Hostname: page-component-cd9895bd7-fscjk Total loading time: 0 Render date: 2024-12-23T18:34:05.266Z Has data issue: false hasContentIssue false
  • English
  • Français

Trophic analyses of opportunistic polychaetes (Ophryotrocha cyclops) at salmonid aquaculture sites

Published online by Cambridge University Press:  11 February 2015

Flora Salvo ,
Dounia Hamoutene  and
Suzanne C. Dufour
Flora Salvo
Affiliation:
Department of Biology, Memorial University of Newfoundland, St John's, NL A1B 3X9, Canada Science Branch, Fisheries and Oceans Canada, P.O. Box 5667, St John's, NL A1C 5X1, Canada
Dounia Hamoutene
Affiliation:
Science Branch, Fisheries and Oceans Canada, P.O. Box 5667, St John's, NL A1C 5X1, Canada
Suzanne C. Dufour*
Affiliation:
Department of Biology, Memorial University of Newfoundland, St John's, NL A1B 3X9, Canada
*
Correspondence should be addressed to: S.C. Dufour, Department of Biology, Memorial University of Newfoundland, St John's, NL A1B 3X9, Canada email: [email protected]
Get access Rights & Permissions [Opens in a new window]

Abstract

A new species of dorvilleid polychaete, Ophryotrocha cyclops, has been observed on the rocky seafloor underneath deep salmonid aquaculture sites on the south coast of Newfoundland, Canada. The distribution of these opportunistic worms is likely related to organic matter accumulation on the seafloor, and this species may have a role in remediation processes. To better understand the functional role of O. cyclops at aquaculture sites, it is important to know what they feed upon. Here, stable isotope analyses (δ13C, δ15N and δ34S) and trace element analyses were performed on dorvilleids and their potential food sources at three aquaculture sites. Stable isotope analyses revealed spatial and temporal variation in the isotopic carbon signature of O. cyclops, highlighting possible differences in the food sources of individual dorvilleids within and between sites. The isotopic composition of dorvilleids was closest to that of fish pellets; the presence of abundant lipid droplets in gut epithelial cells of O. cyclops suggests the assimilation of fish pellet-derived lipids. Trace element analysis indicated that O. cyclops does not concentrate the aquaculture tracers Zn or Cu to a large extent. However, concentrations of sulphur were high in O. cyclops compared with other sources. Taken together, results show that O. cyclops most likely consume both fish pellets and flocculent matter-associated bacteria. As such, they are involved in sulphur cycling and fish pellet degradation at aquaculture sites.

Keywords

Dorvilleidaestable isotopessulphurcarbonnitrogenaquacultureBeggiatoaOphryotrocha
Type
Research Article
Information
Journal of the Marine Biological Association of the United Kingdom , Volume 95 , Issue 4 , June 2015 , pp. 713 - 722
Copyright
Copyright © Marine Biological Association of the United Kingdom 2015 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

