The forgotten feeding ground: patterns in seasonal and depth-specific food intake of adult cod Gadus morhua in the western Baltic Sea.
Atlantic cod, Belt Sea, diet composition, feeding ecology, stomach content analysis, western Baltic cod
Journal
Journal of fish biology
ISSN: 1095-8649
Titre abrégé: J Fish Biol
Pays: England
ID NLM: 0214055
Informations de publication
Date de publication:
Mar 2021
Mar 2021
Historique:
revised:
05
11
2020
received:
16
06
2020
accepted:
15
11
2020
pubmed:
18
11
2020
medline:
17
4
2021
entrez:
17
11
2020
Statut:
ppublish
Résumé
This study presents the diet composition of western Baltic cod Gadus morhua based on 3150 stomachs sampled year-round between 2016 and 2017 using angling, gillnetting and bottom trawling, which enhanced the spatio-temporal coverage of cod habitats. Cod diet composition in shallow areas (<20 m depth) was dominated by benthic invertebrate species, mainly the common shore crab Carcinus maneas. Compared to historic diet data from the 1960s and 1980s (limited to depth >20 m), the contribution of herring Clupea harengus decreased and round goby Neogobius melanostomus occurred as a new prey species. Statistical modelling revealed significant relationships between diet composition, catch depth, fish length and season. Generalized additive modelling identified a negative relationship between catch depth and stomach content weight, suggesting reduced food intake in winter when cod use deeper areas for spawning and during peak summer when cod tend to avoid high water temperatures. The results of this study highlight the importance of shallow coastal areas as major feeding habitats of adult cod in the western Baltic Sea, which were previously unknown because samples were restricted to deeper trawlable areas. The results strongly suggest that historic stomach analyses overestimated the role of forage fish and underestimated the role of invertebrate prey. Eventually, this study shows the importance of a comprehensive habitat coverage for unbiased stomach sampling programmes to provide a more reliable estimation of top predator diet, a key information for food web analyses and multispecies models.
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
707-722Subventions
Organisme : BONUS BLUEWEBS project, supported by BONUS (Art 185), funded jointly by the EU, the Academy of Finland, Projektträger Jülich Germany, the State Education Development Agency of Latvia, the National Centre for Research and Development Poland, and the Swedish Research Council Formas
ID : 03F0772A
Organisme : Bundesministerium für Bildung und Forschung
ID : 01LC17058
Organisme : Federal Ministry of Education and Research
Organisme : Swedish Research Council Formas
Organisme : National Centre for Research and Development
Organisme : State Education Development Agency
Organisme : European Parliament
Organisme : European Union
Organisme : European Maritime and Fisheries Fund
Informations de copyright
© 2020 The Authors. Journal of Fish Biology published by John Wiley & Sons Ltd on behalf of The Fisheries Society of the British Isles.
Références
Akaike, H. (1974). A new look at the statistical model identification. IEEE Transactions on Automatic Control, 19(6), 716-723.
Almqvist, G., Strandmark, A. K., & Appelberg, M. (2010). Has the invasive round goby caused new links in the Baltic food webs? Environmental Biology of Fishes, 89(1), 79-93.
Andersen, N. G., Chabot, D., & Couturier, C. S. (2016). Modelling gastric evacuation in gadoids feeding on crustaceans. Journal of Fish Biology, 88, 1886-1903.
Arntz, W. E. (1974). A contribution to the feeding ecology of juvenile cod (Gadus morhua L.) in the Western Baltic. Rapp. P.-v. Réun. CIEM, 166, 13-19.
Arntz, W. E. (1977). The food of adult cod (Gadus morhua L.) in the western Baltic. Meeresforschung, 26, 61-69.
Bagge, O. (1979). The relationship between the size of predator and the size of prey in cod. ICES C.M., 8, 1-9.
Berner, M., & Vaske, B. (1985). Morphometric and meristic characters of cod stocks in the Baltic Sea. ICES CM, 11, 1-13.
Bleil, M., & Oeberst, R. (2005). Die Reproduktion von Dorschen (Gadus morhua L. und Gadus morhua callarias L.) in der Ostsee unter besonderer Berücksichtigung der Arkonasee. Informationen aus der Fischereiforschung, 52, 74-82.
Bleil, M., Oeberst, R., & Urrutia, P. (2009). Seasonal maturity development of Baltic cod in different spawning areas: importance of the Arkona Sea for the summer spawning stock. Journal of Applied Ichthyology, 25, 10-17.
