DOI: https://doi.org/10.3354/aei00500
copiedFatty acid composition of northern shrimp Pandalus borealis in relation to salmon aquaculture locations in northern Norway
- Guldborg Søvik
- Siri Aaserud Olsen
- Agneta Hansen
- Stian Stiansen
- Einar Magnus Nilssen
- Pål Arne Bjørn
- Sonnich Meier
ABSTRACT:
The fatty acid (FA) content of northern shrimp Pandalus borealis sampled on commercial shrimp fishing grounds in 2 fjords in northern Norway was analyzed to elucidate if the shrimp feed on aquaculture waste from salmon aquaculture farms. Shrimp were sampled in February and June 2021 in 1 fjord without farms (Balsfjord) and 1 fjord with farms (Kvænangen), at varying distances from the farms (1.5 to 13.3 km). A laboratory experiment conducted as part of our study showed that the FA profile of shrimp feeding on salmon feed pellets changed toward the FA profile of the pellets. The terrestrial FAs 18:2n-6 and 18:3n-3 changed the most and were chosen as suitable FA trophic markers (FATMs) for identifying feeding on aquaculture waste by shrimp in the fjords. The terrestrial FATMs were not detected at elevated levels in the lipids of the shrimp from Kvænangen, indicating that none of the sampled shrimp had been feeding on aquaculture waste. FA analysis has the potential to inform diet studies, and we found differences in the shrimp diet between and within the fjords as well as seasonal differences. Calanus finmarchicus was a more abundant prey in outer Kvænangen compared with inner Kvænangen and Balsfjord, while shrimp at the latter 2 sites had a higher content of benthic FATMs. At all sites, C. finmarchicus constituted a more important food item in winter than in summer.
KEYWORDS
Aas TS, Ytrestøyl T, Åsgard T (2019) Utilization of feed resources in the production of Atlantic salmon (Salmo salar) in Norway: an update for 2016. Aquacult Rep 15:100216
Albers CS, Kattner G, Hagen W (1996) The compositions of wax esters, triacylglycerols and phospholipids in Arctic and Antarctic copepods: evidence of energetic adaptations. Mar Chem 55:347-358 Crossref
Anderson TR, Hessen DO, Gentleman WC, Yool A, Mayor DJ (2024) Optimal phenology of life history events in Calanus finmarchicus: exit from diapause in relation to interannual variation in spring bloom timing and predation. J Plankton Res 46:439-451 PubMed Crossref
Baltadakis A, Casserly J, Falconer L, Sprague M, Telfer TC (2020) European lobsters utilise Atlantic salmon wastes in coastal integrated multi-trophic aquaculture systems. Aquacult Environ Interact 12:485-494 Crossref
Barr L (1970) Diel vertical migration of Pandalus borealis in Kachemak Bay, Alaska. J Fish Res Board Can 27:669-676 Crossref
Bechmann RK, Lyng E, Berry M, Kringstad A, Westerlund S (2017) Exposing northern shrimp (Pandalus borealis) to fish feed containing the antiparasitic drug diflubenzuron caused high mortality during molting. J Toxicol Environ Health A 80:941-953 PubMed Crossref
Bechmann RK, Lyng E, Westerlund S, Bamber S and others (2018) Early life stages of northern shrimp (Pandalus borealis) are sensitive to fish feed containing the anti-parasitic drug diflubenzuron. Aquat Toxicol 198:82-91 PubMed Crossref
Bechmann RK, Arnberg M, Gomiero A, Westerlund S and others (2019) Gill damage and delayed mortality of northern shrimp (Pandalus borealis) after short time exposure to anti-parasitic veterinary medicine containing hydrogen peroxide. Ecotoxicol Environ Saf 180:473-482 PubMed Crossref
Bechmann RK, Arnberg M, Bamber S, Lyng E and others (2020) Effects of exposing shrimp larvae (Pandalus borealis) to aquaculture pesticides at field relevant concentrations, with and without food limitation. Aquat Toxicol 222:105453 PubMed Crossref