REFERENCES

Borja, Ã., Rodrìguez, J.G., Black, K., Bodoy, A., Emblow, C., Fernandes, T.F., Forte, J., Karakassis, I., Muxika, I., Nickell, T.D., Papageorgiou, N., Pranovi, F., Sevastou, K., Tomassetti, P. and Angel, D. (2009) Assessing the suitability of a range of benthic indices in the evaluation of environmental impact of fin and shellfish aquaculture located in sites across Europe. Aquaculture 293, 231–240.CrossRefGoogle Scholar
Brooks, K.M. and Mahnken, C.V.W. (2003) Interactions of Atlantic salmon in the Pacific Northwest environment: III. Accumulation of zinc and copper. Fisheries Research 62, 295–305.CrossRefGoogle Scholar
Bungay, T.R. (2013) Assessment of the influence of finfish aquaculture on hard bottom habitats in a boreal/sub-arctic marine environment. MSc thesis. Memorial University of Newfoundland, St. John's, Canada.Google Scholar
Canfield, D.E. (2001) Isotope fractionation by natural populations of sulfate-reducing bacteria. Geochimica et Cosmochimica Acta 65, 1117–1124.CrossRefGoogle Scholar
Carlier, A., Ritt, B., Rodrigues, C., Sarrazin, J., Olu, K., Grall, J. and Clavier, J. (2010) Heterogeneous energetic pathways and carbon sources on deep eastern Mediterranean cold seep communities. Marine Biology 157, 2545–2565.CrossRefGoogle Scholar
Carvalho, S., Barata, M., Pereira, F., Gaspar, M.B., da Fonseca, L.K. and Pousão-Ferreira, P. (2006) Distribution patterns of macrobenthic species in relation to organic enrichment within aquaculture earthen ponds. Marine Pollution Bulletin 52, 1573–1584.CrossRefGoogle ScholarPubMed
Caut, S., Angulo, E. and Courchamp, F. (2008) Caution on isotopic model use for analyses of consumer diet. Canadian Journal of Zoology 86, 438–445.CrossRefGoogle Scholar
Caut, S., Angulo, E. and Courchamp, F. (2009) Variation in discrimination factors (Δ15N and Δ13C): the effect of diet isotopic values and applications for diet reconstruction. Journal of Applied Ecology 46, 443–453.CrossRefGoogle Scholar
Chou, C.L., Haya, K., Paon, L.A., Burridge, L. and Moffatt, J.D. (2002) Aquaculture-related trace metals in sediments and lobsters and relevance to environmental monitoring program ratings for near-field effects. Marine Pollution Bulletin 44, 1259–1268.CrossRefGoogle ScholarPubMed
Connolly, R., Guest, M., Melville, A. and Oakes, J. (2004) Sulfur stable isotopes separate producers in marine food-web analysis. Oecologia 138, 161–167.CrossRefGoogle ScholarPubMed
Coplen, T.B., Böhlke, J.K., De Bievre, P., Ding, T., Holden, N.E., Hopple, J.A., Krouse, H.R., Lamberty, A., Peiser, H.S. and Revesz, K. (2002) Isotope-abundance variations of selected elements (IUPAC Technical Report). Pure and Applied Chemistry 74, 1987–2017.CrossRefGoogle Scholar
Cranford, P., Dowd, M., Grant, J., Hargrave, B. and McGladdery, S. (2003) Ecosystem level effects of marine bivalve aquaculture. Canadian Technical Report of Fisheries and Aquatic Sciences 2450, 12–20.Google Scholar
Crawford, C.M., Mitchell, I.M. and Macleod, C.K.A. (2001) Video assessment of environmental impacts of salmon farms. ICES Journal of Marine Science 58, 445–452.CrossRefGoogle Scholar
Dean, R.J., Shimmield, T.M. and Black, K.D. (2007) Copper, zinc and cadmium in marine cage fish farm sediments: an extensive survey. Environmental Pollution 145, 84–95.CrossRefGoogle ScholarPubMed
Decker, C. and Olu, K. (2010) Does macrofaunal nutrition vary among habitats at the Hakon Mosby mud volcano? Cahiers de Biologie Marine 51, 361–367.Google Scholar
DeNiro, M.J. and Epstein, S. (1978) Influence of diet on the distribution of carbon isotopes in animals. Geochimica et Cosmochimica Acta 42, 495–506.CrossRefGoogle Scholar
Department of Fisheries and Oceans Canada (DFO) (2013) Standard operating procedures (SOP) for underwater video-camera. http://www.dfo-mpo.gc.ca/library/347683.pdf.Google Scholar
