Assessment of the impact of Atlantic bluefin tuna farming on Adriatic benthic habitats by analysing macroinvertebrate assemblage structure at family level


Published: Jul 10, 2018
Keywords:
tuna farming monitoring program environmental impact
PABLO SANCHEZ-JEREZ
VICTORIA FERNANDEZ-GONZALEZ
IVONA MLADINEO
SLAVICA MATIJEVIĆ
DANIJELA BOGNER
LEON GRUBIŠIĆ
DAMIAN FERNANDEZ-JOVER
Abstract

 

The rapidly expanding Atlantic bluefin tuna fattening industry is characterized by high stock densities and a high input food biomass in the form of whole bait seafood.  The environmental impact of this activity must be effectively monitored within a proper sustainable development framework, to address concerns about the potential adverse effects. However, evaluation of monitoring tools for tuna farming has received less attention than other activities. Based on the principles of key taxa (Pocklington & Wells, 1992), we tested the potential use of changes in benthic macroinvertebrate assemblages, polychaetes and amphipods for this purpose. Applying a non-parametric multivariate approach for monitoring the impact of this aquaculture activity on the benthic habitat, we checked for correlations with the physicochemical environmental variables of the sediment. A hierarchical spatial design was followed, using multiple controls. Amphipods and polychaetes showed dissimilarities between impacted and control locations, with significant differences for total assemblage structure at a taxonomic level of families. Total nitrogen (TN) and total sulfur (TS) concentrations were the variables best associated with these changes for amphipods, and d 13C and total phosphorus (TP) were the best for polychaetes. However, total free sulfides (TFS) and TP were the chemical variables that best indicated the effects on sediment. Using this approach, surrogating the whole benthic assemblage to a single taxocene, our data suggest that monitoring tuna farming impact by comparing the changes in amphipod and polychaete assemblages at family level could be an optimal procedure with an excellent cost/benefit ratio.


Article Details
  • Section
  • Research Article
Downloads
Download data is not yet available.
Author Biography
PABLO SANCHEZ-JEREZ, Department of Marine Sciences and Applied Biology, University of Alicante, PO Box 99, 03080 Alicante

Department of Marine Science and Applied Biology.

