Abstract
Criticisms about the safety of biological control of alien plants has resulted in a risk-averse approach, where the risks posed by the agent are paramount and the risks posed by the alien plant are neglected. We argue that the risk associated with non-target damage from agents needs to be assessed relative to that of their target alien plants. A literature review of the non-target risks associated with biological control agents was undertaken in terms of the risk to native species from agents relative to the risk to native species from their alien plant targets. We then developed a framework that compares the consequence with the likelihood of non-target damage for both agents and their targets to provide an overall risk rating. Assessments of the risk of damage from both agents and their target alien plants will enable researchers, managers and policy makers to better assess the risks from biological control.
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References
Adair RJ, Groves RH (1998) Impact of environmental weeds on biodiversity: a review and development of a methodology. Environment Australia, Canberra
Anon (2006) National post-border weed risk management protocol. HB 294. Standards Australia, Standards New Zealand, and Cooperative Research Centre for Australian Weed Management, Sydney
Baker JL, Webber NAP (2008) Feeding impacts of a leafy spurge (Euphorbia esula) biological control agent on a native plant, Euphorbia robusta. Invasive Plant Sci Manag 1:26–30
Barratt BIP, Moeed A (2005) Environmental safety of biological control: policy and practice in New Zealand. Biol Control 35:247–252
Barton J, Fowler SV, Gianotti AF, Winks CJ, de Beurs M, Arnold GC, Forrester G (2007) Successful biological control of mist flower (Ageratina riparia) in New Zealand: agent establishment, impact and benefits to the native flora. Biol Control 40:370–385
Belcher JW, Wilson SD (1989) Leafy spurge and the species composition of a mixed-grass prairie. J Range Manag 42:172–175
Benke KK, Steel JL, Weiss JE (2011) Risk assessment models for invasive species: uncertainty in rankings from multi-criteria analysis. Biol Invasions 13:239–253
Blossey B (1999) Before, during and after: the need for long-term monitoring in invasive plant species management. Biol Invasions 1:301–311
Blossey B, Skinner LC, Taylor J (2001a) Impact and management of purple loosestrife (Lythrum salicaria) in North America. Biodivers Conserv 10:1787–1807
Blossey B, Casagrande R, Tewksbury L, Landis DA, Wiedenmann RN, Ellis DR (2001b) Nontarget feeding of leaf-beetles introduced to control purple loosestrife (Lythrum salicaria L.). Nat Area J 21:368–377
Braithwaite RW, Lonsdale WM, Estbergs JA (1989) Alien vegetation and native biota in tropical Australia: the impact of Mimosa pigra. Biol Conserv 48:189–210
Brand LA, Stromberg JC, Noon BR (2010) Avian density and nest survival on the San Pedro River: importance of vegetation type and hydrologic regime. J Wildl Manag 74:739–754
Briese DT (2003) The centrifugal phylogenetic method used to select plants for host-specificity testing of weed biological control agents: can and should it be modernised? Improving the selection, testing and evaluation of weed biological control agents. In: Spafford Jacob H, Briese DT (Eds) Improving the selection, testing and evaluation of weed biological control agents, Technical Series 7, CRC for Australian Weed Management, Adelaide, pp. 23–33
Briese DT (2005) Translating host-specificity test results into the real world: the need to harmonize the yin and yang of current testing procedures. Biol Control 35(3):208–214
Bull JW, Gordon A, Law EA, Suttle KB, Milner-Gulland EJ (2014) Importance of baseline specification in evaluating conservation interventions and achieving no net loss of biodiversity. Conserv Biol 28:799–809
Butler JL, Cogan DR (2004) Leafy spurge effects on patterns of plant species richness. Rangel Ecol Manag 57:305–311
