Doctoral Programme on Marine Ecosystem Health and Conservation
 PhD Subject Catalogue Fourth Edition - 2013
Impact of non-indigenous species introduced for aquaculture on the functioning of coastal marine ecosystems
PhD Code: MARES_13_10:
Mobility
  • Host institute 1: P9 - Klaipeda University
  • Host institute 2: P1 - Ghent University
Research fields:
  • T2 - Understanding biodiversity effects on the functioning of marine ecosystems
  • T3 - Biological Invasions
  • T4 - Natural Resources: overexploitation, fisheries and aquaculture
Promotor(s):
  • Olenin Sergej - sergej@corpi.ku.lt
  • De Troch Marleen - marleen.detroch@ugent.be
  • Prof. Dr. Sun Song (Institute of Oceanography, Chinese Academy of Sciences, Qingdao, China)
Contact Person and email: De Troch Marleen - marleen.detroch@ugent.be

Subject description
Conceptual framework 
Aquaculture is one of the fastest growing food-producing sectors, supplying approximately 47% of the world's fish food (FAO, 2009). This strong expansion of aquaculture industry has brought significant marine environmental impacts in coastal ecosystems (Silva et al. 2012), such as sediment organic enrichment and eutrophication (Holmer et al., 2005; Kalantzi and Karakassis, 2006), chemical pollution from pharmaceuticals, organics, bactericides and metals (Antunes and Gil, 2004; Cabello, 2006; Sapkota et al., 2008), and changes in the biodiversity and community structure of benthic fauna (Tomassetti et al., 2009; Vezzulli et al., 2008). While most impact studies focus on these rather ‘obvious’, ‘traditional’ effects that can be relatively easily observed in the environment, the effects of non-indigenous species (NIS) introduced for aquaculture is often neglected.
The occurrence and growth of species in high densities in aquaculture installations is one aspect, but next, also their specific ecology should be taken into account. It can be hypothesised that the use of native species in aquaculture installations will imply more mild effects on the natural ecosystems than non-indigenous species would do. However, the latter are often selected for aquaculture purposes in order to achieve higher yield and profits. The specific effects of NIS on the overall functioning of the natural ecosystems remain underdocumented so far. It is however of high societal impact as the production of food is necessary and positive for mankind on the one hand but can have serious negative impacts on the environment on the other hand. 
Environmental impacts resulting from NIS introductions range from single prey-predator interactions between NIS and native species (e.g. Cowx, 1997; Zambrano et al., 2001, Isumbisho et al., 2006) to complete shifts in ecosystem functioning (e.g. Vander Zanden et al., 1999; Mills et al., 2003; Dietrich et al., 2006; Greig & McIntosh, 2006; Olenin & Minchin, 2011). The notion of ecosystem functioning integrates the flux of energy within a system, often measured using food-web characterisation and integrity. This may involve a change from a top-down- to a bottom-up-driven system, shifts from an energy-poor to an energy-rich system or from slow to fast cycling of nutrients (Power, 1992).
 
Studying the impact on the complex interactions between organisms and therefore the integration of functional aspects is a more integrative way of approaching impact studies. On the other hand, the use of interactions in the development of integrated multitrophic aquaculture (IMTA) has received much attention during the past decade as a means of practicing sustainable aquaculture by recycling nutrients through co-cultured species from different trophic levels (Chopin et al., 2008). Integrated aquaculture has been practiced for centuries in China, initially through land-based operations which later expanded to include marine systems (NACA, 1989; Yang et al., 2000). However, most of this IMTA is established on a trial-error basis and any ecological collapse can be nefast.
Taking these gaps in the current knowledge into account, the present study aims to integrate invasion biology in an impact study with special focus on the effects of aquaculture of NIS on trophic interactions in a coastal ecosystem. This aim will be achieved thanks to the intersectoral cooperation between invasion biology, trophic ecology and aquaculture. While the latter aims to maximize the production and yield, the two former wear high priority to the optimal functioning of the natural ecosystem. The different sectors can meet each other in the sustainable use of marine resources.
 
Objectives and Methodology
 
Biomarkers are biochemical variations in tissues or at the level of whole organisms that provide evidence of exposure to and/or effects of environmental changes (Depledge, 1994). More specifically, this study will use trophic biomarkers (fatty acids, stable isotopes) to follow the energy pathways and trophic links in relation to aquaculture impact. This PhD research will focus on benthic invertebrates as main consumers since (1) they are vulnerable to environmental changes because of their limited mobility and tight link with the sediment and (2) they form a pivotal link between primary producers and higher trophic levels. Moreover, the efficiency of energy transfer between primary producers and consumers is highly variable (Micheli, 1999) but yet governs the rest of the food web. 
 
