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BioControl

, Volume 63, Issue 3, pp 405–416 | Cite as

A review of open-field host range testing to evaluate non-target use by herbivorous biological control candidates

  • Urs SchaffnerEmail author
  • Lincoln Smith
  • Massimo Cristofaro
Review

Abstract

One of the fundamental challenges of pre-release studies in classical biological weed control is to assess and predict the likelihood and consequences of non-target effects. Unless a candidate biological control agent is proven to be monophagous through conventional starvation and host-specificity tests in quarantine, open-field host range studies can be important in predicting the likelihood of non-target effects since they reveal the host selection of herbivores displaying the whole array of pre- and post-alightment behaviours. Over the course of its 53-year history, the purpose and the design of open-field host range studies have changed considerably, with more recent studies clarifying or refining specific questions related to one or a few test plant species and using a set design. We discuss the opportunities and challenges of this approach and suggest that future open-field host range studies should be more hypothesis-driven and apply different experimental designs that facilitate the interpretation of the results.

Keywords

Weed biological control Host specificity Risk assessment 

Notes

Acknowledgements

We would like to thank Esther Gerber, Hariet Hinz, Dick Shaw, Patrick Häfliger, Tim Heard, Hariet Hinz, Louise Morin, John Scott, Rieks van Klinken, Jim Cullen, Rose deClerck-Floate, Rob Bourchier, John Goolsby, Brian Rector, René Sforza, Al Cofrancesco and Terry Olckers for providing information on open-field host range tests and the handling editor and two anonymous reviewers for their thoughtful comments. Urs Schaffner was supported by CABI with core financial support from its member countries (see http://www.cabi.org/about-cabi/who-we-work-with/key-donors/).

Supplementary material

10526_2018_9875_MOESM1_ESM.docx (1.7 mb)
Supplementary material 1 (DOCX 1724 kb)