Carvalheiro LG, Buckley YM, Ventim R, Fowler SV, Memmott J (2008) Apparent competition can compromise the safety of highly specific biocontrol agents. Ecol Lett 11:690–700
Cook D, Proctor W (2007) Assessing the threat of exotic plant pests. Ecol Econ 63:594–604
Coutts-Smith AJ, Downey PO (2006) The impact of weeds on threatened biodiversity in New South Wales. Technical Series no. 11. CRC for Australian Weed Management, Adelaide
Dávalos A, Blossey B (2010) The effects of flooding, plant traits, and predation on purple loosestrife leaf-beetles. Entomol Exp Appl 135:85–95
Davis DR, Kassulke RC, Harley KLS, Gillett JD (1991) Systematics, morphology, biology, and host specificity of Neurostrota gunniella (Busck) (Lepidoptera: Gracillariidae), an agent for the biological control of Mimosa pigra L. Proc Entomol Soc Wash 93:16–44
Delfosse ES (2005) Risk and ethics in biological control. Biol Control 35:319–329
Denslow JS, D’Antonio CM (2005) After biocontrol: assessing indirect effects of insect releases. Biol Control 35:307–318
Downey PO, Johnson SB, Virtue JG, Williams PA (2010a) Assessing risk across the spectrum of weed management. CAB Rev 5:38
Downey PO, Williams MC, Whiffen LK, Auld BA, Hamilton MA, Burley AL, Turner PJ (2010b) Managing alien plants for biodiversity outcomes—the need for triage. Invasive Plant Sci Manag 3:1–11
Dudley TL, Deloach CJ (2004) Saltcedar (Tamarix spp.), endangered species, and biological weed control: can they mix? Weed Technol 18:1542–1551
Dudley TL, Kazmer DJ (2005) Field assessment of the risk posed by Diorhabda elongata, a biocontrol agent for control of saltcedar (Tamarix spp.), to a nontarget plant, Frankenia salina. Biol Control 35:265–275
Ferraro PJ, Pattanayak SK (2006) Money for nothing? A call for empirical evaluation of biodiversity conservation investments. PLoS Biol 4(4):e105
Fowler SV, Syrett P, Hill RL (2000) Success and safety in the biological control of environmental weeds in New Zealand. Aust Ecol 25:553–562
Fowler SV, Paynter Q, Hayes L, Dodd S, Groenteman R (2010) Biocontrol of weeds in New Zealand: an overview of nearly 85 years. In: Zydenbos SM (ed) 17th Australasian Weeds Conference. New Zealand Plant Protection Society, Christchurch, pp 211–214
Fowler SV, Paynter Q, Dodd S, Groenteman R (2012) How can ecologists help practitioners minimize non-target effects in weed biocontrol? J Appl Ecol 49:307–310
Freeland WJ (1986) Populations of cane toad, Bufo marinus, in relation to time since colonization. Aust Wildl Res 13:321–329
Funasaki GY, Lai PY, Nakahara LM, Beardsley JW, Ota AK (1988) A review of biological control introductions in Hawaii: 1980 to 1985. Proc Hawaii Entomol Soc 28:105–160
Harris P (1988) Environmental impact of weed-control insects. BioScience 38:542–548
Hill RL, Wittenberg R, Gourlay AH (2001) Biology and host range of Phytomyza vitalbae and its establishment for the biological control of Clematis vitalba in New Zealand. Biocontrol Sci Technol 11:459–473
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 Manag 7:565–579
Hirose Y (1999) Evaluation of environmental impacts of introduced natural enemies. In: Yano E, Matsuo K, Shiyomi M, Andow DA (Eds) Biological invasions of ecosystem by pest and beneficial organisms, National Institute of Agro-Environmental Sciences, Ministry of Agriculture, Forestry, and Fisheries, Tsukuba, pp. 224–232
Howarth FG (1991) Environmental impacts of classical biological control. Ann Rev Entomol 36:485–509
Huffaker CB (1957) Fundamentals of biological control of weeds. Hilgardia 27:101–107
IUCN (2015) The IUCN red list of threatened species, Version 2015.2, IUCN, http://www.iucnredlist.org 14 July 2015
Jarvis PJ, Fowler SV, Paynter Q, Syrett P (2006) Predicting the economic benefits and costs of introducing new biological control agents for Scotch broom Cytisus scoparius into New Zealand. Biol Control 39:135–146
Jetter K (2005) Economic framework for decision making in biological control. Biol Control 35:348–357
