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Hydrobiologia

, Volume 790, Issue 1, pp 49–65 | Cite as

Diet variability in European anchovy: a comparative analysis between larval populations of the inner Bay of Biscay and the NW Mediterranean

  • Lander IntxaustiEmail author
  • Fernando Villate
  • Lorenzo Motos
  • Ibon Uriarte
  • Arantza Iriarte
Primary Research Paper

Abstract

Feeding is critical for larval survival and it becomes a determining factor in the annual recruitment in species such as European anchovy Engraulis encrasicolus. Additionally, since differences in the plankton community may affect the larval feeding patterns, an interregional comparative study may contribute to understand these patterns concerning larval development and environmental features. The diet, feeding pattern and prey selectivity in relation to the ontogeny of the larval anchovy in the Cantabrian Sea (inner Bay of Biscay) and the Catalan Sea (NW Mediterranean) were compared in this study. Larvae fed preferentially on copepod eggs, nauplii and calanoid postnauplii, selecting them actively. Larval diet was similar before notochord flexion in the two areas. Nonetheless, for larvae of comparable size, prey preferences skewed towards small preys in the Cantabrian Sea, and towards large preys in the Catalan Sea. Differences appeared in the middle-sized larvae (6.5–9 mm) due to prey size and type. Diet differences were attributable (a) to the ability of the Catalan Sea larvae to capture bigger preys at a smaller individual size; and (b) to differences in prey preferences and availability. Therefore, geographic variety in larval populations and food environment features may promote variability in the larval anchovy diet.

Keywords

Engraulis encrasicolus Larval feeding Trophic ecology Gut contents Prey preferences Anchovy larvae 

Notes

Acknowledgments

This research was funded by projects CYTMAR MAR99-0328-C03-02 and REN2002-04205-C04-04 granted by the Ministry of Science and Education of the Spanish Government. This work has also been supported by the Basque Government through a PhD researcher training scholarship to L. Intxausti. We are very grateful to colleagues from AZTI-Tecnalia and ICM-CSIC for their help in developing this research.

