Variation in the stable isotope trophic position of the bluefish Pomatomus saltatrix (Linnaeus, 1766) from two Mediterranean sites: insights from a global meta-analysis


Published: Oct 13, 2022
Keywords:
tailor trophic level d13C d15N Mediterranean Sea native invaders
FRANCESCO MANCINI
ANTONIO OSCAR LILLO
ROBERTA BARDELLI
SALVATRICE VIZZINI
GIORGIO MANCINELLI
https://orcid.org/0000-0002-5833-7322
Abstract

A direct consequence of sea warming is the shift in the distribution range of thermo-tolerant species that have the potential to determine novel inter-specific interactions, ultimately altering food web structures and ecosystem processes. In this study, we investigated the trophic position of the bluefish Pomatomus saltatrix (Linnaeus, 1766), a pelagic predator that has recently expanded its distribution in the Mediterranean basin and for which scant information is available on its functional role in recently-colonised areas. Nitrogen and carbon stable isotopes were determined in muscle tissues of bluefish specimens collected in south-east Italy in the Gulf of Taranto (NW Ionian Sea) and in the Strait of Otranto (SW Adriatic Sea) at two coastal sites showing contrasting oceanographic conditions. The bluefish trophic position (TP) was estimated using locally abundant forage fish species as isotopic baselines. The results indicated for bluefish from the Strait of Otranto a TP value of 5.1, significantly higher than that determined in the Gulf of Taranto (4.2), and exceeding stomach content-based estimations reported by the online database FishBase and by literature sources. A synthesis of 30 publications reporting isotopic data for the bluefish and its potential prey at a global scale indicated that the species’ trophic position varied considerably between 2.7 and 5.2. The observed variability depended on location
and on the baseline species used in the estimations. Yet, a significant difference in trophic position was observed for bluefish from transitional and inshore environments as compared with offshore areas, mirroring the results obtained from the Gulf of Taranto and the Strait of Otranto. The findings of the study highlight the high trophic plasticity characterizing the bluefish in recently colonized areas, suggesting that it may play a key role in facilitating the expansion of its distribution range. However, additional investigations are essential to provide an advanced resolution of the bluefish functional role in Mediterranean coastal food webs.

Article Details
  • Section
  • Research Article
Downloads
Download data is not yet available.
Author Biography
GIORGIO MANCINELLI, University of Salento
Dipartimento di Scienze e Tecnologie Biologiche ed Ambientali -DiSTeBA, Unisalento
References
Able, K.W., Rowe, P., Burlas, M., Byrne, D., 2003. Use of ocean and estuarine habitats by young-of-year bluefish (Pomatomus saltatrix) in the New York Bight. Fishery Bulletin, 101 (2), 201-214.
Aiello, A., Canora, F., Pasquariello, G., Spilotro, G., 2013. Shoreline variations and coastal dynamics: A space–time data analysis of the Jonian littoral, Italy. Estuarine, Coastal and Shelf Science, 129, 124-135.
Albo-Puigserver, M., Borme, D., Coll, M., Tirelli, V., Palomera, I. et al., 2019. Trophic ecology of range-expanding round sardinella and resident sympatric species in the NW Mediterranean. Marine Ecology Progress Series, 620, 139-154.
Annabi, A., Bardelli, R., Vizzini, S., Mancinelli, G., 2018. Baseline assessment of heavy metals content and trophic position of the invasive blue swimming crab Portunus segnis (Forskål, 1775) in the Gulf of Gabès (Tunisia). Marine Pollution Bulletin, 136, 454-463.
Artüz, M.L., 2003. 2002-2003 senesinin IX. ve III. ayları arasında Boğaziçi’nde avlanmış olan 1. yaş gurubuna ait lüfer balıkları Pomatomus saltatrix (Linnaeus, 1766) üzerine etüt. Fisheries Advisory Commission Technical Paper.
Azzurro, E., Sbragaglia, V., Cerri, J., Bariche, M., Bolognini, L. et al., 2019. Climate change, biological invasions, and the shifting distribution of Mediterranean fishes: a largescale survey based on local ecological knowledge. Global Change Biology, 25 (8), 2779-2792.
Bal, H., Yanik, T., Türker, D., 2020. Diet composition of bluefish Pomatomus saltatrix (Linnaeus, 1766) in the Sea of Marmara. Marine Science Technology Bulletin, 9 (1), 46-50.
