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Intraguild predation between small pelagic fish in the Bay of Biscay: impact on anchovy (Engraulis encrasicolus L.) egg mortality

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Abstract

Small pelagic fish can play an important role in various ecosystems linking lower and upper trophic levels. Among the factor behind the observed inter-annual variations in small pelagic fish abundance, intra- and inter-specific trophic interactions could have a strong impact on the recruitment variability (e.g. anchovy). Egg cannibalism observed in anchovies has been postulated to be a mechanism that determines the upper limit of the population density and self-regulates the population abundance of the species. On the other hand, predation by other guild species is commonly considered as a regulation mechanism between competing species. This study provides empirical evidence of anchovy cannibalism and predation of the main small pelagic fish species on anchovy eggs and estimates the effect of intraguild predation on the anchovy egg mortality rate. Results show that, depending on the year (2008–2009), up to 33 % of the total anchovy egg mortality was the result of sardine predation and up to 4 % was the result of egg cannibalism together with predation by Atlantic and Atlantic Chub mackerel and sprat. Results also indicate that in the Bay of Biscay, fluctuations in the survival index of the early life stages of anchovy are likely to be attributable at least in part to egg cannibalism and especially to a high sardine predation on anchovy eggs.

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References

  • Alheit J (1987) Egg cannibalism versus egg predation: their significance in anchovies. S Afr J Mar Sci 5:467–470

    Article  Google Scholar 

  • Allain G, Petitgas P, Lazure P (2001) The influence of mesoscale ocean processes on anchovy (Engraulis encrasicolus) recruitment in the Bay of Biscay, estimated with a three-dimensional hydrodynamic model. Fish Oceanogr 10:151–163

    Article  Google Scholar 

  • Bachiller (2012) Trophic ecology of small pelagic fish in the Bay of Biscay: ecological effects of trophic interactions. Ph.D. Thesis, University of the Basque Country (Leioa), Spain

  • Bachiller E, Irigoien X (2013) Allometric relations and consequences for feeding in small pelagic fish in the Bay of Biscay. ICES J Mar Sci 70:232–243

    Article  Google Scholar 

  • Bachiller E, Cotano U, Boyra G, Irigoien X (2013) Spatial distribution of the stomach weights of juvenile anchovy (Engraulis encrasicolus L.) in the Bay of Biscay. ICES J Mar Sci 70:362–378

    Article  Google Scholar 

  • Bakun A (1993) The California Current, Benguela Current, and Southwestern Atlantic Shelf ecosystems: a comparative approach to identifying factors regulating biomass yields. In: Sherman K, Alexander LM, Gold B (eds) Large marine ecosystems: stress, mitigation, and sustainability. American Association for the Advancement of Science, Washington, DC, pp 199–224

    Google Scholar 

  • Baumgartner TR, Soutar A, Ferreira-Bartrina V (1992) Reconstruction of the history of Pacific sardine and northern anchovy populations over the past two millennia from sediments of the Santa Barbara Basin, California. CalCOFI Rep 33:24–40

    Google Scholar 

  • Bernreuther M, Herrmann JP, Temming A (2008) Laboratory experiments on the gastric evacuation of juvenile herring (Clupea harengus L.). J Exp Mar Biol Ecol 363:1–11

    Article  Google Scholar 

  • Bernreuther M, Temming A, Herrmann JP (2009) Effect of temperature on the gastric evacuation in sprat Sprattus sprattus. J Fish Biol 75:1525–1541

    Article  CAS  Google Scholar 

  • Borja A, Uriarte A, Valencia V, Motos L, Uriarte A (1996) Relationships between anchovy (Engraulis encrasicolus L.) recruitment and the environment in the Bay of Biscay. Sci Mar 60:179–192

    Google Scholar 

  • Borja A, Uriarte A, Egaña J, Motos L, Valencia V (1998) Relationships between anchovy (Engraulis encrasicolus L.) recruitment and the environment in the Bay of Biscay (1967–1996). Fish Oceanogr 7:375–380

    Article  Google Scholar 

  • Bromley PJ (1994) The role of gastric evacuation experiments in quantifying the feeding rates of predatory fish. Rev Fish Biol Fish 4:36–66