References

  1. Aldanondo, N., U. Cotano, M. Tiepolo, G. Boyra & X. Irigoien, 2010. Growth and movement patterns of early juvenile European anchovy (Engraulis encrasicolus L.) in the Bay of Biscay based on otolith microstructure and chemistry. Fisheries Oceanography 19: 196–208.CrossRefGoogle Scholar
  2. Arregi, L., E. Puente, P. Lucio, Y. Sagarminaga, R. Castro & A. Uriarte, 2004. Coastal fisheries and demersal estuarine fauna. In Borja, Á. & M. B. Collins (eds), Oceanography and Marine Environment of the Basque Country. Elsevier B.V, Amsterdam: 493–513.CrossRefGoogle Scholar
  3. Arthur, D. K., 1976. Food and feeding of larvae of three fishes occurring in the California Current, Sardinops sagax, Engraulis mordax, and Trachurus symmetricus. Fishery Bulletin 74: 517–530.Google Scholar
  4. Arula, T., J. Kotta, A. Lankov, M. Simm & S. Põlme, 2012. Diet composition and feeding activity of larval spring-spawning herring: importance of environmental variability. Journal of Sea Research 68: 33–40.CrossRefGoogle Scholar
  5. Bachiller, E. & X. Irigoien, 2012. Allometric relations and consequences for feeding in small pelagic fish in the Bay of Biscay. ICES Journal of Marine Science 70: 232–243.CrossRefGoogle Scholar
  6. Bachiller, E., U. Cotano, G. Boyra & X. Irigoien, 2012. Spatial distribution of the stomach weights of juvenile anchovy (Engraulis encrasicolus L.) in the Bay of Biscay. ICES Journal of Marine Science 70: 362–378.CrossRefGoogle Scholar
  7. Bailey, K. M. & E. D. Houde, 1989. Predation on eggs and larvae of marine fishes and the recruitment problem. Advances in Marine Biology 25: 1–83.CrossRefGoogle Scholar
  8. Bakun, A., 1985. Comparative studies and the recruitment problem: searching for generalizations. California Cooperative Oceanic Fisheries Investigations Reports 26: 30–40.Google Scholar
  9. Bakun, A. & R. H. Parrish, 1982. Turbulence, transport and pelagic fish in the California and Peru current system. California Cooperative Oceanic Fisheries Investigations Reports 23: 99–108.Google Scholar
  10. Bergeron, J. P., 2009. Nutritional condition of anchovy Engraulis encrasicolus larvae in connection with mesozooplankton feeding catabolism in the southern Bay of Biscay, NE Atlantic. Journal of Experimental Marine Biology and Ecology 377: 76–83.CrossRefGoogle Scholar
  11. Borja, Á., A. Uriarte, V. Valencia, L. Motos & A. Uriarte, 1996. Relationships between anchovy (Engraulis encrasicolus L.) recruitment and the environment in the Bay of Biscay. Scientia Marina 60: 179–192.Google Scholar
  12. Borja, Á., A. Fontán, J. Sáenz & V. Valencia, 2008. Climate, oceanography, and recruitment: the case of the Bay of Biscay anchovy (Engraulis encrasicolus). Fisheries Oceanography 17: 477–493.CrossRefGoogle Scholar
  13. Borme, D., V. Tirelli, S. B. Brandt, S. Fonda Umani & E. Arneri, 2009. Diet of Engraulis encrasicolus in the northern Adriatic Sea (Mediterranean): ontogenetic changes and feeding selectivity. Marine Ecology Progress Series 392: 193–209.CrossRefGoogle Scholar
  14. Brander, K., 1994. Patterns of distribution, spawning, and growth in North Atlantic cod: the utility of inter-regional comparisons. ICES Marine Science Symposia 198: 406–413.Google Scholar
  15. Bulgakova, Y. V., 1993. Daily feeding dynamics of the Black Sea anchovy, Engraulis encrasicholus. Journal of Ichthyology 33: 78–88.Google Scholar
  16. Calbet, A., S. Garrido, E. Saiz, M. Alcaraz & C. Duarte, 2001. Annual zooplankton succession in coastal NW Mediterranean waters: the importance of the smaller size fractions. Journal of Plankton Research 23: 319–331.CrossRefGoogle Scholar
