Feeding strategy assessment through fatty acid profiles in muscles of adult sea lampreys from the western Iberian coast

Authors

  • Maria João Lança School of Science and Technology, Department of Animal Science, University of Évora - Institute of Mediterranean Agricultural and Environmental Sciences (ICAAM), University of Évora
  • Maria Machado Institute of Mediterranean Agricultural and Environmental Sciences (ICAAM), University of Évora
  • Rui Ferreira Institute of Mediterranean Agricultural and Environmental Sciences (ICAAM), University of Évora - School of Science and Technology, Department of Chemistry, University of Évora
  • Isabel Alves-Pereira Institute of Mediterranean Agricultural and Environmental Sciences (ICAAM), University of Évora - School of Science and Technology, Department of Chemistry, University of Évora
  • Bernardo Ruivo Quintella Center of Oceanography, Faculty of Sciences of the University of Lisbon - Department of Animal Biology, Faculty of Sciences of the University of Lisbon
  • Pedro Raposo de Almeida Center of Oceanography, Faculty of Sciences of the University of Lisbon - School of Science and Technology, Department of Biology, University of Évora

DOI:

https://doi.org/10.3989/scimar.03779.27B

Keywords:

Petromyzon marinus, feeding strategies, marine phase, fatty acids, Portugal

Abstract


The fatty acid signature of sea lamprey Petromyzon marinus (L.) muscle was used as a tool to detect feeding strategies used during the parasitic marine trophic phase of the species. Adult sea lampreys were collected near the mouth of six Portuguese rivers (Minho, Lima, Douro, Vouga, Mondego and Tagus) and muscle fatty acid profile was characterized. The analysis of fatty acid composition of muscle neutral lipids showed the formation of two groups, indicating that two feeding strategies may have been used by sea lampreys during the parasitic phase, based on the availability of ω-3 and ω-6 PUFA and on evidence of phytoplankton/zooplankton and bacterial detritus contribution in the sea lamprey host preferences. Two distinct lipid profiles were observed, probably related to two different trophic approaches, one typical of a top predator of a marine food web with a planktonic support, and the other much more diverse, including the same planktonic markers, together with biochemical clues that probably resulted from a parasitic phase that directly targeted fish that consumed detritus and benthic algae and/or fish from a food web with a detritivorous base.

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References

Ackman R.G. 1999. Comparison of lipids in marine and freshwater organisms. In: Arts M.T., Wainman B.C. (eds), Lipids in Freshwater Ecosystems, Springer-Verlag, New York, pp. 263-298. http://dx.doi.org/10.1007/978-1-4612-0547-0_12

Ackman R.G. 2002. The gas chromatograph in practical analysis of common and uncommon fatty acids for the 21st century. Anal. Chem. Acta 465: 175-192. http://dx.doi.org/10.1016/S0003-2670(02)00098-3

Adams S.M. 1999. Ecological role of lipids in the health and success of fish populations. In: Arts M.T., Wainman B.C. (eds), Lipids in Freshwater Ecosystems, Springer-Verlag, New York, pp. 123-160. http://dx.doi.org/10.1007/978-1-4612-0547-0_8 PMid:10200923

Almeida P.R., Moreira F., Costa J.L., Assis C.A., Costa M.J. 1993. The feeding strategies of Liza ramada (Risso, 1826) in fresh and brackish water in the River Tagus, Portugal. J. Fish Biol. 42: 95-109. http://dx.doi.org/10.1111/j.1095-8649.1993.tb00308.x

Anderson M.J., ter Braak C.J.F. 2003. Permutation tests for multifactorial analysis of variance. J. Stat. Comput. Simul. 73: 85-113. http://dx.doi.org/10.1080/00949650215733

Araújo M.J.F.S. 2011. Ecology and nutritional composition of the sea lamprey (Petromyzon marinus Linnaeus, 1758) in the River Minho's international stretch. MSc thesis. Institute of Biomedical Sciences Abel Salazar, University of Oporto, Oporto, 102 pp.

Beamish F.W.H. 1980. Biology of the North American anadromous sea lamprey. Can. J. Fish. Aquat. Sci. 37: 1924-1943. http://dx.doi.org/10.1139/f80-233

Bell M.V., Henderson R.J., Sargent J.R. 1986. The role of polyunsaturated fatty acids in fish. Comp. Biochem. Physiol. 83B: 711-719.

