Hostname: page-component-848d4c4894-4rdrl Total loading time: 0 Render date: 2024-07-02T09:19:31.909Z Has data issue: false hasContentIssue false

Temporal changes in lipid biomarkers, especially fatty acids, of the deep-sea crustaceans Boreomysis arctica and Nematoscelis megalops: implications of their biological cycle and habitat near the seabed

Published online by Cambridge University Press:  23 December 2010

J.E. Cartes*
Affiliation:
Institut de Ciències del Mar (ICM-CSIC), Passeig Marítim de la Barceloneta 37–49, Spain
*
Correspondence should be addressed to: J.E. Cartes, Institut de Ciències del Mar (ICM-CSIC), Postgrau Marítim de la Barceloneta 37–49, Spain email: jcartes@cmima.csic.es

Abstract

Two species of benthopelagic deep-water crustaceans, the suprabenthic mysid Boreomysis arctica and the bathypelagic euphausiid Nematoscelis megalops were analysed in their lipidic composition, with especial emphasis on fatty acids, from specimens obtained in the north-west of Mallorca (Balearic Islands, western Mediterranean) at depths ranging between 650 and 780 m. Temporal shifts were studied seasonally, based on five cruises performed in August and November 2003, and February, April and June 2004, using a Macer-GIROQ suprabenthic sledge (0.5 mm mesh size). Evidences of omnivorous and carnivorous feeding habits were found for both species derived from their fatty acid and other lipid profiles. Boreomysis arctica showed a more varied fatty acid profile than N. megalops. This suggests that B. arctica feeds on a wider range of food sources and is a more opportunistic feeder. The high proportions of 16:1(n-7), 20:5(n-3) and 22:6(n-3) fatty acids in both species suggests a link between surface primary production and deep slope habitats, while markers such as 18:1(n-9) and the 20:1(n-9) and 22:1(n-11) fatty alcohols indicate a predatory activity, likely on calanoids. These components may arrive both via phytodetritus deposition to the seabed and by migratory movements of prey consumed by B. arctica and N. megalops close to the sea bottom. Seasonal changes in the total lipids and fatty acid composition of both species are related to the seasonal dynamics in their food sources, coupled with changes in the physiological or developmental stage of individuals. The proportion of total lipids and polyunsaturated fatty acids in the two species may be related to the different life histories of B. arctica and N. megalops. The mysid has direct development of embryos within brood pouches, so eggs with large amount of vitelum are generated and gonad is well developed. By contrast, the meso-bathypelagic euphausiids generate planktotrophic larvae, with a high number of free developmental larvae stages (from nauplius to Furcilia/Calyptopis), and eggs with poor storage of lipid compounds compared with B. arctica embryos.

Type
Research Article
Copyright
Copyright © Marine Biological Association of the United Kingdom 2010

