in

Ontogenetic trophic segregation between two threatened smooth-hound sharks in the Central Mediterranean Sea

  • 1.

    Wetherbee, B. & Cortes, E. Food consumption and feeding habits. In The Biology of Sharks and Their Relatives (ed. Hoelzel, A. R.) 225–245 (CRC Press, Boca Raton, FL, 2004).

    Google Scholar 

  • 2.

    Stevens, J. The effects of fishing on sharks, rays, and chimaeras (chondrichthyans), and the implications for marine ecosystems. ICES J. Mar. Sci. 57, 476–494 (2000).

    Google Scholar 

  • 3.

    Ferretti, F., Worm, B., Britten, G. L., Heithaus, M. R. & Lotze, H. K. Patterns and ecosystem consequences of shark declines in the ocean. Ecol. Lett. 13, 1055–1071 (2010).

    PubMed  Google Scholar 

  • 4.

    Ferretti, F., Myers, R. A., Serena, F. & Lotze, H. K. Loss of large predatory sharks from the Mediterranean Sea. Conserv. Biol. 22, 952–64 (2008).

    PubMed  Google Scholar 

  • 5.

    Myers, R. A. & Worm, B. Rapid worldwide depletion of predatory fish communities. Nature 423, 280–283 (2003).

    ADS  CAS  PubMed  Google Scholar 

  • 6.

    Nieto, A. et al. Eur. Red List of Mar. Fish. https://doi.org/10.2779/082723 (2015).

    Article  Google Scholar 

  • 7.

    Myers, R. A. & Baum, J. K. Cascading effects of the loss of apex predatory sharks from a coastal ocean. Science 315, 1846–1850 (2007).

    ADS  CAS  PubMed  Google Scholar 

  • 8.

    Baum, J. K. et al. Collapse and conservation of shark populations in the northwest atlantic published by: American Association for the Advancement of Science Stable URL: https://www.jstor.org/stable/3833388. Am. Assocation Adv. Sci. 299, 389–392 (2003).

  • 9.

    Britten, G. L. et al. Predator decline leads to decreased stability in a coastal fish community. Ecol. Lett. 17, 1518–1525 (2014).

    PubMed  Google Scholar 

  • 10.

    Schoener, T. W. Nonsynchronous spatial overlap of lizards in patchy habitats Author(s): Thomas W . Schoener Reviewed work (s): Published by : Ecological Society of America Stable URL: https://www.jstor.org/stable/1935376. Ecology 51, 408–418 (1970).

  • 11.

    Schoener, T. W. The compression hypothesis and temporal resource partitioning. Proc. Natl. Acad. Sci. USA 71, 4169–4172 (1974).

    ADS  CAS  PubMed  Google Scholar 

  • 12.

    Schückel, S., Sell, A., Kröncke, I. & Reiss, H. Diet composition and resource partitioning in two small flatfish species in the German Bight. J. Sea Res. 66, 195–204 (2011).

    ADS  Google Scholar 

  • 13.

    Browning, N. E., Cockcroft, V. G. & Worthy, G. A. J. Resource partitioning among South African delphinids. J. Exp. Mar. Bio. Ecol. 457, 15–21 (2014).

    Google Scholar 

  • 14.

    Kamler, J. F., Stenkewitz, U., Klare, U., Jacobsen, N. F. & MacDonald, D. W. Resource partitioning among cape foxes, bat-eared foxes, and black-backed jackals in South Africa. J. Wildl. Manag. 76, 1241–1253 (2012).

    Google Scholar 

  • 15.

    Sibbing, F. A. & Nagelkerke, L. A. J. Resource partitioning by Lake Tana barbs predicted from fish morphometrics and prey characteristics. Rev. Fish. Biol. Fish. 10, 393–437 (2001).

    Google Scholar 

  • 16.

    Sibbing, F. A., Nagelkerke, L. A. J., Stet, R. J. M. & Osse, J. W. M. Speciation of endemic Lake Tana barbs (Cyprinidae, Ethiopia) driven by trophic resource partitioning; a molecular and ecomorphological approach. Aquat. Ecol. 32, 217–227 (1998).

    Google Scholar 

  • 17.

    Ross, H. H. Resource partitioning in fish assemblages: a review of field studies. Copeia 1986, 352–388 (1986).

    Google Scholar 

  • 18.

    Sánchez-Hernández, J., Vieira-Lanero, R., Servia, M. J. & Cobo, F. Feeding habits of four sympatric fish species in the Iberian Peninsula: Keys to understanding coexistence using prey traits. Hydrobiologia 667, 119–132 (2011).

    Google Scholar 

  • 19.