  17. Catalán, I. A., A. Folkvord, I. Palomera, G. Quílez-Badía, F. Kallianoti, A. Tselepides & A. Kallianotis, 2010. Growth and feeding patterns of European anchovy (Engraulis encrasicolus) early life stages in the Aegean Sea (NE Mediterranean). Estuarine, Coastal and Shelf Science 86: 299–312.CrossRefGoogle Scholar
  18. Checkley, D., 1982. Selective feeding by Atlantic herring (Clupea harengus) larvae on zooplankton in natural assemblages. Marine Ecology Progress Series 9: 245–253.CrossRefGoogle Scholar
  19. Chesson, J., 1978. Mesuring preference in selective predation. Ecology 59: 211–215.CrossRefGoogle Scholar
  20. Chouvelon, T., A. Chappuis, P. Bustamante, S. Lefebvre, F. Mornet, G. Guillou, L. Violamer & C. Dupuy, 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. Journal of Sea Research 85: 277–291.CrossRefGoogle Scholar
  21. Ciechomski, J., 1967. Investigations of food and feeding habits of larvae and juveniles of the Argentine anchovy Engraulis anchoita. California Cooperative Oceanic Fisheries Investigations Reports 11: 72–81.Google Scholar
  22. Conway, D. V. P., S. H. Coombs & C. Smith, 1998. Feeding of anchovy Engraulis encrasicolus larvae in the northwestern Adriatic Sea in response to changing hydrobiological conditions. Marine Ecology Progress Series 175: 35–49.CrossRefGoogle Scholar
  23. Costalago, D., S. Garrido & I. Palomera, 2015. Comparison of the feeding apparatus and diet of European sardines Sardina pilchardus of Atlantic and Mediterranean waters: ecological implications. Journal of Fish Biology 86: 1348–1362.CrossRefPubMedGoogle Scholar
  24. Costalago, D., J. Navarro, I. Álvarez-Calleja & I. Palomera, 2012. Ontogenetic and seasonal changes in the feeding habits and trophic levels of two small pelagic fish species. Marine Ecology Progress Series 460: 169–181.CrossRefGoogle Scholar
  25. Cotano, U., X. Irigoien, E. Etxebeste, P. Álvarez, L. Zarauz, J. Mader, L. Ferrer, P. Alvarez, L. Zarauz, J. Mader & L. Ferrer, 2008. Distribution, growth and survival of anchovy larvae (Engraulis encrasicolus L.) in relation to hydrodynamic and trophic environment in the Bay of Biscay. Journal of Plankton Research 30: 467–481.CrossRefGoogle Scholar
  26. Cury, P. & C. Roy, 1989. Optimal environmental window and pelagic fish recruitment success in upwelling areas. Canadian Journal of Fisheries and Aquatic Sciences 46: 670–680.CrossRefGoogle Scholar
  27. Cushing, D. H., 1990. Plankton production and year-class strength in fish populations: an update of the match/mismatch hypothesis. Advances in Marine Biology 26: 249–293.CrossRefGoogle Scholar
  28. Dabrowski, K., 1984. The feeding of fish larvae: present « state of the art » and perspectives. Reproduction, Nutrition, Development 24: 807–833.CrossRefGoogle Scholar
  29. Detwyler, R. & E. D. Houde, 1970. Food selection by laboratory-reared larvae of the scaled sardine Harengula pensacolae (Pisces, Clupeidae) and the bay anchovy Anchoa mitchilli (Pisces, Engraulidae). Marine Biology 7: 214–222.CrossRefGoogle Scholar
  30. Díaz, E., V. Valencia & F. Villate, 2007. Size-fractionated seston abundance and biochemical composition, over the anchovy spawning period in the Basque shelf (Bay of Biscay), during years 2000 and 2001. Journal of Experimental Marine Biology and Ecology 341: 45–59.CrossRefGoogle Scholar
  31. Díaz, E., J. M. Txurruka & F. Villate, 2008. Biochemical composition and condition in anchovy larvae Engraulis encrasicolus during growth. Marine Ecology Progress Series 361: 227–238.CrossRefGoogle Scholar
  32. Dickmann, M., C. Moellmann & R. Voss, 2007. Feeding ecology of Central Baltic sprat Sprattus sprattus larvae in relation to zooplankton dynamics: implications for survival. Marine Ecology Progress Series 342: 277–289.CrossRefGoogle Scholar
