Scientia Marina, Vol 78, No 1 (2014)

Feeding of European pilchard (Sardina pilchardus) in the northwestern Mediterranean: from late larvae to adults

David Costalago
Institut de Ciències del Mar (ICM-CSIC) - , Spain

Isabel Palomera
Institut de Ciències del Mar (ICM-CSIC) , Spain


We assessed the relative importance of different prey types of the European pilchard (European sardine) from the late larval to the adult stage. Two different methodologies for analysing stomach contents were used to describe the trophic dynamics of sardine and the relationship of sardine feeding behaviour with the ontogenetic development of body structures used for feeding, such as gill rakers and pyloric caeca. This information is essential to accurately depict the use of the planktonic resources in the area by sardine and to discuss the extent to which the sardine population could be affected by environmental changes in the Mediterranean Sea. We showed that cladocerans in summer and diatoms in winter were numerically the most important prey types for both juveniles and adults. However, decapod larvae were the most important prey during all seasons in terms of carbon content. Accordingly, differences in methodology should be considered in the analysis of sardine diets. An analysis of the composition of the plankton showed that small copepods were strongly selected by sardines at all ages and in both seasons. We also observed that the pyloric caeca began to grow when the sardines were approximately 4-5 cm standard length (SL) and ended their development when the sardines reached approximately 8 cm SL, whereas the gill rakers appeared to be completely functional when the sardines reached 7 cm SL. Therefore, filter feeding of small particles could be performed with total efficacy beginning at 7-8 cm SL. In view of the energetic advantage of filter feeding in a well-adapted filter-feeding species such as sardine, the prospective limited availability of small particles hypothesized by certain authors for the Mediterranean could have negative consequences for sardine. This study demonstrates that sardine populations, given their extremely high dependence on the lower marine trophic levels, could be strongly affected by alterations in the environment and in the planktonic community.


Sardina pilchardus; northwestern Mediterranean; ontogeny; trophic ecology; small pelagic fish

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Andreu B. 1969. Las branquispinas en la caracterización de las poblaciones de Sardina pilchardus (Walb.). Invest. Pesq. 33: 425-607.

Bakun A., Agostini V.N. 2001: Seasonal patterns of wind-induced upwelling/downwelling in the Mediterranean Sea. Sci. Mar. 65: 243-257.

Banaru D., Mellon-Duval C., Roos D., Bigot J.L., Souplet A., Jadaud A., Beaubrun P., Fromentin, J.M. 2013. Trophic structure and fisheries interactions in the Gulf of Lions (north-western Mediterranean). J. Mar. Sys. 111-112: 45-68.

Barange M., Bernal M., Cercole M.C., Cubillos L., Cunningham C.L., Daskalov G.M., de Oliveira J.A.A., Dickey-Collas M., Hill K., Jacobson L., Køster F.W., Masse J., Nishida H., Ñiquen M., Oozeki Y., Palomera I., Saccardo S.A., Santojanni A., Serra R., Somarakis S., Stratoudakis Y., van der Lingen C.D., Uriarte A., Yatsu A., 2009. Current trends in the assessment and management of stocks. In: Checkley D., Roy C., Oozeki Y., Alheit J. (eds), Climate Change and Small Pelagic Fish Stocks. Cambridge University Press, pp. 191-255.

Beaugrand G., Brander, K. M., Lindley J.A., Souissi S., Reid P.C. 2003. Plankton effect on cod recruitment in the North Sea. Nature 426: 661-664.

Blaxter J.H.S., Hunter J.R. 1982. The biology of the clupeoid fishes. Adv.Mar. Biol. 20: 1-223. Academic Press, New York.

Bode A., Carrera P., Lens S. 2003. The pelagic foodweb in the upwelling ecosystem of Galicia (NW Spain) during spring: natural abundance of stable carbon and nitrogen isotopes. ICES J. Mar. Sci. 60: 11-22.

Bode A., Álvarez-Ossorio M.T., Carrera P., Lorenzo J. 2004. Reconstruction of the trophic pathways between plankton and the North Iberia sardine (Sardina pilchardus) using stable isotopes. Sci. Mar. 68: 165-178.

Borme D., Tirelli V., Brandt S., Fonda S., Arneri E. 2009. Diet of Engraulis encrasicolus in the northern Adriatic Sea (Mediterranean): ontogenetic changes and feeding selectivity. Mar. Ecol. Prog. Ser. 392: 193-200.

