Abstract
In Australia the European carp is widespread, environmentally damaging and difficult to control. Genetic control options are being developed for this species but risk-assessment studies to support these options have been limited. The key science challenge in this context is our limited understanding of complex and highly variable ecosystems. Hierarchical models are one way to approach this complexity and heterogeneity. These models treat the factors that determine risk as a joint probability distribution that can be factored into a series of simpler conditional distributions to allow Bayesian inference following observed outcomes. Designing a risk assessment around this approach, however, requires that the assessment endpoints (such as impacts on native species) are measurable, and that monitoring strategies are carefully designed and implemented in order that risk predictions are compared to outcomes. We therefore suggest that an evidence-based framework, supported by careful hazard analysis and quantitative risk assessment, and implemented within a stage-released protocol, is the safest way to move beyond the current emphasis on contained laboratory studies and qualitative risk assessments. We highlight impediments to this approach, and use the non-target impacts of daughterless carp in Australian billabongs as a case study to illustrate three methodological tools that not only provide solutions to some of these impediments but also encourage stakeholder participation in the risk assessment process.
Similar content being viewed by others
References
Andow DA, Lovei GL, Arpaia S (2006) Ecological risk assessment for Bt crops. Nature Biotechnol 24:749–751
AquaBounty Technologies Incorporated (2010) Environmental Assessment for AquAdvantage® Salmon. Technical report, AquaBounty Technologies, Maynard, USA
Arhonditsis GB, Papantou D, Zhang W, Perhar G, Massos E, Shi M (2008) Bayesian calibration of mechanistic aquatic biogeochemical models and benefits for environmental management. J Mar Syst 73:8–30
Bax NJ, Thresher RE (2009) Ecological, behavioral and genetic factors influencing the recombinant control of invasive pests. Ecol Appl 19:873–888
Bedford T, Cooke R (2001) Probabilistic risk analysis: foundations and methods. Cambridge University Press, Cambridge
Bishop CM (2006) Pattern recognition and machine learning. Springer, New York
Bjornstad O, Grenfell BT (2001) Noisy clockwork: time series analysis of population fluctuations in animals. Science 293:638–643
Burgman MA (2005) Risks and decisions for conservation and environmental management. Cambridge University Press, Cambridge
Clark JS (2007) Models for ecological data: an introduction. Princeton University Press, Princeton
Clark JS, Gelfand AE (2006) A future for models and data in environmental science. Trends Ecol Evol 21:375–380
Colvin ME (2012) Impacts of nuisance species in a shallow lake: a systems modeling approach for evaluating restoration and management policies. PhD thesis, Iowa State University, Ames, USA. Available online. http://people.oregonstate.edu/colvinmi/pdfs/ClearLakeFinal.pdf. Accessed 04.10.12
Cox LA (2008) What’s wrong with risk matrices? Risk Anal 28:497–512
Cox LA, Babayev D, Huber W (2005) Some limitations of qualitative risk rating systems. Risk Anal 25:651–662
Cressie N, Calder CA, Clark JS, ver Hoef JM, Wikle CK (2009) Accounting for uncertainty in ecological analysis: the strengths and limitations of hierarchical statistical modeling. Ecol Appl 19:553–570
Dall D, Neumann G (2004) Daughterless carp: an analysis of legal, technical and other risks to delivery. Technical report, Pest Animal CRC, Canberra, Australia
Dambacher JM, Li HW, Rossignol PA (2002) Relevance of community structure in assessing indeterminacy of ecological predictions. Ecology 83:1372–1385
Dambacher JM, Li HW, Rossignol PA (2003) Qualitative predictions in model ecosystems. Ecol Model 161:79–93
Dambacher JM, Ramos-Jiliberto R (2007) Understanding and predicting effects of modified interactions through a qualitative analysis of community structure. Q Rev Biol 82:227–250
Devlin RH, D’Andrade M, Uh M, Biagi CA (2004) Population effects of GH transgenic Salmon are dependant upon food availability and genotype by environment interactions. Proc Nat Acad Sci 101:9303–9308
Duan JJ, Lundgren JG, Naranjo S, Marvier M (2009) Extrapolating non-target risk of bt crops from laboratory to field. Biol Lett. doi:10.1098/rsbl.2009.0612
Ellison AM (2004) Bayesian inference in ecology. Ecol Lett 7:509–520