Breheny, P., & Burchett, W. (2017). Visualization of regression models using visreg. The R Journal, 9, 56-71.
Brenner, M., Buck, B. H., Cordes, S., Dietrich, L., Jacob, U., Mintenbeck, K., et al. (2001). The role of iceberg scours in niche separation within the Antarctic fish genus Trematomus. Polar Biology, 24, 502-507.
Bromley, P. J. (1994). The role of gastric evaluation experiments in the quantifying the feeding rates of predatory fish. Reviews in Fish Biology and Fisheries, 4, 36-66.
Brownrigg, R. (2018). Mapdata: Extra Map Databases. Original S code by Becker, R.A. and Wilks, R. R package version 2.3.0. Retrieved from http://CRAN.R-project.org/package=mapdata
Byrnes, J. E., Reynolds, P. L., & Stachowicz, J. J. (2007). Invasions and extinctions reshape coastal marine food webs. PLoS One, 2(3), e295. http://doi.org/10.1371/journal.pone.0000295.
Casini, M., Käll, F., Hansson, M., Plikshs, M., Baranova, T., Karlsson, O., … Hjelm, J. (2016). Hypoxic areas, density-dependence and food limitation drive the body condition of heavily exploited marine fish predator. Royal Society Open Science, 3, 160416. https://doi.org/10.1098/rsos.160416.
Christoffersen, M., Svendsen, J. C., Behrens, J. W., Jepsen, N., & van Deurs, M. (2019). Using acoustic telemetry and snorkel surveys to study diel activity and seasonal migration of round goby (Neogobius melanostomus) in an estuary of the Western Baltic Sea. Fisheries Management and Ecology, 26(2), 172-182.
Corkum, L. D., Sapota, M. R., & Skora, K. E. (2004). The round goby, Neogobius melanostomus, a fish invader on both sides of the Atlantic Ocean. Biological Invasions, 6(2), 173-181.
dos Santos, J., & Jobling, M. (1995). Test of a food consumption model for the Atlantic cod. ICES Journal of Marine Science, 52, 209-219.
Dries, M., & Adelung, D. (1982). Die Schlei, ein Modell für die Verbreitung der Strandkrabbe Carcinus maenas. Helgoländer Meeresuntersuchungen, 35, 65-77.
Dziaduch, D. (2011). Diet composition of herring (Clupea harengus L.) and cod (Gadus morhua L.) in the southern Baltic Sea in 2007 and 2008. Oceanological and Hydrobiological Studies, 40, 96-109.
Fordham, S. E., & Trippel, E. A. (1999). Feeding behaviour of cod (Gadus morhua) in relation to spawning. Journal of Applied Ichthyology, 15, 1-9.
Freitas, C., Olsen, E. M., Moland, E., Ciannelli, L., & Knutsen, H. (2015). Behavioral response of Atlantic cod to sea temperature changes. Ecology and Evolution, 5(10), 2070-2083.
Freitas, C., Olsen, E. M., Knutsen, H., Albretsen, J., & Moland, E. (2016). Temperature-associated habitat selection in a cold-water marine fish. Journal of Animal Ecology, 85, 628-637.
Funk, S., Krumme, U., Temming, A., & Möllmann, C. (2020). Gillnet fishers' knowledge reveals seasonality in depth and habitat use of cod (Gadus morhua) in the Western Baltic Sea. ICES Journal of Marine Science, 77(5), 1816-1829.
Harvey, C. J., Cox, S. P., Essington, T. E., Hansson, S., & Kitchell, J. F. (2003). An ecosystem model of food web and fisheries interactions in the Baltic Sea. ICES Journal of Marine Science, 60(5), 939-950.
Hastie, T., & Tibshirani, R. (1986). Generalized additive models. Statistical Science, 1(3), 297-318.
Hayward, R. S., Margraf, F. J., Knight, C. T., & Glomski, D. J. (1989). Gear Bias in field estimations of the amount of food consumed by fish. Canadian Journal of Fisheries and Aquatic Sciences, 46(5), 874-876.
Heikinheimo, O. (2011). Interactions between cod, herring and sprat in the changing environment of the Baltic Sea: a dynamic model analysis. Ecological Modelling, 222(10), 1731-1742.