Borme D., Tirelli V., Palomera I. 2013. Feeding habits of European pilchard late larvae in a nursery area in the Adriatic Sea. J. Sea Res. 78: 8-17.

Buddington R.K., Diamond J.M. 1986. Aristotle revisited: The function of pyloric caeca in fish. Proc. Natl. Acad. Sci. USA 83: 8012-8014.

Bulgakova Y. 1996. Feeding in the Black Sea anchovy: diet composition, feeding behaviour, feeding periodicity and daily rations. Sci. Mar. 60(2): 283-284.

Capitanio B.F., Pájaro M., Esnal G.B. 2005. Appendicularians: an important food supply for the Argentine anchovy Engraulis anchoita in coastal waters. J. Appl. Ichthyol. 21: 414-419.

Checkley D., Alheit J., Oozeki Y., Roy C. 2009. Climate change and small pelagic fish. Cambridge University Press, Cambridge, 392 pp.

Clarke K.R., Warwick R.M. 2001. Change in marine communities: an approach to statistical analysis and interpretation, 2nd edition. PRIMER-E, Plymouth, 172 pp.

Coll M., Palomera I., Tudela S., Sarda F. 2006. Trophic flows, ecosystem structure and fishing impacts in the South Catalan Sea, northwestern Mediterranean. J. Mar. Syst. 59: 63-96.

Coll M., Palomera I., Tudela S., Dowd M. 2008a. Food-web dynamics in the South Catalan Sea ecosystem (NW Mediterranean) for 1978-2003. Ecol. Model. 217: 95-116.

Coll M., Libralato S., Tudela S., Palomera I., Pranovi F. 2008b. Ecosystem overfishing in the ocean. PLoS One 3(12): e3881.

Conversi A, Peluso T and Fonda-Umani S. 2009. Gulf of Trieste: A changing ecosystem. J. Geophys. Res. 114.

Conway D.V.P., Coombs S.H., Fernandez de Puelles M.L., Tranter P.R.G. 1994. Feeding of larval sardine, Sardina pilchardus (Walbaum), off the north coast of Spain. Bol. Inst. Esp. Oceanogr. 10: 165-175.

Costalago D., Tecchio S., Palomera I., Álvarez-Calleja I., Ospina-Álvarez A., Raicevich S. 2011. Ecological understanding for fishery management: condition and growth of anchovy late larvae during different seasons in the northwestern Mediterranean. Estuar. Coast. Shelf Sci. 93: 350-358.

Costalago D., Navarro J., Álvarez-Calleja I., Palomera I. 2012. Ontogenetic and seasonal changes in the feeding habits and trophic levels of two small pelagic fish species. Mar. Ecol. Prog. Ser. 460: 169-181.

Costalago D., Palomera I., Tirelli V. 2014. Seasonal comparison of the diets of European anchovy Engraulis encrasicolus and sardine Sardina pilchardus juveniles in the Gulf of Lions. J. Sea Res.

Cushing D.H. 1990. Plankton production and year-class strength in fish populations: an update of the match/mismatch hypothesis. In: Blaxter, J.H.S., Southward, A.J. (eds), Adv. Mar. Biol. Academic Press Limited, San Diego, CA, pp. 250-313.

de Laender F., Van Oevelen D., Soetaert K., Middelburg J.J. 2010. Carbon transfer in herbivore- and microbial loop-dominated pelagic food webs in the southern Barents Sea during spring and summer. Mar. Ecol. Prog. Ser. 398: 93-107.

Demirhindi U. 1961. Nutrition of the sardine (Sardina pilchardus Walb.). P. Techn. Papers GFCM 6: 253-259.

Durbin A.G. 1979. Food selection by plankton feeding fishes. In Clepper H. (ed.) Predator-prey systems in fisheries management. Sport Fishing Institute. Washington DC, pp. 203-218.

Eggers D.M. 1979. Comments on some recent methods for estimating food consumption by fish. J. Fish. Res. B. Canada 36: 1018-1019.

Elliott J.M. 1972. Rates of gastric evacuation in brown trout, Salmo tnitta. L. Freshwat. Biol. 2: 1-18.