Bell JG, McGhee F, Campbell PJ, Sargent JR (2003) Rapeseed oil as an alternative to marine fish oil in diets of post-smolt Atlantic salmon (Salmo salar): changes in flesh fatty acid composition and effectiveness of subsequent fish oil ‘wash out’. Aquaculture 218:515-528 Crossref
Berenboim BI (1981) Feeding of the shrimp Pandalus borealis in the Barents Sea region. Biol Mora (Vladivost) 5:28-32
Bergström BI (2000) The biology of Pandalus. In: Southward AJ, Tyler PA, Young CM, Fuiman L (eds) Advances in marine biology, Vol 38. Academic Press, London, p 55-245
Drolet D, Riley C, Robert S, Estrada R, Gianasi BL, McKindsey CW (2022) Effect of aquaculture-related diets on the long-term performance and condition of the rock crab, Cancer irroratus. Front Mar Sci 9:865390
Eilertsen HC, Skarðhamar J (2006) Temperatures of north Norwegian fjords and coastal waters: variability, significance of local processes and air-sea heat exchange. Estuar Coast Shelf Sci 67:530-538 Crossref
Fernandez-Jover D, Martinez-Rubio L, Sanchez-Jerez P, Bayle-Sempere JT and others (2011) Waste feed from coastal fish farms: a trophic subsidy with compositional side-effects for wild gadoids. Estuar Coast Shelf Sci 91:559-568 Crossref
Frantzen M, Bytingsvik J, Tassara L, Reinardy HC, Refseth GH, Watts EJ, Evenset A (2020) Effects of the sea lice bath treatment pharmaceuticals hydrogen peroxide, azamethiphos and deltamethrin on egg-carrying shrimp (Pandalus borealis). Mar Environ Res 159:105007 PubMed Crossref
Gonzalez-Silvera D, Izquierdo-Gomez D, Sanchez-Jerez P, Elbal MT, Lopez-Jimenez JA, Martinez-Lopez FJ (2020) Influence of aquaculture waste on fatty acid profiles and gonad maturation of wild fish aggregations at fish farms. Mar Environ Res 156:104902 PubMed Crossref
Handå A, Min HJE, Wang XX, Broch OJ, Reitan KI, Reinertsen H, Olsen Y (2012) Incorporation of fish feed and growth of blue mussels (Mytilus edulis) in close proximity to salmon (Salmo salar) aquaculture: implications for integrated multi-trophic aquaculture in Norwegian coastal waters. Aquaculture 356-357:328-341 Crossref
Hansen A, Westgaard JI, Søvik G, Hanebrekke T and others (2021) Genetic differentiation between inshore and offshore populations of northern shrimp (Pandalus borealis). ICES J Mar Sci 78:3135-3146 Crossref
Hopkins C (2022) The bigger they are, the faster they fall. Implications of size selective fishing on the spawning stock of Pandalus borealis in the Svartnes basin (Balsfjord, northern Norway), as relates to size, age, growth, and abundance. MSc thesis, UiT The Arctic University of Norway, Tromsø
Hopkins CCE, Nilssen EM (1990) Population biology of the deep-water prawn (Pandalus borealis) in Balsfjord, northern Norway: I. Abundance, mortality, and growth, 1979-1983. J Cons Cons Int Explor Mer 47:148-166 Crossref
Hopkins CCE, Sargent JR, Nilssen EM (1993) Total lipid content, and lipid and fatty acid composition of the deep-water prawn Pandalus borealis from Balsfjord, northern Norway: growth and feeding relationships. Mar Ecol Prog Ser 96:217-228 Crossref
Irisarri J, Fernandez-Reiriz MJ, Labarta U, Cranford PJ, Robinson SMC (2015) Availability and utilization of waste fish feed by mussels Mytilus edulis in a commercial integrated multi-trophic aquaculture (IMTA) system: a multi-indicator assessment approach. Ecol Indic 48:673-686 Crossref
Jónasdóttir SH (2019) Fatty acid profiles and production in marine phytoplankton. Mar Drugs 17:151 PubMed Crossref
Madgett AS, Yates K, Webster L, McKenzie C, Moffat CF (2019) Understanding marine food web dynamics using fatty acid signatures and stable isotope ratios: improving contaminant impacts assessments across trophic levels. Estuar Coast Shelf Sci 227:106327 Crossref
Meier S, van der Meeren T, Skjæraasen JE, Bannister RJ, Rasinger JD, Karlsen Ø (2023) Terrestrial fatty acids from feed oil in feed for farmed salmonids are transferred to the liver, gonads, and muscle of wild Atlantic cod (Gadus morhua). ICES J Mar Sci 80:1143-1154 Crossref