FAO (2014) http://www.fao.org/fishery/affris/species-profiles/atlantic-salmon/feed-production/en/.Google Scholar
Franco-Nava, M.-A., Blancheton, J.-P., Deviller, G.V. and Le-Gall, J.-Y. (2004) Particulate matter dynamics and transformations in a recirculating aquaculture system: application of stable isotope tracers in seabass rearing. Aquacultural Engineering 31, 135–155.CrossRefGoogle Scholar
Grey, J., Waldron, S. and Hutchinson, R. (2004) The utility of carbon and nitrogen isotope analyses to trace contributions from fish farms to the receiving communities of freshwater lakes: a pilot study in Esthwaite Water, UK. Hydrobiologia 524, 253–262.CrossRefGoogle Scholar
Hamoutene, D. (2014) Sediment sulphides and redox potential associated with spatial coverage of Beggiatoa spp. at finfish aquaculture sites in Newfoundland, Canada. ICES Journal of Marine Science, doi: 10.1093/icesjms/fst223.CrossRefGoogle Scholar
Hamoutene, D., Mabrouk, G., Sheppard, L., MacSween, C., Coughlan, E. and Grant, C. (2013) Validating the use of Beggiatoa sp. and opportunistic polychaete worm complex (OPC) as indicators of benthic habitat condition at finfish aquaculture sites in Newfoundland. Canadian Technical Report of Fisheries and Aquatic Sciences 3028, 1–19.Google Scholar
Holmer, M. and Kristensen, E. (1994) Organic matter mineralization in an organic-rich sediment: experimental stimulation of sulfate reduction by fish food pellets. FEMS Microbiology Ecology 14, 33–44.CrossRefGoogle Scholar
Holmer, M. and Kristensen, E. (1996) Seasonality of sulfate reduction and pore water solutes in a marine fish farm sediment: the importance of temperature and sedimentary organic matter. Biogeochemistry 32, 15–39.CrossRefGoogle Scholar
Husa, V., Kutti, T., Ervik, A., Sjøtun, K., Hansen, P. K. and Aure, J. (2013) Regional impact from fin-fish farming in an intensive production area (Hardangerfjord, Norway). Marine Biology Research 10, 241–252.CrossRefGoogle Scholar
Kutti, T., Ervik, A. and Hansen, P.K. (2007) Effects of organic effluents from a salmon farm on a fjord system. I. Vertical export and dispersal processes. Aquaculture 262, 367–381.CrossRefGoogle Scholar
Kutti, T., Ervik, A. and Høisæter, T. (2008) Effects of organic effluents from a salmon farm on a fjord system. III. Linking deposition rates of organic matter and benthic productivity. Aquaculture 282, 47–53.CrossRefGoogle Scholar
Lehmann, M.F., Bernasconi, S.M., Barbieri, A. and McKenzie, J.A. (2002) Preservation of organic matter and alteration of its carbon and nitrogen isotope composition during simulated and in situ early sedimentary diagenesis. Geochimica et Cosmochimica Acta 66, 3573–3584.CrossRefGoogle Scholar
Levin, L.A. and Michener, R.H. (2002) Isotopic evidence for chemosynthesis-based nutrition of macrobenthos: the lightness of being at Pacific methane seeps. Limnology and Oceanography 47, 1336–1345.CrossRefGoogle Scholar
Levin, L.A., James, D.W., Martin, C.M., Rathburn, A.E., Harris, L.H. and Michener, R.H. (2000) Do methane seeps support distinct macrofaunal assemblages? Observations on community structure and nutrition from the northern California slope and shelf. Marine Ecology Progress Series 208, 21–39.CrossRefGoogle Scholar
Levin, L.A., Mendoza, G.F., Konotchick, T. and Lee, R. (2009) Macrobenthos community structure and trophic relationships within active and inactive Pacific hydrothermal sediments. Deep-Sea Research II 56, 1632–1648.CrossRefGoogle Scholar
Levin, L.A., Ziebis, W., Mendoza, G., Bertics, V.J., Washington, T., Gonzalez, J., Thurber, A.R., Ebbe, B. and Lee, R.W. (2013) Ecological release and niche partitioning under stress: lessons from dorvilleid polychaetes in sulfidic sediments at methane seeps. Deep Sea Research II 92, 214–233.CrossRefGoogle Scholar