    Article  Google Scholar 

  • Chavez FP, Ryan J, Lluch-Cota SE, Ñiquen M (2003) From anchovies to sardines and back: multidecadal change in the Pacific Ocean. Science 299:217–221

    Article  CAS  Google Scholar 

  • Ciechomski JD (1967) Investigations of food and feeding habits of larvae and juveniles of the Argentine anchovy Engraulis anchoita. CalCOFI Rep 11:72–81

    Google Scholar 

  • Conway CVP, Coombs SH, Lindley JA, Llewellyn CA (1999) Diet of mackerel (Scomber scombrus) larvae at the shelf-edge to the south-west of the British Isles and the incidence of piscivory and coprophagy. Vie et milieu 49:213–220

    Google Scholar 

  • Cotano U, Irigoien X, Etxebeste E, Alvarez P, Zarauz L, Mader J, Ferrer L (2008) Distribution, growth and survival of anchovy larvae (Engraulis encrasicolus L.) in relation to hydrodynamic and trophic environment in the Bay of Biscay. J Plankton Res 30:467–481

    Article  Google Scholar 

  • Dahl K, Kirkegaard E (1986) Stomach contents of mackerel, horse mackerel and whiting in the eastern part of the North Sea in July 1985. ICES CM 1986/H:68

  • Dahl K, Kirkegaard E (1987) The diet and consumption of horse mackerel (Trachurus trachurus) in the eastern North Sea, August 1986. ICES CM 1987/H:43

  • Darbyson E, Swain DP, Chabot D, Castonguay M (2003) Diel variation in feeding rate and prey composition of herring and mackerel in the southern Gulf of St Lawrence. J Fish Biol 63:1235–1257

    Article  Google Scholar 

  • De Mendiola BR (1969) Contenido estomacal de anchoveta en cuatro áreas de la costa Peruana. vol 27. Instituto del Mar del Perú  (IMARPE), Callao, Perú

  • Fox LR (1975) Cannibalism in natural populations. Ann Rev Ecol Syst 6:87–106

    Article  Google Scholar 

  • 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 Progr Ser 330:189–199

    Article  Google Scholar 

  • Garrido S, Ben-Hamadou R, Oliveira PB, Cunha ME, Chicharo MA, van der Lingen CD (2008) Diet and feeding intensity of sardine Sardina pilchardus: correlation with satellite-derived chlorophyll data. Mar Ecol Progr Ser 354:245–256

    Article  Google Scholar 

  • Gennotte V, Torre M, Kallianiotis A (2007) Cannibalism in anchovy (Engraulis encrasicolus) in the North Aegean Sea (Greece). Rapp Comm Int Mer Médit 38:484

    Google Scholar 

  • Gislason H (1999) Single and multispecies reference points for Baltic fish stocks. ICES J Mar Sci 56:571–583

    Article  Google Scholar 

  • Goñi N, Logan J, Arrizabalaga H, Jarry M, Lutcavage M (2011) Variability of albacore (Thunnus alalunga) diet in the Northeast Atlantic and Mediterranean Sea. Mar Biol 158:1057–1073

    Article  Google Scholar 

  • Harris RP, Wiebe PH, Lenz J, Skjoldal HR, Huntley M (2000) Zooplankton methodology manual, vol 1. Academic Press, London, p 684

    Google Scholar 

  • Hayasi S (1967) A note on the biology and fishery of the Japanese anchovy Engraulis japonica (Houttuyn). CalCOFI Rep 11:44–57

    Google Scholar 

  • Hunter JR, Kimbrell CA (1980) Egg cannibalism in the northern anchovy, Engraulis mordax. Fish Bull 78:811–816

    Google Scholar 

  • Huse G, Holst JC, Utne K, Nøttestad L, Melle W, Slotte A, Ottersen G, Fenchel T, Uiblein F (2012) Effects of interactions between fish populations on ecosystem dynamics in the Norwegian Sea—results of the INFERNO project. Mar Biol Res 8:415–419

    Article  Google Scholar 

  • ICES (2008) Report of the Working Group on Anchovy (WGANC), 13–16 June, ICES Headquarters, Copenhagen. ICES CM 2008/ACOM:04

  • ICES (2009) Report of the Working Group on Anchovy and Sardine (WGANSA), 15–20 June, ICES Headquarters, Copenhagen. ICES CM 2009/ACOM:13

