Abstract
Small pelagic fish represent an essential link between lower and upper trophic levels in marine pelagic ecosystems and often support important fisheries. In the Bay of Biscay in the north-east Atlantic, no obvious controlling factors have yet been described that explain observed fluctuations in European sardine Sardina pilchardus and European anchovy Engraulis encrasicolus stocks, in contrast to other systems. The aim of this study was therefore to investigate to which extent these fluctuations could be trophodynamically mediated. The trophic ecology of both fish species was characterised over three contrasting periods (spring 2010 and 2011 and autumn 2011) in the area, in relation to potential variation in the abundance and composition of the mesozooplankton resource. Stable isotope analyses of carbon (δ13C) and nitrogen (δ15N) were performed on potential mesozoplanktonic prey items and in the muscle of adult fish, as well as in the liver whenever available, and mixing models were applied. In both springs, the mesozooplankton resource was abundant but qualitatively different. During this period of the year, results based on muscle isotope values in particular showed that S. pilchardus and E. encrasicolus likely do not compete strongly for food. On the medium term, E. encrasicolus always presented a greater trophic plasticity than S. pilchardus, both in terms of feeding areas and in the size of the mesozooplanktonic prey consumed. In autumn, mesozooplankton abundances were lower, and it was likely that S. pilchardus and E. encrasicolus share food resources during this period. No clear links between the variation in the mesozooplanktonic resource and the trophic segregation maintained between adults of both fish species in spring could be made. Although a certain potential exists for trophodynamically mediated fluctuations of both species under specific abiotic conditions (i.e. due to the existing trophic segregation in spring in particular), the overall results suggest that fluctuations in abundance of both fish species are probably not directly linked to their trophic ecology in the Bay of Biscay, at least at the level of adult individuals.
Similar content being viewed by others
References
Albaina A, Irigoien X (2004) Relationships between frontal structures and zooplankton communities along a cross-shelf transect in the Bay of Biscay (1995 to 2003). Mar Ecol Prog Ser 284:65–75
Alheit J, Pohlmann T, Casini M, Greve W, Hinrichs R, Mathis M, O’Driscoll K, Vorberg R, Wagner C (2012) Climate variability drives anchovies and sardines into the North and Baltic Seas. Prog Oceanogr 96:128–139
Bachiller E, Cotano U, Boyra G, Irigoien X (2012) Spatial distribution of the stomach weights of juvenile anchovy (Engraulis encrasicolus L.) in the Bay of Biscay. ICES J Mar Sci. doi:10.1093/icesjms/fss176
Barange M, Coetzee J, Takasuka A, Hill K, Gutierrez M, Oozeki Y, Van der Lingen C, Agostini V (2009) Habitat expansion and contraction in anchovy and sardine populations. Prog Oceanogr 83:251–260
Beaugrand G, Brander KM, Lindley JA, Souissi S, Reid PC (2003) Plankton effect on cod recruitment in the North Sea. Nature 426:661–664
Bode A, Álvarez-Ossorio MT, Carrera P, Lorenzo J (2004) Reconstruction of trophic pathways between plankton and the North Iberian sardine (Sardina pilchardus) using stable isotopes. Sci Mar 68:165–178
Bond AL, Diamond AW (2011) Recent Bayesian stable-isotope mixing models are highly sensitive to variation in discrimination factors. Ecol Appl 21:1017–1023
Buchheister A, Latour RJ (2010) Turnover and fractionation of carbon and nitrogen stable isotopes in tissues of a migratory coastal predator, summer flounder (Paralichthys dentatus). Can J Fish Aquat Sci 67:445–461
Cabal J, González-Nuevo G, Nogueira E (2008) Mesozooplankton species distribution in the NW and N Iberian shelf during spring 2004: relationship with frontal structures. J Mar Syst 72:282–297
Caut S, Angulo E, Courchamp F (2009) Variation in discrimination factors (Δ15N and Δ13C): the effect of diet isotopic values and applications for diet reconstruction. J Appl Ecol 46:443–453
