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Trophic partitioning between abundant demersal sharks coexisting in the North Aegean Sea

Published online by Cambridge University Press:  27 March 2019

Emre Yemisken ,
Joan Navarro ,
Manuela Forero ,
Persefoni Megalofonou  and
Lutfiye Eryilmaz
Emre Yemisken*
Affiliation:
Department of Biology, Section of Hydrobiology, Faculty of Science, Istanbul University, Turkey
Joan Navarro
Affiliation:
Institut de Ciencies del Mar – CSIC, Passeig Maritim de la Barceloneta, 37-49 08003 Barcelona, Spain
Manuela Forero
Affiliation:
Department of Conservation Biology, Estacion Biologica de Donana (EBD-CSIC), Avda. Americo Vespucio s/n, Sevilla 41092, Spain
Persefoni Megalofonou
Affiliation:
Department of Conservation Biology, Estacion Biologica de Donana (EBD-CSIC), Avda. Americo Vespucio s/n, Sevilla 41092, Spain
Lutfiye Eryilmaz
Affiliation:
Department of Biology, Section of Hydrobiology, Faculty of Science, Istanbul University, Turkey Department of Biology, Section of Zoology Marine Biology, National and Kapodistrian University of Athens, Greece
*
Author for correspondence: Emre Yemisken, E-mail: [email protected]
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Abstract

We examined the feeding ecology (diet, trophic width and trophic position) of five demersal shark species (Mustelus mustelus Linnaeus, 1758, Galeus melastomus Rafinesque, 1810, Scyliorhinus canicula Linnaeus, 1758, Scyliorhinus stellaris Linnaeus, 1758, Squalus blainville, Risso, 1826) coexisting in the north-eastern Aegean Sea (around Gökçeda Island) by combining stomach content and stable isotope analyses. The results indicate clear differences in diet between the five sharks. Cephalopods were mainly found in diet of S. stellaris and M. mustelus and the stomachs of G. melastomus, S. canicula and S. blainville included fish. S. blainville showed the highest trophic position in respect of stable isotope analysis (TPsia = 4.89) around Gökçeada Island. It was followed by G. melastomus (TPsia = 4.57). Direct isotopic values (both stable nitrogen and carbon) and isotopic niche width based on the Standard Ellipse Area (SEA) clearly differed among the five shark species. In particular, S. blainville was isotopically segregated from the other shark species studied, showing a narrow isotopic trophic niche and higher trophic level. In contrast, M. mustelus had the widest trophic niche of the five species studied. The niche width of S. stellaris was narrower than M. mustelus and S. canicula but wider than S. blainville and G. melastomus. SEA showed that G. melastomus has a specialized feeding strategy in the area. There is no overlap between S. canicula and S. stellaris in trophic width.

Keywords

Aegean Seademersal sharksfeeding ecologyGokceada Islandstable isotopestrophic position
Type
Research Article
Information
Journal of the Marine Biological Association of the United Kingdom , Volume 99 , Issue 5 , August 2019 , pp. 1213 - 1219
Copyright
Copyright © Marine Biological Association of the United Kingdom 2019 

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References

Abdul Malak, D, Livingstone, SR, Pollard, D, Polidoro, BA, Cuttelod, A, Bariche, M, Bilecenoglu, M, Carpenter, KE, Collette, BB, Francour, P, Goren, M, Kara, MH, Enric, M, Papaconstantinou, C and Tunesi, L (2011) Overview of the Conservation Status of the Marine Fishes of the Mediterranean Sea. Gland, Switzerland and Malaga, Spain: International Union for Conservation of Nature (IUCN) ISBN: 978-2-8317-1307-6.Google Scholar