Bird D.J., Potter I.C. 1983. Changes in the fatty acid composition of triacylglycerols and phospholipids during the life cycle of the lamprey Geotria australis Gray. Comp. Biochem. Physiol. 75 B: 31-41.

Bird D.J., Ellis D.J., Potter I.C. 1993. Comparisons between the fatty acid composition of the muscle and ovary of the nonparasitic lamprey Lampetra planeri (Bloch) and their counterparts in the anadromous and parasitic Lampetra fluviatilis (L.). Comp. Biochem. Physiol. 105B: 327-332.

Brett M.T., Muller-Navarra D.C., Persson J. 2009. Crustacean zooplankton fatty acid composition. In: M.T. Arts, M. Brett and M. Kainz, (eds), Lipids in Aquatic Ecosystems, Springer, New York, pp. 115-146. http://dx.doi.org/10.1007/978-0-387-89366-2_6

Budge S.M., Iverson S.J., Koopman H.N. 2006. Studying trophic ecology in marine ecosystems using fatty acids: a primer on analysis and interpretation. Mar. Mammal Sci. 22: 759-801. http://dx.doi.org/10.1111/j.1748-7692.2006.00079.x

Cabral M.J., Almeida J., Almeida P.R., Dellinger T., Ferrand de Almeida N., Oliveira M.E., Palmeirim J.M., Queiroz A.I., Rogado L., Santos-Reis M. (eds). 2005. Livro vermelho dos vertebrados de Portugal. Instituto de Conservação da Natureza, Lisbon, 660 pp.

Clarke K.R. 1993. Non-parametric multivariate analysis of changes in community structure. Am. J. Ecol. 18: 117-143.

Dalsgaard J., St John M., Kattner G., Muller-Navarra D., Hagen W. 2003. Fatty acid trophic markers in the pelagic marine environment. Adv. Mar. Biol. 46: 225-340. http://dx.doi.org/10.1016/S0065-2881(03)46005-7

Doadrio I. 2001. Atlas y libro rojo de los peces continentales de Espa-a. Dirección General de Conservación de la Naturaleza, Museo Nacional de Ciencias Naturales, Madrid, 364 pp. PMCid:PMC1088741

Drevnick P.E., Horgan M., Oris J., Kynard B.E. 2006. Ontogenic dynamics of mercury accumulation in Northwest Atlantic sea lamprey (Petromyzon marinus). Can. J. Fish. Aquat. Sci. 63: 1058-1066. http://dx.doi.org/10.1139/f06-012

Dunn M.R., Szabo A., McVeagh M.S., Smith P.J. 2010. The diet of deepwater sharks and the benefits of using DNA identification of prey. Deep-Sea Res. Pt. I 57: 923-930. http://dx.doi.org/10.1016/j.dsr.2010.02.006

Falk-Petersen S., Dahl T.M., Scott C.I., Sargent J.R., Gulliksen B., Kwasniewski S., Hop H., Millar R. 2002. Lipid biomarkers and trophic linkages between ctenophores and copepods in Svalbard waters. Mar. Ecol. Progr. Ser. 227: 187-194. http://dx.doi.org/10.3354/meps227187

Farmer G.J. 1980. Biology and physiology of feeding in adult lampreys. Can. J. Fish. Aquat. Sci. 37: 1751-1760. http://dx.doi.org/10.1139/f80-220

Freyhof J., Brooks E. 2011. European Red List of freshwater fishes. Publications Office of the European Union, Luxembourg, 61 pp.

Freyhof J., Kottelat M. 2008. Petromyzon marinus. In: IUCN 2012. IUCN Red List of Threatened Species. Version 2012.2. <www.iucnredlist.org> (accessed on 05 April 2013).

Gallant J., Harvey-Clark C., Myers R.A., Stokesbury M.J.W. 2006. Sea lamprey attached to a Greenland Shark in the St. Lawrence Estuary, Canada. NE. Naturalist 13: 35-38.

