encouraging their reconsideration. This special issue compiles a collection of papers revealing that risks of several exotic GABCAs were overestimated, not all generalists are riskier than specialists and their environmental risk assessment (ERA) solely based on exposure analysis is inadequate. Three papers demonstrated that generalists were not involved in predicted non-target interactions: generalist idiobiont parasitoids probably do not exhibit interference competition with each other, an oligophagous exotic egg-larval koinobiont parasitoid does not compete with a native larval koinobiont, and an invasive generalist predator does not escape from its enemies. Two innovative methods for selecting non-target species are proposed, one based on existing food web data to predict indirect non-target effects, and the other on functional traits to predict competition with native natural enemies. Also a comprehensive GABCA-ERA method is proposed that integrates adverse effect analysis to the ‘conventional’ exposure analysis. The method was scrutinized by two studies: one suggesting that it could have resulted in faster and less costly decisions on two exotic generalists in New Zealand, and the other suggesting that eight exotic GABCAs released in Argentina might potentially reduce native natural enemies. We hope this special issue will stimulate the continued advance in the biosafety research of GABCAs so their safe use does not stagnate.

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References

  • 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, Evans AA, Ferguson CM, Barker GM, McNeill MR, Phillips CB (1997) Laboratory nontarget host range of the introduced parasitoids Microctonus aethiopoides and Microctonus hyperodae (Hymenoptera: Braconidae) compared with field parasitism in New Zealand. Environ Entomol 26:694–702

    Article  Google Scholar 

  • Barratt BIP, Todd JH, 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

    Article  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

    Book  Google Scholar 

  • Caltagirone LE, Doutt RL (1989) The history of the vedalia beetle importation to California and its impact on the development of biological control. Ann Rev Entomol 34:1–16

    Article  Google Scholar 

  • Cédola CV, Luna MG, Anchinelly MF, Sánchez NE (2021) Contributions to improve current environmental risk assessment procedures of generalist arthropod biological control agents (GABCAs) in Argentina. BioControl. https://doi.org/10.1007/s10526-020-10063-6

    Article  Google Scholar 

  • De Clercq P (2002) Dark clouds and their silver linings: exotic generalist predators in augmentative biological control. Neotrop Entomol 31:169–176

    Article  Google Scholar 

  • Desneux N, Blahnik R, Delebecque CJ, Heimpel GE (2012) Host phylogeny and specialisation in parasitoids. Ecol Lett 5:453–460

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • Gerard PJ, Barratt BIP (2021) Risk assessment procedures for biological control agents in New Zealand: two case studies for generalists. BioControl. https://doi.org/10.1007/s10526-020-10049-4, https://doi.org/10.1007/s10526-020-10055-6

  • Hagen KS, Mills NJ, Gordh G, McMurtry JA (1999) Terrestrial arthropod predators of insect and mite pests. In: Bellow TS, Fisher TW (eds) Handbook of biological control: principles and applications of biological control. Academic Press, San Diego, pp 383–504

  • Hokkanen HMT, Lynch JM (1995) Biological control: benefits and risks. Cambridge University Press, Cambridge

    Book  Google Scholar 

  • Howarth FG (1991) Environmental impacts of classical biological control. Annual Rev Entomol 36:485–509

    Article  Google Scholar 

  • Huffaker CB, Messenger PS (1976) Theory and practice of biological control. Academic Press, New York

    Google Scholar 

  • Huffaker CB, Messenger PS, DeBach P (1971) The natural enemy component in natural control and the theory of biological control. In: Huffaker CB (ed) Biological control. Springer, New York, pp 16–67

    Google Scholar 

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

    Google Scholar 

  • Landis DA, Fox TB, Costamagna AC (2004) Impact of multicolored Asian lady beetle as a biological control agent. Am Nat 50:153–154

    Google Scholar 

  • Le Pelley R (1955) Annual report of the senior entomologist, 1954, annual report, vol 2. Department of Agriculture Kenya, pp 1–12

  • Lockwood JA (1993) Environmental issues involved in biological control of rangeland grasshoppers (Orthoptera: Acrididae) with exotic agents. Environ Entomol 22:503–518

    Article  Google Scholar 

  • Loomans AJM (2021) Every generalist biological control agent requires a special risk assessment. BioControl. https://doi.org/10.1007/s10526-020-10022-1

    Article  Google Scholar 

  • McGrath Z, MacDonald F, Walker G, Ward D (2021) 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 18:297–321

    Google Scholar 

  • Messelink GJ, Bloemhard CMJ, Hoogerbrugge H, van Schelt J, Ingegno BL, Tavella L (2015) Evaluation of mirid predatory bugs and release strategy for aphid control in sweet pepper. J Appl Entomol 139:333–341

    Article  Google Scholar 

  • Moutia LA, Mamet R (1946) A review of twenty-five years of economic entomology in the island of Mauritius. Bull Entomol Res 36:439–472

    Article  CAS  Google Scholar 

  • Nechols JR (2021) The potential impact of climate change on non-target risks from imported generalist natural enemies and on biological control. BioControl. https://doi.org/10.1007/s10526-020-10032-z

    Article  Google Scholar 

  • Olkowski W, Zhang A (1998) Habitat management for biological control, examples from China. In: Pickett CH, Bugg RL (eds) Enhancing biological control: Habitat management to promote natural enemies of agricultural pests. University of California Press, Berkeley, pp 255–270

    Google Scholar 

  • Paranhos BAG, Poncio S, Morelli R, Nava DE, de Sá LAN, Manoukis NC (2021) Non-target effects of the exotic generalist parasitoid wasp Fopius arisanus (Sonan) estimated via competition assays against Doryctobracon areolatus (Szepligeti) on both native and exotic fruit fly hosts. BioControl. https://doi.org/10.1007/s10526-020-10057-4