Albo-Puigserver, M, Navarro, J, Coll, M, Aguzzi, J, Cardona, L and Sáez-Liante, R (2015) Feeding ecology and trophic position of three sympatric demersal chondrichthyans in the northwestern Mediterranean. Marine Ecology Progress Series 524, 255–268.Google Scholar
Amundsen, PA, Gabler, HM and Staldvik, FJ (1996) A new approach to graphical analysis of feeding strategy from stomach contents data – modification of the Costello (1990) method. Journal of Fish Biology 48, 607–614.Google Scholar
Anastasopoulou, A, Mytilineou, C, Lefkaditou, E, Dokos, J, Smith, CJ, Siapatis, A, Bekas, P and Papadopoulou, KN (2013) Diet and feeding strategy of blackmouth catshark Galeus melastomus. Journal of Fish Biology 83, 1637–1655.Google Scholar
Barría, C, Navarro, J, Coll, M, Fernandez-Arcaya, U and Sáez-Liante, R (2015) Morphological parameters of abundant and threatened chondrichthyans of the northwestern Mediterranean Sea. Journal of Applied Ichthyology 31, 114–119.Google Scholar
Barría, C., Navarro, J. and Coll, M. (2018) Feeding habits of four sympatric sharks in two deep-water fishery areas of the western Mediterranean Sea. Deep-Sea Research Part I: Oceanographic Research Papers 142, 34–43.Google Scholar
Baum, JK and Worm, B (2009) Cascading top-down effects of changing oceanic predator abundances. Journal of Animal Ecology 78, 699–714.Google Scholar
Bello, G (1997) Cephalopods from the stomach contents of demersal chondrichthyans caught in the Adriatic Sea. Vie et Milieu 47, 221–227.Google Scholar
Bozzano, A, Murgia, AR, Vallerga, S, Hirano, J and Archer, S (2001) The photoreceptor system in the retinae of two dogfishes, Scyliorhinus canicula and Galeus melastomus: possible relationship with depth distribution and predatory lifestyle. Journal of Fish Biology 59, 1258–1278.Google Scholar
Bradai, MN, Saidi, B and Enajjar, S (2012) Elasmobranchs of the Mediterranean and Black Sea: Status, Ecology and Biology: A Bibliographic Analysis. Rome: FAO.Google Scholar
Çakır, DT, Koç, HT and Başusta, A (2006) Length-weight relationship of 24 fish species from Edremit Bay, Aegean Sea. e-Journal of New World Sciences Academy Natural and Engineering Sciences 3, 47–51.Google Scholar
Capapé, C (1974) Contribution a la biologie des Scyliorhinidae des cotes Tunisiennes. Annales de l'Institut Michel Pacha 7, 13–29.Google Scholar
Cihangir, B, Ünlüoğlu, B and Tıraşın, EM (1997) Distribution and some biological aspects of the lesser spotted dogfish (Chondrichthyes, Scyliorhinus canicula, Linnaeus, 1758) from the northern Aegean Sea. In Mediterranean Fisheries Congress, 9–11 April 1997, Izmir, pp. 585–603.Google Scholar
Compagno, LJV (1984) FAO species catalogue. Vol. 4. Sharks of the World. An annotated and illustrated catalogue of shark species known to date. Part 2 – Carcharhiniformes. FAO Fisheries Synopsis 125, 4/2, 251–655. Rome: FAO, ISBN 92-5-101383-7.Google Scholar
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, 726–738.Google Scholar
Cortés, E (1999) Standardized diet compositions and trophic levels of sharks. ICES Journal of Marine Science 56, 707–717.Google Scholar
De Niro, MJ and Epstein, S (1981) Isotopic composition of cellulose from aquatic organisms. Geochimica et Cosmochimica Acta 45, 1885–1894.Google Scholar