Balzani, P., Vizzini, S., Frizzi, F., Masoni, A., Lessard, J.P. et al., 2021. Plasticity in the trophic niche of an invasive ant explains establishment success and long-term coexistence. Oikos, 130 (5), 691-696.
Bartley, T.J., McCann, K.S., Bieg, C., Cazelles, K., Granados, M. et al., 2019. Food web rewiring in a changing world. Nature Ecology & Evolution, 3 (3), 345-354.
Buckel, J.A., McKown, K.A., 2002. Competition between juvenile striped bass and bluefish: resource partitioning and growth rate. Marine Ecology Progress Series, 234, 191-204.
Buckel, J., Fogarty, M., Conover, D., 1999a. Foraging habits of bluefish, Pomatomus saltatrix, on the US east coast continental shelf. Fishery Bulletin, 97 (4), 758-775.
Buckel, J.A., Conover, D.O., Steinberg, N.D., McKown, K.A., 1999b. Impact of age-0 bluefish (Pomatomus saltatrix) predation on age-0 fishes in the Hudson River estuary: evidence for density-dependent loss of juvenile striped bass (Morone saxatilis). Canadian Journal of Fisheries and Aquatic Sciences, 56 (2), 275-287.
Carey, M.P., Sanderson, B.L., Barnas, K.A., Olden, J.D., 2012. Native invaders - Challenges for science, management, policy, and society. Frontiers in Ecology and the Environment, 10 (7), 373-381.
Carlucci, R., Bandelj, V., Ricci, P., Capezzuto, F., Sion, L. et al., 2018. Exploring spatio-temporal changes in the demersal and benthopelagic assemblages of the north-western Ionian Sea (central Mediterranean Sea). Marine Ecology Progress Series, 598, 1-19.
Champely, S., Ekstrom, C., Dalgaard, P., Gill, J., Weibelzahl, S. et al., 2020. pwr: Power analysis functions along the lines of Cohen (1988). R package version 1.3-0. http://cran.rproject. org/web/packages/pwr.
Cataudella, S., Spagnolo, M., 2011. Lo Stato della Pesca e dell’Acquacoltura nei Mari Italiani. Ministero delle Politiche Agricole Alimentari e Forestali, Rome, Italy. Avalable at: https://www.politicheagricole.it/flex/cm/pages/ServeBLOB. php/L/IT/IDPagina/5164
Ciancia, E., Coviello, I., Di Polito, C., Lacava, T., Pergola, N. et al., 2018. Investigating the chlorophyll-a variability in the Gulf of Taranto (North-western Ionian Sea) by a multi-temporal analysis of MODIS-Aqua Level 3/Level 2 data. Continental Shelf Research, 155, 34-44.
Darmaraki, S., Somot, S., Sevault, F., Nabat, P., Cabos Narvaez, W.D. et al., 2019. Future evolution of marine heatwaves in the Mediterranean Sea. Climate Dynamics, 53 (3), 1371-1392.
Dhieb, K., Ghorbel, M., Bouain, A., 2001. Regime alimentaire de Pomatomus saltatrix (Teleostei, Pomatomidae) dans le Golfe de Gabes, Tunisie. Rapport Commission International Mer Mediterranee, 36, 259.
Federico, I., Pinardi, N., Lyubartsev, V., Maicu, F., Causio, S. et al., 2020. Observational evidence of the basin-wide gyre reversal in the Gulf of Taranto. Geophysical Research Letters, 47 (22), e2020GL091030.
Froese, R., Pauly, D., 2022. FishBase. World Wide Web Electronic Publication, version (02/2022). Avaiable at www. fishbase.org.
Georgieva, Y.G., Daskalov, G.M., 2019. Shift in growth of an apex marine predator: bluefish Pomatomus saltatrix (L., 1766) (Perciformes: Potamonidae) in relation to changes in feeding. Acta Zoologica Bulgarica, 71 (1), 63-72.
Giraldo, C., Ernande, B., Cresson, P., Kopp, D., Cachera, M. et al., 2017. Depth gradient in the resource use of a fish community from a semi-enclosed sea. Limnology and Oceanography, 62 (5), 2213-2226.
Givan, O., Edelist, D., Sonin, O., Belmaker, J., 2018. Thermal affinity as the dominant factor changing Mediterranean fish abundances. Global Change Biology, 24 (1), e80-e89.
Habib, B., Yanik, T., Türker, D., 2020. Diet composition of bluefish Pomatomus saltatrix (Linnaeus, 1766) in the Sea of Marmara. Marine Science Technology Bulletin, 9 (1), 46-50.