Elliott J.M., Persson L. 1978. The estimation of daily rates of food consumption for fish. J. Anim. Ecol. 47: 977-991.

Espinoza P., Bertrand, A. 2008. Revisiting Peruvian anchovy (Engraulis ringens) trophodynamics provides a new vision of the Humboldt Current system. Prog. Oceanogr. 79: 215-227.

Estrada M. 1996. Primary production in the northwestern Mediterranean. In: Palomera I., Rubiés, P. (eds), The European anchovy and its environment. Sci. Mar. 60(2): 55-64.

Forget P., André G. 2007. Can satellite-derived chlorophyll imagery be used to trace surface dynamics in coastal zone? A case study in the northwestern Mediterranean Sea. Sensors 7: 884-904.

Frederiksen M., Edwards M., Richardson A.J., Halliday N.C., Wanless S. 2006. From plankton to top predators: bottom-up control of a marine food web across four trophic levels. J. Anim. Ecol. 75: 1259-1268.

Fu C., Gaichas S., Link J.S., Bundy A., Boldt J.L., Cook A.M., Gamble R., Utne K.R., Liu H., Friedland K.D. 2012. Relative importance of fisheries, trophodynamic and environmental drivers in a series of marine ecosystems. Mar. Ecol. Prog. Ser. 459: 169-184.

Garrido S., Marçalo A., Zwolinski J., van der Lingen C.D. 2007. Laboratory investigations on the effect of prey size and concentration on the feeding behaviour of Sardina pilchardus. Mar. Ecol. Prog. Ser. 330: 189-199.

Garrido S., Ben-Hamadou R., Oliveira P.B., Cunha M.E., Chícharo M.A., van der Lingen C.D. 2008. Diet and feeding intensity of sardine Sardina pilchardus: correlation with satellite-derived chlorophyll data. Mar. Ecol. Prog. Ser. 354: 245-256.

Gerking S. 1994. Feeding ecology of fish. Academic Press, San Diego. US. 416 pp.

General Fisheries Commission for the Mediterranean 2012, Working Group on Stock Assessment of Small Pelagic Species. Meeting Report, Split, Croacia.

Giannoulaki M.M.P., Liorzou B., Leonori I., Valavanis V.D., Tsagarakis K., Bigot L.J., Roos D., de Felice A., Campanella F., Somarakis S., Arneri E., Machias A. 2011. Habitat suitability modelling for sardine juveniles (Sardina pilchardus) in the Mediterranean Sea. Fish. Oceanogr. 20: 367-382.

Giannoulaki M., Iglesias M., Tugores M.P., Bonnano A., Patti B., De Felice A., Leonori, I., Bigot, J.L., Tičina, V., Pyrounaki, M.M., Tsagarakis, K., Machias, A., Somarakis, S., Schismenou E., Quinci E., Basilone G., Cuttita A., Campanella F., Miquel J., O-ate D., Roos D., Valavanis V. 2013. Characterising the potential habitat of European anchovy Engraulis encrasicolus in the Mediterranean Sea, at different life stages. Fish. Oceanogr. 22(2): 69-89.

Hynes H.B.N. 1950. The food of freshwater sticklebacks (Gasterosteus aculeatus and Pygosteus pungitius) with a review of methods used in studies of the food of fishes. J. An. Ecol. 19: 36-58.

Hyslop E.J. 1980. Stomach contents analysis- a review of methods and their application. J. Fish Biol. 17: 411-429.

Ivlev V.S. 1961. Experimental ecology of the feeding of fishes. Yale University Press, New Haven. 302 pp.

James A.G. 1986. Are clupeid microphagists herbivorous or omnivorous? A review of the diets of some commercially important clupeids. S. Afr. J. Mar. Sci. 7: 61-177.

King D.P.F., Macleod P.R. 1976. Comparison of the food and the filtering mechanism of pilchard Sardinops ocellata and anchovy Engraulis capensis off South West Africa. Invest. Rep. Sea Fish. Br. S. Afr. 111: 1-22.

Lasker R. 1970. Utilization of zooplankton energy by a Pacific sardine population in the California current. In: Steele, J.H. (ed) Marine Food Chains. Oliver and Boyd, Edinburgh, pp. 265-284.

Lebour M.V. 1921. The food of young clupeoids. J. Mar. Biol. Ass. UK 12(3): 458-467.