Dulvy, NK, Fowler, SL, Musick, JA, Cavanagh, RD, Kyne, PM, Harrison, LR, Carlson, JK, Davidson, LNK, Fordham, SV, Francis, MP, Pollock, CM, Simpfendorfer, CA, Burgess, GH, Carpenter, KE, Compagno, LJV, Ebert, DA, Gibson, C, Heupel, MR, Livingstone, SR, Sanciangco, JC, Stevens, JD, Valenti, S and White, WT (2014) Extinction risk and conservation of the world's sharks and rays. eLife 3, 1–83.Google Scholar
Ellis, JR, Pawson, MG and Shackley, SE (1996) The comparative feeding ecology of six species of shark and four species of ray (Elasmobranchii) in the North-East Atlantic. Journal of the Marine Biological Association of the United Kingdom 76, 89–106.Google Scholar
Eronat, E.G. (2012) Orta Ege Denizi'ndeki chondrichthyes (kıkırdaklı balık) türlerinin beslenme özelliklerinin belirlenmesi, Science Institute of Ege University (Master Thesis) 58 pp. [In Turkish].Google Scholar
Fanelli, E, Rey, J, Torre, P and Gil de Sola, L (2009) Feeding habits of blackmouth catshark Galeus melastomus Rafinesque, 1810 and velvet belly lantern shark Etmopterus spinax (Linnaeus, 1758) in the western Mediterranean. Journal of Applied Ichthyology 25, 83–93.Google Scholar
Ferretti, F, Osio, GC, Jenkins, CJ, Rosenberg, AA and Lotze, HK (2013) Long-term change in a meso-predator community in response to prolonged and heterogeneous human impact. Scientific Reports 3, 1057 pp.Google Scholar
Filiz, H (2009) Diet composition of smooth-hound, Mustelus mustelus (Linnaeus, 1758), in Aegean Sea, Turkey. Belgian Journal of Zoology 139, 81–84.Google Scholar
Filiz, H and Taskavak, E (2006) Sexual dimorphism in the head, mouth, and body morphology of the smallspotted catshark, Scyliorhinus canicula (Linnaeus, 1758) (Chondrichthyes: Scyliorhinidae) from Turkey. Acta Adriatica 47, 37–47.Google Scholar
Fry, B (2007) Stable Isotope Ecology. New York, NY: Springer Science and Business Media. ISBN-10: 0-387-30513-0.Google Scholar
Güreşen, A, Okudan, EŞ, Dural, B and Aysel, V (2015) An updated checklıst of marine flora on the continental shelf of Gökçeada Island (Northern Aegean Sea, Turkey). Aquaculture Engineering and Fisheries Research 3, 171–187.Google Scholar
Heithaus, MR, Vaudo, JJ, Kreicker, S, Layman, CA, Krützen, M, Burkholder, DA, Gastrich, K, Bessey, C, Sarabia, R and Cameron, K (2013) Apparent resource partitioning and trophic structure of large-bodied marine predators in a relatively pristine seagrass ecosystem. Marine Ecology Progress Series 481, 225–237.Google Scholar
Hussey, NE, Brush, J, McCarthy, ID and Fisk, AT (2010) Δ15n and δ 13C diet – tissue discrimination factors for large sharks under semi-controlled conditions. Comparative Biochemistry and Physiology Part A: Molecular and Integrative Physiology 155, 445–453.Google Scholar
Hyslop, EJ (1980) Stomach contents analysis – a review of methods and their application. Journal of Fish Biology 17, 411–429.Google Scholar
Jackson, AL, Inger, R, Parnell, AC and Bearhop, S (2011) Comparing isotopic niche widths among and within communities: SIBER-stable isotope Bayesian ellipses in R. Journal of Animal Ecology 80, 595–602.Google Scholar
Jardas, I, Šantić, M, Nerlović, V and Pallaoro, A (2007) Diet of the smooth-hound Mustelus mustelus (Chondrichthyes: Triakidae) in the eastern Adriatic Sea. Cybium 31, 459–464.Google Scholar
Jennings, S, Reñones, O, Morales-Nin, B, Polunin, NVC, Moranta, J and Coll, J (1997) Spatial variation in the 15N and 13C stable isotope composition of plants, invertebrates and fishes on Mediterranean reefs: implications for the study of trophic pathways. Marine Ecology Progress Series 146, 109–116.Google Scholar