Kennedy TA, Finlay JC, Hobbie SE (2005) Eradication of invasive Tamarix ramosissima along a desert stream increases native fish density. Ecol Appl 15:2072–2083
Klein H, Hill MP, Zachariades C, Zimmermann HG (2011) Regulation and risk assessment for importations and releases of biological control agents against invasive alien plants in South Africa. Afr Entomol 19:488–497
Kok LT, McAvoy TJ, Maleckij RA, Hight SD, Drea JJ, Coulson JR (1992) Host specificity tests of Galerucella calmariensis (L.) and G. pusilla (Duft.) (Coleoptera: Chrysomelidae), potential biological control agents of purple loosestrife, Lythrum salicaria L. (Lythraceae). Biol Control 2:282–290
Linkov I, Satterstrom FK, Kiker G, Batchelor C, Bridges T, Ferguson E (2006) From comparative risk assessment to multi-criteria decision analysis and adaptive management: recent developments and applications. Environ Int 32:1072–1093
Lonsdale WM, Briese DT, Cullen JM (2001) Risk analysis and weed biological control. In: Wajnberg E, Scott JK, Quimby PC (eds) Evaluating indirect ecological effects of biological control. CABI Publishing, Wallingford, pp 185–210
Loope L, Starr F, Starr K (2004) Protecting endangered plant species from displacement by invasive plants in Maui, Hawaii. Weed Technol 18:1472–1474
Louda SM, Pemberton RW, Johnson MT, Follett PA (2003) Nontarget effects—the Achilles’ heel of biological control? Retrospective analyses to reduce risk associated with biocontrol introductions. Ann Rev Entomol 48:365–396
Martin N, Paynter Q (2010) Assessing the biosecurity risk from pathogens and herbivores to indigenous plants: lessons from weed biological control. Biol Invasions 12:3237–3248
McClay AS, Balciunas JK (2005) The role of pre-release efficacy assessment in selecting classical biological control agents for weeds—applying the Anna Karenina principle. Biol Control 35:197–207
McConnachie MM, van Wilgen BW, Ferraro PJ, Forsyth AT, Richardson DM, Gaertner M, Cowling RM (2016) Using counterfactuals to evaluate the cost-effectiveness of controlling biological invasions. Ecol Appl 26(2):475–483
McFadyen REC (1998) Biological control of weeds. Ann Rev Entomol 43:369–393
McFadyen REC, Vitelli M, Setter C (2002) Host specificity of the Rubber vine moth Euclasta whalleyi Popescu-Gorj and Constantinescu (Lepidoptera:Crambidae: Pyraustinae): field host range compared to the predicted by laboratory tests. Aust J Entomol 41:321–323
Mendoza GA, Martins H (2006) Multi-criteria decision analysis in natural resource management: a critical review of methods and new modelling paradigms. For Ecol Manag 230:1–22
Messing RH, Wright MG (2006) Biological control of invasive species: solution or pollution? Front Ecol Environ 4:132–140
Meyer J-Y, Fourdrigniez M, Taputuarai R (2011) Restoring habitat for native and endemic plants through the introduction of a fungal pathogen to control the alien invasive tree Miconia calvescens in the island of Tahiti. Biol Control 57:191–198
Moran VC, Hoffmann JH (2015) The fourteen international symposia on biological control of weeds, 1969-2014: delegates, demographics and inferences from the debate on non-target effects. Biol Control 87:23–31
Moran VC, Zimmermann HG (1984) The biological control of Cactaceae: success ratings and the contribution of individual agent species. In: Delfosse ES (ed) Proceedings of the VI international symposium on biological control of weeds. Agriculture Canada, Ottawa, pp 69–75
Moran VC, Hoffman JH, Zimmermann HG (2005) Biological control of invasive alien plants in South Africa: necessity, circumspection, and success. Front Ecol Environ 3:71–77
Müller-Schärer H, Schaffner U (2008) Classical biological control: exploiting enemy escape to manage plant invasions. Biol Invasions 10:859–874
Ogle CC, La Cock GD, Arnold G, Mickleson N (2000) Impact of an exotic vine Clematis vitalba (F. Ranunculaceae) and control measures on plant biodiversity in indigenous forest, Taihape, New Zealand. Aust Ecol 25:539–551
Page AR, Lacey KL (2006) Economic impact assessment of Australian weed biological control. Technical Series No. 10, CRC for Australian Weed Management, Adelaide