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

Albers, C.S., Kattner, G. and Hagen, W. (1996) The compositions of wax esters, triacylglycerols and phospholipids in Arctic and Antarctic copepods: evidence of energetic adaptations. Marine Chemistry 55, 347358.CrossRefGoogle Scholar
Andersen, V., Devey, C., Gubanovai, A., Picheral, M., Melniko, V., Tsarin, S. and Prieura, L. (2004) Vertical distributions of zooplankton across the Almeria–Oran frontal zone (Mediterranean Sea). Journal of Plankton Research 26, 275293.CrossRefGoogle Scholar
Auel, H., Harjes, M., da Rocha, R., Stübing, D. and Hagen, W. (2002) Lipid biomarkers indicate different ecological niches and trophic relationships of the Arctic hyperiid amphipods Themisto abyssorum and T. libellula. Polar Biology 25, 374383.CrossRefGoogle Scholar
Barangé, M., Gibbons, M.J. and Carola, M. (1991) Diet and feeding of Euphausia hanseni and Nematoscelis megalops (Euphausiacea) in the Northern Benguela Current: ecological significance of vertical space partitioning. Marine Ecology Progress Series 73, 173181.CrossRefGoogle Scholar
Brett, M.T and Müller-Navarra, D.C. (1997) The role of highly unsaturated fatty acids in aquatic foodweb processes. Freshwater Biology 38, 483499.CrossRefGoogle Scholar
Bühring, S.I. and Christiansen, B. (2001) Lipids in selected abyssal benthopelagic animals: links to the epipelagic zone? Progress in Oceanography 50, 369382.CrossRefGoogle Scholar
Cartes, J.E. and Sorbe, J.C. (1998) Aspects of population structure and feeding ecology of the deep-water mysids Boreomysis arctica, a dominant species in western Mediterranean slope assemblages. Journal of Plankton Research 20, 22732290.CrossRefGoogle Scholar
Cartes, J.E. and Maynou, F. (2001) Trophodynamics of the deep-water suprabenthic mysid Boreomysis arctica in the Catalan Sea (western Mediterranean). Marine Ecology Progress Series 211, 225234.CrossRefGoogle Scholar
Cartes, J.E. and Carrassón, M. (2004) The influence of trophic variables in the depth-range distribution and zonation rates of deep-sea megafauna: the case of the western Mediterranean assemblages. Deep-Sea Research I 51, 263279.CrossRefGoogle Scholar
Cartes, J.E., Brey, T., Sorbe, J.C. and Maynou, F. (2002) Comparing production–biomass ratios of benthos and suprabenthos in macrofaunal marine crustaceans. Canadian Journal of Fisheries and Aquatic Sciences 59, 16161625.CrossRefGoogle Scholar
Cartes, J.E., Jaume, D. and Madurell, T. (2003) Local changes in the composition and community structure of suprabenthic peracarid crustaceans on the bathyal Mediterranean: influence of environmental factors. Marine Biology 143, 745758.CrossRefGoogle Scholar
Cartes, J.E., Maynou, F., Moranta, J., Massutí, E., Lloris, D. and Morales-Nin, B. (2004) Changes in the patterns of bathymetric distribution among deep-sea fauna at local spatial scale: comparison of mainland vs. insular areas. Progress in Oceanography 60, 2945.CrossRefGoogle Scholar
Cartes, J.E., Madurell, T., Fanelli, E. and López-Jurado, J.L. (2008) Dynamics of suprabenthos and zooplankton around Mallorca (Balearic Islands, NW Mediterranean): influence of environmental variables and effect on higher trophic levels. Journal of Marine Systems 71, 316335.CrossRefGoogle Scholar
Cartes, J.E., Fanelli, E., Papiol, V. and Zucca, L. (2010) Distribution and diversity of open-ocean, near-bottom macroplankton in the western Mediterranean: analysis at different spatio-temporal scales. Deep-Sea Research I, 57, 14851498.CrossRefGoogle Scholar
Casanova, B. (1974) Les euphasiaces de Mediterranée. Systématique et développment larvaire. Biogeography et biologie. Université de Provence (Aix-Marseille I), CNRS A0 9446.Google Scholar
Clarke, K.R. and Warwick, R.M. (1995) Change in marine communities: an approach to statistical analysis and interpretation. Plymouth: Natural Environment Research Council, UK, 144 pp.Google Scholar
Cook, E.J., Bell, M.V., Black, K.D. and Kelly, M.S. (2000) Fatty acid composition of gonadal material and diets of the sea urchin, Psammechinus miliaris: trophic and nutritional implications. Journal of Experimental Marine Biology and Ecology 255, 261274.CrossRefGoogle ScholarPubMed
Cook, E.J., Shucksmith, R., Orr, H., Ashton, G.V. and Berge, J. (2010) Fatty acid composition as a dietary indicator of the invasive caprellid, Caprella mutica (Crustacea: Amphipoda). Marine Biology 157, 1927.CrossRefGoogle Scholar
