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Integrating the Concept of Resilience into an Ecosystem Approach to Bivalve Aquaculture Management

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Abstract

Bivalve aquaculture has become increasingly important for marine protein production and is an alternative to exploiting natural resources. Its further and sustainable development should follow an ecosystem approach, to maintain both biodiversity and ecosystem functioning. The identification of critical thresholds to development remains difficult. The present work aims at combining the calculation of the system’s ecological carrying capacity (ECC) with the ecosystem view of resilience for a bay system exposed to bivalve (scallop) aquaculture. Using a trophic food-web model, a stepwise further expansion of culture activities was simulated, and the impact on the system was evaluated twofold: First, a recently developed approach to estimating ECC was used, and second, a resilience indicator was calculated, which is based on the distribution of consumption flows within the trophic network (sensu Arreguín-Sanchez in Ecol Model 272: 27–276, 2014). Results suggest that a culture expansion beyond present-day scale would (a) cause a shift in community composition towards a system dominated by secondary consumers, (b) lead to the loss of system compartments, affecting ecosystem functioning, and (c) result in a decrease in resilience, emphasizing the need to regulate aquaculture activities. The applicability and potential of this presented method in the context of an ecosystem-based approach to aquaculture is discussed. This work aims at adding to the ongoing discussion on sustainable bivalve aquaculture and is expected to help guide aquaculture management.

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References

  • Arreguín-Sánchez F. 2014. Measuring resilience in aquatic trophic networks from supply-demand-of-energy relationships. Ecological Modelling 272:27–276.

    Article  Google Scholar 

  • Bellwood DR, Hughes TP, Folke C, Nyström M. 2004. Confronting the coral reef crisis. Nature 429:827–33. doi:10.1038/nature02691.

    Article  CAS  PubMed  Google Scholar 

  • Buchary EA, Cheung WL, Sumaila UR, Pitcher TJ. 2003. Back to the future: a paradigm shift for restoring Hong Kong marine ecosystem. American Fisheries Society 38:727–46.

    Google Scholar 

  • Byron CJ, Bengtson D, Costa-Pierce BA, Calanni J. 2011. Integrating science into management: ecological carrying capacity of bivalve shellfish aquaculture. Marine Policy 35(3):363–70. doi:10.1016/j.marpol.2010.10.016.

    Article  Google Scholar 

  • Byron CJ, Costa-Pierce BA. 2013. Carrying capacity tools for use in the implementation of an ecosystems approach to aquaculture. In: Ross LG, Telfer TC, Falconer L, Soto D, Aguilar-Manjarrez J, Eds. Site selection and carrying capacities for inland and coastal aquaculture. pp. 87–101. FAO/Institute of Aquaculture, University of Stirling, Expert Workshop, 6-8 December 2010. Stirling, the United Kingdom of Great Britain and Northern Ireland. FAO Fisheries and Aquaculture Proceedings No. 21. Rome, FAO. 282 pp.

  • Cavers S, Cottrell JE. 2015. The basis of resilience in forest tree species and its use in adaptive forest management in Britain. Forestry 88:13–26. doi:10.1093/forestry/cpu027.

    Article  Google Scholar 

  • Chapi FS, Walker BH, Hobbs JR, Hooper DU, Lawton JH, Sala OE, Tilman D. 1997. Biotic control over the functioning of ecosystems. Science 277:500–4. doi:10.1126/science.277.5325.500.

    Article  Google Scholar 

  • Chen Z, Qiu Y, Jia X, Xu S. 2008. Simulating fisheries management options for the Beibu Gulf by means of an ecological modelling optimization routine. Fisheries Research 89:257–65.

    Article  Google Scholar 

  • Cheung WL, Watson R, Pitcher TJ. 2002. Policy simulation of fisheries in the Hong Kong marine ecosystem. Fisheries Centre Research Report, University of British Columbia, Vancouver, British Columbia, Canada. 10(2):46–53.