Specific objectives of this PhD research are to study 
  • (1) the use of different food sources by primary and secondary consumers in aquaculture area vs. control sites. Documenting modified feeding strategies of benthic consumers in relation to  aquaculture activities and environmental conditions is pivotal to understand any impact on the overall functioning of the ecosystem.
  • (2) the specific effect of different aquaculture installations on benthic organisms. By contrasting IMTA with ponds with seasonal rotation of species (e.g. shrimp/jellyfish/sea cucumbers), the differential settlement of material to the bottom and its use by the benthic community will be analysed. This will give insight in the sustainability of different aquaculture techniques.
  • (3) to contribute to an early warning system by deducing which parameter gives a good indication of any impact on the ecosystem. To identify a parameter that can be easily monitored and is informative about any environmental changes is important for sustainable aquaculture applications on the long term.
 
The objectives will be achieved by collecting organisms from the field prior to the biochemical analyses. One sampling campaign (max. 3 weeks) per year will be planned in the first two years of the PhD (year 1: objective 1; year 2: objective 2), financed by UGent funding (outside MARES benchfee). Samples will be collected in the coastal area of Qingdao (China) as it has unique, extensive IMTA installations with a wide range of non-indigenous target species: Argopecten irradians (scallop) introduced from America, Patinopecten yessoenssi (scallop) from Japan and the shrimp Penaeus vannamei from South-America. Sampling sites will be selected based on available environmental data: water parameters, nutrient levels and sediment characteristics. The sampling design will include triplicate samples taken with a 3.6 cm inner diameter sediment core while scuba diving in the vicinity of the aquaculture installations and in control sites. From the collected sediment, primary producers (microphytobenthos, mainly diatoms), meiofauna (38 µm – 1 mm) and macrofauna (>1 mm) will be extracted and stored frozen for biochemical analyses. The energy flux through these compartments of the food web will be analysed by means of trophic markers (fatty acids, stable isotopes) (see reviews by Boecklen et al. 2011, Kelly and Scheibling 2012).
 
Consortium description and feasibility
This PhD subject will be imbedded in the research interests of two academic partners (Klaipeda University and Ghent University). In view of the research focus of the promotors (Prof. Olenin: invasion biology; Dr. De Troch: trophic interactions), this consortium guarantees the necessary expertise and facilities to conduct an integrative impact study. Thanks to the cooperation between Dr. De Troch and Prof. Dr. S. Song (Institute of Oceanography, Chinese Academy of Sciences, Qingdao, China) there is good access to a unique area of aquaculture installations to conduct the field sampling and obtain the detailed environmental data. The necessary expertise, protocols and equipment to analyse the biochemical markers are available at the UGent partner (see e.g. De Troch et al. in press). Prof. Olenin (Klaipeda University) is an expert in invasion biology and will guide the measurement of the necessary parameters of NIS to be included. The mobility of the PhDstudent will be linked to the transfer of knowledge in these fields of expertise. The well-defined sampling and the biochemical analyses make it feasible that this PhD topic yields a PhD thesis in the foreseen timeframe of 3 years.
 