Senior Lecture

References
Aguado, F., Martinez, F., Garcia-Garcia, B., 2004. In vivo total nitrogen and total phosphorous digestibility in Atlantic bluefin tuna (Thunnus thynnus thynnus Linnaeus, 1758) under industrially intensive fattening conditions in Southeast Spain Mediterranean coastal waters. Aquaculture Nutrition, 10, 413-419.
Aguado-Giménez, F., Gairín, J.I., Martinez-Garcia, E., Fernandez-Gonzalez, V., Ballester Moltó, M. et al., 2015. Application of “taxocene surrogation” and “taxonomic sufficiency” concepts to fish farming environmental monitoring. Comparison of BOPA index versus polychaete assemblage structure. Marine Environmental Research, 103, 27-35.
Aksu, M., Kaymakçi-Başaran, A., Egemen, Ȍ., 2010. Long-term monitoring of the impact of a capture-based bluefin tuna aquaculture on water column nutrient levels in the Eastern Aegean Sea, Turkey. Environmental Monitoring and Assessment, 171, 681-688.
Anderson, M.J., 2001. A new method for non-parametric multivariate analysis of variance. Austral Ecology, 26, 32-46.
Anderson, M.J., Gorley, R.N., Clarke, K.R., 2008. PERMANOVA for PRIMER: Guide to Software and Statistical Methods. PRIMER-E, Plymouth, UK.
Arvanitidis, C., Somerfield, P.J., Chatzigeorgiou, G., Reizopoulou, S., Kevrekidis, T. et al., 2009. Do multivariate analyses incorporating changes in pattern across taxonomic levels reveal anthropogenic stress in Mediterranean lagoons? Journal of Experimental Marine Biology and Ecology, 369 (2), 100-109.
Birk, S., Bonne, W., Borja, A., Brucet, S., Courrat, A. et al., 2012. Three hundred ways to assess Europe's surface waters: An almost complete overview of biological methods to implement the Water Framework Directive. Ecological Indicators, 18, 31-41.
Borja, A., Muxika, I., 2005. Guidelines for the use of AMBI (AZTI's Marine Biotic Index) in the assessment of the benthic ecological quality. Marine Pollution Bulletin, 50 (7), 787-789.
Bouchard, R.W., Huggins, D., Kriz., J., 2005. A review of the issues related to taxonomic resolution in biological monitoring aquatic ecosystems with an emphasis on macroinvertebrates. Kansas Biological Survey, Lawrence, KS Report No. 133, (p p38). https://biosurvey.ku.edu/sites/biosurvey.ku.edu/files/publishedworks/pdfs/KBSRept133_TaxResol.pdf. Accessed 20 october 2016.
Buchanan, J.B., 1984. Sediment analysis. p. 41-64. In: Methods for the study of marine benthos. Holme, N.A., McIntyre, A.D. (Eds) Blackwell Scientific Publications, Oxford.
Cabana, D., Sigala, K., Nicolaidou, A., Reizopoulou, S., 2013. Towards the implementation of the Water Framework Directive in Mediterranean transitional waters: the use of macroinvertebrates as biological quality elements. Advances in Oceanography and Limnology, 4 (2), 212-240.
Callier, M.D., McKindsey, C.W., Desrosiers, G., 2008. Evaluation of indicators used to detect mussel farm influence on the benthos: two case studies in the Magdalen Islands, Eastern Canada. Aquaculture, 278, 77-88.
Carvalho, S., Barata, M., Pereira, F., Gaspar, M.B., Cancela da Fonseca, L. et al., 2006. Distribution patterns of macrobenthic species in relation to organic enrichment within aquaculture earthen ponds. Marine Pollution Bulletin, 52, 1573-1584.
Carvalho, S., Barata, M., Gaspar, M.B., Pousão-Ferreira, P., da Fonseca, L.C., 2007. Enrichment of aquaculture earthen ponds with Hediste diversicolor: consequences for benthic dynamics and natural productivity. Aquaculture, 262 (2), 227-236.
Carvalho, S., Cunha, M.R., Pereira, F., Pousão-Ferreira, P., Santos, M.N. et al., 2012. The effect of depth and sediment type on the spatial distribution of shallow soft-bottom amphipods along the southern Portuguese coast. Helgoland Marine Research, 66(4), 489-501.
Chapman, M.G., Underwood, A.J., Skilleter, G.A., 1995. Variability at different spatial scales between a subtidal assemblage exposed to the discharge of sewage and two control assemblages. Journal of Experimental Marine Biology and Ecology, 189, 103−122.
Clarke, K.R., 1993. Non-parametric multivariate analysis of change in community structure. Austral Journal of Ecology, 18, 11-143.
Clarke, K.R., Gorley, R.N., 2006. PRIMER v6: user manual/tutorial. PRIMER-E, Plymouth.
Dauvin, J.C., Alizier, S., Rolet, C., Bakalem, A., Bellan, G. et al., 2012. Response of different benthic indices to diverse human pressures. Ecological Indicators, 12, 143-153.
Dean, H.K., 2008. The use of polychaetes (Annelida) as indicator species of marine pollution: a review. International Journal of Tropical Biology and Conservation, 56, 11-38
De-la-Ossa-Carretero, A., Del-Pilar-Ruso, Y., Giménez-Casalduero, F., Sánchez-Lizaso, L., Dauvin, J.C., 2011. Sensitivity of amphipods to sewage pollution. Estuarine, Coastal and Shelf Science, 96, 129-138.
Ellis, D., 1985. Taxonomic sufficiency in pollution assessment. Marine Pollution Bulletin, 16, 459.