    Google Scholar 

  • Christensen V. 1995. Ecosystem maturity—towards quantification. Ecological Modelling 77:3–32.

    Article  Google Scholar 

  • Christensen V, Walters CJ. 2004. Ecopath with Ecosim: methods, capabilities and limitations. Ecological Modelling 172(2–4):109–39. doi:10.1016/j.ecolmodel.2003.09.003.

    Article  Google Scholar 

  • Christensen V, Walters CJ, Pauly D. 2005. Ecopath with Ecosim: A user’s guide. Vancouver, BC: Fisheries Centre, University of British Columbia. p 154.

    Google Scholar 

  • Cranford P, Dowd M, Grant J, Hargrave B, McGladdery S. 2003. Ecosystem level effects of marine bivalve aquaculture. Canada: Fisheries and Oceans. pp 51–96.

    Google Scholar 

  • Cranford PJ, Kamermans P, Krause G, Mazurié J, Buck BH, Dolmer P, Fraser D, Van Nieuwenhove K, O’Beirn FX, Sanchez-Mata A, Thorarinsdóttir GG, Strand O. 2012. An ecosystem-based approach and management framework for the integrated evaluation of bivalve aquaculture impacts. Aquaculture Environmental Interactions 2:193–213. doi:10.3354/aei00040.

    Article  Google Scholar 

  • Dame RF, Prins TC. 1998. Bivalve carrying capacity in coastal ecosystems. Aquatic Ecology 31:409–21.

    Article  Google Scholar 

  • D’Amours O, Archambault P, McKindsey CW, Johnson LE. 2008. Local enhancement of epibenthic macrofauna by aquaculture activities. Marine Ecology Progress Series 371:73–84. doi:10.3354/meps07672.

    Article  Google Scholar 

  • Dealteris JT, Kilpatrick BD, Rheault RB. 2004. A comparative evaluation of the habitat value of shellfish aquaculture gear, submerged aquatic vegetation and non-vegetated seabed. Journal of Shellfish Research 23(3):867–74.

    Google Scholar 

  • DeAngelis DL. 1980. Energy flow, nutrient cycling, and ecosystem resilience. Ecology 61(4):764–71.

    Article  Google Scholar 

  • DeAngelis DL, Gardner RH, Mankin JB, Post WM, Carney JH. 1978. Energy flow and the number of trophic levels in ecological communities. Nature 273:406–7.

    Article  Google Scholar 

  • DeAngelis DL, Mulholland PJ, Palumbo AV, Steinman AD, Huston MA, Elwood JW. 1989. Nutrient dynamics and food-web stability. Annual Review of Ecology and Systematics 20:71–95.

    Article  Google Scholar 

  • Díaz López B. 2011. Aquaculture systems. In: Jørgensen SE, Ed. Handbook of ecological models used in ecosystem and environment management. Boca Raton, FL: CRC Press. p 241–56.

    Chapter  Google Scholar 

  • Dowd M. 2003. Seston dynamics in a tidal inlet with shellfish aquaculture: a model study using tracer equations. Estuarine Coastal and Shelf Science 57:523–37. doi:10.1016/S0272-7714(02)00397-9.

    Article  Google Scholar 

  • Duffy JE. 2002. Biodiversity and ecosystem function: the consumer connection. Oikos 99:201–19. doi:10.1034/j.1600-0706.2002.990201.x.

    Article  Google Scholar 

  • Dumbauld BR, Ruesink JL, Rumrill SS. 2009. The ecological role of bivalve shellfish aquaculture in the estuarine environment: A review with application to oyster and clam culture in West Coast (USA) estuaries. Aquaculture 290(3–4):196–223. doi:10.1016/j.aquaculture.2009.02.033.

    Article  Google Scholar 

  • FAO. 2014. A-0—World fisheries production by capture and aquaculture (AQ), by ISSCAAP divisions (1950–2011). Downloaded at 01.09.2015 from ftp://fao.org/fi/Cdrom/CD_yearbook_2012/root/aquaculture/a0.pdf.