  33. Ferreira, P. L. & P. Ré, 1993. Feeding of larval anchovy, Engraulis encrasicolus (L.), in the Mira estuary (Portugal). Portugaliae Zoologica 2: 25–37.Google Scholar
  34. Fox, C. J., R. Harrop & A. Wimpenny, 1999. Feeding ecology of herring (Clupea harengus) larvae in the turbid Blackwater Estuary. Marine Biology 134: 353–365.CrossRefGoogle Scholar
  35. Govoni, J. J., P. B. Ortner, F. Al-Yamani & L. C. Hill, 1986. Selective feeding of spot, Leiostomus xanthurus, and Atlantic croaker, Micropogonias undulatus, larvae in the northern Gulf of Mexico. Marine Ecology Progress Series 28: 175–183.CrossRefGoogle Scholar
  36. Hillgruber, N., L. J. Haldorson & A. J. Paul, 1995. Feeding selectivity of larval walleye pollock Theragra chalcogramma in the oceanic domain of the Bering Sea. Marine Ecology Progress Series 120: 1–10.CrossRefGoogle Scholar
  37. Hjort, J., 1926. Fluctuations in the year classes of important food fishes. ICES Journal of Marine Science 1: 5–38.CrossRefGoogle Scholar
  38. Hunter, J. R., 1980. The feeding behaviour and ecology of marine fish larvae. In Bardach, J. E., J. J. Magnuson, R. C. May, & J. M. Reinhart (eds), Fish Behavior and Its Use in the Capture and Culture of Fishes. ICLARM Conference Proceedings, Manila: 287–330.Google Scholar
  39. Iles, T. D. & M. Sinclair, 1982. Atlantic herring: stock discreteness and abundance. Science 215: 627–633.CrossRefPubMedGoogle Scholar
  40. Intxausti, L., 2016. Ecología trófica y patrones morfométricos en las poblaciones larvarias de anchoa europea Engraulis encrasicolus del mar Cantábrico y el mar Catalán. University of the Basque Country, UPV/EHU, Leioa.Google Scholar
  41. Irigoien, X., Ø. Fiksen, U. Cotano, A. Uriarte, P. Alvarez, H. Arrizabalaga, G. Boyra, M. Santos, Y. Sagarminaga, P. Otheguy, E. Etxebeste, L. Zarauz, I. Artetxe & L. Motos, 2007. Could Biscay Bay Anchovy recruit through a spatial loophole? Progress in Oceanography 74: 132–148.CrossRefGoogle Scholar
  42. Irigoien, X., U. Cotano, G. Boyra, M. Santos, P. Álvarez, P. Otheguy, E. Etxebeste, A. Uriarte, L. Ferrer & L. Ibaibarriaga, 2008. From egg to juvenile in the Bay of Biscay: spatial patterns of anchovy (Engraulis encrasicolus) recruitment in a non-upwelling region. Fisheries Oceanography 17: 446–462.CrossRefGoogle Scholar
  43. Islam, M. S. & M. Tanaka, 2009. Diet and prey selection in larval and juvenile Japanese anchovy Engraulis japonicus in Ariake Bay, Japan. Aquatic Ecology 43: 549–558.CrossRefGoogle Scholar
  44. Last, J. M., 1980. The food of twenty species of fish larvae in the west-central North Sea. Fisheries Research Technical Report. Fisheries Research Technical Report. Ministry of Agriculture, Fisheries and Food. Directorate of Fisheries Research, Lowestoft.Google Scholar
  45. Llopiz, J. K. & R. Cowen, 2009. Variability in the trophic role of coral reef fish larvae in the oceanic plankton. Marine Ecology Progress Series 381: 259–272.CrossRefGoogle Scholar
  46. May, R. C., 1974. Larval mortality in marine fishes and the critical period concept. In Blaxter, J. H. S. (ed.), The Early Life History of Fish. Springer, Berlin: 3–19.CrossRefGoogle Scholar
  47. Maynou, F., M. P. Olivar & M. Emelianov, 2008. Patchiness and spatial structure of the early developmental stages of clupeiforms in the NW Mediterranean Sea. Journal of Plankton Research 30: 873–883.CrossRefGoogle Scholar
  48. Morote, E., M. P. Olivar, F. Villate & I. Uriarte, 2008. Diet of round sardinella, Sardinella aurita, larvae in relation to plankton availability in the NW Mediterranean. Journal of Plankton Research 30: 807–816.CrossRefGoogle Scholar