Cripps, G.C. and Atkinson, A. (2000) Fatty acid composition as an indicator of carnivory in Antarctic krill, Euphasia superba. Canadian Journal of Fisheries and Aquatic Sciences 57, 3137.CrossRefGoogle Scholar
Dalsgaard, J., St John, M., Kattner, G., Muller-Navarra, D. and Hagen, W. (2003) Fatty acid trophic markers in the pelagic marine environment. Advances in Marine Biology 46, 225340.CrossRefGoogle ScholarPubMed
Estrada, M., Vives, F. and Alcaraz, M. (1985) Life and the productivity of the Open Ocean. In Margalef, R. (ed.) Western Mediterranean (key environments). Oxford: Pergamon Press, pp. 198232.Google Scholar
Falk-Petersen, S., Hagen, W., Kattner, G., Clarke, A. and Sargent, J. (2000) Lipids, trophic relationships, and biodiversity in Arctic and Antarctic krill. Canadian Journal of Fisheries and Aquatic Sciences 57 (Supplement 3), 178191.CrossRefGoogle Scholar
Fanelli, E., Cartes, J.E., Rumolo, P. and Sprovieri, M. (2009) Food web structure and trophodynamics of mesopelagic–suprabenthic bathyal macrofauna of the Algerian basin (Western Mediterranean) based on stable isotopes of carbon and nitrogen. Deep-Sea Research I 56, 15041520.CrossRefGoogle Scholar
García-Guerra, J.M., Martínez-Pita, I. and Pita, M.L. (2004) Fatty acid composition of the Caprellidea (Crustacea: Amphipoda) from the Strait of Gibraltar. Scientia Marina 68, 501510.CrossRefGoogle Scholar
Graeve, M., Kattner, G. and Hagen, W. (1994a) Diet-induced changes in the fatty acid composition of Arctic herbivorous copepods: experimental evidence of trophic markers. Journal of Experimental Marine Biology and Ecology 182, 97110.CrossRefGoogle Scholar
Graeve, M., Hagen, W. and Kattner, G. (1994b) Herbivorous or omnivorous? On the significance of lipid compositions as trophic markers in Antarctic copepods. Deep-Sea Research 41, 915924.CrossRefGoogle Scholar
Gurney, L.J., Froneman, P.W., Pakhomov, E.A. and McQuaid, C.D. (2001) Trophic positions of three euphausiid species from the Prince Edward Islands (Southern Ocean): implications for the pelagic food web structure. Marine Ecology Progress Series 217, 167174.CrossRefGoogle Scholar
Hagen, W. and Kattner, G. (1998) Lipid metabolism of the Antarctic euphausiid Thysanoessa macrura and its ecological implications. Limnology and Oceanography 43, 18941901.CrossRefGoogle Scholar
Hagen, W., Kattner, G., Terbrüggen, A. and Van Vleet, E.S. (2001) Lipid metabolism of the Antarctic krill Euphausia superba and its ecological implications. Marine Biology 139, 95104.CrossRefGoogle Scholar
Hudson, I.R., Pond, D.W., Billett, D.S.M., Tyler, P.A., Lampitt, R.S. and Wolff, G.A. (2004) Temporal variations in fatty acid composition of deep-sea holothurians: evidence of bentho-pelagic coupling. Marine Ecology Progress Series 281, 109120.CrossRefGoogle Scholar
Jeffreys, R.M., Wolff, G.A. and Murty, S.J. (2009) The trophic ecology of key megafaunal species at the Pakistan Margin: evidence from stable isotopes and lipid biomarkers. Deep-Sea Research I 56, 18161833.CrossRefGoogle Scholar
Ju, S. and Harvey, H.R. (2004) Lipids as markers of nutritional condition and diet in the Antarctic krill Euphausia superba and Euphausia crystallorophias during austral winter. Deep-Sea Research II 51, 21992214.CrossRefGoogle Scholar
Kharlamenko, V.I., Zhukova, N.V., Khotimchenko, S.V., Svetashev, V.I. and Kamenev, G.M. (1995) Fatty acids as markers of food sources in a shallow-water hydrothermal ecosystem (Kraternaya Bight, Yankich Island, Kurile Islands). Marine Ecology Progress Series 120, 231241.CrossRefGoogle Scholar
Kiriakoulakis, K., Stutt, E., Rowland, S.J., Vangriesheim, A., Lampitt, R.S. and Wolff, G.A. (2001) Controls on the organic chemical composition of settling particles in the Northeast Atlantic Ocean. Progress in Oceanography 50, 6587.CrossRefGoogle Scholar
Kiriakoulakis, K., White, M., Bett, B.J. and Wolff, G.A. (2004) Organic biogeochemistry of the Darwin Mounds, a deep-water coral ecosystem, of the NE Atlantic. Deep-Sea Research I 51, 19371954.CrossRefGoogle Scholar
Lee, R.F., Hagen, W. and Kattner, G. (2006) Lipid storage in marine zooplankton. Marine Ecology Progress Series 307, 273306.CrossRefGoogle Scholar
Madurell, T., Fanelli, E. and Cartes, J.E. (2008) Isotopic composition of carbon and nitrogen of suprabenthos fauna in the NW Balearic Islands (western Mediterranean). Journal of Marine Systems 71, 336345.CrossRefGoogle Scholar
Mauchline, J. (1980) The biology of mysids and euphausiids. Advances in Marine Biology 18, 1681.Google Scholar