Haedrich R.C. 1977. A sea lamprey from the deep ocean. Copeia 4: 767-768. http://dx.doi.org/10.2307/1443185

Halliday R.C. 1991. Marine distribution of the sea lamprey (Petromyzon marinus) in the Northwest Atlantic. Can. J. Fish. Aquat. Sci. 48: 832-842. http://dx.doi.org/10.1139/f91-099

Hendersen R.J., Sargent J.R. 1981. Lipid biosynthesis in rainbow trout Salmo gairdnerii, fed diets of differing lipid content. Comp. Biochem. Physiol. 69C: 31-37.

Henderson R.J., Tocher D.R. 1987. The lipid composition and biochemistry of freshwater fish. Prog. Lipid Res. 26: 281-347. http://dx.doi.org/10.1016/0163-7827(87)90002-6

Iverson S.J. 2009. Tracing aquatic food webs using fatty acids: from qualitative indicators to quantitative determination. In: Arts M.T., Brett M., Kainz M. (eds), Lipids in Aquatic Ecosystems, Springer, New York, pp. 281-307. http://dx.doi.org/10.1007/978-0-387-89366-2_12

IUCN France, MNHN, SFI, ONEMA 2010. La liste rouge des espèces menacées en France—poissons d'eau douce de France métropolitaine. IUCN, Paris. Available at www.uicn.fr/IMG/pdf/Liste_rouge_France_Poissonsd_eau_douce_de_metropole.pdf

Japha A. 1910. Weitere Beiträge zur Kenntnis der Walhaut. Zool. Jahrb. 12: 711-718.

Jensen C., Schwartz F.J. 1994. Atlantic Ocean occurrences of the sea lamprey, Petromyzon marinus (Petromyzontiformes, Petromyzontidae), parasitizing sand-bar, Carcharhinus plumbeus, and dusky, C. obscurus (Carcharhiniformes: Carcharhinidae), sharks off North and South Carolina. Brimleyana 21: 69-72.

Jensen C., Schwartz F.J., Hopkins G. 1998. A sea lamprey (Petromyzon marinus)-tiger shark (Galeocerdo cuvier) parasitic relationship off North Carolina. J. Elisha Mitchell Scient. Soc. 114: 72-73.

Johns, R.B., Nichols P.D., Perry G.J. 1979. Fatty acid composition of ten marine algae from Australian waters. Phytochemistry 18: 799-802. http://dx.doi.org/10.1016/0031-9422(79)80018-7

Kaiser K.L.E., Esterby S.R. 1991. Regression and cluster analysis of the acute toxicity of 207 chemicals to six species of biota and octanol/water partition coefficient. Sci. Total Environ. 109-110: 499-514. http://dx.doi.org/10.1016/0048-9697(91)90204-R

Käkelä R., Hyvärinen H., Vainiotalo P. 1993. Fatty acid composition in liver and blubber of the Saimaa ringed seal (Phoca hispida saimensis) compared with that of the ringed seal (Phoca hispid botnica) and grey seal (Halichoerus grypus) from the Baltic. Comp. Biochem. Physiol. 105B: 553-565.

Kaneda T. 1991. Isoand Anteiso-Fatty Acids in Bacteria: Biosynthesis, Function, and Taxonomic Significance. Microbiol. Rev. 55: 288-302. PMid:1886522 PMCid:PMC372815

Khotimchenko S.V., Vaskousky V.E. 1990. Distribution of C20 polyenoic fatty acids in red macrophytic algae. Bot. Mar. 33: 525-528. http://dx.doi.org/10.1515/botm.1990.33.6.525

Kozlova T.A., Khotimchenko S.V. 2000. Lipids and fatty acids of two pelagic cottoid fishes (Comephorus spp) endemic to Lake Baikal. Comp. Biochem. Physiol. 126B: 477-485.

Lança M.J., Rosado C., Machado M., Ferreira R., Alves-Pereira I., Quintella B.R., Almeida P.R. 2011. Can muscle fatty acid signature be used to distinguish diets during the marine trophic phase of sea lamprey (Petromyzon marinus, L.)? Comp. Biochem. Physiol. 159B: 26-39.