Kabasakal, H (2001) Preliminary data on the feeding ecology of some selachians from North-Eastern Aegean Sea. Acta Adriatica 42, 15–24.Google Scholar
Kabasakal, H (2002 a) Elasmobranch species of the seas of Turkey. Annales Series Historia Naturalis 12, 15–22.Google Scholar
Kabasakal, H (2002 b) Cephalopods in the stomach contents of four elasmobranch species from the northern Aegean Sea. Acta Adriatica 43, 17–24.Google Scholar
Kabasakal, H (2002 c) Stomach contents of the longnose spurdog, Squalus blainvillei (Risso, 1826) from the north-eastern Aegean Sea. Annales Series Historia Naturalis 12, 173–176.Google Scholar
Karachle, P and Stergiou, KI (2010) Food and feeding habits of nine elasmobranch species in the Aegean Sea. Rapports de la Commission Internationale pour L‘Exploration Scientifique de la Mer Mediterranee 39, 553.Google Scholar
Kim, SL and Koch, PL (2012) Methods to collect, preserve, and prepare elasmobranch tissues for stable isotope analysis. Environmental Biology Fishes 95, 53–63.Google Scholar
Kim, SL, del Rio, CM, Casper, D and Koch, P.L (2012) Isotopic incorporation rates for shark tissues from a long-term captive feeding study. Journal of Experimental Biology 215, 2495–2500.Google Scholar
Kousteni, V, Karachle, PK and Megalofonou, P (2017 a) Diet of the small-spotted catshark Scyliorhinus canicula in the Aegean Sea (eastern Mediterranean). Marine Biology Research 13, 161–173.Google Scholar
Kousteni, V, Karachle, PK and Megalofonou, P (2017 b) Diet and trophic level of the longnose spurdog Squalus blainville (Risso, 1826) in the deep waters of the Aegean Sea. Deep Sea Research Part I: Oceanographic Research Papers 124, 93–102.Google Scholar
Machias, A, Giannoulaki, M, Somarakis, S and Siapatis, A (2007) Small pelagic fish. In Papaconstantinou, C, Zenetos, A, Vassilopoulou, V and Tserpes, G (eds), State of Hellenic Fisheries. Athens: Hellenic Center for Marine Research Publications, pp. 192–207.Google Scholar
Macpherson, E (1981) Resource partitioning in a Mediterranean demersal fish community. Marine Ecology Progress Series 4, 183–193.Google Scholar
Mnasri, N, El Kamel, O, Boumaiza, M, Reynaud, C and Capape, C (2012) Food and feeding habits of the small-spotted catshark, Scyliorhinus canicula (Chondrichthyes: Scyliorhinidae) from the northern coast of Tunisia (central Mediterranean). Cahiers de Biologie Marine 53, 139–150.Google Scholar
Navarro, J, Lopez, L, Coll, M, Barria, C and Saez-Liante, R (2014) Short-and long-term importance of small sharks in the diet of the rare deep-sea shark Dalatias licha. Journal of Marine Biology 161, 1697–1707.Google Scholar
Navia, AF, Mejía-Falla, PA, López-García, J, Giraldo, A and Cruz-Escalona, VH (2017) How many trophic roles can elasmobranchs play in a marine tropical network? Marine and Freshwater Research 68, 12.Google Scholar
Olaso, I, Velasco, F and Pérez, N (1998) Importance of discarded blue whiting (Micromesistius poutassou) in the diet of lesser spotted dogfish (Scyliorhinus canicula) in the Cantabrian Sea. ICES Journal of Marine Science 55, 331–341.Google Scholar
Olin, JA, Hussey, NE, Grgicak-Mannion, A, Fritts, MW, Wintner, SP and Fisk, AT (2013) Variable δ 15N diet-tissue discrimination factors among sharks: implications for trophic position, diet and food web models. PLoS ONE 8, 10.Google Scholar
Öztürk, B (2009) Marine protected areas in the high seas of the Aegean and Eastern Mediterranean Seas, some proposals. Journal of Black Sea/Mediterranean Environment 15, 69–82.Google Scholar