Mayzaud, P., Boutoute, M. and Alonzo, F. (2003) Lipid composition of the euphausiids Euphausia vallentini and Thysanoessa macrura during summer in the Southern Indian Ocean. Antarctic Science 15, 463475.CrossRefGoogle Scholar
Mees, J. and Jones, M.B. (1997) The hyperbenthos. Oceanography and Marine Biology: an Annual Review 35, 221255.Google Scholar
Miquel, J.C., Fowler, S.W., La Rosa, J. and Buat-Menard, P. (1994) Dynamics of the downward flux of particles and carbon in the open northwestern Mediterranean Sea. Deep-Sea Research 41, 243261.CrossRefGoogle Scholar
Nelson, M.M., Mooney, B.D., Nichols, P.D. and Phleger, C.F. (2001) Lipids of Antarctic Ocean amphipods: food chain interactions and the occurrence of novel biomarkers. Marine Chemistry 73, 5364.CrossRefGoogle Scholar
Nyssen, F., Brey, T., Dauby, P. and Graeve, M. (2005) Trophic position of Antarctic amphipods—enhanced analysis by a 2-dimensional biomarker assay. Marine Ecology Progress Series 300, 135145.CrossRefGoogle Scholar
Phleger, C.F., Nelson, M.M., Mooney, B.D. and Nichols, P.D. (2002) Interannual and between species comparison of the lipids, fatty acids and sterols of Antarctic krill from the US AMLR Elephant Island survey area. Comparative Biochemistry and Physiology Part B 131, 733747.CrossRefGoogle ScholarPubMed
Polunin, N.V.C., Morales-Nin, B., Pawsey, W.E., Cartes, J.E., Pinnegar, J.K. and Moranta, J. (2001) Feeding relationships in Mediterranean bathyal assemblages elucidated by stable nitrogen and carbon isototpe data. Marine Ecology Progress Series 220, 1323.CrossRefGoogle Scholar
Richoux, N., Deibel, D., Thompson, R.J. and Parrish, C.C. (2005) Seasonal and developmental variation in the fatty acid composition of Mysis mixta (Mysidacea) and Acanthostepheia malmgreni (Amphipoda) from the hyperbenthos of a cold-ocean environment (Conception Bay, Newfoundland). Journal of Plankton Research 27, 719733.CrossRefGoogle Scholar
Sainte-Marie, B. and Brunel, P. (1985) Suprabenthic gradients of swimming activity by cold-water gammaridean amphipod Crustacea over a muddy shelf in the Gulf of Saint Lawrence. Marine Ecology Progress Series 23, 5769.CrossRefGoogle Scholar
Saito, H., Kotani, Y., Keriko, J.M., Xue, C., Taki, K., Ishihara, K., Ueda, T. and Miyata, S. (2002) High levels of n-3 polyunsaturated fatty acids in Euphausia pacifica and its role as a source of docosahexaenoic and icosapentaenoic acids for higher trophic levels. Marine Chemistry 78, 928.CrossRefGoogle Scholar
Sano, M., Omori, M. and Taniguchi, K. (2003) Predator–prey systems of drifting seaweed communities of the Tohoku coast, northern Japan, as determined by feeding habit analysis of phytal animals. Fisheries Science 69, 260268.CrossRefGoogle Scholar
Sargent, J.R. and Henderson, R.J. (1986) Lipids. In Corner, E.D.S. and O'Hara, S.C.M. (eds) The biological chemistry of marine copepods. Oxford: Clarendon Press, pp. 59108.Google Scholar
Sargent, J.R., Parkes, R.J., Mueller-Harvey, I. and Henderson, R.J. (1987) Lipid biomarkers in marine ecology. In Sleigh, M.A. (ed.) Microbes in the sea. Chichester: Ellis Horwood, pp. 119138.Google Scholar
Scott, C.L., Falk-Petersen, S., Sargent, J.R., Hop, H., Lonne, O.J. and Poltermann, M. (1999) Lipids and trophic interactions of ice fauna and pelagic zooplankton in the marginal ice zone of the Barents Sea. Polar Biology 21, 6570.CrossRefGoogle Scholar
Stübing, D. and Hagen, W. (2003) Fatty acid biomarker ratios—suitable trophic indicators in Antarctic euphausiids? Polar Biology 26, 774782.CrossRefGoogle Scholar
Suhr, S.B., Pond, D.W., Gooday, A.J. and Smith, C.R. (2003) Selective feeding by benthic foraminifera on phytodetritus on the western Antarctic Peninsula shelf: evidence from fatty acid biomarker analysis. Marine Ecology Progress Series 262, 153162.CrossRefGoogle Scholar
Tyler, P.A. (2003) The peripheral seas. In Tyler, P.A. (ed.) Ecosystems of the deep ocean. Amsterdam: Elsevier, pp. 261295.Google Scholar
Virtue, P., Mayzaud, P., Nichols, P.D. and Albessard, E. (2000) The use of fatty acids as dietary indicators in krill, Meganyctiphanes norvegica from the north-eastern Atlantic, Kattegat and Mediterranean during summer and winter. Canadian Journal of Fisheries and Aquatic Sciences 57, 107114.CrossRefGoogle Scholar
Werner, I. and Auel, H. (2005) Seasonal variability in abundance, respiration and lipid composition of Arctic under-ice amphipods. Marine Ecology Progress Series 292, 251262.CrossRefGoogle Scholar