  • ICES (2011a) Report of the Working Group on Anchovy and Sardine (WGANSA), 24–28 June, Vigo, Spain. ICES CM 2011/ACOM:16

  • ICES (2011b) Report of the Working Group on Widely Distributed Stocks (WGWIDE), 23–29 August, ICES Headquarters, Copenhagen. ICES CM 2011/ACOM:15

  • Irigoien X, De Roos A (2011) The role of intraguild predation in the population dynamics of small pelagic fish. Mar Biol 158:1683–1690

    Article  Google Scholar 

  • Irigoien X, Fiksen O, Cotano U, Uriarte A, Alvarez P, Arrizabalaga H, Boyra G, Santos M, Sagarminaga Y, Otheguy P, Etxebeste E, Zarauz L, Artetxe I, Motos L (2007) Could Biscay Bay Anchovy recruit through a spatial loophole? Progr Oceanogr 74:132–148

    Article  Google Scholar 

  • Irigoien X, Cotano U, Boyra G, Santos M, Alvarez P, Otheguy P, Etxebeste E, Uriarte A, Ferrer L, Ibaibarriaga L (2008) From egg to juvenile in the Bay of Biscay: spatial patterns of anchovy (Engraulis encrasicolus) recruitment in a non-upwelling region. Fish Oceanogr 17:446–462

    Article  Google Scholar 

  • James AG, Findlay KP (1989) Effect of particle size and concentration on feeding behaviour, selectivity and rates of food ingestion by the Cape anchovy Engraulis capensis. Mar Ecol Progr Ser 50:275–294

    Article  Google Scholar 

  • Lasker R (1985) An egg production method for estimating spawning biomass of pelagic fish: application to the Northern anchovy Engraulis mordax. NOAA Technical Report NMFS 1985/36, p 110

  • Loukashkin AS (1970) On the diet and feeding behaviour of the Northern anchovy, Engraulis mordax (Girard). Proc Cal Ac Sci 37:419–458

    Google Scholar 

  • MacCall AD (1981) The consequences of cannibalism in the stock-recruitment relationship of planktivorous pelagic fishes such as Engraulis. Report and Supporting Documentation of the Workshop on the Effects of Environmental Variation on the Survival of Larval Pelagic Fishes, Lima (Peru), 20 Apr 1980. Sharp, G.D. (Conv. Ed.). Paris; Unesco: 201–220 (I.O.C. Workshop Rep. 28)

  • Massé J (1996) Acoustic observations in the Bay of Biscay: schooling, vertical distribution, species assemblages and behaviour. Sci Mar 60:227–234

    Google Scholar 

  • McCullagh P, Nelder JA (1989) Generalized linear models, monographs on statistics and applied probability, vol 37, 2nd edn. Champman and Hall, London, p 512

    Google Scholar 

  • Motos L (1994) Estimación de la biomasa desovante de la población de anchoa del Golfo de Vizcaya, Engraulis encrasicolus, a partir de su producción de huevos. Bases metodológicas y aplicación. Ph.D. Thesis, University of the Basque Country (Leioa), Spain

  • Motos L, Uriarte A, Valencia V (1996) The spawning environment of the Bay of Biscay anchovy (Engraulis encrasicolus L.). Sci Mar 60:117–140

    Google Scholar 

  • Motos L, Uriarte A, Prouzet P, Santos M, Alvarez P, Sagarminaga Y (2005) Assessing the Bay of Biscay anchovy population by DEPM: a review 1989–2001. In: Castro LR, Fréon P, van der Lingen CD, Uriarte A (eds) Report of the SPACC meeting on small pelagic fish spawning habitat dynamics and the daily egg production method (DEPM). GLOBEC Report 20

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

    Article  Google Scholar 

  • Olaso I (1990) Distribución y abundancia del megabentos invertebrado en fondos de la plataforma cantábrica. Publ Esp IEO 5:128

    Google Scholar 

  • Olaso I, Velasco F, Pérez N (1998) Importance of discarded blue whiting (Micromesistius poutassou) in the diet of lesser spotted dogfish (Scyliorhinus canicula) in the Cantabrian Sea. ICES J Mar Sci 55:331–341