FAO, 2009. Environmental impact assessment and monitoring in aquaculture. FAO Fisheries and Aquaculture Technical Paper. No. 527. Rome, FAO. 2009. 57 pp. (http://www.fao.org/docrep/012/i0970e/i0970e00.htm). Accessed 9 September 2016.
Fernandez–Gonzalez, V., Sanchez–Jerez, P., 2011. Effects of sea bass and sea bream farming (Western Mediterranean Sea) on peracarid crustacean assemblages. Animal Biodiversity and conservation, 34 (1), 179-190.
Fernandez-Gonzalez, V., Aguado Giménez, F., Gairin Deulofeu, J.I., Sanchez-Jerez, P., 2013. Exploring patterns of variation in amphipod assemblages at multiple spatial scales: natural variability versus coastal aquaculture effect. Aquaculture Environment Interactions, 3, 93-105.
Folk, R.L., 1954. The distinction between grain size and mineral composition in sedimentary rock nomenclature. Journal of Geology, 62, 344-356.
Forrest, B.M., Creese, R.G., 2006. Benthic Impacts of Intertidal Oyster Culture, with Consideration of Taxonomic Sufficiency. Environmental Monitoring and Assessment, 112, doi:10.1007/s10661-006-0359-3.
Giangrande, A., Licciano M., Musco, L., 2005. Polychaetes as environmental indicators revisited. Marine Pollution Bulletin, 50, 1153-1162.
Gomez-Gesteira, J., Dauvin, J.C., 2000. Amphipods are good bioindicators of the impact of oil spills on soft-bottom macrobenthic communities. Marine Pollution Bulletin, 40 (11), 1017-1027.
Gomez-Gesteira, J.L., Dauvin, J.C., Salvande Fraga, M., 2003. Taxonomic level for assessing oil spill effects on soft-bottom sublittoral benthic communities. Marine Pollution Bulletin, 46, 562- 572.
Hall-Spencer, J., Bamber, R., 2007. Effects of salmon farming on benthic Crustacea. Ciencias Marinas, 33(4), 353-366.
Hargrave, B.T., Holmer, M., Newcombe, C.P., 2008. Towards a classification of organic enrichment in marine sediments based on biogeochemical indicators. Marine Pollution Bulletin, 56, 810-824.
Holmer, M., Hansen, P.K., Karakassis, I., Borg, J.A. Schembri, P.J., 2008. Monitoring of environmental impacts of marine aquaculture. p. 47-85. In: Aquaculture in the ecosystem. Holmer, M., Black, K., Duarte, C.M., Marba, N., Karakassis, I. (Eds). Springer, the Netherlands.
Hurlbert, S.J., 1984. Pseudoreplication and the design of ecological field experiments. Ecological Monographs, 54, 187-211.
Karakassis, I., Hatziyanni, E., 2000. Benthic disturbance due to fish farming analyzed under different levels of taxonomic resolution. Marine Ecology Progress Series, 203, 247-253.
Karakassis, I., Tsapakis, M., Hatziyanni, E., Papadopoulou, K.N., Plaiti, W., 2000. Impact of cage farming of fish on the seabed in three Mediterranean coastal areas. ICES Journal of Marine Science, 57, 1462-1471.
Kruskal, J.B., Wish, M., 1978. Multidimensional scaling. Series: Quantitative Applications in the Social Science. Sage Publications, Beverly Hills. 96 pp.
Labrune, C., Romero-Ramírez, A., Amouroux, J.M., Duchêne, J.C., Desmalades, M. et al., 2012. Comparison of ecological quality indices based on benthic macrofauna and sediment profile images: a case study along an organic enrichment gradient off the Rhône River. Ecological Indicators, 12, 133-142.
La Rosa, T., Mirto, S., Mazzola, A., Danovaro, R., 2001. Differential responses of benthic microbes and meiofauna to fish-farm disturbance in coastal sediments. Environmental Pollution, 112(3), 427-434.
Lee, H.W., Bailey-Brock, J.H., McGurr, M.M., 2006. Temporal changes in the polychaete assemblage surrounding a Hawaiian mariculture operation. Marine Ecological Progress Series, 307, 175-185.
Mangion, M., Borg, J.A., Thompson, R., Schembri, P.J., 2014. Influence of tuna penning activities on soft bottom macrobenthic assemblages. Marine Pollution Bulletin, 79, 164-174.
Martinez-Garcia, E., Sanchez-Jerez, P., Aguado-Giménez, F., Ávila, P., Guerrero, A. et al., 2013. Meta-analysis approach to the effects of fish farming on soft bottom polychaeta assemblages in temperate regions. Marine Pollution Bulletin, 69, 165-171.
Matijević, S., Kušpilić, G., Barić, A., 2006. Impact of a fish farm on physical and chemical properties of sediment and water column in the middle Adriatic sea. Fresenius Environmental Bulletin, 15 (9a), 1058-1063.
Matijević, S., Kljakovicc-Gašpić, Z., Bogner, D., Gugić, A., Martinović, I., 2008. Vertical distribution of phosphorus species and iron in sediment at open sea stations in the middle Adriatic region. Acta Adriatica, 49 (2), 165-184.
Méndez, N., Flos, J., Romero, J., 1998. Littoral soft-bottom polychaetes communities in a pollution gradient in front of Barcelona (Western Mediterranean, Spain). Bulletin of Marine Science, 63, 167-178.
Metian, M., Pouil, S., Boustany, A., Troell, M., 2014. Farming of Bluefin Tuna Reconsidering Global Estimates and Sustainability Concerns. Reviews in Fisheries Science & Aquaculture, 22 (3), 184-192.