Melaa KW, Zimmermann F, Søvik G, Thangstad TH (2022) Historic landings of northern shrimp (Pandalus borealis) in Norway: data per county for 1908-2021. Norw Inst Mar Res Rep No. 2022-24
Moe SJ, Hjermann DØ, Ravagnan E, Bechmann RK (2019) Effects of an aquaculture pesticide (diflubenzuron) on non-target shrimp populations: extrapolation from laboratory experiments to the risk of population decline. Ecol Modell 413:108833 Crossref
Nilssen EM, Larsen RB, Hopkins CCE (1986) Catch and size-selection of Pandalus borealis in a bottom trawl and implications for population dynamics analyses. ICES CM 1986/K:4
Olsen RE, Henderson RJ, Ringø E (1991) Lipids of arctic charr, Salvelinus alpinus (L.) 1. Dietary induced changes in lipid class and fatty-acid composition. Fish Physiol Biochem 9:151-164 PubMed Crossref
Olsen SA, Ervik A, Grahl-Nielsen O (2009) Deep-water shrimp (Pandalus borealis, Kroyer 1838) as indicator organism for fish-farm waste. J Exp Mar Biol Ecol 381:82-89 Crossref
Olsen SA, Ervik A, Grahl-Nielsen O (2012) Tracing fish farm waste in the northern shrimp Pandalus borealis (Kroyer, 1838) using lipid biomarkers. Aquacult Environ Interact 2:133-144 Crossref
Olsen RE, Taranger GL, Svåsand T, Skilbrei OT (2013) Improved method for triacylglycerol-derived fatty acid profiling by various non-lethal and lethal sampling techniques in Atlantic salmon. Aquacult Environ Interact 4:251-261 Crossref
Oug E, Høisœter T (2000) Soft-bottom macrofauna in the high-latitude ecosystem of Balsfjord, northern Norway: species composition, community structure and temporal variability. Sarsia 85:1-13 Crossref
Parkes RJ, Taylor J (1983) The relationship between fatty acid distributions and bacterial respiratory types in contemporary marine sediments. Estuar Coast Shelf Sci 16:173-189 Crossref
Parsons DG (2005) Predators of northern shrimp, Pandalus borealis (Pandalidae), throughout the North Atlantic. Mar Biol Res 1:48-58 Crossref
Pedersen T, Fuhrmann MM, Lindstrøm U, Nilssen EM and others (2018) Effects of the invasive red king crab on food web structure and ecosystem properties in an Atlantic fjord. Mar Ecol Prog Ser 596:13-31 Crossref
Redmond KJ, Magnesen T, Hansen PK, Strand Ø, Meier S (2010) Stable isotopes and fatty acids as tracers of the assimilation of salmon fish feed in blue mussels (Mytilus edulis). Aquaculture 298:202-210 Crossref
Sardenne F, Simard M, Robinson SMC, McKindsey CW (2020) Consumption of organic wastes from coastal salmon aquaculture by wild decapods. Sci Total Environ 711:134863 PubMed Crossref
Shumway SE, Perkins HC, Schick DF, Stickney AP (1985) Synopsis of biological data on the pink shrimp, Pandalus borealis Krøyer, 1838. NOAA Tech Rep NMFS 30
Søvik G, Nedreaas K, Zimmermann F, Husson B and others (2020) Kartlegging av fjordøkosystemene i Tana- og Porsangerfjorden. Råd og kunnskapsbidrag fra Havforskningsinstituttet i forbindelse med vurdering av en eventuell åpning av direktefiske etter reker med bunntrål i Tana- og Porsangerfjorden. Norw Inst Mar Res Rep No. 2020-39
Søvik G, Falkenhaug T, Zimmerman F, Gallo ND and others (2023) Toktrapport fra økosystemtokt i vestlandsfjordene. Hydrografi, vannkjemi, reker, krill, bunnfisk, tobis og perifylla. Norw Inst Mar Res Cruise Rep No. 11-2023
Svendsen H (1995) Physical oceanography of coupled fjord-coast systems in northern Norway with special focus on frontal dynamics and tides. In: Skjoldal HR, Hopkins C, Erikstad KE, Leinaas HP (eds) Ecology of fjords and coastal waters. Elsevier, Amsterdam, p 149-164
Urban P, Praebel K, Bhat S, Dierking J, Wangensteen OS (2022) DNA metabarcoding reveals the importance of gelatinous zooplankton in the diet of Pandalus borealis, a keystone species in the Arctic. Mol Ecol 31:1562-1576 PubMed Crossref