  • Ferreira JG, Grant J, Verner-Jeffreys DW, Taylor NGH. 2013. Modeling frameworks for determination of carrying capacity for aquaculture. In: Christou P, Savin R, Costa-Pierce BA, Misztal I, Whitelaw CBA, Eds. Sustainable food production. New York: Springer. p 417–48. doi:10.1007/978-1-4614-5797-8

    Chapter  Google Scholar 

  • Filgueira R, Comeau LA, Guyondet T. 2015. Modelling carrying capacity of bivalve aquaculture: a review of definitions and methods. DFO Canadian Science Advisory Secretariat, Research Document 2015/002. v + 31 p.

  • Finn JT. 1976. Measures of ecosystem structure and function derived from analysis of flows. Journal of theoretical Biology 56:363–80.

    Article  CAS  PubMed  Google Scholar 

  • Folke C. 2006. Resilience: The emergence of a perspective for social–ecological systems analyses. Global Environmental Change 16:253–67.

    Article  Google Scholar 

  • Folke C, Carpenter S, Walker B, Scheffer M, Elmqvist T, Gunderson L, Holling CS. 2004. Regime shifts, resilience and biodiversity in ecosystem management. Annual Review of Ecology, Evolution, and Systematics 35:557–81.

    Article  Google Scholar 

  • Gibbs MT. 2004. Interactions between bivalve shellfish farms and fishery resources. Aquaculture 240:267–96.

    Article  Google Scholar 

  • Grimm V, Wissel C. 1997. Babel, or the ecological stability discussions: an inventory and analysis of terminology and a guide for avoiding confusion. Oecologia 109:323–34.

    Article  CAS  PubMed  Google Scholar 

  • Guthrie W, Filliben J, Heckert A. 2012. Chapter 4—Process Modeling. NIST/SEMATECH e-Handbook of Statistical Methods. http://www.itl.nist.gov/div898/handbook/, accessed at 30.07.2015.

  • Heymans JJ. 2003. Comparing the Newfoundland-Southern Labrador marine ecosystem models using information theory. Heymans JJ, editor. Ecosystem models of Newfoundland and Southeastern Labrador (2J3KLNO): additional information and analyses for “back to the future”, vol. 11(5): Fisheries Centre Research Reports, pp 62–71.

  • Heymans JJ, Coll M, Libralato S, Morissette L, Christensen V. 2014. Global patterns in ecological indicators of marine food webs: A modelling approach. PLoS ONE 9(4):e95845. doi:10.1371/journal.pone.0095845.

    Article  PubMed  PubMed Central  Google Scholar 

  • Heymans JJ, Guénette S, Christensen V. 2007. Evaluating network analysis indicators of ecosystem status in the Gulf of Alaska. Ecosystems 10:488–502.

    Article  CAS  Google Scholar 

  • Holling CS. 1973. Resilience and stability of ecological systems. Annual Review of Ecoligy and Systematics 4:1–23.

    Article  Google Scholar 

  • Huang CH, Lin HJ, Huang TC, Su HM, Hung JJ. 2008. Responses of phytoplankton and periphyton to system-scale removal of oyster-culture racks from a eutrophic tropical lagoon. Marine Ecology Progress Series 358:1–12. doi:10.3354/meps07465.

    Article  CAS  Google Scholar 

  • Hursh SR. 1980. Economic concepts for the analysis of behavior. Journal of the Experimental Analysis of Behavior 34:219–38.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Inglis GJ, Gust N. 2003. Potential indirect effects of shellfish culture on the reproductive success of benthic predators. Journal of Applied Ecology 40:1077–89.

    Article  Google Scholar 

  • Inglis GJ, Hayden BJ, Ross AH. 2000. An overview of factors affecting the carrying capacity of coastal embayment for mussel culture. NIWA Client Report CHC00/69, Christchurch, New Zealand.