Hempel, M. (2017). Ecological niche of invasive round goby Neogobius melanostomus (Pallas, 1814) in the Kiel Canal and adjacent section of the Elbe River (Doctoral thesis), University of Hamburg, Hamburg, Germany. Retrieved from https://ediss.sub.uni-hamburg.de/volltexte/2018/9012/
Hop, H., Gjøsaeter, J., & Danielssen, D. S. (1992). Seasonal feeding ecology of cod (Gadus morhua L.) on the Norwegian Skagerrak coast. ICES Journal of Marine Science, 49, 453-461.
Horbowy, J. (1989). A multispecies model of fish stocks in the Baltic Sea. Dana, 7, 22-43.
Hüssy, K., St. John, M. A., & Böttcher, U. (1997). Food resource utilization by juvenile Baltic cod Gadus morhua: A mechanism potentially influencing recruitment success at the demersal juvenile stage? Marine Ecology Progress Series, 155, 199-208.
Hüssy, K., Hinrichsen, H.-H., Eero, M., Mosegaard, H., Hemmer-Hansen, J., Lehmann, A., & Lundgaard, L. S. (2016). Spatio-temporal trends in stock mixing of eastern and western Baltic cod in the Arkona Basin and the implications for recruitment. ICES Journal of Marine Science, 73(2), 293-303.
ICES. (2017). Manual for the Baltic International Trawl Surveys (BITS). Series of ICES Survey Protocols SISP 7 - BITS. 95pp. Retrieved from http://www.ices.dk/sites/pub/Publication%20Reports/ICES%20Survey%20Protocols%20%28SISP%29/SISP%207%20-%20Manual%20for%20the%20Baltic%20International%20Trawl%20Surveys%20%28BITS%29.pdf
ICES. (2019a). Benchmark workshop on Baltic cod stocks (WKBALTCOD2). ICES Scientific Reports 9, 1, 310.
ICES (2019b). Herring assessment working Group for the Area South of 62° N (HAWG). ICES scientific reports. 1:2. 971 pp. Retrieved from http://doi.org/10.17895/ices.pub.5460
ICES. (2019c). Herring (Clupea harengus) in subdivisions 20-24, spring spawners (Skagerrak, Kattegat, and western Baltic). In Report of the ICES Advisory Committee, 2019, her.27.20-24. Retrieved from http://doi.org/10.17895/ices.advice.4715
Iyabo, U. B. (2014). Diet composition, feeding habitats and condition factor of Chrysichthys nigrodigitatus in Ebonyi river (a tropical flood river system), southeastern Nigeria. Continental Journal of Agricultural Science, 8(1), 29-37.
James, G., Witten, D., Hastie, T., & Tibshirani, R. (2013). An Introduction to statistical learning with applications in R (6th ed.). Springer: New York, NY.
Kulatska, N., Neuenfeldt, S., Beier, U., Elvarsson, B. Þ., Wennhage, H., Stefansson, G., & Bartolino, V. (2019). Understanding otongenetic and temporal variability of eastern Baltic cod diet using multispecies model and stomach data. Fisheries Research, 211, 338-349.
Leppäranta, M., & Myrberg, K. (2009). Physical Oceanography of the Baltic Sea. Berlin, Germany: Springer.
Lindegren, M., Möllmann, C., Nielsen, A., Brander, K., MacKenzie, B. R., & Stenseth, N. C. (2010). Ecological forecasting under climate change: The case of Baltic cod. Proceedings Biological Sciences, 277(1691), 2121-2130.
Lindegren, M., Andersen, K. H., Casini, M., & Neuenfeldt, S. (2014). A metacommunity perspective on source-sink dynamics and management: The Baltic Sea as a case study. Ecological Applications, 24(7), 1820-1832.
McFadden, D. (1974). Conditional logit analysis of qualitative choice behavior. In P. Zarembka (Ed.), Frontiers in econometrics (pp. 105-142). Academic Press: New York, NY.
McQueen, K., Hrabowski, J., & Krumme, U. (2019). Age validation of juvenile cod in the Western Baltic Sea. ICES Journal of Marine Science, 76(2), 430-441.
Möllmann, C., Diekmann, R., Müller-Karulis, B., Kornilovs, G., Plikshs, M., & Axe, P. (2009). Reorganization of large marine ecosystem due to atmospheric and anthropogenic pressure: a discontinuous regime shift in the Central Baltic Sea. Global Change Biology, 15(6), 1377-1393.