Walker EZ, Wiedmann I, Nikolopoulos A, Skarðhamar J, Jones EM, Renner AHH (2022) Pelagic ecosystem dynamics between late autumn and the post spring bloom in a sub-Arctic fjord. Elementa 10:00070 Crossref
Wassmann P, Svendsen H, Keck A, Reigstad M (1996) Selected aspects of the physical oceanography and particle fluxes in fjords of northern Norway. J Mar Syst 8:53-71 Crossref
White CA, Bannister RJ, Dworjanyn SA, Husa V, Nichols PD, Kutti T, Dempster T (2017) Consumption of aquaculture waste affects the fatty acid metabolism of a benthic invertebrate. Sci Total Environ 586:1170-1181 PubMed Crossref
White CA, Bannister RJ, Dworjanyn SA, Husa V, Nichols PD, Dempster T (2018) Aquaculture-derived trophic subsidy boosts populations of an ecosystem engineer. Aquacult Environ Interact 10:279-289 Crossref
Wienberg R (1981) On the food and feeding habits of Pandalus borealis Krøyer 1838. Arch FischWiss 31:123-137
Woodcock SH, Troedsson C, Strohmeier T, Balseiro P, Skaar KS, Strand Ø (2017) Combining biochemical methods to trace organic effluent from fish farms. Aquacult Environ Interact 9:429-443 Crossref
Woodcock SH, Strohmeier T, Strand Ø, Olsen SA, Bannister RJ (2018) Mobile epibenthic fauna consume organic waste from coastal fin-fish aquaculture. Mar Environ Res 137:16-23 PubMed Crossref
Woodcock SH, Meier S, Keeley NB, Bannister RJ (2019) Fate and longevity of terrestrial fatty acids from caged fin-fish aquaculture in dynamic coastal marine systems. Ecol Indic 103:43-54 Crossref
Ytrestøyl T, Aas TS, Åsgard T (2015) Utilisation of feed resources in production of Atlantic salmon (Salmo salar) in Norway. Aquaculture 448:365-374 Crossref
Zimmermann F, Nedreaas K, Thangstad TH, Søvik G (2021) Kartlegging av bunnfisk og reker på rekefelt i vestlandsfjorder (toktnummer 2021854). Norw Inst Mar Res Cruise Rep No. 16-2021
Guldborg Søvik (Corresponding Author)
- Institute of Marine Research, Nordnesgaten 50, 5005 Bergen, Norway
Siri Olsen (Co-author)
- Institute of Marine Research, Nordnesgaten 50, 5005 Bergen, Norway
Agneta Hansen (Co-author)
- Institute of Marine Research, Framsenteret, Hjalmar Johansens gate 14, 9007 Tromsø, Norway
Stian Stiansen (Co-author)
- Institute of Marine Research, Nye Flødevigveien 20, 4817 His, Norway
Einar Nilssen (Co-author)
- Institute of Marine Research, Framsenteret, Hjalmar Johansens gate 14, 9007 Tromsø, Norway
- Department of Arctic and Marine Biology, UiT The Arctic University of Norway, 9019 Tromsø, Norway
Pål Bjørn (Co-author)
- Institute of Marine Research, Framsenteret, Hjalmar Johansens gate 14, 9007 Tromsø, Norway
Sonnich Meier (Co-author)
- Institute of Marine Research, Nordnesgaten 50, 5005 Bergen, Norway
Handling Editor:
Adam Hughes, Oban, UK
Reviewers:
V. A. Laudicella and 1 anonymous referee
Acknowledgements:
The study was funded by Troms and Finnmark counties through the project ‘Coexistence fishery and aquaculture: effects of salmon farming on shrimp and cod—Coexist’ (contract FHAV-2019-082) as well as by the Norwegian Ministry of Trade, Industry and Fisheries through the Norwegian Institute of Marine Research project ‘Coastal shellfish resources’ in the research program Coastal Ecosystems. The Norwegian Research Council projects ‘Assessing cumulative impacts on the Norwegian coastal ecosystem and its services—CoastRisk’ (project no. 299554) and ‘Impacts of salmon farming on Atlantic cod stocks—Salcod’ (project no. 29463) are also thanked for funding. Eskil Dahl Olaussen was responsible for collecting shrimp samples during the 2 UiT surveys. We thank the technical staff at the Flødevigen research station for their assistance in laboratory work during the feeding experiment. The authors also thank Therese Smith-Jahnsen Aase and Arve Fossen for technical assistance with the lipid analysis and 2 anonymous referees for constructive and useful comments on an earlier version of the manuscript.