Chavez FP, Ryan J, Lluch-Cota SE, Ñiquen CM (2003) From anchovies to sardines and back: multidecadal change in the Pacific Ocean. Science 299:217–221
Chouvelon T, Spitz J, Caurant F, Mèndez-Fernandez P, Chappuis A, Laugier F, Le Goff E, Bustamante P (2012) Revisiting the use of δ15N in meso-scale studies of marine food webs by considering spatio-temporal variations in stable isotopic signatures—the case of an open ecosystem: the Bay of Biscay (North-East Atlantic). Prog Oceanogr 101:92–105
Chouvelon T, Chappuis A, Bustamante P, Lefebvre S, Mornet F, Guillou G, Violamer L, Dupuy C (2014) Trophic ecology of European sardine Sardina pilchardus and European anchovy Engraulis encrasicolus in the Bay of Biscay (north-east Atlantic) inferred from δ13C and δ15N values of fish and identified mesozooplanktonic organisms. J Sea Res 85:277–291
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
Cury P, Roy C (1989) Optimal environmental window and pelagic fish recruitment success in upwelling areas. Can J Fish Aquat Sci 46:670–680
Cury P, Bakun A, Crawford RJM, Jarre A, Quiñones RA, Shannon LJ, Verheye HM (2000) Small pelagics in upwelling systems: patterns of interaction and structural changes in “wasp-waist” ecosystems. ICES J Mar Sci 57:603–618
De Niro MJ, Epstein S (1977) Mechanism of carbon fractionation associated with lipid synthesis. Science 197:261–263
De Niro MJ, Epstein S (1978) Influence of diet on the distribution of carbon isotopes in animals. Geochim Cosmochim Acta 42:495–506
De Niro MJ, Epstein S (1981) Influence of diet on the distribution of nitrogen isotopes in animals. Geochim Cosmochim Acta 45:341–351
Dubreuil J, Petitgas P (2009) Energy density of anchovy Engraulis encrasicolus in the Bay of Biscay. J Fish Biol 74:521–534
Dupuy C, Talarmin A, Hartmann HJ, Delmas D, Courties C, Marquis E (2011) Community structure and grazing of the nano-microzooplankton on the continental shelf of the Bay of Biscay. Estuar Coast Shelf Sci 95:1–13
Espinoza P, Bertrand A, Van der Lingen CD, Garrido S, Rojas de Mendiola B (2009) Diet of sardine (Sardinops sagax) in the northern Humboldt Current system and comparison with the diets of clupeoids in this and other eastern boundary upwelling systems. Prog Oceanogr 83:242–250
FAO (Food and Agriculture Organization of the United Nations) (2012) The state of world fisheries and aquaculture 2010. FAO, Rome
France RL (1995) Carbon-13 enrichment in benthic compared to planktonic algae: food web implications. Mar Ecol Prog Ser 124:307–312
Fry B (1988) Food web structure on Georges Bank from stable C, N, and S isotopic compositions. Limnol Oceanogr 33:1182–1190
Garrido S, Marçalo A, Zwolinski J, Van der Lingen CD (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, Rosa R, Ben-Hamadou R, Cunha ME, Chícharo MA, Van der Lingen CD (2008) Spatio-temporal variability in fatty acid trophic biomarkers in stomach contents and muscle of Iberian sardine (Sardina pilchardus) and its relationship with spawning. Mar Biol 154:1053–1065
Gohin F, Lampert L, Guillaud JF, Herbland A, Nézan E (2003) Satellite and in situ observations of a late winter phytoplankton bloom, in the northern Bay of Biscay. Cont Shelf Res 23:1117–1141
Guelinckx J, Maes J, Van Den Driessche P, Geysen B, Dehairs F, Ollevier F (2007) Changes in δ13C and δ15N in different tissues of juvenile sand goby Pomatoschistus minutus: a laboratory diet-switch experiment. Mar Ecol Prog Ser 341:205–215
Herbland A, Delmas D, Laborde P, Sautour B, Artigas F (1998) Phytoplankton spring bloom of the Gironde plume waters in the Bay of Biscay: early phosphorus limitation and food web consequences. Oceanol Acta 21:279–291
Hobson KA (1999) Tracing origins and migration of wildlife using stable isotopes: a review. Oecologia 120:314–326
Hobson KA, Clark RG (1992) Assessing avian diets using stable isotopes. I: turnover of C in tissues. Condor 94:181–188
Holligan PM, Groom SB (1986) Phytoplankton distributions along the shelf break. Proc R Soc Edinb B 88:239–263
ICES (2010a) Report of the working group on Anchovy and Sardine (WGANSA). ICES WGANSA report 2010, ICES, 289 p