    Article  Google Scholar 

  • Padovani LN, Viñas MD, Pájaro M (2011) Importance of the Río de la Plata estuarine front (Southwest Atlantic Ocean) in the feeding ecology of Argentine anchovy, Engraulis anchoita (Clupeiformes, Clupeidae). Lat Am J Aquat Res 39:205–213

    Article  Google Scholar 

  • Pájaro M (1993) Consideraciones sobre la alimentación de la caballa con especial énfasis en la depredación de huevos y larvas de peces. INIDEP Documento Científico 2:19–29

    Google Scholar 

  • Pájaro M (1998) El canibalismo como mecanismo regulador denso-dependiente de mortalidad natural en la anchoíta argentina (Engraulis anchoita). Su relación con las estrategias reproductivas de la especie. Ph.D. Thesis, Universidad Nacional de Mar del Plata, Facultad de Ciencias Exactas y Naturales (Mar del Plata), Argentina

  • Pájaro M, Ciechomski JD (1996) Canibalismo de la anchoíta adulta (Engraulis anchoita) sobre sus postlarvas, en un área de cría de la especie. Frente Marítimo 16:131–139

    Google Scholar 

  • Pájaro M, Curelovich J, Macchi GJ (2007) Egg cannibalism in the northern population of the Argentine anchovy, Engraulis anchoita (Clupeidae). Fish Res 83:253–262

    Article  Google Scholar 

  • Parker K (1980) A direct method for estimating northern anchovy, Engraulis mordax, spawning biomass. Fish Bull 78:541–544

    Google Scholar 

  • Planque B, Bellier E, Lazure P (2007) Modelling potential spawning habitat of sardine (Sardina pilchardus) and anchovy (Engraulis encrasicolus) in the Bay of Biscay. Fish Oceanogr 16:16–30

    Article  Google Scholar 

  • Plirú A, van der Kooij J, Engelhard GH, Fox CJ, Milligan SP, Hunter E (2012) Sprat feeding behaviour, selective predation, and impact on plaice egg mortality. ICES J Mar Sci 69:1019–1029

    Article  Google Scholar 

  • Plounevez S, Champalbert G (1999) Feeding behaviour and trophic environment of Engraulis encrasicolus (L.) in the Bay of Biscay. Est Coast Shelf Sci 49:177–191

    Article  Google Scholar 

  • Plounevez S, Champalbert G (2000) Diet, feeding behaviour and trophic activity of the anchovy (Engraulis encrasicolus L.) in the Gulf of Lions (Mediterranean Sea). Oceanol Acta 23:175–192

    Article  Google Scholar 

  • Ricker W (1958) Handbook of computation for biological studies of fish populations. Bull Fish Res Board Can 119:300

    Google Scholar 

  • Ricker W (1973) Linear regressions in fishery research. J Fish Res Board Can 30:409–434

    Article  Google Scholar 

  • Sánchez F, Olaso I (2004) Effects of fisheries on the Cantabrian Sea shelf ecosystem. Ecol Model 172:151–174

    Article  Google Scholar 

  • Santander H, Alheit J, MacCall AD, Alamo A (1983) Egg mortality of the Peruvian anchovy (Engraulis ringens) caused by cannibalism and predation by sardines (Sardinops sagax). In: Sharp GD, Csirke J (eds) Proceedings of the expert consultation to examine changes in abundance and species composition of neritic fish resources. FAO Fisheries Report 291, pp 1012–1025

  • Schwartzlose R, Alheit J, Bakun A, Baumgartner T, Cloete R, Crawford R, Fletcher W, Green-Ruiz Y, Hagen E, Kawasaki T (1999) Worldwide large-scale fluctuations of sardine and anchovy populations. S Afr J Mar Sci 21:289–347

    Article  Google Scholar 

  • Smith C, Reay P (1991) Cannibalism in teleost fish. Rev Fish Biol Fish 1:41–64

    Article  Google Scholar 

  • Smith PE, Flerx W, Hewitt RH (1985) The CalCOFI vertical egg tow (CalVET) net. NOAA Technical Report NMFS 36. In: Lasker R (ed) An egg production method for estimating spawning biomass of pelagic fish: application to the northern anchovy, Engraulis mordax. US Dep Commer, Washington, DC

    Google Scholar 

  • Somarakis S, Koutsikopoulos C, Machias A, Tsimenides N (2002) Applying the daily egg production method (DEPM) to small stocks in highly heterogeneous seas. Fish Res 55:193–204