Levin, L.A., Ziebis, W., Mendoza, G.F., Growney-Cannon, V. and Walther, S. (2006) Recruitment response of methane-seep macrofauna to sulfide-rich sediments: an in situ experiment. Journal of Experimental Marine Biology and Ecology 330, 132–150.CrossRefGoogle Scholar
McCutchan, J.H. Jr., Lewis, W.M. Jr., Kendall, C. and McGrath, C.C. (2003). Variation in trophic shift for stable isotope ratios of carbon, nitrogen, and sulfur. Oikos 102, 378–390.CrossRefGoogle Scholar
McGhie, T.K., Crawford, C.M., Mitchell, I.M. and O'Brien, D. (2000) The degradation of fish-cage waste in sediments during fallowing. Aquaculture 187, 351–366.CrossRefGoogle Scholar
McLeod, R.J., Wing, S.R. and Skilton, J.E. (2010) High incidence of invertebrate-chemoautotroph symbioses in benthic communities of the New Zealand fjords. Limnology and Oceanography 55, 2097–2106.CrossRefGoogle Scholar
Mendiguchía, C., Moreno, C., Mánuel-Vez, M.P. and García-Vargas, M. (2006) Preliminary investigation on the enrichment of heavy metals in marine sediments originated from intensive aquaculture effluents. Aquaculture 254, 317–325.CrossRefGoogle Scholar
Moore, J.W. and Semmens, B.X. (2008) Incorporating uncertainty and prior information into stable isotope mixing models. Ecology Letters 11, 470–480.CrossRefGoogle ScholarPubMed
Moreno, R., Jover, L., Munilla, I., Velando, A. and Sanpera, C. (2010) A three-isotope approach to disentangling the diet of a generalist consumer: the yellow-legged gull in northwest Spain. Marine Biology 157, 545–553.CrossRefGoogle Scholar
Nelson, D.C. and Castenholz, R.W. (1981) Use of reduced sulfur compounds by Beggiatoa sp. Journal of Bacteriology 147, 140–154.CrossRefGoogle ScholarPubMed
Nickell, L.A., Black, K.D., Hughes, D.J., Overnell, J., Brand, T., Nickell, T.D., Breuer, E. and Martyn Harvey, S. (2003) Bioturbation, sediment fluxes and benthic community structure around a salmon cage farm in Loch Creran, Scotland. Journal of Experimental Marine Biology and Ecology 285–286, 221–233.CrossRefGoogle Scholar
Paxton, H. (2009) A new species of Palpiphitime (Annelida: Dorvilleidae) from Western Canada. Proceedings of the Biological Society of Washington 122, 26–31.CrossRefGoogle Scholar
Paxton, H. and Davey, A. (2010) A new species of Ophryotrocha (Annelida: Dorvilleidae) associated with fish farming at Macquarie Harbour, Tasmania, Australia. Zootaxa 2509, 53–61.CrossRefGoogle Scholar
Pereira, P.M.F., Black, K.D., McLusky, D.S. and Nickell, T.D. (2004) Recovery of sediments after cessation of marine fish farm production. Aquaculture 235, 315–330.CrossRefGoogle Scholar
Peterson, B.J. (1999) Stable isotopes as tracers of organic matter input and transfer in benthic food webs: a review. Acta Oecologia 20, 479–487.CrossRefGoogle Scholar
Peterson, B.J. and Fry, B. (1987) Stable isotopes in ecosystem studies. Annual Review of Ecology and Systematics 18, 293–320.CrossRefGoogle Scholar
Post, D.M., Layman, C.A., Arrington, D.A., Takimoto, G., Quattrochi, J. and Montaña, C.G. (2007) Getting to the fat of the matter: models, methods and assumptions for dealing with lipids in stable isotope analyses. Oecologia 152, 179–189.CrossRefGoogle Scholar
Robinson, J.J. and Cavanaugh, C.M. (1995) Expression of form I and form II Rubisco in chemoautotrophic symbioses: implications for the interpretation of stable carbon isotope values. Limnology and Oceanography 40, 1496–1502.CrossRefGoogle Scholar
Sahling, H., Rickert, D., Lee, R.W., Linke, P. and Suess, E. (2002) Macrofaunal community structure and sulfide flux at gas hydrate deposits from the Cascadia convergent margin, NE Pacific. Marine Ecology Progress Series 231, 121–138.CrossRefGoogle Scholar