References

  1. Andres LA, Angalet GW (1963) Notes on the ecology and host specificity of Microlarinus lareynii and M. lyprijormis (Coleoptera: Curculionidae) and the biological control of puncture vine, Tribulus terrestris. J Econ Entomol 56:333–400CrossRefGoogle Scholar
  2. Antonini G, Coletti G, Serrani L, Tronci C, Cristofaro M, Smith L (2009) Using molecular genetics to identify immature specimens of the weevil Ceratapion basicorne (Coleoptera, Apionidae). Biol Control 51:152–157CrossRefGoogle Scholar
  3. Babendreier D, Kuske S, Bigler F (2003) Parasitism of non-target butterflies by Trichogramma brassicae Bezdenko (Hymenoptera: Trichogrammatidae) under field cage and field conditions. Biol Control 26:139–145CrossRefGoogle Scholar
  4. Blossey B, Schroeder D, Hight SD, Malecki RA (1994) Host specificity and environmental impact of two leaf beetles (Galerucella calmariensis and G. pusilla) for biological control of purple loosestrife (Lythrum salicaria). Weed Sci 42:134–140Google Scholar
  5. Briese DT (1999) Open field host-specificity tests: is “natural” good enough for risk assessment? In: Withers TM, Barton Browne L, Stanley J (eds) Host specificity testing in Australasia: towards improved assays for biological control. Scientific Publ, Indooroopilly, pp 44–59Google Scholar
  6. Briese DT, Zapater M, Andorno A, Perez-Camargo G (2002) A two-phase open-field test to evaluate the host-specificity of candidate biological control agents for Heliotropium amplexicaule. Biol Control 25:259–272CrossRefGoogle Scholar
  7. Cao Z, Wang H, Meng L, Li B (2011) Risk to nontarget plants from Ophraella communa (Coleoptera: Chrysomelidae), a potential biological control agent of alien invasive weed Ambrosia artemisiifolia (Asteraceae) in China. Appl Entomol Zool 46:375–381CrossRefGoogle Scholar
  8. Catton HA, Lalonde RG, De Clerck-Floate RA (2014) Differential host-finding abilities by a weed biocontrol insect create within-patch spatial refuges for nontarget plants. Environ Entomol 43:1333–1344CrossRefPubMedGoogle Scholar
  9. Catton HA, Lalonde RG, De Clerck-Floate RA (2015) Nontarget herbivory by a weed biocontrol insect is limited to spillover, reducing the chance of population-level impacts. Ecol Appl 25:517–530CrossRefPubMedGoogle Scholar
  10. Clement SL, Cristofaro M (1995) Open-field tests in host-specificity determination of insects for biological control of weeds. Biocontrol Sci Technol 5:395–406CrossRefGoogle Scholar
  11. Clement SL, Sobhian R (1991) Host-use patterns of capitulum-feeding insects of yellow starthistle: results from a garden plot study in Greece. Environ Entomol 20:724–730CrossRefGoogle Scholar
  12. Cock MJW, van Lenteren JC, Brodeur J, Barratt BIP, Bigler F, Bolckmans K, Cônsoli FL, Haas F, Mason PG, Parra JRP (2010) Do new access and benefit sharing procedures under the convention on biological diversity threaten the future of biological control? BioControl 55:199–218CrossRefGoogle Scholar
  13. Colpetzer K, Hough-Goldstein J, Ding J, Fu W (2004) Host specificity of the Asian weevil, Rhinoncomimus latipes Korotyaev (Coleoptera: Curculionidae), a potential biological control agent of mile-a-minute weed, Polygonum perfoliatum L. (Polygonales: Polygonaceae). Biol Control 30:511–522CrossRefGoogle Scholar
  14. Courtney SP, Chen GK, Gardner A (1989) A general model for individual host selection. Oikos 55:55–65CrossRefGoogle Scholar
  15. Cristofaro M, De Biase A, Smith L (2013) Field release of a prospective biological control agent of weeds, Ceratapion basicorne, to evaluate potential risk to a nontarget crop. Biol Control 64:305–314CrossRefGoogle Scholar
  16. Culliney TW (2005) Benefits of classical biological control for managing invasive plants. Crit Rev Plant Sci 24:131–150CrossRefGoogle Scholar
  17. Dunn PH, Campobasso G (1993) Open field tests of the weevil Hadroplonthus trimaculatus and the flea beetle Psylliodes chalcomera against musk thistle, Carduus nutans. Weed Sci 41:656–663Google Scholar
  18. Frye MJ, Lake EC, Hough-Goldstein J (2010) Field host-specificity of the mile-a-minute weevil, Rhinoncomimus latipes Korotyaev (Coleoptera: Curculionidae). Biol Control 55:234–240CrossRefGoogle Scholar