Mohrholz, V., Naumann, M., Nausch, G., Krüger, S., & Gräwe, U. (2015). Fresh oxygen for the Baltic Sea - an exceptional saline inflow after a decade of stagnation. Journal of Marine Systems, 148, 152-166.
Murtagh, F., & Legendre, P. (2014). Ward's hierarchical agglomerative clustering method: which algorithms implement Ward's criterion? Journal of Classification, 31, 274-295.
Neuenfeldt, S., Bartolino, V., Orio, A., Andersen, K. H., Andersen, N. G., Niiranen, S., et al. (2019). Feeding and growth of Atlantic cod (Gadus morhua L.) in the eastern Baltic Sea under environmental change. ICES Journal of Marine Science, 77(2), 624-632.
Neuenfeldt, S., & Köster, F. W. (2000). Trophodynamic control on recruitment success in Baltic cod: the influence of cannibalism. ICES Journal of Marine Science, 57(2), 300-309.
Nielsen, E. E., Hansen, M. M., Ruzzante, D. E., Meldrup, D., & Grønkjaer, P. (2003). Evidence of a hybrid-zone in Atlantic cod (Gadus morhua) in the Baltic and the Danish Belt Sea revealed by individual admixture analysis. Molecular Ecology, 12, 1497-1508.
Nissling, N., & Westin, L. (1997). Salinity requirements for successful spawning of Baltic and Belt Sea cod and the potential for cod stock interactions in the Baltic Sea. Marine Ecology Progress Series, 152, 261-271.
Norkko, A., Thrush, S. F., Cummings, V. J., Gibbs, M. M., Andrew, N. L., Norkko, J., & Schwarz, A.-M. (2007). Trophic structure of coastal and Antarctic food webs associated with changes in sea ice and food supply. Ecology, 88, 2810-2820.
Oesterwind, D., Bock, C., Förster, A., Gabel, M., Henseler, C., Kotterba, P., … Winkler, H. M. (2017). Predator and prey: the role of the round gobyNeogobius melanostomusin the western Baltic. Marine Biology Research, 13(2), 188-197.
Pachur, M. E., & Horbowy, J. (2013). Food composition and prey selection of cod, Gadus morhua (Actinopterygii: Gadiformes: Gadidae), in the southern Baltic Sea. Acta Ichthyologica et Piscatoria, 43(2), 109-118.
Paul, K., Oeberst, R., & Hammer, C. (2013). Evaluation of otolith shape analysis as a tool for discriminating adults of Baltic cod stocks. Journal of Applied Ichthyology, 29(4), 743-750.
Petereit, C., Hinrichsen, H.-H., Franke, A., & Köster, F. W. (2014). Floating along buoyancy levels: dispersal and survival of western Baltic fish eggs. Progress in Oceanography, 122, 131-152.
Pihl, L., & Rosenberg, R. (1982). Production, abundance, and biomass of mobile epibenthic marine fauna in shallow waters, western Sweden. Journal of Experimental Marine Biology and Ecology, 57, 273-301.
R Development Core Team. (2017). R: A language and environment for statistical computing. Vienna, Austria: R Foundation for Statistical Computing. Retrieved from https://www.R-project.org/.
Røjbek, M. C., Tomkiewicz, J., Jacobsen, C., & Støttrup, J. G. (2014). Forage fish quality: seasonal lipid dynamics of herring (Clupea harengus L.) and sprat (Sprattus sprattus L.) in the Baltic Sea. ICES Journal of Marine Science, 71(1), 56-71.
Sala, E., Aburto-Oropeza, O., Reza, M., Peredes, G., & López-Lemus, L. G. (2004). Fishing down coastal food webs in the Gulf of California. Fisheries, 29(3), 19-25.
Saunders, R. L. (1963). Respiration of Atlantic cod. Journal of the Fisheries Research Board of Canada, 20(2), 373-386.
Sapota, M. R., & Skóra, K. E. (2005). Spread of alien (non-indigenous) fish species Neogobius melanostomus in the Gulf of Gdansk (South Baltic). Biological Invasions, 7, 157-164.
Sapota, M. R. (2012). NOBANIS - Invasive Alien Species Fact Sheet - Neogobius melanostomus. - From: Online Database of European Network on Invasive Alien Species - NOBANIS. Retrieved from http://www.nobanis.org
Schulz, N. (1987). First results of cod stomach investigations in the Western Baltic (ICES subdivisions 22 and 24) since 1978. ICES CM, 25, 1-23.