ICES (2010b) Life-cycle spatial patterns of small pelagic fish in the Northeast Atlantic. ICES cooperative research report, ICES, 94 p
Irigoien X, De Roos A (2011) The role of intraguild predation in the population dynamics of small pelagic fish. Mar Biol 158:1683–1690
Irigoien X, Head RN, Harris RP, Cummings D, Harbour D, Meyer-Harms B (2000) Feeding selectivity and egg production of Calanus helgolandicus in the English Channel. Limnol Oceanogr 45:44–54
Irigoien X, Fernandes JA, Grosjean P, Denis K, Albaina A, Santos M (2009) Spring zooplankton distribution in the Bay of Biscay from 1998 to 2006 in relation with anchovy recruitment. J Plankton Res 31:1–17
Isla JA, Ceballos S, Huskin I, Anadón R, Álvarez-Marqués F (2004) Mesozooplankton distribution, metabolism and grazing in an anticyclonic slope water oceanic eddy (SWODDY) in the Bay of Biscay. Mar Biol 145:1201–1212
James AG, Findlay KP (1989) Effect of particle size and concentration on feeding behavior, selectivity and rates of food ingestion by the Cape anchovy Engraulis capensis. Mar Ecol Prog Ser 50:275–294
James AG, Probyn T (1989) The relationship between respiration rate, swimming speed and feeding behaviour in the Cape anchovy Engraulis capensis Gilchrist. J Exp Mar Biol Ecol 131:81–100
Koutsikopoulos C, Le Cann B (1996) Physical processes and hydrological structures related to the Bay of Biscay anchovy. Sci Mar 60:9–19
Labry C, Herbland A, Delmas D, Laborde P, Lazure P, Froidefond JM, Jégou AM, Sautour B (2001) Initiation of winter phytoplankton blooms within the Gironde plume waters in the Bay of Biscay. Mar Ecol Prog Ser 212:117–130
Lassalle G, Lobry J, Le Loc’h F, Bustamante P, Certain G, Delmas D, Dupuy C, Hily C, Labry C, Le Pape O, Marquis E, Petitgas P, Pusineri C, Ridoux V, Spitz J, Niquil N (2011) Lower trophic levels and detrital biomass control the Bay of Biscay continental shelf food web: implications for ecosystem management. Prog Oceanogr 91:561–575
Lefebvre S, Marín Leal JC, Dubois S, Orvain F, Blin JL, Bataillé MP, Ourry A, Galois R (2009) Seasonal dynamics of trophic relationships among co-occurring suspension feeders in two shellfish culture dominated ecosystems. Estuar Coastal Shelf Sci 82:415–425
Lluch-Belda D, Crawford RJM, Kawasaki T, MacCall AD, Parrish RH, Schwartzlose RA, Smith PE (1989) World-wide fluctuations of sardine and anchovy stocks: the regime problem. S Afr J Mar Sci 8:195–205
Lluch-Belda D, Schwartzlose RA, Serra R, Parrish R, Kawasaki T, Hedgecock D, Crawford RJM (1992) Sardine and anchovy regime fluctuations of abundance in four regions of the world oceans: a workshop report. Fish Oceanogr 1:339–347
Lorance P, Bertrand JA, Brind’Amour A, Rochet MJ, Trenkel VM (2009) Assessment of impacts from human activities on ecosystem components in the Bay of Biscay in the early 1990s. Aquat Living Resour 22:409–431
Louw GG, Van der Lingen CD, Gibbons MJ (1998) Differential feeding by sardine Sardinops Sagax and anchovy Engraulis capensis recruits in mixed shoals. S Afr J Mar Sci 19:227–232
Loyer S, Lampert L, Menesguen A, Cann P, Labasque T (2006) Seasonal evolution of the nutrient pattern on Biscay Bay continental shelf over the years 1999–2000. Sci Mar 70:31–46
Marquis E, Niquil N, Vézina AF, Petitgas P, Dupuy C (2011) Influence of planktonic food web structure on a system’s capacity to support pelagic production: an inverse analysis approach. ICES J Mar Sci 68:803–812
Martínez del Rio C, Wolf N, Carleton SA, Gannes LZ (2009) Isotopic ecology ten years after a call for more laboratory experiments. Biol Rev 84:91–111
McClelland JM, Valiela I, Michener RH (1997) Nitrogen-stable isotope signatures in estuarine food webs: a record of increasing urbanization in coastal watersheds. Limnol Oceanogr 42:930–937
Michener RH, Kaufman L (2007) Stable isotope ratios as tracers in marine food webs: an update. In: Michener R, Lajtha K (eds) Stable isotopes in ecology and environmental science. Blackwell, Malden, pp 238–282
Montoya JP (2007) Natural abundance of 15N in marine planktonic ecosystems. In: Michener R, Lajtha K (eds) Stable isotopes in ecology and environmental science. Blackwell, Malden, pp 76–201