References
  • - Antunes P., Gil O., 2004. PCB and DDT contamination in cultivated and wild sea bass from Ria de Aveiro, Portugal. Chemosphere 54(10):1503–7.
  • - Boecklen W.J., Yarnes C.T., Cook B.A., James A.C., 2011. On the use of stable isotopes in trophic ecology. Annual Review in Ecology and Systematics 42:411-440.
  • - Cabello F.C., 2006. Heavy use of prophylactic antibiotics in aquaculture: a growing problem for human and animal health and for the environment. Environmental Microbiology 8(7): 1137–44.
  • - Chopin, T., Robinson, S.M.C., Troell, M., Neori, A., Fang, J., 2008. Multitrophic integration for sustainable marine aquaculture. In: Jørgensen, S.E., Fath, B.D. (Eds.), The Encyclopedia of Ecology, Ecological Engineering, vol. 3. Elsevier, Oxford, pp. 2463–2475. 
  • - Cowx, I.G., 1997. Introduction of fish species into European fresh waters: Economic successes or ecological disasters? Bulletin Francais De La Peche Et De La Pisciculture 344/345: 57-77.
  • - Depledge, M., 1994. The rationale basis for the use of biomarkers as ecotoxicological tools, in Nondestructive Biomarkers in vertebrates, M.C. Fossiand C. Leonzio, Editors. CRC Press: Boca Raton, Florida, USA. p. 271-295.
  • - De Troch, M., Boeckx, P., Cnudde, C., Van Gansbeke, D., Vanreusel, A., Vincx, M. & Caramujo, M.J.,in press. Bioconversion of fatty acids at the basis of marine food webs: insights from a compound-specific stable isotope analysis. Marine Ecology Progress Series. DOI 10.3354/meps09920. 
  • - Dietrich, J.P., Fvlorrison, B.J. & Hoyle, J.A., 2006. Alternative ecological pathways in the Eastern Lake Ontario food web-round goby in the diet of lake trout. Journal of Great Lakes Research 32: 395-400
  • - FAO, 2009. State of world aquaculture 2008. Rome: Fisheries and Aquaculture Department, Food and Agriculture Organization of the UN. http://www.fao.org/docrep/011/i0250e/i0250e00.HTM.
  • - Greig, H.S. & McIntosh, A.R., 2006. Indirect effects of predatory trout on organic matter processing in detritus-based stream food webs. Oikos 112: 31-40
  • - Holmer M., Wildish D., Hargrave B.T., 2005. Organic enrichment from marine finfish aquaculture and effects on sediment biogeochemical processes. In: Hargrave BT, editor. Environmental effects of marine finfish aquaculture. Berlin: Springer, p. 181–206
  • - Isumbisho, M., Sarmento, H., Kaningini, B., Micha, J.C., and Descy, J.P., 2006. Zooplankton of Lake
  • Kivu, East Africa, half a century after the Tanganyika sardine introduction. Journal of Plankton
  • Research 28: 971-989
  • - Kalantzi I., Karakassis I., 2006. Benthic impacts of fish farming: meta-analysis of community and geochemical data. Marine Pollution Bulletin 52:479–83
  • -Kelly J.R., Scheibling R.E., 2012. Fatty acids as dietary tracers in benthic food webs. Marine Ecology Progress Series 446:1-22
  • - Micheli F., 1999. Eutrophication, fisheries, and consumer-resource dynamics in marine pelagic ecosystems. Science 285:1396-1398
  • - Mills, E.L., Casselman, J.M., Dermott, R., Fitzsimons, J.D., Gal, G., Holeck, K.T., Hoyle, J.A., Johannsson, O.E., Lantry, B.F., Makarewicz, J.C., Millard, E.S., Munawar, I.F., Munawar, M., O'Gorman, R., Owens, R.W., Rudstam, L.G., Schaner, T., and Stewart, T.J. (2003) Lake Ontario: food web dynamics in a changing ecosystem (1970-2000). Canadian Journal of Fisheries and Aquatic Sciences 60: 471-490
  • - NACA, 1989. Integrated Fish Farming in China. FAO NACA Technical Manual 7. A World Food Day Publication of the Network of Aquaculture Centres in Asia and the Pacific, Bangkok, Thailand, 278 pp. 
  • - Olenin S., Minchin, D., 2011. Biological Introductions to the Systems: Macroorganisms. In: Wolanski E. and McLusky D.S. (eds.) Treatise on Estuarine and Coastal Science 8: 149–183
  • - Power, M.E., 1992. Habitat Heterogeneity and the Functional-Significance of Fish in River Food Webs. Ecology 73: 1675-1688
  • Sapkota A., Sapkota A.R., Kucharski M., Burke J., McKenzie S., Walker P., et al., 2008. Aquaculture practices and potential human health risks: current knowledge and future priorities. Environment International 34: 1215–26
  • - Silva C., Mattioli M., Fabbri E., Yáñez E., Angel DelValls T., Martín-Díaz M.L., 2012. Benthic community structure and biomarker responses of the clam Scrobicularia plana in a shallow tidal creek affected by fish farm effluents (Rio San Pedro, SW Spain). Environment International 47: 86-98
  • - Tomassetti P., Persia E., Mercatali I., Vani D., Marussso V., Porrello S., 2009. Effects of mariculture on macrobenthic assemblages in a western Mediterranean site. Marine Pollution Bulletin 58: 533–41.
  • - Vezzulli L., Moreno M., Marin V., Pezzati E., Bartoli M., Fabiano M., 2008. Organic waste impact of captured-based Atlantic bluefin tuna aquaculture at an exposed site in the Mediterranean Sea. Estuarine Coastal and Shelf Science 78: 369
  • - Vander Zanden, M.J., Casselman, J.M., and Rasmussen, J.B., 1999. Stable isotope evidence for the food web consequences of species invasions in lakes. Nature 401: 464-46
  • - Yang, H., Wang, J., Zhou, Y., Zhang, T., Wang, P., He, Y., Zhang, F., 2000. Comparison of efficiencies of different culture systems in the shallow sea along Yantai. Journal of Fishery Sciences of China 24: 140–145
  • - Zambrano L., Scheffer M. & Martinez-Ramos M., 2001. Catastrophic response of lakes to benthivorous fish introduction. Oikos 94: 344-350


Expected outcomes
This PhD project will add relevant ecological information on optimal functioning of marine ecosystems in a changing environment. More specifically, the outcome of this project will contribute to a better understanding of potential impact of aquaculture installations and the use of non-indigenous species on the basis of marine food webs. This is essential for the sustainable use of the oceans worldwide in order to feed the increasing world population. In addition, this PhD project will contribute to the further implementation of trophic biomarkers in marine research. Practical benefits include: (1) a doctoral student who is trained in up-to-date multidisciplinary techniques including biochemical markers; (2) dissemination of the gathered data to the scientific community in the form of peer-reviewed publications (preferably in open access journals, both ecological and more applied (impact) journals will be targeted), oral presentations at international congresses and a PhD thesis.

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