Trophic interactions of uncommon batoid species in the Sea of Marmara

Trophic interactions of uncommon batoid species in the Sea of Marmara

Güzin Gül, Nazli Demirel

ORCID IDs: G.G. 0000-0001-5888-3211; N.D. 0000-0003-4542-9276

Institute of Marine Sciences and Management, İstanbul University, TURKEY


The feeding habits and trophic levels of three uncommon batoid species (Dasyatis pastinaca, Myliobatis aquila, Torpedo marmorata) were investigated in the Sea of Marmara, with two different methodical approaches: stomach content analysis and stable isotope analysis. The stomach contents indicated that the teleost species is the most important prey group for D. pastinaca and T. marmorata, while Mollusca is the main prey group for M. aquila. Niche breadths were calculated 0.54 for D. pastinaca while 0.29 for M. aquila. No significant diet overlap was detected between D. pastinaca and M. aquila (0.21) based on Pianka index. δ15N muscle and δ15N liver values statistically differed between D. pastinaca and M. aquila (Fpseudomuscle=33.736, p=0.03; Fpseudoliver= 26.173, p= 0.01). The trophic levels were 4.20±0.73 for D. pastinaca, 4.04±0.63 for M. aquila and for T. marmorata 4.46±0.79 by stomach content analysis. The trophic levels of species from stable isotope analysis by δ15N were calculated as 3.67 for T. marmorata, 3.32 for D. pastinaca and 2.56 for M. aquila. The difference in trophic levels may be explained by long-term and short-term feeding strategy of these species. Torpedo marmorata and M. aquila have higher δ15N values compared to samples from other regions of the Mediterranean.

Keywords: Elasmobranchii, stomach content analysis, stable isotope analysis, trophic levels, diet overlap, niche breadth

pdf-dl icon


Abdel-Aziz, S.H. (1994) Observations on the biology of the common torpedo (Torpedo torpedo, Linnaeus, 1758) and marbled electric ray (Torpedo marmorata, Risso, 1810) from Egyptian Mediterranean waters. Marine and Freshwater Research 45: 693-704.

Barría, C., Coll, M., Navarro, J. (2015) Unravelling the ecological role and trophic relationships of uncommon and threatened elasmobranchs in the western Mediterranean Sea. Marine Ecology Progress Series 539: 225-240.

Baum, J.K., Myers, R.A., Kehler, D.G., Worm, B., Harley, S.J., Doherty, P.A. (2003) Collapse and conservation of shark populations in the Northwest Atlantic. Science 299: 389-392.

Baum, J.K., Worm, B. (2009) Cascading top‐down effects of changing oceanic predator abundances. Journal of Animal Ecology 78: 699-714.

Beşiktepe, Ş.T., Sur, H.İ., Özsoy, E., Latif, M.A., Oǧuz, T., Ünlüata, Ü. (1994) The circulation and hydrography of the Marmara Sea. Progress in Oceanography 34: 285-334.

Bligh, E.G., Dyer, W.J. (1959) A rapid method of total lipid extraction and purification. Canadian Journal of Biochemistry and Physiology 37: 911-917.

Carlisle, A.B., Litvin, S.Y., Madigan, D.J., Lyons, K., Bigman, J.S., Ibarra, M., Bizzarro, J.J. (2017) Interactive effects of urea and lipid content confound stable isotope analysis in elasmobranch fishes. Canadian Journal of Fisheries and Aquatic Sciences 74: 419-428.

Cortés, E. (1997) A critical review of methods of studying fish feeding based on analysis of stomach contents: application to elasmobranch fishes. Canadian Journal of Fisheries and Aquatic Sciences 54(3): 726-738.

Dulvy, N.K., Fowler, S.L., Musick, J.A., Cavanagh, R.D., Kyne, P.M., Harrison, L.R., Carlsoni J.K., Davidson, L.N.K., Fordham, S.V., Francis, M.P., Pollock, C. M., Simpfendorfer, C.A., Burgess, G.H., Carpenter, K.E., Compagno, L.J.V., Ferretti, F., Worm, B., Britten, G.L., Heithaus, M.R., Lotze, H.K. (2010) Patterns and ecosystem consequences of shark declines in the ocean. Ecology Letters 13: 1055-1071.

Froese, R., D. Pauly. (Eds.) (2020) FishBase. World Wide Web electronic publication., (accessed 8 Oct 2020).