Motos L (1996) Reproductive biology and fecundity of the Bay of Biscay anchovy population (Engraulis encrasicolus L.). Sci Mar 60:195–207
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: an “end-to-end” field study. Mar Ecol Prog Ser 453:173–188
Nøttestad L, Giske J, Holst JC, Huse G (1999) A length-based hypothesis for feeding migrations in pelagic fish. Can J Fish Aquat Sci 56:26–34
OSPAR (2010) Quality status report 2010. OSPAR Commission, London 176 p
Parnell AC, Inger R, Bearhop S, Jackson AL (2010) Source partitioning using stable isotopes: coping with too much variation. PLoS ONE 5:e9672. doi:10.1371/journal.pone.0009672
Parnell AC, Phillips DL, Bearhop S, Semmens BX, Ward EJ, Moore JW, Jackson AL, Grey J, Kelly DJ, Inger R (2013) Bayesian stable isotope mixing models. Environmetrics 24:387–399
Peterson BJ, Fry B (1987) Stable isotopes in ecosystem studies. Annu Rev Ecol Syst 18:293–320
Phillips DL, Gregg JW (2003) Source partitioning using stable isotopes: coping with too many sources. Oecologia 136:261–269
Phillips DL, Newsome SD, Gregg JW (2005) Combining sources in stable isotope mixing models: alternative methods. Oecologia 144:520–527
Phillips DL, Inger R, Bearhop S, Jackson AL, Moore JW, Parnell AC, Semmens BX, Ward EJ (2014) Best practices for use of stable isotope mixing models in food web studies. Can J Zool. doi:10.1139/cjz-2014-0127
Pinnegar JK, Polunin NVC (1999) Differential fractionation of δ13C and δ15N among fish tissues: implications for the study of trophic interactions. Funct Ecol 13:225–231
Planque B, Lazure P, Jégou AM (2004) Detecting hydrological landscapes over the Bay of Biscay continental shelf in spring. Clim Res 28:41–52
Plounevez S, Champalbert G (1999) Feeding behaviour and trophic environment of Engraulis encrasicolus (L.) in the Bay of Biscay. Estuar Coast Shelf S 49:177–191
Post DM (2002) Using stable isotopes to estimate trophic position: models, methods and assumptions. Ecology 83:703–718
Puillat I, Lazure P, Jégou AM, Lampert L, Miller PI (2004) Hydrographical variability on the French continental shelf in the Bay of Biscay, during the 1990s. Cont Shelf Res 24:1143–1163
Puillat I, Lazure P, Jégou AM, Lampert L, Miller PI (2006) Mesoscale hydrological variability induced by northwesterly wind on the French continental shelf of the Bay of Biscay. Sci Mar 70S1:15–26
Raab K, Nagelkerke LAJ, Boerée C, Rijnsdorp AD, Temming A, Dickey-Collas M (2011) Anchovy Engraulis encrasicolus diet in the North and Baltic Seas. J Sea Res 65:131–140
Rose M (1933) Copépodes pélagiques. Faune de France 26, Paris
Sautour B, Artigas LF, Delmas D, Herbland A, Laborde P (2000) Grazing impact of micro and mesozooplankton during a spring situation in coastal waters off the Gironde estuary. J Plankton Res 22:531–552
Schimmelmann A, De Niro MJ (1986) Stable isotopic studies on chitin. II. The 13C/12C and 15N/14N ratios in arthropod chitin. Contrib Mar Sci 29:113–130
Schwartzlose RA, Alheit J, Bakun A, Baumgartner TR, Cloete R, Crawford RJM, Fltechern WJ, Green-Ruiz Y, Hagen E, Kawasaki T, Lluch-Belda D, Lluch-Cota SE, MacCall AD, Matsuura Y, Nevarez-Martinez MO, Parrish RH, Roy C, Serra R, Shust KV, Ward MN, Zuzunaga JZ (1999) Worlwide large-scale fluctuations of sardine and anchovy populations. S Afr J Mar Sci 21:289–347
Sherwood GD, Rose GA (2005) Stable isotope analysis of some representative fish and invertebrates of the Newfoundland and Labrador continental shelf food web. Estuar Coast Shelf S 63:537–549
Sourisseau M, Carlotti F (2006) Spatial distribution of zooplankton size spectra on the French continental shelf of the Bay of Biscay during spring 2000 and 2001. J Geophys Res Oceans 111:C05S09
Sponheimer M, Robinson TF, Cerling TE, Tegland L, Roeder BL, Ayliffe L, Dearing MD, Ehleringer JR (2006) Turnover of stable carbon isotopes in the muscle, liver, and breath CO of alpacas (Lama pacos). Rapid Commun Mass Spectrom 20:1395–1399
Stergiou KI, Karpouzi VS (2002) Feeding habits and trophic levels of Mediterranean fish. Rev Fish Biol Fish 11:217–254