  19. Gandolfo D, McKay F, Medal JC, Cuda JP (2007) Open-field host specificity test of Gratiana boliviana (Coleoptera; Chrysomelidae), a biological control agent of Tropical Soda Apple (Solanaceae) in the United States. Fla Entomol 90:223–228CrossRefGoogle Scholar
  20. Hinz HL, Schwarzländer M, Gassmann A, Bourchier RS (2014) Successes we may not have had: a retrospective analysis of selected weed biological control agents in the United States. Invasive Plant Sci Manage 7:565–579CrossRefGoogle Scholar
  21. Horner T (2004) Permitting. In: Coombs EM, Clark JK, Piper GL, Cofrancesco AF Jr (eds) Biological control of invasive plants in the United States. Oregon State University Press, Corvallis, pp 42–46Google Scholar
  22. Lake EC, Smith MC, Dray FA, Pratt PD (2015) Ecological host-range of Lilioceris cheni (Coleoptera: Chrysomelidae), a biological control agent of Dioscorea bulbifera. Biol Control 85:18–24CrossRefGoogle Scholar
  23. Marohasy J (1998) The design and interpretation of host-specificity tests for weed biological control with particular reference to insect behaviour. Biocontrol News Inf 19:13N–20NGoogle Scholar
  24. Monfreda R, Nuzzaci G, De Lillo E (2007) Detection, extraction, and collection of eriophyoid mites. Zootaxa 1662:35–43Google Scholar
  25. Müller-Schärer H, Schaffner U (2008) Classical biological control: exploiting enemy escape to manage plant invasions. Biol Invasions 10:859–874CrossRefGoogle Scholar
  26. Olckers T, Borea CK (2009) Assessing the risks of releasing a sap-sucking lace bug, Gargaphia decoris, against the invasive tree Solanum mauritianum in New Zealand. BioControl 54:143–154CrossRefGoogle Scholar
  27. Page AR, Lacey KL (2006) Economic impact assessment of Australian weed biological control. CRC for Australian Weed Manage, AdelaideGoogle Scholar
  28. Park I-J, Eigenbrode SD, Cook S, Harmon BL, Hinz HL, Schaffner U, Schwarzländer M (2018) Examining olfactory and visual cues governing host-specificity of a weed biological control candidate species to refine pre-release risk assessment. BioControl.  https://doi.org/10.1007/s10526-018-9867-7 CrossRefGoogle Scholar
  29. Paynter QE, Fowler SV, Gourlay AH, Haines ML, Harman HM, Hona SR, Peterson PG, Smith LA, Wilson-Davey JRA, Winks CJ, Withers TM (2004) Safety in New Zealand weed biocontrol: a nationwide survey for impacts on non-target plants. NZ Plant Prot 57:102–107Google Scholar
  30. Prince JS, LeBlanc WG, Macia S (2004) Design and analysis of multiple choice feeding experiments. Oecologia 138:1–4CrossRefPubMedGoogle Scholar
  31. Rausher MD (1978) Search image for leaf shape in a butterfly. Science 200:1071–1073CrossRefPubMedGoogle Scholar
  32. Rector BG, De Biase B, Cristofaro M, Primerano S, Belvedere S, Antonini G, Sobhian R (2010) DNA fingerprinting to improve data collection efficiency and yield in an open-field host-specificity test of a weed biological control candidate. Invasive Plant Sci Manage 3:429–439CrossRefGoogle Scholar
  33. Rizza A, Campobasso G, Dunn PH, Stazi M (1988) Cheilosia corydon (Diptera: Syrphidae), a candidate for the biological control of musk thistle in North America. Ann Entomol Soc Am 81:225–232CrossRefGoogle Scholar
  34. Roitberg BD (2000) Threats, flies and protocol gaps: can evolutionary ecology save biological control? In: Hochberg ME, Ives AR (eds) Parasitoid population biology. Princeton University Press, Princeton (NJ), pp 254–265Google Scholar
  35. Schaffner U (2001) Host range testing in biological control of weeds: what can it tell us, and how can it be better interpreted? BioScience 51:1–9CrossRefGoogle Scholar
  36. Schooler SS, Coombs EM, McEvoy PB (2003) Nontarget effects on crepe myrtle by Galerucella pusilla and G. calmariensis (Chrysomelidae), used for biological control of purple loosestrife (Lythrum salicaria). Weed Sci 51:449–455CrossRefGoogle Scholar
  37. Sheppard AW, van Klinken R, Heard TA (2005) Scientific advances in the analysis of direct risks of weed biological control agents to nontarget plants. Biol Control 35:215–226CrossRefGoogle Scholar