Laposata M. 1998. Fatty acid ethyl esters: ethanol metabolites with mediate ethanol-induced organ damage and serve as markers of ethanol intake. Prog. Lipid Res. 37: 307-316. http://dx.doi.org/10.1016/S0163-7827(98)00013-7

Larsen L.O. 1980. Physiology of adult lampreys, with special regard to natural starvation, reproduction, and death after spawning. Can. J. Fish. Aquat. Sci. 37: 1762-1777. http://dx.doi.org/10.1139/f80-221

Lechevalier M.P. 1982. Lipids in bacterial taxonomy. In: Laskin A.I., Lechevalier H.A. (eds), CRC Handbook of Microbiology, CRC Press, Inc. Boca Raton, Florida, pp. 435-541.

Leger C., Fremont L., Boudon M. 1981. Fatty acid composition of the lipids in the trout – I. Influence of dietary fatty acids on the triglyceride fatty acid desaturation in serum, adipose tissue, liver, white and red muscle. Comp. Biochem. Physiol. 69 B: 99-105.

Mansueti J. 1962. Distribution of small, newly metamorphosed sea lampreys, Petromyzon marinus, and their parasitism on menhaden, Brevoortia tyrannus, in mid-Chesapeake Bay during winter months. Chesapeake Sci. 3: 137-139. http://dx.doi.org/10.2307/1351229

Mateus C.S., Rodríguez-Mu-oz R., Quintella B.R., Alves M.J., Almeida P.R. 2012. Lampreys of the Iberian Peninsula: distribution, population status and conservation. Endang. Spec. Res. 16: 183-198. http://dx.doi.org/10.3354/esr00405

Mayzaud P., Chanut J.P., Ackman R.G. 1989. Seasonal changes of the biochemical composition of marine particulate matter with special reference to fatty acids and sterols. Mar. Ecol. Prog. Ser. 56: 189-204. http://dx.doi.org/10.3354/meps056189

Morrison W.R., Smith L.M. 1964. Preparation of fatty acid methyl esters and dimethylacetals from lipids with boron fluoridemethanol. J. Lipid Res. 5: 600-608. PMid:14221106

Muri G., Wakeham S.G., PeaseT.K., Fanganeli J. 2004. Evaluation of lipid biomarkers as indicators of changes in organic matter delivery to sediments from Lake Planina, a remote mountain lake in NW Slovenia. Org. Geochem. 35: 1083-1093. http://dx.doi.org/10.1016/j.orggeochem.2004.06.004

Napolitano G.E. 1999. Fatty acids as trophic and chemical markers in freshwater ecosystems. In: Arts M.T., Wainman B.C. (eds), Lipids in Freshwater Ecosystems, Springer-Verlag, New York, pp. 21-44. http://dx.doi.org/10.1007/978-1-4612-0547-0_3

Nichols O.C., Hamilton P.K. 2004. Occurrence of the parasitic sea lamprey, Petromyzon marinus, on western North Atlantic right whales, Eubalaena glacialis. Environ. Biol. Fishes 71: 413-417. http://dx.doi.org/10.1007/s10641-004-0776-5

Nichols O.C., Tscherter U.T. 2011. Feeding of sea lampreys Petromyzon marinus on minke whales Balaenoptera acutorostrata in the St Lawrence Estuary, Canada. J. Fish Biol. 78: 338-343. http://dx.doi.org/10.1111/j.1095-8649.2010.02842.x PMid:21235565

Orlov A.M., Savinykh V.F., Pelenev D.V. 2008. Features of spatial distribution and size composition of Pacific lamprey Lampetra tridentata in the North Pacific. Russ. J. Mar. Biol. 34: 276-287. http://dx.doi.org/10.1134/S1063074008050039

Parrish C.C., Abrajano T.A., Budge S.M., Helleur R.J., Hudson E.D., Pulchan K., Ramos C. 2000. Lipid and phenolic biomarkers in marine ecosystems: analysis and applications. In: Wangersky P. (ed.), The Handbook of Environmental Chemistry Part D, Marine Chemistry, Springer-Verlag, Berlin Heidelberg, pp. 193-223.