  • Johnson KH, Vogt KA, Clark HJ, Schmitz OJ, Vogt DJ. 1996. Biodiversity and the productivity and stability of ecosystems. Trends in Ecology and Evolution 11:372–7. doi:10.1016/0169-5347(96)10040-9.

    Article  CAS  PubMed  Google Scholar 

  • Jones CG, Lawton JH, Shachak M. 1994. Organisms as ecosystem engineers. Oikos 69(3):373–86.

    Article  Google Scholar 

  • Jones CG, Lawton JH, Shachak M. 1997. Positive and negative effects of organisms as physical ecosystem engineers. Ecology 78(7):1946–57.

    Article  Google Scholar 

  • Kluger LC, Taylor MH, Mendo J, Wolff M. 2016a. Carrying capacity simulations as a tool for ecosystem-based management of a scallop aquaculture system. Ecological Modelling 331:44–55. doi:10.1016/j.ecolmodel.2015.09.002.

    Article  Google Scholar 

  • Kluger LC, Taylor MH, Barriga Rivera E, Torres Silva E, Wolff M. 2016b. Assessing the ecosystem impact of scallop bottom culture through a community analysis and trophic modelling approach. Marine Ecology Progress Series 547:121–35. doi:10.3354/meps11652.

    Article  Google Scholar 

  • Laliberte E, Wells JA, DeClerck F, Metcalfe DJ, Catterall CP, Queiroz C, Aubin I, Bonser SP, Ding Y, Fraterrigo JM, McNamara S, Morgan JW, Sánchez Merlos D, Vesk PA, Mayfield MM. 2010. Land-use intensification reduces functional redundancy and response diversity in plant communities. Ecology Letters 13:76–86. doi:10.1111/j.1461-0248.2009.01403.x.

    Article  PubMed  Google Scholar 

  • Leguerrier D, Niquil N, Petiau A, Bodoy A. 2004. Modeling the impact of oyster culture on a mudflat food web in Marennes-Oléron Bay (France). Marine Ecology Progress Series 273:147–62. doi:10.3354/meps273147.

    Article  Google Scholar 

  • MacArthur R. 1955. Fluctuations of animal populations and a measure of community stability. Ecology 36(3):533. doi:10.2307/1929601.

    Article  Google Scholar 

  • Mageau MT, Costanza R, Ulanowicz RE. 1998. Quantifying the trends expected in developing ecosystems. Ecological Modelling 112:1–22.

    Article  Google Scholar 

  • McKindsey CW. 2013. Carrying capacity for sustainable bivalve aquaculture. In: Christou P, Savin R, Costa-Pierce BA, Misztal I, Whitelaw CBA, Eds. Sustainable food production. New York, NY: Springer. p 417–48. doi:10.1007/978-1-4614-5797-8

    Google Scholar 

  • Mckindsey CW, Archambault P, Callier MD, Olivier F. 2011. Influence of suspended and off-bottom mussel culture on the sea bottom and benthic habitats: a review. Canadian Journal of Zoology 89(7):622–46.

    Article  Google Scholar 

  • McKindsey CW, Thetmeyer H, Landry T, Silvert W. 2006. Review of recent carrying capacity models for bivalve culture and recommendations for research and management. Aquaculture 261(2):451–62. doi:10.1016/j.aquaculture.2006.06.044.

    Article  Google Scholar 

  • Murray LG, Newell CR, Seed R. 2007. Changes in the biodiversity of mussel assemblages induced by two methods of cultivation. Journal of Shellfish Research 26(1):153–62.

    Article  Google Scholar 

  • Newell RIE. 2004. Ecosystem influences of natural and cultivated populations of suspension feeding bivalve molluscs: a review. Journal of Shellfish Research 23(1):51–61.

    Google Scholar 

  • Odum EP. 1969. The strategy of ecosystem development. Science 164:262–70.

    Article  CAS  PubMed  Google Scholar 

  • Pearson TH, Rosenberg R. 1978. Macrobenthic succession in relation to organic enrichment and pollution of the marine environment. Oceanography and Marine Biology—Annual Review 16:229–311.