    Maduna, S. N. & Bester-van der Merwe, A. E. Molecular research on the systematically challenging smoothhound shark genus Mustelus: a synthesis of the past 30 years. Afr. J. Mar. Sci. 39, 373–387 (2017).

    Google Scholar 

  • 20.

    Compagno, L. J. V. An annotated and illustrated catalogue of shark species known to date. FAO Fish. Synop. 1254(2), 251–655 (1984).

    Google Scholar 

  • 21.

    Heemstra, P. C. A review of the smooth-hound sharks (genus Mustelus, family triakidae) of the western atlantic ocean, with descriptions of two new species and a new subspecies. Bull. Mar. Sci. 60, 894–928 (1997).

    Google Scholar 

  • 22.

    Weigmann, S. Annotated checklist of the living sharks, batoids and chimaeras (Chondrichthyes) of the world, with a focus on biogeographical diversity. J. Fish Biol. 88, 837–1037 (2016).

    CAS  PubMed  Google Scholar 

  • 23.

    Rosa, M. R. & Gadig, O. B. F. Taxonomic comments and an identification key to species for the Smooth-hound sharks genus Mustelus Link, 1790 (Chondrichthyes: Triakidae) from the Western South Atlantic. Panam. J. Aquat. Sci. 5, 401–413 (2011).

    Google Scholar 

  • 24.

    Ritchie, E. G. & Johnson, C. N. Predator interactions, mesopredator release and biodiversity conservation. Ecol. Lett. 12, 982–998 (2009).

    PubMed  Google Scholar 

  • 25.

    Saïdi, B., Bradaï, M. N. & Bouaïn, A. Reproductive biology and diet of Mustelus punctulatus (Risso, 1826) (Chondrichthyes: Triakidae) from the Gulf of Gabès, central Mediterranean Sea. Sci. Mar. 73, 249–258 (2009).

    Google Scholar 

  • 26.

    Ozcan, E. I. & Başusta, N. Preliminary study on age, growth and reproduction of Mustelus mustelus (Elasmobranchii: Carcharhiniformes: Triakidae) inhabiting the gulf of Iskenderun, north-eastern mediterranean sea. Acta Ichthyol. Piscat. 48, 27–36 (2018).

    Google Scholar 

  • 27.

    Marino, I. A. M. et al. Multiple paternity and hybridization in two smooth-hound sharks. Sci. Rep. 5, 1–11 (2015).

    Google Scholar 

  • 28.

    Abella, A. J. & Serena, F. Comparison of elasmobranch catches from research trawl surveys and commercial landings at Port of Viareggio, Italy, in the Last Decade. J. Northwest Atl. Fish. Sci. 37, 345–356 (2005).

    Google Scholar 

  • 29.

    Colloca, F., Enea, M., Ragonese, S. & Di Lorenzo, M. A century of fishery data documenting the collapse of smooth-hounds (Mustelus spp.) in the Mediterranean Sea. Aquat. Conserv. Mar. Freshw. Ecosyst. 27, 1145–1155 (2017).

    Google Scholar 

  • 30.

    Morales-Muñiz, A. & Roselló, E. 20,000 years of fishing in the Strait: archaeological fish and shellfish assemblages from southern Iberia. Hum. Impacts Anc. Mar. Environ. 2008, 243–278 (2008).

    Google Scholar 

  • 31.

    Garcia, S. Long-term trends in small pelagic and bottom fisheries in the Mediterranean: 1950–2008. PlanBleuUNEP/MAP Regional Activity Centre. Valbonne: 102 p. (2011).

  • 32.

    Echwikhi, K., Saidi, B., Bradai, M. N. & Bouain, A. Preliminary data on elasmobranch gillnet fishery in the Gulf of Gabès, Tunisia. J. Appl. Ichthyol. 29, 1080–1085 (2013).

    Google Scholar 

  • 33.

    Riginella, E. et al. Contrasting life-history traits of two sympatric smoothhound species: implication for vulnerability. J. Fish. Biol. 96, 853–857 (2020).

    PubMed  Google Scholar 

  • 34.

    Barausse, A. et al. The role of fisheries and the environment in driving the decline of elasmobranchs in the northern Adriatic Sea. ICES J. Mar. Sci. 71(7), 1593–1603 (2014).

    Google Scholar 

  • 35.

    Akyol, O. Fish by-catch species from coastal small-scale shrimp trammel net fishery in the Aegean Sea (Izmir Bay, Turkey). J. Appl. Ichthyol. 24, 339–341 (2008).

    Google Scholar 

  • 36.