Harding, J.M., Mann, R., 2001. Diet and habitat use by bluefish, Pomatomus saltatrix, in a Chesapeake Bay estuary. Environmental Biology of Fishes, 60 (4), 401-409.
Henry, A.K., Sorte, C.J.B., 2022. Impact assessment of coastal marine range shifts to support proactive management. Frontiers in Ecology and the Environment, 20 (3), 161-169.
Hijmans, R.J., Williams, E., Vennes, C., 2019. Geosphere. R package version 1.5-10. http://cran.r-project.org/web/packages/ geosphere.
Iveša, N., Piria, M., Gelli, M., Trnski, T., Špelić, I. et al., 2021. Feeding habits of predatory thermophilic fish species and species with subtropical affinity from recently extended distributional range in northeast Adriatic Sea, Croatia. Diversity, 13 (8), 357.
Jepsen, D.B., Winemiller, K.O., 2002. Structure of tropical river food webs revealed by stable isotope ratios. Oikos, 96 (1), 46-55.
Juanes, F., Conover, D.O., 1994. Rapid growth, high feeding rates, and early piscivory in young-of-the-year bluefish (Pomatomus saltatrix). Canadian Journal of Fisheries and Aquatic Sciences, 51 (8), 1752-1761.
Juanes, F., Hare, J.A., Miskiewicz, A.G., 1996. Comparing early life history strategies of Pomatomus saltatrix: a global approach. Marine and Freshwater Research, 47 (2), 365- 379.
Karachle, P., Stergiou, K., 2017. An update on the feeding habits of fish in the Mediterranean Sea (2002-2015). Mediterranean Marine Science, 18 (1), 43-52.
Karachle, P.K., Stergiou, K.I., 2008. The effect of season and sex on trophic levels of marine fishes. Journal of Fish Biology, 72 (6), 1463-1487.
Kellnreitner, F., 2012. The trophic structure of a Wadden Sea fish community and its feeding interactions with alien species, Mathematisch-Naturwissenschaftlichen Fakultät. Universität zu Kiel, Kiel, p. 55.
Kjeldgaard, M.K., Hewlett, J.A., Eubanks, M.D., 2021. Widespread variation in stable isotope trophic position estimates: patterns, causes, and potential consequences. Ecological Monographs, 91 (3), e01451.
Kopp, D., Lefebvre, S., Cachera, M., Villanueva, M.C., Ernande, B., 2015. Reorganization of a marine trophic network along an inshore–offshore gradient due to stronger pelagic– benthic coupling in coastal areas. Progress in Oceanography, 130, 157-171.
Lasiak, T.A., McLachlan, A., 1987. Opportunistic utilization of mysid shoals by surf-zone teleosts. Marine Ecology Progress Series, 37 (1), 7.
Lawson, C.L., Suthers, I.M., Smith, J.A., Schilling, H.T., Stewart, J. et al., 2018. The influence of ontogenetic diet variation on consumption rate estimates: a marine example. Scientific Reports, 8 (1), 10725.
Lejeusne, C., Chevaldonné, P., Pergent-Martini, C., Boudouresque, C.F., Pérez, T., 2010. Climate change effects on a miniature ocean: the highly diverse, highly impacted Mediterranean Sea. Trends in Ecology & Evolution, 25 (4), 250- 260.
Logan, J.M., Jardine, T.D., Miller, T.J., Bunn, S.E., Cunjak, R.A. et al., 2008. Lipid corrections in carbon and nitrogen stable isotope analyses: comparison of chemical extraction and modelling methods. Journal of Animal Ecology, 77 (4), 838-846.
Lucena, F.M., Vaske, T., Ellis, J.R., O’Brien, C.M., 2000. Seasonal variation in the diets of bluefish, Pomatomus saltatrix (Pomatomidae) and striped weakfish, Cynoscion guatucupa (Sciaenidae) in southern Brazil: implications of food partitioning. Environmental Biology of Fishes, 57 (4), 423-434.
Malavolti, S., De Felice, A., Costantini, I., Biagotti, I., Canduci, G. et al., 2018. Distribution of Engraulis encrasicolus eggs and larvae in relation to coastal oceanographic conditions (the South-western Adriatic Sea case study). Mediterranean Marine Science, 19 (1), 180-192.
Mancinelli, G., 2012. On the trophic ecology of Gammaridea (Crustacea: Amphipoda) in coastal waters: a European- scale analysis of stable isotopes data. Estuarine, Coastal and Shelf Science, 114, 130-139.