Lee J.Y. 1961. La sardine du golfe du lion (Sardina pilchardus sardina Regan). Rev. Trav. Inst. Pêch. Mar. 25(4) : 418-513.

Lleonart J., Maynou F. 2003. Fish stock assessments in the Mediterranean: state of the art. Sci. Mar. 67(Suppl. 1): 37-49.

Lloret J., Palomera I., Salat J., Sole I. 2004. Impact of freshwater input and wind on landings of anchovy (Engraulis encrasicolus) and sardine (Sardina pilchardus) in shelf waters surrounding the Ebre (Ebro) River delta (north-western Mediterranean). Fish. Oceanogr. 13: 102-110.

Margalef R. 1960. Fluctuations in abundance and availability cause by biotic factors. Proceedings of the World Scientific Meeting on biology of sardines and related species, FAO 3: 1265-1285.

Massuti M., Oliver M. 1948. Estudio de la biometría y biología de la sardina de Mahón (Baleares), especialmente de su alimentación. Bol. Instit. Esp. Oceanogr. 3: 1-15.

Molinero J.C., Ibanez F., Nival P., Buecher E., Souissi S. 2005. The North Atlantic Climate and northwestern Mediterranean plankton variability. Limnol. Oceanogr. 50: 1213-1220.

Morote E., Olivar M.P., Villate F., Uriarte I. 2008. Diet of round sardinella, Sardinella aurita, larvae in relation to plankton availability in the NW Mediterranean. J. Plank. Res. 30(7): 807-816.

Morote E., Olivar M.P., Villate F., Uriarte I. 2010. A comparison of anchovy (Engraulis encrasicolus) and sardine (Sardina pilchardus) larvae feeding in the Northwest Mediterranean: influence of prey availability and ontogeny. ICES J. Mar. Sci. 67: 897-908.

Motoda S. 1959. Devices of simple plankton apparatus. Mem. Fac. Fish. Hokkaido Univ. 7: 73-94.

Munuera I., González-Quirós R. 2006. Analysis of feeding of Sardina pilchardus (Walbaum, 1792) larval stages in the central Cantabrian Sea. Sci. Mar. 70S1: 131-139.

Nikolioudakis N., Palomera I., Machias A., Somarakis S. 2011. Diel feeding intensity and daily ration of the sardine Sardina pilchardus. Mar. Ecol. Prog. Ser. 437: 215-228.

Nikolioudakis N., Isari S., Pitta P., Somarakis S. 2012. Diet of sardine Sardina pilchardus: and 'end-to-end' field study. Mar. Ecol. Prog. Ser. 453: 173-188.

Palomera I., Olivar M.P., Salat J., Sabates A., Coll M., Garcia A., Morales-Nin B. 2007. Small pelagic fish in the NW Mediterranean Sea: an ecological review. Progr. Oceanogr. 74: 377-396

Pinkas L., Oliphant M.S., Iverson I.L.K. 1971. Food habits of albacore, bluefin tuna, and bonito in California waters. Calif. Dep. Fish Game Fish. Bul. 152: 1-105.

Preciado I., Velasco F., Olaso I. 2008. The role of pelagic fish as forage for the demersal fish community in the southern Bay of Biscay. J. Mar. Syst. 72: 407-417.

Rasoanarivo R., Folack J., Champalbert G., Becker B. 1991. Relations entre les communautés phytoplanctoniques et l'alimentation de Sardina pilchardus Walb. dans de golfe de Fos (Méditerrané occidentale): influence de la lumière sur l'activité alimentaire des larves. J. Exp. Mar. Biol. Ecol. 151: 83-92.

Sabatés A., Martín P., Lloret J., Raya V. 2006. Sea warming and fish distribution: the case of the small pelagic fish, Sardinella aurita, in the western Mediterranean. Global Change Biol. 12(11): 2209-2219.

Saiz E., Calbet A. 2007. Scaling of feeding in marine calanoid copepods. Limnol. Oceanogr. 52(2): 668-675.

Salat J. 1996. Review of hydrographic environmental factors that may influence anchovy habitats in northwestern Mediterranean. In: Palomera I., Rubiés, P. (eds), The European anchovy and its environment. Sci. Mar. 60, 21-32.

Scofield E.C. 1934. Early life history of the California sardina (Sardina caerulea) with special reference to the distribution of the eggs and larvae. Cal. Div. Fish Game Fish. Bull. 41: 1-49.