Ferson S, Hajagos JG (2004) Arithmetic with uncertain numbers: rigorous and (often) best possible answers. Reliab Eng Syst Saf 85:135–152
Ferson S, Nelsen RB, Hajagos J, Berleant DJ, Zhang J, Tucker WT, Ginzburg LR, Oberkampf WL (2004) Dependence in probabilistic modeling, dempster-shafer theory and probability bounds analysis. Technical report, SAND2004-3072, Sandia National Laboratories, Albuquerque, New Mexico, USA
Fisher N, Cribb J (2005) Monitoring community attitudes to using gene technology methods (daughterless carp) for managing common carp. Technical report, Pest Animal CRC, Canberra, Australia
Fletcher R, Morison A, Hume D (1985) Effects of carp Cyprinus carpio L. on communities of aquatic vegetation and turbidity of waterbodies in the Lower Goulbourn river basin. Aust J Mar Freshw Res 36:311–327
Fung K, Yau P (2002) Daughterless carp technology business plan. Technical report. Report prepared for Murray-Darling Basin Commission
Gehrke PC, Brown P, Schiller CB, Moffatt DB, Bruce AM (1995) River regulation and fish communities in the Murray-Darling river system, Australia. Regul Rivers Res Manag 11:363–375
Gehrke PC, Clarke M, Matveev V, St Pierre S, Palmer A (2011) Carp control improves the health of aquatic ecosystems. Water 35:91–95
Gehrke PC, St Pierre S, Matveev V, Clake M (2010) Ecosystem responses to carp population reduction in the Murray-Darling Basin. Technical report, Project MD923 Final Report to the Murray-Darling Basin Authority, Canberra, Australia
Gilligan D, Rayner T (2007) The distribution, spread, ecological impacts and potential control of carp in the upper Murray River. Technical report, NSW Department of Primary Industries Fisheries Research Report 14, NSW Department of Primary Industries, Cronulla, NSW
Gong Z, Maclean N, Devlin RH, Martinez R, Omitogun O, Estrada MP (2007) Gene construct and expression: information relevant for risk assessment and management, chapter 4. In: Kapuscinski AR, Hayes KR, Li S, Dana G (eds) Environmental risk assessment of genetically modified organisms, vol 3: methodologies for transgenic fish. CABI Publishing, Oxfordshire
Hayes K, Gregg P, Gupta V, Jessop R, Lonsdale M, Sindel B, Stanley J, Williams C (2004) Identifying hazards in complex ecological systems, Part 3: Hierarchical Holographic Model for herbicide tolerant oilseed rape. Environ BioSaf Res 3:1–20
Hayes KR (2002a) Identifying hazards in complex ecological systems, Part 1: fault tree analysis for biological invasions. Biol Invasions 4:235–249
Hayes KR (2002b) Identifying hazards in complex ecological systems. Part 2: infection modes and effects analysis for biological invasions. Biol Invasions 4:251–261
Hayes KR (2011) Uncertainty and uncertainty analysis methods. Technical report, CSIRO Division of Mathematics, Informatics and Statistics, Hobart, Australia, 136 pp. Available online. http://www.acera.unimelb.edu.au/materials/core.html. Accessed 25.10.11
Hayes KR, Kapuscinski AR, Dana G, Li S, Devlin RH (2007) Introduction to environmental risk assessment for transgenic fish, chapter 1. In: Kapuscinski AR, Hayes KR, Li S, Dana G (eds) Environmental risk assessment of genetically modified organisms, vol 3: methodologies for transgenic fish. CABI Publishing, Oxfordshire, pp 1–28
Hoey P, Mitchell G, Krueger C (2008) An independent review of the freshwater products and strategies program of the invasives animals. Technical report, Murray Darling Basin Commission
Hosack GR, Hayes KR, Dambacher JM (2008) Assessing model structure uncertainty through an analysis of system feedback and bayesian networks. Ecol Appl 18:1070–1082
Hosack GRH, Li W, Rossignol PA (2009) Sensitivity of system stability to model structure. Ecol Model 220:1054–1062
Inland Fisheries Service (2009) Carp management program. Technical report. Annual report (2008–2009) of the Inland Fisheries Service, New Norfolk, Tasmania, Australia
Kapuscinksi AR, Hard JJ, Paulson KM, Neira R, Ponniah A, Kamonrat W, Mwanja W, Fleming IA, Gallardo J, Devlin RH, Trisak J (2007) Approaches to assessing gene flow, chapter 5. In: Kapuscinski AR, Hayes KR, Li S, Dana G (eds) Environmental risk assessment of genetically modified organisms, vol 3: methodologies for transgenic fish. CABI Publishing, Oxfordshire, pp 112–150
Kapuscinski AR, Hayes KR, Li S, Dana G (eds) (2007) Environmental risk assessment of genetically modified organisms, vol 3: methodologies for transgenic fish. CABI Publishing, Oxfordshire