Salvo, F., Wiklund, H., Dufour, S.C., Hamoutene, D., Pohle, G. and Worsaae, K. (2014) A new annelid species from whalebones in Greenland and aquaculture sites in Newfoundland: Ophryotrocha cyclops, sp. nov. (Eunicida: Dorvilleidae). Zootaxa 3887, 555–568.CrossRefGoogle ScholarPubMed
Sarà, G., Scilipoti, D., Mazzola, A. and Modica, A. (2004) Effects of fish farming waste to sedimentary and particulate organic matter in a southern Mediterranean area (Gulf of Castellammare, Sicily): a multiple stable isotope study (δ13C and δ15N). Aquaculture 234, 199–213.CrossRefGoogle Scholar
Shahidul Islam, M. and Tanaka, M. (2004) Impacts of pollution on coastal and marine ecosystems including coastal and marine fisheries and approach for management: a review and synthesis. Marine Pollution Bulletin 48, 624–649.CrossRefGoogle ScholarPubMed
Sutherland, T.F., Petersen, S.A., Levings, C.D. and Martin, A.J. (2007) Distinguishing between natural and aquaculture-derived sediment concentrations of heavy metals in the Broughton Archipelago, British Columbia. Marine Pollution Bulletin 54, 1451–1460.CrossRefGoogle ScholarPubMed
Teske, A. and Nelson, D.C. (2006) The genera Beggiatoa and Thioploca . In Dworkin, M., Falkow, S., Rosenberg, E., Schleifer, K.-H. and Stackebrandt, E. (eds) The prokaryotes Volume 6: Proteobacteria: Gamma Subclass. New York, NY: Springer, pp. 784–810.CrossRefGoogle Scholar
Thornhill, D.J., Struck, T.H., Ebbe, B., Lee, R.W., Mendoza, G.F., Levin, L.A. and Halanych, K.M. (2012) Adaptive radiation in extremophilic Dorvilleidae (Annelida): diversification of a single colonizer or multiple independent lineages? Ecology and Evolution 2, 1958–1970.CrossRefGoogle ScholarPubMed
Thurber, A.R., Kröger, K., Neira, C., Wiklund, H. and Levin, L.A. (2010) Stable isotope signatures and methane use by New Zealand cold seep benthos. Marine Geology 272, 260–269.CrossRefGoogle Scholar
Thurber, A.R., Levin, L.A., Orphan, V.J. and Marlow, J.J. (2012) Archaea in metazoan diets: implications for food webs and biogeochemical cycling. ISME Journal 6, 1602–1612.CrossRefGoogle ScholarPubMed
Vizzini, S., Savona, B., Caruso, M., Savona, A. and Mazzola, A. (2005) Analysis of stable carbon and nitrogen isotopes as a tool for assessing the environmental impact of aquaculture: a case study from the western Mediterranean. Aquaculture International 13, 157–165.CrossRefGoogle Scholar
Wiklund, H., Altamira, I.V., Glover, A.G., Smith, C.R., Baco, A.R. and Dahlgren, T.G. (2012) Systematics and biodiversity of Ophryotrocha (Annelida, Dorvilleidae) with descriptions of six new species from deep-sea whale-fall and wood-fall habitats in the north-east Pacific. Systematics and Biodiversity 10, 243–259.CrossRefGoogle Scholar
Wiklund, H., Glover, A.G. and Dahlgren, T.G. (2009a) Three new species of Ophryotrocha (Annelida: Dorvilleidae) from a whale-fall in the North-East Atlantic. Zootaxa 2228, 43–56.CrossRefGoogle Scholar
Wiklund, H., Glover, A.G., Johannessen, P.J. and Dahlgren, T.G. (2009b) Cryptic speciation at organic-rich marine habitats: a new bacteriovore annelid from whale-fall and fish farms in the North-East Atlantic. Zoological Journal of the Linnean Society 155, 774–785.CrossRefGoogle Scholar
Ye, L.-X., Ritz, D.A., Fenton, G.E. and Lewis, M.E. (1991) Tracing the influence on sediments of organic waste from a salmonid farm using stable isotope analysis. Journal of Experimental Marine Biology and Ecology 145, 161–174.CrossRefGoogle Scholar
Yokoyama, H., Abo, K. and Ishihi, Y. (2006) Quantifying aquaculture-derived organic matter in the sediment in and around a coastal fish farm using stable carbon and nitrogen isotope ratios. Aquaculture 254, 411–425.CrossRefGoogle Scholar