  49. Morote, E., M. P. Olivar, F. Villate & I. Uriarte, 2010. A comparison of anchovy (Engraulis encrasicolus) and sardine (Sardina pilchardus) larvae feeding in the Northwest Mediterranean: influence of prey availability and ontogeny. ICES Journal of Marine Science 67: 897–908.CrossRefGoogle Scholar
  50. Motos, L., A. Uriarte & V. Valencia, 1996. The spawning environment of the Bay of Biscay anchovy (Engraulis encrasicolus L.). Scientia Marina 60: 117–140.Google Scholar
  51. Motos, L., U. Cotano, S. H. Coombs, P. Álvarez & M. Santos, 2004. Ichthyoplankton assemblages. In Borja, Á. & M. Collins (eds), Oceanography and Marine Environment of the Basque Country. Elsevier, Amsterdam: 425–454.CrossRefGoogle Scholar
  52. Munuera, I. & R. Gonzalez-Quiros, 2007. Analysis of feeding of Sardina pilchardus (Walbaum, 1792) larval stages in the central Cantabrian Sea. Scientia Marina 70: 131–139.CrossRefGoogle Scholar
  53. Neville, C. M., & C. J. Beamish, 2007. Diets of larval Pacific hake, walleye pollock and Pacific herring in the Strait of Georgia. In Brace, S., & J. Longo (eds), Georgia Basin Puget Sound Research Conference Proceedings. Vancouver: 7.Google Scholar
  54. Palomera, I., 1992. Spawning of anchovy Engraulis encrasicolus in the northwestern Mediterranean relative to hydrographic features in the region. Marine Ecology Progress Series 79: 215–223.CrossRefGoogle Scholar
  55. Palomera, I., M. P. Olivar, J. Salat, A. Sabatés, M. Coll, A. García & B. Morales-Nin, 2007. Small pelagic fish in the NW Mediterranean Sea: an ecological review. Progress in Oceanography 74: 377–396.CrossRefGoogle Scholar
  56. Pavlovskaja, R. M., 1961. La survie des larves de l’anchois de la mer Noire en fonction de leur alimentation. Rapport de la Commission International pour l’exploration de la Mer Mediterranee 16: 345–350.Google Scholar
  57. Pearre, S., 1986. Ratio-based trophic niche breadths of fish, the Sheldon spectrum, and the size-efficiency hypothesis. Marine Ecology Progress Series 27: 287–297.CrossRefGoogle Scholar
  58. Pepin, P. & R. W. Penney, 1997. Patterns of prey size and taxonomic composition in larval fish: are there general size-dependent models? Journal of Fish Biology 51: 84–100.CrossRefGoogle Scholar
  59. Pertierra, J. P. & J. Lleonart, 1996. NW Mediterranean anchovy fisheries. Scientia Marina 60: 257–267.Google Scholar
  60. Plounevez, S. & G. Champalbert, 1999. Feeding behaviour and trophic environment of Engraulis encrasicolus (L.) in the Bay of Biscay. Estuarine, Coastal and Shelf Science 49: 177–191.CrossRefGoogle Scholar
  61. Plounevez, S. & G. Champalbert, 2000. Diet, feeding behaviour and trophic activity of the anchovy (Engraulis encrasicolus L.) in the Gulf of Lions (Mediterranean Sea). Oceanologica Acta 23: 175–192.CrossRefGoogle Scholar
  62. Raab, K., L. A. J. Nagelkerke, C. Boerée, A. D. Rijnsdorp, A. Temming & M. Dickey-Collas, 2011. Anchovy Engraulis encrasicolus diet in the North and Baltic Seas. Journal of Sea Research 65: 131–140.CrossRefGoogle Scholar
  63. Ré, P., 1986. Otolith microstructure and the detection of life history events in sardine and anchovy larvae. Ciencia Biologica. Ecology and Systematics 6: 9–17.Google Scholar
  64. Sabatés, A. & E. Saiz, 2000. Intra- and interspecific variability in prey size and niche breadth of myctophiform fish larvae. Marine Ecology Progress Series 201: 261–271.CrossRefGoogle Scholar
  65. Sampey, A., A. D. McKinnon, M. G. G. Meekan & M. I. McCormick, 2007. Glimpse into guts: overview of the feeding of larvae of tropical shorefishes. Marine Ecology Progress Series 339: 243–257.CrossRefGoogle Scholar