Fry, B. (2006) Stable Isotope Ecology. London; England: Springer.

Grossman, G.D. (1986) Food resource partitioning in a rocky intertidal fish assemblage. Journal of Zoology 1: 317-355.

Hairston, N.G., Smith, F.E., Slobodkin, L.B. (1960) Community structure, population control, and competition. American Naturalist 421-425.

Heupel, M.R., Knip, D.M., Simpfendorfer, C.A., Dulvy, N.K. (2014) Sizing up the ecological role of sharks as predators. Marine Ecology Progress Series 495: 291-298.

Hindell, J. S., Jenkins, G. P., Keough, M. J. (2000) Variability in abundances of fishes associated with seagrass habitats in relation to diets of predatory fishes. Marine Biology 136(4): 725-737.

Hussey, N.E., MacNeil, M.A., Fisk, A.T. (2010) The requirement for accurate diet-tissue discrimination factors for interpreting stable isotopes in sharks. Hydrobiologia 654: 1-5.

Hussey, N.E., MacNeil, M.A., McMeans, B.C., Olin, J.A., Dudley, S.F., Cliff, G., Winter, S.P., Fennesy, S.T., Fisk, A.T. (2014) Rescaling the trophic structure of marine food webs. Ecology Letters 17(2): 239-250.

Hussey, N.E., MacNeil, M.A., Olin, J.A., McMeans, B.C., Kinney, M.J., Chapman, D.D., Fisk, A.T. (2012) Stable isotopes and elasmobranchs: tissue types, methods, applications and assumptions. Journal of Fish Biology 80: 1449-1484.

Hyslop, E.J. (1980) Stomach contents analysis a review of methods and their application. Journal of Fish Biology 17: 411-429.

İşmen, A. (2003) Age, growth, reproduction and food of common stingray (Dasyatis pastinaca L., 1758) in Iskenderun Bay, the eastern Mediterranean. Fisheries Research 60: 169-176.

İşmen, A., Yigin, C.C., Inceoglu, H., Arslan, M., Daban, B., Kale, S., Kocabas, E., Sirin, M. (2013) Chondrichthyan bycatches in the beam trawl shrimp fishery of the Marmara Sea. Rapp Comm int Mer Médit 40: 487.

Jacobsen, I.P., Bennett, M.B. (2013) A comparative analysis of feeding and trophic level ecology in stingrays (Rajiformes; Myliobatoidei) and electric rays (Rajiformes: Torpedinoidei). PLoS ONE 8: e71348.

Jardas, I., Šantić, M., Pallaoro, A. (2004) Diet composition of the eagle ray, Myliobatis aquila (Chondrichthyes: Myliobatidae), in the eastern Adriatic. Cybium 28(4): 372-374.

Jeschke, J.M., Kokko, H. (2009) The roles of body size and phylogeny in fast and slow life histories. Evolutionary Ecology 23: 867-878.

Kabasakal, H. (2016) Status of cartilaginous fishes in the Sea of Marmara. In: The Sea of Marmara-Marine Biodiversity, Fisheries, Conservation and Governance, (eds., Özsoy, E., Çağatay, M. N., Balkıs, N., Balkıs, N., Öztürk, B.) Turkish Marine Research Foundation, İstanbul, pp. 903-918.

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.

Karachle, P.K., Stergiou, K.I. (2010) Food and feeding habits of nine elasmobranch species in the N Aegean Sea. Rapp Comm int Mer Médit 39: 553.

Karachle, P.K., Stergiou, K.I. (2017) An update on the feeding habits of fish in the Mediterranean Sea (2002-2015). Mediterranean Marine Science 18(1): 43-52.

Keskin, C. (2007) Temporal variation of fish assemblages in different shallow-water habitats in Erdek Bay, Marmara Sea, Turkey. Journal of the Black Sea/Medit Environ 13: 215-234.

Kim, S.L., Koch, P.L. (2012) Methods to collect, preserve, and prepare elasmobranch tissues for stable isotope analysis. Environmental Biology of Fishes 95: 53-63.

Levins, R. (1968) Evolution in Changing Environments. Princeton University Press, Princeton, USA.

MEDITS (2013) MEDITS Handbook. Version n.7, 2013, MEDITS Working Group.