    Ceyhan, T., Hepkafadar, O. & Lu, Z. T. Catch and size selectivity of small-scale fishing gear for the smooth-hound shark Mustelus mustelus (Linnaeus, 1758) (Chondrichthyes: Triakidae). Medit. Mar. Sci. 11(2), 213–224 (2010).

    Google Scholar 

  • 37.

    Jardas, I., Šantić, M., Nerlović, V. & Pallaoro, A. Diet composition of blackspotted smooth-hound, Mustelus punctulatus (Risso, 1826), in the eastern Adriatic Sea. J. Appl. Ichthyol. 23, 279–281 (2007).

    Google Scholar 

  • 38.

    Saïdi, B., Bradaï, M. N. & Bouaïn, A. Reproductive biology of the smooth-hound shark Mustelus mustelus (L.) in the Gulf of Gabès (south-central Mediterranean Sea). J. Fish Biol. 72, 1343–1354 (2008).

    Google Scholar 

  • 39.

    Lipej, L., Mavrič, B., Rešek, S., Chérif, M. & Capapé, C. Food and feeding habits of the blackspotted smooth-hound, Mustelus punctulatus (Elasmobranchii: Carcharhiniformes: Triakidae), from the northern Adriatic. Acta Ichthyol. Piscat. 41, 171–177 (2011).

    Google Scholar 

  • 40.

    Saïdi, B., Enajjar, S., Bradaï, M. N. & Bouaïn, A. Diet composition of smooth-hound shark, Mustelus mustelus (Linnaeus, 1758), in the Gulf of Gabès, southern Tunisia. J. Appl. Ichthyol. 25, 113–118 (2009).

    Google Scholar 

  • 41.

    Di Lorenzo, M., Sinerchia, M. & Colloca, F. The North sector of the Strait of Sicily: a priority area for conservation in the Mediterranean Sea. Hydrobiologia https://doi.org/10.1007/s10750-017-3389-7 (2017).

    Article  Google Scholar 

  • 42.

    Coll, M. et al. The biodiversity of the Mediterranean Sea: estimates, patterns, and threats. PLoS ONE 5, e11842 (2010).

    ADS  PubMed  PubMed Central  Google Scholar 

  • 43.

    Consoli, P. et al. Fish distribution and habitat complexity on banks of the strait of sicily (Central Mediterranean Sea) from remotely-operated vehicle (ROV) explorations. PLoS ONE 11, e0167809 (2016).

    PubMed  PubMed Central  Google Scholar 

  • 44.

    Garofalo, G., Fiorentino, F., Gristina, M., Cusumano, S. & Sinacori, G. Stability of spatial pattern of fish species diversity in the Strait of Sicily (central Mediterranean). Hydrobiologia 580, 117–124 (2007).

    Google Scholar 

  • 45.

    Gristina, M., Bahri, T., Fiorentino, F. & Garofalo, G. Comparison of demersal fish assemblages in three areas of the Strait of Sicily under different trawling pressure. Fish. Res. 81, 60–71 (2006).

    Google Scholar 

  • 46.

    de Juan, S. et al. A regional network of sustainable managed areas as the way forward for the implementation of an Ecosystem-Based Fisheries Management in the Mediterranean. Ocean Coast. Manag. 65, 51–58 (2012).

    Google Scholar 

  • 47.

    Tuset, V. M., Lombarte, A. & Assis, C. A. Otolith atlas for the western Mediterranean, north and central eastern Atlantic. Sci. Mar. 72(S1), 7–198 (2008).

    Google Scholar 

  • 48.

    Ragonese, S., Vitale, S., Dimech, M. & Mazzola, S. Abundances of Demersal sharks and chimaera from 1994–2009 scientific surveys in the Central Mediterranean Sea. PLoS ONE 8, e74865 (2013).

    ADS  CAS  PubMed  PubMed Central  Google Scholar 

  • 49.

    Colloca, F., Scarcella, G. & Libralato, S. Recent trends and impacts of fisheries exploitation on Mediterranean stocks and ecosystems. Front. Mar. Sci. 4, 244 (2017).

    Google Scholar 

  • 50.

    Béthoux, J. P. Budgets of the Mediterranean Sea-their dependence on the local climate and on the characteristics of the Atlantic waters. Oceanol. acta 2, 157–163 (1979).

    Google Scholar 

  • 51.

    Astraldi, M., Gasparini, G. P., Gervasio, L. & Salusti, E. Dense water dynamics along the strait of sicily (Mediterranean Sea). J. Phys. Oceanogr. 31, 3457–3475 (2001).

    ADS  Google Scholar 

  • 52.

    Medits Working. Instruction manual Version 8. (2016).