Miyake, P.M., De la Serna, J.M., Di Natale, A., Farrugia, A., Katavic, I. et al., 2003. General review of bluefin tuna farming in the Mediterranean area. Collective Volume Scientific Paper ICCAT, 55 (1), 114-124.
Moraitis, M., Papageorgiou, N., Dimitriou, P.D., Petrou, A., Karakassis, I., 2013. Effects of offshore tuna farming on benthic assemblages in the Eastern Mediterranean. Aquaculture Environment Interactions, 4, 41-51.
Mueller, M., Pandere, J., Geist, J., 2014. A new tool for assessment and monitoring of community and ecosystem change based on multivariate abundance data integration from different taxonomic groups. Environmental Systems Research, 3 (12), doi: 10.1186/2193-2697-3-12.
Naser, H.A., 2010. Testing taxonomic resolution levels for detecting environmental impacts using macrobenthic assemblages in tropical waters. Environmental Monitoring and Assessment, 170, 435-444.
Olsgard, F., Sommerfield, P.J., 2000. Surrogates in marine benthic investigations: which taxonomic unit to target? Journal of Aquatic Ecosystem Stress and Recovery, 7, 25-42.
Olsgard, F., Brattegard, T., Holthe, T., 2003. Polychaetes as surrogates for marine biodiversity: lower taxonomic resolution and indicators groups. Biodiversity Conservation, 12, 1033-1049.
Ottolenghi, F., 2008. Capture-based aquaculture of bluefin tuna. p. 169-182. In: Capture-based aquaculture. Global overview. Lovatelli, A., Holthus, P.F. (Eds). FAO Fisheries Technical Paper. No. 508. Rome, FAO.
Pagliosa, P.R., 2005. Another diet of worms: the applicability of polychaetes feeding guilds as a useful conceptual framework and biological variable. Marine Ecology 26, 246-254
Pinedo, S., Jordana, E., Ballesteros, E., 2015. A critical analysis on the response of macroinvertebrate communities along disturbance gradients: description of MEDOCC (MEDiterranean OCCidental) index. Marine Ecology, 36, 141-154.
Pocklington, P., Wells, P.G., 1992. Polychaetes. Key taxa for marine environmental quality monitoring. Marine Pollution Bulletin, 24, 593-598.
Quintino, V., Elliott, M., Rodrigues, A.M., 2006. The derivation, performance and role of univariate and multivariate indicators of benthic change: case studies at different spatial scales. Journal of Experimental Marine Biology and Ecology, 330, 368-382.
Quintino, V., Azevedo, A., Magalhaes, L., Sampaio, L., Freitas, R. et al., 2012. Indices, multispecies and synthesis descriptors in benthic assessments: intertidal organic enrichment from oyster farming. Estuarine Coastal and Shelf Science, 110, 190-201.
Sanchez-Jerez, P., Espla-Ramos, A.A., 1996. Detection of environmental impacts by bottom trawling on Posidonia oceanica (L.) Delile meadows: sensitivity of fish and macroinvertebrate communities. Journal of Aquatic Ecosystem Health, 5 (4), 239-253.
Simboura, N., Zenetos, A., 2002. Benthic indicators to use in ecological quality classification of Mediterranean soft bottom marine ecosystems, including a new Biotic index. Mediterranean Marine Science, 3 (2), 77-111.
Somerfield, P.J., Clarke, K.R., 1995. Taxonomic levels in marine community studies, revisited. Marine Ecological Progress Series, 127, 113-119.
Tomassetti, P., Porrello, S., 2005. Polychaetes as indicators of marine fish farm organic enrichment. Aquaculture International, 13, 109-128.
Tveteras, R., Nystoyl, R., Jory, D., 2015. Aquaculture production forecast. Global Aquaculture Alliance GOAL 2015 meeting. Vancouver, BC Canada, October.
Underwood, A.J., 1994. On beyond BACI: sampling designs that might reliably detect environmental disturbances. Ecological Applications, 4 (1), 3-15.
Van Hoey, G., Borja, A., Birchenough, S., Buhl-Mortensen, L., Degraer, S. et al., 2010. The use of benthic indicators in Europe: From the Water Framework Directive to the Marine Strategy Framework Directive. Marine Pollution Bulletin, 60 (12), 2187-2196.
Vezzulli, L., Moreno, M., Marin, V., Pezzati, E., Bartoli, M. et al., 2008. Organic waste impact of capture-based Atlantic bluefin tuna aquaculture at an exposed site in the Mediterranean Sea. Estuarine Coastal and Shelf Science, 78, 368-384.
Vita, R., Marin, A., Jimenez-Brinquis, B., Cesar, A., Marin-Guirao, I. et al., 2004. Aquaculture of Bluefin tuna in the Mediterranean: evaluation of organic particulate wastes. Aquaculture Research, 35, 1384-1387.
Warwick, R., 1988. The level of taxonomic discrimination required to detect pollution effects on marine benthic communities. Marine Pollution Bulletin, 19, 259-268.
Wildish, D.J., Akagiu, H.M., Hamilton, N., Hargrave, B.T., 1999. A recommended method for monitoring sediments to detect organic enrichment from mariculture in the Bay of Fundy. Canadian Technical Report of Fisheries and Aquatic Science, 2286, 31 iii.
Wlodarska-Kowalczuk, M., Kedra, M., 2007. Surrogacy in natural patterns of benthic distribution and diversity: selected taxa versus lower taxonomic resolution. Marine Ecology Progress Series, 351, 53-63.
Most read articles by the same author(s)