    Google Scholar 

  • Petersen JK, Nielsen TG, van Duren L, Maar M. 2008. Depletion of plankton in a raft culture of Mytilus galloprovincialis in Ría de Vigo, NW Spain. I. Phytoplankton. Aquatic Biology 4:113–25. doi:10.3354/ab00124.

    Article  Google Scholar 

  • Petersen JK, Saurel C, Nielsen P, Timmermann K. 2015. The use of shellfish for eutrophication control. Aquaculture International 24(3):857–78. doi:10.1007/s10499-015-9953-0.

    Article  Google Scholar 

  • Petersen JK, Hasler B, Timmermann K, Torring DB, Larsen MM, Holmer M. 2014. Mussels as a tool for mitigation of nutrients in the marine environment. Marine Pollution Bulletin 82(1–2):137–43. doi:10.1016/j.marpolbul.2014.03.006.

    Article  CAS  PubMed  Google Scholar 

  • Powers MJ, Peterson CH, Summerson HC, Powers SP. 2007. Macroalgal growth on bivalve aquaculture netting enhances nursery habitat for mobile invertebrates and juvenile fishes. Marine Ecology Progress Series 339:109–22. doi:10.3354/meps339109.

    Article  Google Scholar 

  • R Core Team (2014) R—A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. http://www.R-project.org.

  • Soto D, Aguilar-Manjarrez J, Brugère C, Angel D, Bailey C, Black K, Edwards P, Costa-Pierce B, Chopin T, Deudero S, Freeman S, Hambrey J, Hishamunda N, Knowler D, Silvert W, Marba N, Mathe S, Norambuena R, Simard F, Tett P, Troell M, Wainberg A. 2008. Applying an ecosystem-based approach to aquaculture: principles, scales and some management measures. Soto D, Aguilar-Manjarrez J, Hishamunda, editors. Building an ecosystem approach to aquaculture. FAO/Universitat de les Illes Balears Expert Workshop. 7–11 May 2007, Palma de Mallorca, Spain. FAO Fisheries and Aquaculture Proceedings. No. 14. Rome, FAO. pp. 15–35.

  • Standish RJ, Hobbs RJ, Mayfield MM, Bestelmeyer BT, Suding KN, Battaglia LL, Eviner V, Hawkes CV, Temperton VM, Cramer VA, Harris JA, Funk JL, Thomas PA. 2014. Resilience in ecology: Abstraction, distraction, or where the action is? Biological Conservation 177:43–51. doi:10.1016/j.biocon.2014.06.008.

    Article  Google Scholar 

  • Stenton-Dozey J, Jackson LF, Busby A. 1999. Impact of Mussel Culture on Macrobenthic Community Structure in Saldanha Bay. South Africa. Marine Pollution Bulletin 39(1–12):357–66.

    Article  CAS  Google Scholar 

  • Stenton-Dozey J, Probyn T, Busby A. 2001. Impact of mussel (Mytilus galloprovincialis) raftculture on benthic macrofauna, in situ oxygen uptake, and nutrient fluxes in Saldanha Bay, South Africa. Canadian Journal of Fisheries and Aquatic Science 58(5):1021–31. doi:10.1139/f01-034.

    Article  CAS  Google Scholar 

  • Tallman JC, Forrester GE. 2007. Oyster grow-out cages function as artificial reefs for temperate fishes. Transactions of the American Fisheries Society 136(3):790–9. doi:10.1577/T06-119.1.

    Article  Google Scholar 

  • Taylor MH, Wolff M, Vadas F, Yamashiro C. 2008. Trophic and environmental drivers of the Sechura bay ecosystem (Peru) over an ENSO cycle. Helgoland Marine Research 62:15–32. doi:10.1007/s10152-007-0093-4.