Mulas, A., Bellodi, A., Cannas, R., Carbonara, P., Cau, A., Marongiu, M.F., Pesci, P., Follesa, M.C. (2019) Resource partitioning among sympatric elasmobranchs in the central-western Mediterranean continental shelf. Marine Biology 166: 153.

Novakowski, G.C., Hahn, N.S., Fugi, R. (2008) Diet seasonality and food overlap of the fish assemblage in a pantanal pond. Neotropical Ichthyology 6(4): 567-576.

Pauly, D., Froese, R., Saa, P., Palomares, M.L., Christensen, V., Rius, J. (2000) TrophLab in MS access. Available at: download/ (accessed 8 Oct 2020).

Pianka, E.R. (1974) Niche overlap and diffuse competition. Proceedings of the National Academy of Sciences 71: 2141-2145.

Ponte, D., Barcelos, L.M.D., Santos, C., Medeiros, J., Barreiros, J.P. (2016) Diet of Dasyatis patinaca and Myliobatis aquila (Myliobatiformes) from the Azores, NE Atlantic. Cybium 40: 209-214.

Post, D.M., Layman, C.A., Arrington, D.A., Takimoto, G., Quattrochi, J., Montana, C.G. (2007) Getting to the fat of the matter: models, methods and assumptions for dealing with lipids in stable isotope analyses. Oecologia 152: 179-189.

Rosenblatt, A.E., Heithaus, M.R., Mather, M.E., Matich, P., Nifong, J.C., Ripple, W.J., Silliman, B.R. (2013) The roles of large top predators in coastal ecosystems: new insights from long term ecological research. Oceanography 26: 156-167.

Saadaoui, A., Saidi, B., Enajjar, S., Bradai, M.N. (2015) Reproductive biology of the common stingray Dasyatis pastinaca (Linnaeus, 1758) off the Gulf of Gabès (Central Mediterranean Sea). Cahiers de Biologie Marine 56: 389-96.

Saglam, H., Orhan, A. K., Kutlu, S., Aydin, I. (2010) Diet and feeding strategy of the common stingray Dasyatis pastinaca (Linnaeus, 1758) on the Turkish coast of southeastern Black Sea. Cahiers de Biologie Marine 51: 37-44.

Simpson, E.H. (1949) Measurement of diversity. Nature 163: 688.

Stergiou, K.I., Karpouzi, V.S. (2002) Feeding habits and trophic levels of Mediterranean fish. Reviews in Fish Biology and Fisheries 11(3): 217-254.

Stevens, J.D., Bonfil, R., Dulvy, N.K., Walker, P.A. (2000) The effects of fishing on sharks, rays, and chimaeras (chondrichthyans), and the implications for marine ecosystems. ICES Journal of Marine Science 57: 476-494.

Tiralongo, F., Messina, G., Lombardo, B.M. (2020) Biologic aspects of juveniles of the common stingray, Dasyatis pastinaca (Linnaeus, 1758) (Elasmobranchii, Dasyatidae), from the central Mediterranean Sea. Journal of Marine Science and Engineering 8: 269-280.

TUIK (2019) Turkish Statistical Institute. Fishery Statistics 2019: Turkey. Available at: (accessed 20 Sep 2020).

Ulman, A., Zengin, M., Demirel, N., Pauly, D. (2020) The lost fish of Turkey: A recent history of disappeared species and commercial fishery extinctions for the Turkish Marmara and Black Seas. Frontiers in Marine Science 7: 650.

Valls, M., Quetglas, A., Ordines, F., Moranta, J. (2011) Feeding ecology of demersal elasmobranchs from the shelf and slope off the Balearic Sea (western Mediterranean). Scientia Marina 75: 633-639.

Yeldan, H., Avsar, D., Manaşırlı, M. (2009) Age, growth and feeding of the common stingray (Dasyatis pastinaca, L., 1758) in the Cilician coastal basin, northeastern Mediterranean Sea. Journal of Applied Ichthyology 25: 98-102.

Yemişken, E. (2017) Comparison of the Effects of Trawl Fishing on Cartilaginous Fish Species in the Eastern Mediterranean Fishing Regions. PhD thesis. İstanbul University. (in Turkish).

Zanden, M. J.V., Rasmussen, J.B. (2001) Variation in δ15N and δ13C trophic fractionation: implications for aquatic food web studies. Limnology and Oceanography 46: 2061-2066.