    Article  Google Scholar 

  • Paula DP, Togni PHB, Costa VA, Souza LM, Sousa AATC, Tostes GM, Pires CSS, Andow DA (2021) Scrutinizing the enemy release hypothesis: population effects of parasitoids on Harmonia axyridis and local host coccinellids in Brazil. BioControl. https://doi.org/10.1007/s10526-020-10041-y

    Article  Google Scholar 

  • Paula DP, Andow DA, Barratt BIP, Pfannenstiel RS, Gerard PJ, Todd JH, Zazievo T, Luna MG, Cédola CV, Loomans AJM, Howe AG, Day MD, Ehlers C, Green C, Arpaia S, Yano E, Lövei GL, Hinomoto N, Fontes EMG, Pires CSS, Togni PHB, Nechols JR, Eubanks MD, van Lenteren JC (2021a) Integrating adverse effect analysis into environmental risk assessment for exotic generalist arthropod biological control agents: a three-tiered framework. BioControl. https://doi.org/10.1007/s10526-020-10053-8

    Article  Google Scholar 

  • Pemberton CE (1948) History of the entomology department experiment station, H.S.P.A., 1904–1945. Hawaiian Planters’ Record 52:53–90

    Google Scholar 

  • Perkins RCL (1897) The introduction of beneficial insects into the Hawaiian islands. Nature 55:499–500

    Article  Google Scholar 

  • Pilkington LJ, Messelink G, van Lenteren JC, Le Mottee K (2010) Protected biological control, biological pest management in the greenhouse industry. Biol Control 52:216–220

    Article  Google Scholar 

  • Simberloff D, Stiling P (1996a) How risky is biological control? Ecology 77:1965–1974

    Article  Google Scholar 

  • Simberloff D, Stiling P (1996b) Risks of species introduced for biological control. Biol Conserv 78:185–192

    Article  Google Scholar 

  • Simmonds FJ (1959) Biological control—past, present and future. J Econ Entomol 52:1099–1102

    Article  Google Scholar 

  • Simmonds FJ, Franz JM, Sailer RI (1976) History of biological control. In: Huffaker CB, Messenger PS (eds) Theory and practice of biological control. Academic, New York, pp 17–41

    Chapter  Google Scholar 

  • Suter GW II (2007) Ecological risk assessment, 2nd edn. CRC Press, Boca Raton

    Google Scholar 

  • Symondson WO, Sunderland KD, Greenstone MH (2002) Can generalist predators be effective biocontrol agents? Ann Rev Entomol 47:561–594.

    Article  CAS  Google Scholar 

  • Taylor THC (1935) The campaign against Aspidiotus destructor, Sign, in Fiji. Bull Entomol Res 26:1–102

    Article  Google Scholar 

  • Taylor JM, Snyder WE (2021) Are specialists really safer than generalists for classical biocontrol? BioControl. https://doi.org/10.1007/s10526-020-10037-8

    Article  Google Scholar 

  • Todd JH, Barratt BI, 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

    Article  Google Scholar 

  • Todd JH, Barratt BI, Withers TM, Berndt LA, Gresham B, Avila GA, Malone LA (2017) A comparison of methods for selecting non-target species for risk assessment of the biological control agent Cotesia urabae. BioControl 62:39–52

    Article  Google Scholar 

  • Todd JH, Pearce BM, Barratt BIP (2021) Using qualitative food webs to predict species at risk of indirect effects from a proposed biological control agent. BioControl. https://doi.org/10.1007/s10526-020-10038-7

    Article  Google Scholar 

  • US Environmental Protection Agency (US EPA) (1998) Guidelines for ecological risk assessment. EPA/630/R-95/002F. US Environmental Protection Agency, Washington, DC.

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

    Article  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

    Article  Google Scholar 

  • Vesey-Fitzgerald D (1953) Review of the biological control of coccids on coconut palms in the Seychelles. Bull Entomol Res 44:405–413

    Article  Google Scholar 

  • Wang X-G, Wang X-Y, Kenis M, Cao L-M, Duan JJ, Gould JR, Hoelmer KA (2021) Exploring the potential for novel associations of generalist parasitoids for biological control of invasive woodboring beetles. BioControl. https://doi.org/10.1007/s10526-020-10039-6

    Article  Google Scholar 

  • Withers TM, Todd JH, Gresham BA, Barratt BI (2018) Comparing traditional methods of test species selection with the PRONTI tool for host-range testing of Eadya daenerys (Braconidae). N Z Plant Protect 71:221–231

    Google Scholar 

  • Wyckhuys KA, Koch RL, Heimpel GE (2007) Physical and ant-mediated refuges from parasitism: implications for non-target effects in biological control. Biol Control 40:306–313

    Article  Google Scholar 

Download references

Acknowledgements

We thank the many biological control experts who contributed to the works in this Special Issue. This work was funded in part by Embrapa grant number SEG 12.13.12.005.00.00, United States Department of Agriculture National Institute of Food and Agriculture Grant Number 2019-67013-29406, and the New Zealand Better Border Biosecurity Research Collaboration.

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DAA wrote first draft, BIPB, RSP and DPP revised and approved the submitted version.

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Correspondence to David A. Andow.

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Andow, D.A., Barratt, B.I.P., Pfannenstiel, R.S. et al. Exotic generalist arthropod biological control agents: need to improve environmental risk assessment to ensure safe use. BioControl 66, 1–8 (2021). https://doi.org/10.1007/s10526-020-10067-2

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