  66. Sánchez-Velasco, L., 1998. Diet composition and feeding habits of fish larvae of two co-occurring species (Pisces: Callionymidae and Bothidae) in the North-western Mediterranean. ICES Journal of Marine Science 55: 299–308.CrossRefGoogle Scholar
  67. Sassa, C., 2009. Feeding ecology of Symbolophorus californiensis larvae (Teleostei: Myctophidae) in the southern transition region of the western North Pacific. Journal of the Marine Biological Association of the United Kingdom 90: 1249–1256.CrossRefGoogle Scholar
  68. Sassa, C. & K. Kawaguchi, 2004. Larval feeding habits of Diaphus garmani and Myctophum asperum (Pisces: Myctophidae) in the transition region of the western North Pacific. Marine Ecology Progress Series 278: 279–290.CrossRefGoogle Scholar
  69. Shannon, C., 1948. A mathematical theory of communication. Bell System Technology Journal 27: 379:423, 623–656.Google Scholar
  70. Somarakis, S. & N. Nikolioudakis, 2007. Oceanographic habitat, growth and mortality of larval anchovy (Engraulis encrasicolus) in the northern Aegean Sea (eastern Mediterranean). Marine Biology 152: 1143–1158.CrossRefGoogle Scholar
  71. Somarakis, S. & N. Nikolioudakis, 2010. What makes a late anchovy larva? The development of the caudal fin seen as a milestone in fish ontogeny. Journal of Plankton Research 32: 317–326.CrossRefGoogle Scholar
  72. Strydom, N. A., K. Sutherland & T. H. Wooldridge, 2014. Diet and prey selection in late-stage larvae of five species of fish in a temperate estuarine nursery. African Journal of Marine Science 36: 85–98.CrossRefGoogle Scholar
  73. Tudela, S. & I. Palomera, 1997. Trophic ecology of the European anchovy Engraulis encrasicolus in the Catalan Sea (northwest Mediterranean). Marine Ecology Progress Series 160: 121–134.CrossRefGoogle Scholar
  74. Tudela, S., I. Palomera & G. Quílez, 2002. Feeding of anchovy Engraulis encrasicolus larvae in the north-west Mediterranean. Journal of the Marine Biological Association of the United Kingdom 82: 349–350.CrossRefGoogle Scholar
  75. Uriarte, A., P. Prouzet & B. Villamor, 1996. Bay of Biscay and Ibero Atlantic anchovy populations and their fisheries. Scientia Marina 60: 237–255.Google Scholar
  76. Urtizberea, A. & Ø. Fiksen, 2013. Effects of prey size structure and turbulence on feeding and growth of anchovy larvae. Environmental Biology of Fishes 96: 1045–1063.CrossRefGoogle Scholar
  77. Urtizberea, A., Ø. Fiksen, A. Folkvord & X. Irigoien, 2008. Modelling growth of larval anchovies including diel feeding patterns, temperature and body size. Journal of Plankton Research 30: 1369–1383.CrossRefGoogle Scholar
  78. Voss, R., F. W. Köster & M. Dickmann, 2003. Comparing the feeding habits of co-occurring sprat (Sprattus sprattus) and cod (Gadus morhua) larvae in the Bornholm Basin, Baltic Sea. Fisheries Research 63: 97–111.CrossRefGoogle Scholar
  79. Yasue, N., R. Doiuchi, Y. Yoshimoto & T. Takeuchi, 2010. Diet of late larval Japanese anchovy Engraulis japonicus in the Kii Channel, Japan. Fisheries Science 76: 63–73.CrossRefGoogle Scholar

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© Springer International Publishing Switzerland 2016

Authors and Affiliations

  1. 1.Department of Science EducationBegoñako Andra Mari Teacher Training University College, BAMBilbaoSpain
  2. 2.Department of Plant Biology and Ecology, Faculty of Science and TechnologyUniversity of the Basque Country, UPV/EHUBilbaoSpain
  3. 3.Marine Research UnitAZTI-TecnaliaPasaiaSpain
  4. 4.Department of Plant Biology and Ecology, Faculty of PharmacyUniversity of the Basque Country, UPV/EHUVitoria-GasteizSpain

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