Mancinelli, G., Bardelli, R., Zenetos, A., 2021. A global occurrence database of the Atlantic blue crab Callinectes sapidus. Scientific Data, 8 (111), 1-10.
Mancinelli, G., Glamuzina, B., Petrić, M., Carrozzo, L., Glamuzina, L. et al., 2016. The trophic position of the Atlantic blue crab Callinectes sapidus Rathbun 1896 in the food web of Parila Lagoon (South Eastern Adriatic, Croatia): a first assessment using stable isotopes. Mediterranean Marine Science, 17 (3), 634-643.
Mancinelli, G., Guerra, M.T., Alujević, K., Raho, D., Zotti, M. et al., 2017. Trophic flexibility of the Atlantic blue crab Callinectes sapidus in invaded coastal systems of the Apulia region (SE Italy): A stable isotope analysis. Estuarine, Coastal and Shelf Science, 198, 421-431.
Mancinelli, G., Vizzini, S., Mazzola, A., Maci, S., Basset, A., 2013. Cross-validation of δ 15N and FishBase estimates of fish trophic position in a Mediterranean lagoon: the importance of the isotopic baseline. Estuarine, Coastal and Shelf Science, 135, 77-85.
Mancini, F., De Giorgi, R., Ludovisi, A., Vizzini, S., Mancinelli, G., 2021. Ontogenetic shift in the trophic role of the invasive killer shrimp Dikerogammarus villosus: a stable isotope study. Biological Invasions, 23, 1-15.
Marbà, N., Jorda, G., Agusti, S., Girard, C., Duarte, C.M., 2015. Footprints of climate change on Mediterranean Sea biota. Frontiers in Marine Science, 2 (56), 1-11.
Ojea, E., Lester, S.E., Salgueiro-Otero, D., 2020. Adaptation of Fishing Communities to Climate-Driven Shifts in Target Species. One Earth, 2 (6), 544-556.
Pantusa, D., D’Alessandro, F., Riefolo, L., Principato, F., Tomasicchio, G.R., 2018. Application of a coastal vulnerability index. A case study along the Apulian Coastline, Italy. Water, 10 (9), 1218.
Pellicani, R., Argentiero, I., Fidelibus, M.D., Zanin, G.M., Parisi, A. et al., 2020. Dynamics of the Basilicata Ionian coast: human and natural drivers. Rendiconti Lincei. Scienze Fisiche e Naturali, 31 (2), 353-364.
Pethybridge, H., Choy, C.A., Logan, J.M., Allain, V., Lorrain, A. et al., 2018. A global meta-analysis of marine predator nitrogen stable isotopes: relationships between trophic structure and environmental conditions. Global Ecology and Biogeography, 27 (9), 1043-1055.
Pilati, A., Vanni, M.J., 2007. Ontogeny, diet shifts, and nutrient stoichiometry in fish. Oikos, 116 (10), 1663-1674. Pita, I., Mouillot, D., Moullec, F., Shin, Y.-J., 2021. Contrasted patterns in climate change risk for Mediterranean fisheries. Global Change Biology, 27 (22), 5920-5933.
Post, D.M., 2002. Using stable isotopes to estimate trophic position: models, methods, and assumptions. Ecology, 83 (3), 703-718.
Post, D.M., Layman, C.A., Arrington, D.A., Takimoto, G., Quattrochi, J. et al., 2007. Getting to the fat of the matter: models, methods and assumptions for dealing with lipids in stable isotope analyses. Oecologia, 152 (1), 179-189.
Potts, W.M., Bealey, R.S.J., Childs, A.R., 2016. Assessing trophic adaptability is critical for understanding the response of predatory fishes to climate change: a case study of Pomatomus saltatrix in a global hotspot. African Journal of Marine Science, 38 (4), 539-547.
R Development Core Team, 2022. R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. http://www.R-project.org/.
Ricci, P., Libralato, S., Capezzuto, F., D’Onghia, G., Maiorano, P. et al., 2019. Ecosystem functioning of two marine food webs in the North-Western Ionian Sea (Central Mediterranean Sea). Ecology and Evolution, 9 (18), 10198-10212.
Rumolo, P., Bonanno, A., Barra, M., Fanelli, E., Calabrò, M. et al., 2016. Spatial variations in feeding habits and trophic levels of two small pelagic fish species in the central Mediterranean Sea. Marine Environmental Research, 115, 65-77.