    Article  Google Scholar 

  • Tett P, Portilla E, GillibrandPA Inall M. 2011. Carrying and assimilative capacities: the ACExR-LESV model for sea-loch aquaculture. Aquaculture Research 42:51–67.

    Article  Google Scholar 

  • Ulanowicz RE. 1980. An Hypothesis on the Development of Natural Communities. Journal of Theoretical Biology 85:223–45.

    Article  CAS  PubMed  Google Scholar 

  • Ulanowicz RE. 1986. Growth and development: Ecosystems phenomenology. New York: Springer-Verlag. p 203.

    Book  Google Scholar 

  • Ulanowicz RE. 2000. Toward the measurement of ecological integrity. In: Pimentel D, Westra L, Noss RF, Eds. Ecological integrity: integrating environment, conservation, and health. Washington DC: Island Press. p 99–113.

    Google Scholar 

  • Ulanowicz RE. 2004. Quantitative methods for ecological network analysis. Computational Biology and Chemistry 28:321–39. doi:10.1016/j.compbiolchem.2004.09.001.

    Article  CAS  PubMed  Google Scholar 

  • Ulanowic RE, Abarca-Arenas LG. 1997. An informational synthesis of ecosystem structure and function. Ecological Modelling 95:1–10.

    Article  Google Scholar 

  • Valdemarsen T, Kristensen E, Holmer M. 2010. Sulfur, carbon, and nitrogen cycling in faunated marine sediments impacted by repeated organic enrichment. Marine Ecology Progress Series 400:37–53. doi:10.3354/meps08400.

    Article  CAS  Google Scholar 

  • Walker B, Holling CS, Carpenter SR, Kinzig A. 2004. Resilience, adaptability and transformability in social-ecological systems. Ecology and Society 9(2): 5. http://www.ecologyandsociety.org/vol9/iss2/art5.

  • Walker B, Kinzig A, Langridge J. 1999. Plant attribute diversity, resilience, and ecosystem function: The nature and significance of dominant and minor species. Ecosystems 2:95–113. doi:10.1007/s100219900062.

    Article  Google Scholar 

  • Walker BH. 1992. Biodiversity and ecological redundancy. Conservation Biology 6(1):18–23.

    Article  Google Scholar 

  • Wickham H. 2009. GGplot2: elegant graphics for data analysis. New York: Springer.

    Book  Google Scholar 

  • Worm B, Hilborn R, Baum JK, Branch TA, Collie JS, Costello C, Fogarty MJ, Fulton EA, Hutchings JA, Jennings S, Jensen OP, Lotze HK, Mace PM, McClanahan TR, Minto C, Palumbi SR, Parma AM, Ricard D, Rosenberg AA, Watson R, Zeller D. 2009. Rebuilding global fisheries. Science 325:578–86.

    Article  CAS  PubMed  Google Scholar 

  • Ysebaert T, Hart M, Herman PMJ. 2009. Impacts of bottom and suspended cultures of mussels Mytilus spp. on the surrounding sedimentary environment and macrobenthic biodiversity. Helgoland Marine Research 63:59–74. doi:10.1007/s10152-008-0136-5.

    Article  Google Scholar 

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Acknowledgements

This paper was prepared as part of the bilateral SASCA project (“Sustainability Analysis of Scallop Culture in Sechura bay (Peru)”), financed by the German Federal Ministry of Education and Research (BMBF, SASCA 01DN12131). The first author is grateful for having received a travelling grant as awarded by the Bremer Studienfonds e.V. allowing her to visit the second author for a short research stay during which the main content of this work was developed.

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Correspondence to Lotta Clara Kluger.

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The first author wrote the manuscript, for which idea and content was developed jointly with the second author. The third author provided input on the ongoing research process and the different versions of the manuscript.

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Kluger, L.C., Filgueira, R. & Wolff, M. Integrating the Concept of Resilience into an Ecosystem Approach to Bivalve Aquaculture Management. Ecosystems 20, 1364–1382 (2017). https://doi.org/10.1007/s10021-017-0118-z

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