    Article  Google Scholar 

  • Somarakis S, Palomera I, Garcia A, Quintanilla L, Koutsikopoulos C, Uriarte A, Motos L (2004) Daily egg production on anchovy in European waters. ICES J Mar Sci 61:944–958

    Article  Google Scholar 

  • Stratoudakis Y, Bernal M, Ganias K, Uriarte A (2006) The daily egg production method: recent advances, current applications and future challenges. Fish Fish 7:35–57

    Article  Google Scholar 

  • Takasuka A, Yoshioki O, Ichiro A (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

    Article  Google Scholar 

  • 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 Progr Ser 129:55–61

    Article  Google Scholar 

  • Tudela S, Palomera I (1997) Trophic ecology of the European anchovy Engraulis encrasicolus in the Catalan Sea (northwest Mediterranean). Mar Ecol Progr Ser 160:121–134

    Article  Google Scholar 

  • Uriarte A, Prouzet P, Villamor B (1996) Bay of Biscay and Ibero Atlantic anchovy populations and their fisheries. Sci Mar 60:237–255

    Google Scholar 

  • Uriarte A, Motos L, Alvarez P, Santos M, Prouzet P, Massé J (1999) Population estimates of the Bay of Biscay anchovy by the Daily Egg Production Method. Final Rep Eur Comm Proj 96:34

  • Valdés Szeinfeld E (1991) Cannibalism and intraguild predation in clupeoids. Mar Ecol Progr Ser 79:17–26

    Article  Google Scholar 

  • Valdés ES, Shelton PA, Armstrong MJ, Field JG (1987) Cannibalism in South African anchovy: egg mortality and egg consumption rates. In: Payne AIL, Gulland JA, Brink KH (eds) The Benguela and comparable ecosystems, vol 5. South African Journal of Marine Science, pp 613–622

  • 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 28:465–477

    Article  Google Scholar 

  • van der Lingen CD, Bertrand A, Bode A, Brodeur R, Cubillos LA, Espinoza P, Friedland K, Garrido S, Irigoien X, Miller T, Möllmann C, Rodríguez-Sánchez R, Tanaka H, Temming A (2009) Trophic dynamics. In: Checkley D, Alheit J, Oozeki Y, Roy C (eds) Climate change and small pelagic fish. Cambridge University Press, Cambridge, pp 112–157

    Google Scholar 

  • Villamor B, González Pola C, Lavín A, Valdés L, Lago de Lanzós A, Franco C, Cabanas J, Bernal M, Hernández C, Iglesias M (2011) Environmental control of Northeast Atlantic mackerel (Scomber scombrus) recruitment in the southern Bay of Biscay: case study of failure in the year 2000. Fish Oceanogr 20:397–414

    Article  Google Scholar 

  • Wiebe PH, Benfield MC (2003) From the Hensen net toward four-dimensional biological oceanography. Progr Oceanogr 56:7–136

    Article  Google Scholar 

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Acknowledgments

We are grateful to the captains and crew of the research vessel R/V Emma Bardán, as well as to the onboard scientists and analysts for their support during the sampling and laboratory work. Very special thanks are due to Marcelo Pájaro (INIDEP) for his help with the parameter calculations. We would also like to thank the Editor and the four anonymous reviewers who provided insightful comments that greatly improved the manuscript. This work was funded by the Ecoanchoa project (FEP Project, Department of Agriculture, Fisheries and Food of the Basque Country Government) and the EU FP7 FACTS (Forage Fish Interactions) project, Grant Agreement No. 244966. Eneko Bachiller was supported by a doctoral fellowship (2007–2011) from the Iñaki Goenaga Zentru Teknologikoen Fundazioa (IG-ZTF) and by a postdoctoral fellowship (2014–2016) from the Department of Education, Language policy and Culture of the Basque Country Government (EJ-GV). This is Contribution No. 712 from AZTI-Tecnalia (Marine Research Division).

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Bachiller, E., Cotano, U., Ibaibarriaga, L. et al. Intraguild predation between small pelagic fish in the Bay of Biscay: impact on anchovy (Engraulis encrasicolus L.) egg mortality. Mar Biol 162, 1351–1369 (2015). https://doi.org/10.1007/s00227-015-2674-0

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