Sabatés, A., Martín, P., Raya, V., 2012. Changes in life-history traits in relation to climate change: bluefish (Pomatomus saltatrix) in the northwestern Mediterranean. ICES Journal of Marine Science, 69 (6), 1000-1009.
Sanchez-Jerez, P., Fernandez-Jover, D., Bayle-Sempere, J., Valle, C., Dempster, T. et al., 2008. Interactions between bluefish Pomatomus saltatrix (L.) and coastal sea-cage farms in the Mediterranean Sea. Aquaculture, 282 (1), 61- 67.
Schiettekatte, N.M.D., Barneche, D.R., Villéger, S., Allgeier, J.E., Burkepile, D.E. et al., 2020. Nutrient limitation, bioenergetics and stoichiometry: A new model to predict elemental fluxes mediated by fishes. Functional Ecology, 34 (9), 1857-1869.
Schilling, H.T., Hughes, J.M., Smith, J.A., Everett, J.D., Stewart, J. et al., 2017. Latitudinal and ontogenetic variation in the diet of a pelagic mesopredator (Pomatomus saltatrix), assessed with a classification tree analysis. Marine Biology, 164 (4), 75.
Schindler, D.E., Eby, L.A., 1997. Stoichiometry of fishes and their prey: implications for nutrient recycling. Ecology, 78 (6), 1816-1831.
Signa, G., Mazzola, A., Tramati, C.D., Vizzini, S., 2017. Diet and habitat use influence Hg and Cd transfer to fish and consequent biomagnification in a highly contaminated area: Augusta Bay (Mediterranean Sea). Environmental Pollution, 230, 394-404.
Simberloff, D., 2011. Native Invaders, in: Simberloff, D., Rejmánek, M. (Eds.), Encyclopedia of Biological Invasions. University of California Press, Berkeley and Los Angeles, CA, pp. 472-475.
Sunday, J.M., Pecl, G.T., Frusher, S., Hobday, A.J., Hill, N. et al., 2015. Species traits and climate velocity explain geographic range shifts in an ocean-warming hotspot. Ecology Letters, 18, 944-953.
Szczebak, J.T., Taylor, D.L., 2011. Ontogenetic patterns in bluefish (Pomatomus saltatrix) feeding ecology and the effect on mercury biomagnification. Environmental Toxicology and Chemistry, 30, 1447-1458.
Tortonese, E., 1986. Pomatomidae, in: Whitehead, P.J.P., Bauchot, M.L., Hureau, J.C., Nielsen, J., Tortonese, E. (Eds.), Fishes of the Northeastern Atlantic and Mediterranean. UNESCO, Paris, pp. 812-813.
Vander Zanden, M.J., Cabana, G., Rasmussen, J.B., 1997. Comparing trophic position of freshwater fish calculated using stable nitrogen isotope ratios (δ15N) and literature dietary data. Canadian Journal of Fisheries and Aquatic Sciences, 54 (5), 1142-1158.
Verri, G., Pinardi, N., Oddo, P., Ciliberti, S.A., Coppini, G., 2018. River runoff influences on the Central Mediterranean overturning circulation. Climate Dynamics, 50 (5), 1675- 1703.
Villegas-Hernández, H., Lloret, J., Muñoz, M., 2015. Reproduction, condition and abundance of the Mediterranean bluefish (Pomatomus saltatrix) in the context of sea warming. Fisheries Oceanography, 24 (1), 42-56.
Vinagre, C., Madeira, C., Dias, M., Narciso, L., Mendonça, V., 2019. Reliance of coastal intertidal food webs on river input - Current and future perspectives. Ecological Indicators, 101, 632-639.
Wallingford, P.D., Morelli, T.L., Allen, J.M., Beaury, E.M., Blumenthal, D.M. et al., 2020. Adjusting the lens of invasion biology to focus on the impacts of climate-driven range shifts. Nature Climate Change, 10 (5), 398-405.
Wilk, S.J., 1977. Biological and fisheries data on bluefish, Pomatomus saltatrix (Linnaeus), NOAA (National Oceanic and Atmospheric Administration) Technical Report, p. 56.
Woodward, G., Benstead, J.P., Beveridge, O.S., Blanchard, J., Brey, T. et al., 2010. Ecological networks in a changing climate, in: Woodward, G. (Ed.), Advances in Ecological Research. Academic Press, pp. 71-138.
Most read articles by the same author(s)