Pinela S., Quintella B.R., Almeida P.R., Lança M.J. 2009. Comparison of the fatty acid profile of muscle neutral lipids and phospholipids of up-river anadromous sea lamprey (Petromyzon marinus L.) from three Portuguese river basins. Sci. Mar. 73: 785-795. http://dx.doi.org/10.3989/scimar.2009.73n4785

Plisetskaya E. 1980. Fatty acid levels in blood of cyclostomes and fish. Environ. Biol. Fish 5: 273-290. http://dx.doi.org/10.1007/BF00005363

Potter I.C. 1980. Ecology of larval and metamorphosing lampreys. Can. J. Fish. Aquat. Sci. 37: 1641-1656. http://dx.doi.org/10.1139/f80-212

Rajendran N., SuwaY., Urushigawa Y. 1993. Distribution of phospholipid ester-linked fatty acids biomarkers for bacteria in the sediment of Ise Bay. Mar. Chem. 42: 39-56. http://dx.doi.org/10.1016/0304-4203(93)90248-M

Renaud C.B., Gill H.S., Potter I.C. 2009. Relationships between the diets and characteristics of the dentition, buccal glands and velar tentacles of the adults of the parasitic species of lamprey. J. Zool. 278: 231-242. http://dx.doi.org/10.1111/j.1469-7998.2009.00571.x

Rielley G., Collier R.J., Jones D.M., Egliton G. 1991. The biogeochemistry of Ellesmene Lake, UK – I: source correlation of leaf wax inputs to the sedimentary lipid record. Org. Geochem. 17: 901-912. http://dx.doi.org/10.1016/0146-6380(91)90031-E

Samarra F.I.P., Fennell A., Aoki K., Deecke V.B., Miller P.J.O. 2012. Persistence of skin marks on killer whales (Orcinus orca) caused by the parasitic sea lamprey (Petromyzon marinus) in Iceland. Mar. Mammal Sci. 28: 395-401. http://dx.doi.org/10.1111/j.1748-7692.2011.00486.x

Sargent J.R., Whittle K.J. 1981. Lipids and hydrocarbons in the marine food web. In: Longhurst A.R. (ed.), Analysis of Marine Ecosystems, Academic Press, London, pp. 491-533.

Sargent J.R., Parkes R.J. Muller-Harvey L., Henderson R.J. 1987. Lipid biomarkers in marine ecology. In: Sleigh M.A. (ed.), Microbes in the Sea, Wiley and Sons, New York, pp. 119-138.

Sheridan M.A. 1988. Lipid dynamics in fish: aspects of absorption, transportation, deposition and mobilization. Comp. Biochem. Physiol. 90B: 679-690.

Silva S., Servia M.J., Vieira-Lanero R., Barca S., Cobo F. 2013a. Life cycle of the sea lamprey Petromyzon marinus: duration of and growth in the marine life stage. Aquat. Biol. 18: 59-62. http://dx.doi.org/10.3354/ab00488

Silva S., Servia M.J., Vieira-Lanero R., Cobo F. 2013b. Down-stream migration and hematophagous feeding of newly metamorphosed sea lampreys (Petromyzon marinus Linnaeus, 1758). Hydrobiologia 700: 277-286. http://dx.doi.org/10.1007/s10750-012-1237-3

Tocher R.D. 2003. Metabolism and functions of lipids and fatty acids in teleost fish. Rev. Fish. Sci. 11: 107-184. http://dx.doi.org/10.1080/713610925

van Utrecht W.L. 1959. Wounds and scars in the skin of the common porpoise Phocaena phocaena (L.). Mammalia 13: 100-122.

Wannigama G.P., Volkman J.K., Gillan F.T., Nichols P.D., Johns R.B. 1981. A comparison of lipid components of the fresh and dead leaves and pneumatophores of the mangrove Avicennia marina. Phytochemistry 20: 659-666. http://dx.doi.org/10.1016/0031-9422(81)85152-7

Warwick R.M., Platt H.M., Clarke K.R., Agard J., Gobin J. 1990. Analysis of macrobenthic and microbenthic community structure in relationship to pollution and disturbance in Hamilton Harbour, Bermuda. J. Exp. Biol. Ecol. 138: 119-142. http://dx.doi.org/10.1016/0022-0981(90)90180-K

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2013-06-30

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Lança MJ, Machado M, Ferreira R, Alves-Pereira I, Ruivo Quintella B, Raposo de Almeida P. Feeding strategy assessment through fatty acid profiles in muscles of adult sea lampreys from the western Iberian coast. Sci. mar. [Internet]. 2013Jun.30 [cited 2024Mar.29];77(2):281-9. Available from: https://scientiamarina.revistas.csic.es/index.php/scientiamarina/article/view/1462

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