Schulz, N. (1988). Erste Ergebnisse der Nahrungsuntersuchungen zum Dorsch (Gadus morhua L.) der westlichen Ostsee unter besonderer Berücksichtigung seines Einflusses auf die Herings- und Sprottbestände in diesem Seegebiet. Fischereiforschung, 26, 29-36.
Schulz, N. (1989a). An analysis of the food intake of cod as a basis for multispecies assessments in the Western Baltic. Rapp. P.-v. Réun. CIEM, 190, 67-71.
Schulz, N. (1989b). Untersuchungen zur täglichen Nahrungsaufnahme (Tagesration) des Dorsches der westlichen Ostsee. Fischereiforschung, 27, 37-44.
Sick, K. (1965). Haemoglobin polymorphism of cod in the Baltic and the Danish Belt Sea. Hereditas, 54, 19-48.
Skora, K. E., & Stolarski, J. (1993). Neogobius melanostomus (Pallas 1811) a new immigrant species in the Baltic Sea. In Estuarine ecosystems and species: Proceedings of 2nd international estuary symposium (pp. 101-108). Gdynia, Crangon.
Snoeijs-Leijonmalm, P., & Andrén, E. (2017). Why is the Baltic Sea so special to live in? In P. Snoeijs-Leijonmalm, H. Schubert, & T. Radziejewska (Eds.), Biological oceanography of the Baltic Sea (pp. 23-84). Springer: Dordrecht, The Netherlands.
Stäbler, M., Kempf, A., Smout, S., & Temming, A. (2019). Sensitivity of multispecies maximum sustainable yields to trends in the top (marine mammals) and bottom (primary production) compartments of the southern North Sea food-web. PLoS One, 14(1), e0210882.
Temming, A., & Herrmann, P. (2003). Gastric evacuation in cod: Prey-specific evacuation rates for use in North Sea, Baltic Sea and Barents Sea multi-species models. Fisheries Research, 63, 21-41.
Tomczak, M. T., Niiranen, S., Hjerne, O., & Blenckner, T. (2012). Ecosystem flow dynamics in the Baltic proper - Using a multi-trophic dataset as a basis for food web modelling. Ecologial Modelling, 230, 123-147.
Ursin, E., & Arntz, W. (1985). On the prey size of cod (Gadus morhua) in the western Baltic. ICES CM, 14, 1-18.
Van Leeuwen, A., De Roos, A. M., & Persson, L. (2008). How cod shapes its world. Journal of Sea Research, 60(1-2), 89-104.
Venables, W. N., & Ripley, B. D. (2002). Modern applied statistics with S (4th ed.). New York, NY: Springer.
Weber, W., & Damm, U. (1991). Investigations on cod stomachs in the western Baltic 1981-1989. ICES CM, 23, 1-17.
Weist, P., Schade, F. M., Damerau, M., Barth, J. M. I., Dierking, J., André, C., … Krumme, U. (2019). Assessing SNP-markers to study population mixing and ecological adaptation in Baltic cod. PLoS One, 14(6), e0218127. http://doi.org/10.1371/journal.pone.0218127.
Wickham, H. (2007). Reshaping data with the reshape package. Journal of Statistical Software, 21(12), 1-20.
Wickham, H. (2009). ggplot2: Elegant graphics for data analysis. New York, NY: Springer.
Wickham, H. (2011). The Split-apply-combine strategy for data analysis. Journal of Statistical Software, 40(1), 1-29.
Wilke, C.O. (2017). cowplot: Streamlined Plot Theme and Plot Annotations for ‘ggplot2’. R package version 0.9.2. Retrieved from http://CRAN.R-project.org/package=cowplot
Wood, S. N. (2011). Fast stable restricted maximum likelihood estimation of semiparametric generalized linear models. Journal of the Royal Statistical Society (B), 73(1), 3-36.
Zarkeschwari, N. (1977). Nahrungsuntersuchungen am Dorsch (Gadus morhua) im Flachwasser vor Surendorf (Kieler Bucht). (Diplom Thesis, Christian-Albrechts-Universität Kiel, Institut für Meereskunde, Germany). (The thesis has been lodged at the library of the Christian-Albrechts-Universität Kiel as a permanent addition to the collection there)