Özcan, Eİ and Başusta, N (2015) Kuzeydoğu Akdeniz Bölgesi'nde yaşayan Benekli Kedibalığı, (Scyliorhinus canicula (Linnaeus, 1758))’nın mide içeriği. Su Ürünleri Dergisi 32, 193–195 [In Turkish].Google Scholar
Özcan, Eİ and Başusta, N (2016) Kuzeydoğu Akdeniz Bölgesinde Yaşayan Adi Köpekbalığı, Mustelus mustelus (Linnaeus, 1758)’un Mide İçeriği. Fırat Üniversitesi Fen Bilimleri Dergisi 28, 7–12 [In Turkish].Google Scholar
Özütemiz, Ş, Kaya, M and Özaydın, O (2009) Sığacık Körfezi'nde (Ege Denizi) Bulunan İki Tür Köpekbalığının [Galeus melastomus Rafinesque, 1810 ve Squalus blainvillei (Risso, 1826)] Boy-Ağırlık İlişkisi ve Beslenme Özellikleri Üzerine Bir Ön Çalışma. Ege Üniversitesi Su Ürünleri Dergisi, 26, 211–217 [In Turkish].Google Scholar
Pauly, D, Froese, R, Sa-a, PS, Palomares, ML, Christensen, V and Rius, J (2000) TrophLab Manual. Manila: ICLARM.Google Scholar
Peterson, BJ and Fry, B (1987) Stable isotopes in ecosystem studies. Annual Review of Ecology and Systematics 1, 293–320.Google Scholar
Pethiakis, G, Tsiaras, K, Triantafyllou, G, Kalaroni, S and Pollani, A (2014) Sensitivity of the N. Aegean Sea ecosystem to Black Sea Water inputs. Mediterranean Marine Science 15, 790–804.Google Scholar
Pianka, ER (2000) Evolutionary Ecology, 6th edition. San Francisco, CA: Harper Collins.Google Scholar
Saidi, B, Enajjar, S, Bradai, MN andBouain, A (2009) Diet composition of smooth-hound shark, Mustelus mustelus (Linnaeus, 1758), in the Gulf of Gabès, southern Tunisia. Journal of Applied Ichthyology 25, 113–118.Google Scholar
Šantić, M, Rađa, B and Pallaoro, A (2012) Feeding habits of small-spotted catshark (Scyliorhinus canicula Linnaeus, 1758) from the eastern central Adriatic Sea. Marine Biology Research 8, 1003–1011.Google Scholar
Shiffman, D, Gallagher, A, Boyle, M, Hammerschlag-Peyer, C and Hammerschlag, N (2012) Stable isotope analysis as a tool for elasmobranch conservation research: a primer for non-specialists. Marine and Freshwater Research 63, 635–643.Google Scholar
Stergiou, KI and Karpouzi, VS (2001) Feeding habits and trophic levels of Mediterranean fish. Reviews in Fish Biology and Fisheries 11, 217–254.Google Scholar
Stergiou, KI, Christou, ED, Georgopoulos, D, Zenetos, A and Souvermesoglou, C (1997) Hellenic Seas: physics, chemistry, biology and fisheries. Oceanography and Marine Biology: An Annual Review 35, 415–538.Google Scholar
Valls, M, Quetglas, A, Ordines, F and Moranta, J (2011) Feeding ecology of demersal elasmobranchs from the shelf and slope off the Balearic Sea (western Mediterranean). Scientia Marina 75, 633–639.Google Scholar
Vaudo, JJ and Heithaus, MR (2011) Dietary niche overlap in a nearshore elasmobranch mesopredator community. Marine Ecology Progress Series 425, 247–260.Google Scholar
White, WT, Platell, ME and Potter, IC (2004) Comparisons between the diets of four abundant species of elasmobranchs in a subtropical embayment: implications for resource partitioning. Marine Biology 144, 439–448.Google Scholar
Yığın, CÇ, İşmen, A, Önal, U and Arslan Ihsanoglu, M (2015) In Katagan, T, Tokaç, A, Besiktepe, S and Öztürk, B (eds), The Aegean Sea. Marine Biodiversity, Fisheries, Conservation and Governance. Istanbul: Turkish Marine Research Foundation (Tudav), pp. 286–302.Google Scholar
Zanden, M and Rasmussen, JB (2001) Variation in δ 15N and δ 13C trophic fractionation: implications for aquatic food web studies. Limnology and Oceanography 46, 2061–2066.Google Scholar