Suzuki KW, Kasai A, Nakayama K, Tanaka M (2005) Differential isotopic enrichment and half-life among tissues in Japanese temperate bass (Lateolabrax japonicus) juveniles: implications for analysing migration. Can J Fish Aquat Sci 62:671–678
Sweeting CJ, Barry JT, Barnes C, Polunin NVC, Jennings S (2007a) Effects of body size and environment on diet-tissue δ15 N fractionation in fishes. J Exp Mar Biol Ecol 340:1–10
Sweeting CJ, Barry JT, Barnes C, Polunin NVC, Jennings S (2007b) Effects of body size and environment on diet-tissue δ13C fractionation in fishes. J Exp Mar Biol Ecol 352:165–176
Takasuka A, Oozeki Y, Aoki I (2007) Optimal growth temperature hypothesis: why do anchovy flourish and sardine collapse or vice versa under the same ocean regime? Can J Fish Aquat Sci 64:768–776
Tieszen LL, Boutton TW, Tesdahl KG, Slade NA (1983) Fractionation and turnover of stable carbon isotopes in animal tissues: implications for δ13C analysis of diet. Oecologia 57:32–37
Trueman CN, McGill RAR, Guyard PH (2005) The effect of growth rate on tissue-diet isotopic spacing in rapidly growing animals. An experimental study with Atlantic salmon (Salmo salar). Rapid Commun Mass Spectrom 19:3239–3247
Valdés L, Moral M (1998) Time-series analysis of copepod diversity and species richness in the southern Bay of Biscay off Santander, Spain, in relation to environmental conditions. ICES J Mar Sci 55:783–792
Valdés L, López-Urrutia A, Cabal J, Alvarez-Ossorio M, Bode A, Miranda A, Cabanas M, Huskin I, Anadón R, Alvarez-Marqués F, Llope M, Rodríguez N (2007) A decade of sampling in the Bay of Biscay: What are the zooplankton time series telling us? Prog Oceanogr 74:98–114
Van der Lingen CD (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 CD, Hutchings L, Field JG (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 28:465–478
Vander Zanden MJ, Cabana G, Rasmussen JB (1997) Comparing trophic position of freshwater fish calculated using stable nitrogen isotope ratios (δ15N) and literature dietary data. Can J Fish Aquat Sci 54:1142–1158
Vanderklift MA, Ponsard S (2003) Source of variation in consumer-diet δ15N enrichment: a meta-analysis. Oecologia 136:169–182
Villate F, Moral M, Valencia V (1997) Mesozooplankton community indicates climate changes in a shelf area of the inner Bay of Biscay throughout 1988 to 1990. J Plankton Res 19:1617–1636
Vizzini S, Mazzola A (2006) The effects of anthropogenic organic matter inputs on stable carbon and nitrogen isotopes in organisms from different trophic levels in a southern Mediterranean coastal area. Sci Total Environ 368:723–731
Williams R, Conway DVP, Hunt HG (1994) The role of copepods in the planktonic ecosystems of mixed and stratified waters of the European shelf seas. Hydrobiologia 292(293):521–530
Zarauz L, Irigoien X, Urtizberea A, Gonzalez M (2007) Mapping plankton distribution in the Bay of Biscay during three consecutive spring surveys. Mar Ecol Prog Ser 345:27–39
Acknowledgments
This work was supported by the European project REPRODUCE (EratNet-Marifish, FP7). Authors are very grateful to J. Massé, P. Petitgas and M. Doray from IFREMER for facilitating the sampling during PELGAS surveys. Many thanks to M. Huret and P. Bourriau (IFREMER) too for their help during plankton sample collection and P. Lespagnol (IFREMER) for fish sampling. Authors also thank G. Guillou and P. Richard (UMR LIENSs) for assistance in stable isotope analysis and finally the anonymous reviewers of the earlier version of the manuscript for facilitating its improvement.
Author information
Authors and Affiliations
Corresponding author
Additional information
Communicated by C. Harrod.
T. Chouvelon and L. Violamer have contributed equally to this work.
Rights and permissions
About this article
Cite this article
Chouvelon, T., Violamer, L., Dessier, A. et al. Small pelagic fish feeding patterns in relation to food resource variability: an isotopic investigation for Sardina pilchardus and Engraulis encrasicolus from the Bay of Biscay (north-east Atlantic). Mar Biol 162, 15–37 (2015). https://doi.org/10.1007/s00227-014-2577-5
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00227-014-2577-5