Strickler J.R., Udvadia A.J., Marino J., Radabaugh N., Ziarek J., Nihongi A. 2005. Visibility as a factor in the copepod-planktivorous fish relationship. Sci. Mar. 69(Suppl. 1): 111-124.

Tanaka H., Aoki I., Ohshimo S. 2006. Feeding habits and gill raker morphology of three planktivorous pelagic fish species off the coast of northern and western Kyushu in summer. J. Fish Biol. 68: 1041-1061.

Tsagarakis K., Pyrounaki M.M., Giannoulaki M., Somarakis S., Machias A. 2012. Ontogenetic shift in the schooling behaviour of sardines, Sardina pilchardus. An. Behav. 84: 437-443.

Tudela S., Palomera I. 1995. Diel feeding intensity and daily ration in the anchovy Engraulis encrasicolus in the northwest Mediterranean Sea during the spawning period. Mar. Ecol. Prog. Ser. 129: 55-61.

Tudela S., Palomera I. 1997. Trophic ecology of European anchovy Engraulis encrasicolus in the Catalan Sea (Northwest Mediterranean). Mar. Ecol. Prog. Ser. 160, 121-134.

Turingan R.G., Beck J.L., Krebs J.M., Licamele J.D. 2005. Development of feeding mechanisms in marine fish larvae and the swimming behavior of zooplankton prey: implications for rearing marine fishes. In: Lee C.S., O'Bryen P.J., Marcus N.M. (eds), Copepods in Aquaculture. Blackwell Publishing Professional, Ames, IA, USA, pp. 119-132.

Turner J.T. 2004. The importance of small planktonic copepods and their roles in pelagic marine food webs. Zoo. Stud. 43(2): 255-266.

Urtizberea A., Fiksen O., Folkvord A., Irigoien X. 2008. Modelling growth of larval anchovies including diel feeding patterns, temperature and body size. J. Plank. Res. 30(12): 1369-1383.

Uye S 1982. Length-weight relationships of important zooplankton from the Inland Sea of Japan. J. Oceanog. Soc. Japan 38: 149-158.

van der Lingen C.D. 1994. Effect of particle size and concentration on the feeding behaviour of adult pilchard Sardinops sagax. Mar. Ecol. Prog. Ser. 109: 1-13.

van der Lingen C.D. 2002. Diet of sardine Sardinops sagax in the southern Benguela upwelling ecosystem. Afr. J. Mar. Sci. 24: 301-316.

van der Lingen C.D., Hutchings L. 1998. Comparative trophodynamics of sardine Sardinops sagax and anchovy Engraulis capensis in the southern Benguela. Afr. J. Trop. Hydrobiol. Fish. 8: 11-18.

van der Lingen C.D., Hutchings L., Field J.G. 2006. Comparative trophodynamics of anchovy Engraulis encrasicolus and sardine Sardinops sagax in the southern Benguela: are species alternations between small pelagic fish trophodynamically mediated? Afr. J. Mar. Sci. 29(3 and 4): 465-477.

van der Lingen C.D., Bertrand A., Bode A., Brodeur R., Cubillos L., Espinoza P., Friedland K., Garrido S., Irigoien X., Möllman C., Rodriguez-Sanchez R., Tanaka H., Temming A. 2009. Trophic dynamics. In: Checkley D.M., Roy C., Alheit J., Oozeki Y. (eds), Climate change and small pelagic fish. GLOBEC Project Office, Plymouth (UK): 112-157.

Varela M., Alvarez-Ossorio M.T., Valdes L. 1990. Metodo para el estudio cuantitativo del contenido estomacal de la sardina. Resultados preliminares. Bol. Ins. Esp. Oceanogr. 6: 117-126.

Voulgaridou P., Stergiou K.I. 2003. Trends in various biological parameters of the European sardine, Sardina pilchardus (Walbaum, 1792), in the Eastern Mediterranean Sea. Sci. Mar. 67(Suppl. 1): 269-280.

Wainwright P.C., Richard B.A. 1995. Predicting patterns of prey use from morphology of fishes. Env. Biol. Fish. 44: 97-113.

Wootton R.J. 1999. Ecology of Teleost Fishes. 2nd Edition. Springer, New York, 386 pp.

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