Palmer WA, Heard TA, Sheppard AW (2010) A review of Australian classical biological control of weeds programs and research activities over the past 12 years. Biol Control 52:271–287
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. N Z Plant Prot 57:102–107
Paynter Q, Waipara N, Peterson P, Hona S, Fowler S, Gianotti A, Wilkie P (2006) The impact of two introduced biocontrol agents, Phytomyza vitalbae and Phoma clematidina, on Clematis vitalba in New Zealand. Biol Control 36:350–357
Paynter Q, Martin N, Berry J, Hona S, Peterson P, Gourlay AH, Wilson-Davey J, Smith L, Winks C, Fowler SV (2008) Non-target impacts of Phytomyza vitalbae a biological control agent of the European weed Clematis vitalba in New Zealand. Biol Control 44:248–258
Paynter Q, Fowler SV, Gourlay AH, Peterson PG, Smith LA, Winks CJ (2015) Relative performance on test and target plants in laboratory tests predicts the risk of non-target attack in the field for arthropod weed biocontrol agents. Biol Control 80:133–142
Pearson DE, Callaway RM (2008) Weed biocontrol insects reduce native-plant recruitment through second-order apparent competition. Ecol Appl 18:1489–1500
Pemberton RW (1985) Native plant considerations in biological control of leafy spurge. In: Delfosse ES (ed) Proceedings of the VI international symposium on biological control of weeds. Agriculture Canada, Ottawa, pp 57–71
Pemberton RW (2000) Predictable risk to native plants in weed biological control. Oecologia 125:489–494
Pemberton RW, Liu H (2007) Control and persistence of native Opuntia on Nevis and St. Kitts 50 years after the introduction of Cactoblastis cactorum. Biol Control 41:272–282
Pendleton RL, Pendleton BK, Finch D (2011) Displacement of native riparian shrubs by woody exotics: effects on arthropod and pollinator community composition. Nat Resour Env Iss 16:185–195
Pimentel D (2002) Biological invasions: economic and environmental costs of alien plant, animal and microbe species. CRC Press, London
Rand TA, Russell FL, Louda SM (2004) Local- vs. landscape-scale indirect effects of an invasive weed on native plants. Weed Technol 18:1250–1254
Richardson DM, van Wilgen BW (2004) Invasive alien plants in South Africa: how well do we understand the ecological impacts? S Afr J Sci 100:45–52
Scheiman DM, Bollinger EK, Johnson DH (2003) Effects of leafy spurge infestation on grassland birds. J Wildl Manag 67:115–121
Shaw RH, Tanner R, Djeddour D, Cortat G (2011) Classical biological control of Fallopia japonica in the United Kingdom—lessons for Europe. Weed Res 51:552–558
Sheppard AW, Hill R, DeClerck-Floate RA, McClay A, Olckers T, Quimby PC Jr, Zimmermann HG (2003) A global review of risk-benefit–cost analysis for the introduction of classical biological control agents against weeds: a crisis in the making? Biocontrol News Inf 24:91N–108N
Sheppard AW, van Klinken RD, Heard TA (2005) Scientific advances in the analysis of direct risks of weed biological control agents to nontarget plants. Biol Control 35:215–226
Simberloff D, Alexander M (1998) Assessing risks to ecological systems from biological introductions. In: Calow P (ed) Handbook of environmental risk assessment and management. Blackwell Science, London, pp 147–176
Simberloff D, Stiling P (1996a) How risky is biocontrol? Ecol 77:1965–1974
Simberloff D, Stiling P (1996b) Risks of species introduced for biological control. Biol Conserv 78:185–192
Sinden J, Downey PO, Cacho O, Hester SM (2013) Cost effectiveness in site selection to protect native plant communities from the weed, bitou bush, in New South Wales, Australia. J Environ Manag 128:1071–1080
Smith L (2006) Risk assessment of Ceratapion basicorne, a rosette weevil of yellow starthistle. In: Hoddle MS, Johnson MW (eds) Proceedings of the California conference on biological control V. Riverside, California, pp 47–54
Suckling DM, Sforza RFH (2014) What magnitude are observed non-target impacts from weed biocontrol. PLoS ONE 9(1):e84847