King AJ, Robertson AI, Healey MR (1997) Experimental manipulations of the biomass of introduced carp (Cyprinus carpio) in billabongs 1. Impacts on water-column properties. Mar Freshw Res 48:435–443
Kletz T (1999) HAZOP and HAZAN: identifying and assessing process industry hazards. Taylor and Francis, London
Klir GJ, Folger TA (1988) Fuzzy sets, uncertainty and information. Prentice Hall, Englewood Cliffs
Koehn J, Brumley A, Gehrke P (2000) Managing the impact of carp. Technical report, Bureau of Rural Sciences, Canberra, Australia. Available online. http://www.daff.gov.au/__data/assets/pdf_file/0010/1193167/Impacts_of_Carpv1.pdf. Accessed 01.11.11
Koehn JD (2004) Carp (Cyprinus carpio) as a powerful invader in Australian waterways. Freshw Biol 49:882–894
Kuhnert PM, Martin TG, Griffiths SP (2010) A guide to eliciting and using expert knowledge in Bayesian ecological models. Ecol Lett. doi:10.1111/j.1461-0248.2010.01477.x
Kurle CM, Croll DA, Tershy BR (2008) Introduced rats indirectly change marine rocky intertidal communities from algae- to invertebrate-dominated. Proc Nat Acad Sci 105:3800–3804
Kynn M (2008) The “heuristics and biases” bias in expert elicitation. J R Stat Soc Series A 171:239–264
Lapidge KE (2003) Proceedings of the national carp control workshop. Technical report, Pest Animal Control CRC, Canberra, Australia. Available online. http://www.feral.org.au/wp-content/uploads/2010/03/CarpProc.pdf. Accessed 01.11.11
Lever C (2002) Naturalized fishes of the world. Academic Press, New York
Levins R (1974) The qualitative analysis of partially specified systems. Ann N Y Acad Sci 231:123–138
Lonsdale M, Hayes KR, Mahon R, Oakeshott J, Pech R, Williams K (2002) Internal csiro review of risks of the daughterless technology for the control of carp in australia. Technical report, CSIRO Executive, CSIRO, Australia
Metcalf SJ, Dambacher JM, Hobday AJ, Lyle JM (2008) Importance of trophic information, simplification and aggregation error in ecosystem models. Mar Ecol Prog Ser 360:25–36
Morris WF, Doak DF (2002) Quantitative conservation biology. Sinauer Associates, Sunderland
Novak M, Wootton JT, Doak DF, Emmerson M, Estes JA, Tinker MT (2011) Predicting community responses to perturbations in the face of imperfect knowledge and network complexity. Ecology 92:836–846
NRC (2002) Environmental effects of transgenic plants: the scope and adequacy of regulation. National Academies Press, Washington, DC
Pascual MA, Kareiva P, Hilborn R (1997) The influence of model structure on conclusions about the viability and harvesting of serengti wildebeest. Conserv Biol 11:966–976
Pate-Cornell ME (1984) Fault trees vs event trees in reliability analysis. Risk Anal 4:177–186
Pearl J (1986) Fusion, propagation and structuring in belief networks. Artif Intell 29:241–288
Regan HM, Colyvan M, Burgman MA (2002) A taxonomy and treatment of uncertainty for ecology and conservation biology. Ecol Appl 12:618–628
Robertson AI, R HM, J KA (1997) Experimental manipulations of the biomass of introduced carp (Cyprinus carpio) in billabongs 2. Impacts on benthic properties and processes. Mar Freshw Res 48:445–454
Swirepik J (1999) Physical disturbance of Potamogeton tricarinatus and sediment by carp (Cyprinus carpio) in experimental ponds. Master’s thesis, University of Canberra, Canberra, Australia
Wood SN, Thomas MB (1999) Super-sensitivity to structure in biological models. Proc R Soc Lond Series B Biol Sci 266:565–570
Woodbridge M (2008) Microbial risk analysis of foods, chapter qualitative risk assessment. ASM Press, Washington, DC, pp 1–26
Acknowledgments
We sincerely thank Anne Kapuscinski and Leah Sharpe for organising, and the Minnesota Sea Grant Program for supporting the international symposium on which this paper is based, and the diverse participants in the symposium, whose insightful comments on the emerging technology greatly facilitated development of the ideas expressed in this paper. We are indebted to Stan Roberts (CSIRO Marine and Atmospheric Research) for useful comments on the fault tree analysis for viral mediated gene flow. We also thank Peter Caley (CSIRO) and two anonymous reviewers for comments that helped improve the manuscript.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Hayes, K.R., Leung, B., Thresher, R. et al. Meeting the challenge of quantitative risk assessment for genetic control techniques: a framework and some methods applied to the common Carp (Cyprinus carpio) in Australia. Biol Invasions 16, 1273–1288 (2014). https://doi.org/10.1007/s10530-012-0392-9
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10530-012-0392-9