  38. Sheppard A, Haines M, Thomann T (2006) Native-range research assists risk analysis for non-targets in weed biological control: the cautionary tale of the broom seed beetle. Austl J Entomol 45:292–297CrossRefGoogle Scholar
  39. Smith L, Hayat R, Cristofaro M, Tronci C, Tozlu G, Lecce F (2006) Assessment of risk of attack to safflower by Ceratapion basicorne (Coleoptera: Apionidae), a prospective biological control agent of Centaurea solstitialis (Asteraceae). Biol Control 36:337–344CrossRefGoogle Scholar
  40. Smith L, Cristofaro M, de Lillo E, Monfreda R, Paolini A (2009) Field assessment of host plant specificity and potential effectiveness of a prospective biological control agent, Aceria salsolae, of Russian thistle, Salsola tragus. Biol Control 48:237–243CrossRefGoogle Scholar
  41. Smith L, De Lillo E, Amrine JW (2010) Effectiveness of eriophyid mites for biological control of weedy plants and challenges for future research. Exp Appl Acarol 51:115–149CrossRefPubMedGoogle Scholar
  42. Suckling DM, Sforza RFH (2014) What magnitude are observed non-target impacts from weed biocontrol? PLoS ONE 9(1):e84847CrossRefPubMedPubMedCentralGoogle Scholar
  43. USDA (2000) Reviewer’s manual for the Technical Advisory Group for biological control agents of weeds. Guidelines for evaluating the safety of candidate biological control agents. United States Department of Agriculture, Marketing and Regulatory Programs, Animal and Plant Health Inspection Service, Plant Protection and Quarantine, 1st editionGoogle Scholar
  44. van Lenteren JC, Cock MJW (2009) IOBC Reports to FAO on access and benefit sharing. Biocontrol News Inf 30:67N–87NGoogle Scholar
  45. van Lenteren JC, Bale JS, Bigler F, Hokkanen HMT, Loomans AJM (2006) Assessing risks of releasing exotic biological control agents of arthropod pests. Annu Rev Entomol 51:609–634CrossRefPubMedGoogle Scholar
  46. van Wilgen BW, Moran VC, Hoffmann JH (2013) Some perspectives on the risks and benefits of biological control of invasive alien plants in the management of natural ecosystems. Environ Manage 52:531–540CrossRefPubMedGoogle Scholar
  47. Wapshere AJ (1974) A strategy for evaluating the safety of organisms for biological weed control. Ann Appl Biol 77:201–211CrossRefGoogle Scholar
  48. Wapshere AJ (1989) A testing sequence for reducing rejection of potential biological control agents for weeds. Ann Appl Biol 114:515–526CrossRefGoogle Scholar
  49. Watson MC, Withers TM, Hill RL (2009) Two-phase open-field test to confirm host range of a biocontrol agent Cleopus japonicas. NZ Plant Prot 62:184–190Google Scholar
  50. Winston RL, Schwarzländer M, Hinz HL, Day MD, Cock MJW, Julien MH (2014) Biological control of weeds: a world catalogue of agents and their target weeds, 5th edn. United States Department of Agriculture, Forest Service, Morgantown, FHTET-2014-04Google Scholar
  51. Zar JH (1984) Biostatistical analysis, 2nd edn. Prentice-Hall Inc, Englewood CliffsGoogle Scholar
  52. Zeilinger AR, Olson DM, Andow DA (2014) A likelihood-based biostatistical model for analyzing consumer movement in simultaneous choice experiments. Environ Entomol 43:977–988CrossRefPubMedGoogle Scholar
  53. Zhang J, Zhang F, Gariepy T, Mason P, Gillespie D, Talamas E, Haye T (2017) Seasonal parasitism and host specificity of Trissolcus japonicus in northern China. J Pest Sci 90:1127–1141CrossRefGoogle Scholar
  54. Zhou Z-S, Guo J-Y, Zheng X-W, Luo M, Chen HS, Wan F-H (2011) Re-evaluation of biosecurity of Ophraella communa against sunflower (Helianthus annuus). Biocontrol Sci Technol 21:1147–1160CrossRefGoogle Scholar
  55. Zwölfer H, Harris P (1971) Host specificity determination of insects for biological control of weeds. Annu Rev Entomol 16:159–178CrossRefGoogle Scholar

Copyright information

© International Organization for Biological Control (IOBC) 2018

Authors and Affiliations

  • Urs Schaffner
    • 1
    Email author
  • Lincoln Smith
    • 2
  • Massimo Cristofaro
    • 3
    • 4
  1. 1.CABIDelémontSwitzerland
  2. 2.USDA-ARS European Biological Control LaboratoryMontferrier-Sur-LezFrance
  3. 3.BBCA OnlusRomeItaly
  4. 4.ENEA CasacciaRomeItaly

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