Syrett P, Harman HM (1995) Identification of risk to kowhai, a New Zealand native plant Sophora microphylla Ait., from a potential biological control agent for broom, Cytisus scoparius (L.) Link. N Z J Zool 22:305–309
Taylor DBJ, Heard TA, Paynter Q, Spafford H (2007) Nontarget effects of a weed biological control agent on a native plant in Northern Australia. Biol Control 42:25–33
Thomas MB, Reid AM (2007) Are exotic natural enemies an effective way of controlling invasive plants? Trends Ecol Evol 22:447–453
Trammell MA, Butler JL (1995) Effects of exotic plants on native ungulate use of habitat. J Wildl Manag 59:808–816
Turner PJ, Downey PO (2010) Ensuring invasive alien plant management delivers biodiversity conservation: insights from a new approach using Lantana camara. Plant Prot Q 25:102–110
van den Bosch R, Messenger PS (1973) The Biological Control. Intext Press Inc., New York
van Wilgen BW, de Wit MP, Anderson HJ, Le Maitre DC, Kotze IM, Ndala S, Brown B, Rapholo MB (2004) Costs and benefits of biological control of invasive alien plants: case studies from South Africa. S Afr J Sci 100:113–122
Wan FH, Harris P (1997) Use of risk analysis for screening weed biocontrol agents: Altica carduorum Guer. (Coleoptera: Chrysomelidae) from China as a biocontrol agent of Cirsium arvense (L.) Scop. in North America. Biocontrol Sci Technol 7:299–308
Wapshere AJ (1974) A strategy for evaluating the safety of organisms for biological weed control. Ann Appl Biol 77:201–211
Wilcove DS, Rothstein D, Dubow J, Phillips A, Losos E (1998) Quantifying threats to imperilled species in the United States. BioScience 48:607–615
Willis AJ, Kilby MJ, McMaster K, Cullen JM, Groves RH (2003) Predictability and acceptability: potential for damage to nontarget native plant species by biological control agents for weeds. In: Spafford-Jacob H, Briese DT (eds) Improving the selection, testing and evaluation of weed biological control agents, Technical Series 7. CRC for Australian Weed Management, Adelaide, pp 35–49
Wright MG, Hoffmann MP, Kuhar TP, Gardner J, Pitcher SA (2005) Evaluating risks of biological control introductions: a probabilistic risk-assessment approach. Biol Control 35:338–347
Zwölfer H, Harris P (1971) Host specificity determination of insects for biological control of weeds. Ann Rev Entomol 16:159–178
Zwölfer H, Harris P (1984) Biology and host specificity of Rhynocyllus conicus (Froel.) (Coleoptera, Curculionidae), a successful agent for biocontrol of the thistle, Cardus nutans L. Zeitschrift für Angewandte Entomologie 97:36–62
Acknowledgments
This work was undertaken as part of an Outside Study Program (OSP) in which POD was relieved from teaching responsibilities at the University of Canberra, Australia. POD undertook part of this program at Rhodes University, South Africa. The University of Canberra, and the South African Working for Water (WfW) Programme of the Department of Environmental Affairs: National Resource Management programme provided funding. Funding for part of this work was provided by the South African Research Chairs Initiative of the Department of Science and Technology and the National Research Foundation of South Africa. Any opinion, finding, conclusion or recommendation expressed in this material is that of the authors and the NRF does not accept any liability in this regard. We are grateful to Martin Hill for his valuable inputs and comments on a previous draft. Lastly we would like to thank the anonymous referees who made constructive comments on how to improve the manuscript as well as around improving usability of the framework.
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Downey, P.O., Paterson, I.D. Encompassing the relative non-target risks from agents and their alien plant targets in biological control assessments. BioControl 61, 615–630 (2016). https://doi.org/10.1007/s10526-016-9744-1
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DOI: https://doi.org/10.1007/s10526-016-9744-1