  • 53.

    Marino, I. A. M. et al. Resolving the ambiguities in the identification of two smooth-hound sharks (Mustelus mustelus and Mustelus punctulatus) using genetics and morphology. Mar. Biodivers. 48, 1551–1562. https://doi.org/10.1007/s12526-017-0701-8 (2018).

    Article  Google Scholar 

  • 54.

    Pinkas, L., Oliphant, M. S. & Inverson, I. L. K. Food habits of albacore bluefin tuna and bonito in California waters Calif Dep Fish Game. Fish. Bull. 152, 98–105 (1971).

    Google Scholar 

  • 55.

    Hacunda, J. S. Trophic relationships among demersal fishes in a coastal area of the Gulf of Maine. Fish. Bull. 79, 775–788 (1981).

    Google Scholar 

  • 56.

    Anderson, M. J. Permutation tests for univariate or multivariate analysis of variance and regression. Can. J. Fish. Aquat. Sci. 58, 626–639 (2001).

    Google Scholar 

  • 57.

    Clarke, K.R. & Gorley, R.N. PRIMER v5: User Manual/Tutorial PRIMER-E Ltd Playmouth (2001).

  • 58.

    Sotiropoulos, M., Tonn, W. M. & Wassenaar, L. I. Effects of lipid extraction on stable carbon and nitrogen isotope analyses of fish tissues: potential consequences for food web studies. Ecol. Freshw. Fish 13, 155–160 (2004).

    Google Scholar 

  • 59.

    Hussey, N. E., Olin, J. A., Kinney, M. J., McMeans, B. C. & Fisk, A. T. Lipid extraction effects on stable isotope values (δ 13C and δ 15N) of elasmobranch muscle tissue. J. Exp. Mar. Bio. Ecol. 434–435, 7–15 (2012).

    Google Scholar 

  • 60.

    Kim, S. L. & Koch, P. L. Methods to collect, preserve, and prepare elasmobranch tissues for stable isotope analysis. Environ. Biol. Fishes 95, 53–63 (2012).

    Google Scholar 

  • 61.

    Jackson, A. L., Inger, R., Parnell, A. C. & Bearhop, S. Comparing isotopic niche widths among and within communities: SIBER—stable isotope Bayesian ellipses in R. J. Anim. Ecol. 80, 595–602 (2011).

    PubMed  Google Scholar 

  • 62.

    Zanden, M. J. V. & Rasmussen, J. B. Variation in δ15N and δ13C trophic fractionation: Implications for aquatic food web studies. Limnol. Oceanogr. 46, 2061–2066 (2001).

    ADS  Google Scholar 

  • 63.

    Post, D. M. Using stable isotopes to estimate trophic position: models, methods, and assumptions. Ecology 83, 703–718 (2002).

    Google Scholar 

  • 64.

    Hussey, N. E., Brush, J., McCarthy, I. D. & Fisk, A. T. δ 15 N and δ 13 C diet-tissue discrimination factors for large sharks under semi-controlled conditions. Comput. Biochem. Physiol. A Mol. Integr. Physiol. 155, 445–453 (2010).

    Google Scholar 

  • 65.

    Rigolet, C., Thiébaut, E. & Dubois, S. F. Food web structures of subtidal benthic muddy habitats: Evidence of microphytobenthos contribution supported by an engineer species. Mar. Ecol. Prog. Ser. 500, 25–41 (2014).

    ADS  CAS  Google Scholar 

  • 66.

    Carlier, A., Riera, P., Amouroux, J. M., Bodiou, J. Y. & Grémare, A. Benthic trophic network in the Bay of Banyuls-sur-Mer (northwest Mediterranean, France): An assessment based on stable carbon and nitrogen isotopes analysis. Estuar. Coast. Shelf Sci. 72, 1–15 (2007).

    ADS  Google Scholar 

  • 67.

    Cortés, E. Standardized diet compositions and trophic levels of sharks. ICES J. Mar. Sci. 56, 707–717 (1999).

    Google Scholar 

  • 68.

    Kim, S. L., Del Rio, C. M., Casper, D. & Koch, P. L. Isotopic incorporation rates for shark tissues from a long-term captive feeding study. J. Exp. Biol. 215, 2495–2500 (2012).

    PubMed  Google Scholar 

  • 69.

    Malpica-Cruz, L., Herzka, S. Z., Sosa-Nishizaki, O. & Lazo, J. P. Tissue-specific isotope trophic discrimination factors and turnover rates in a marine elasmobranch: empirical and modeling results. Can. J. Fish. Aquat. Sci. 69, 551–564 (2012).

    CAS  Google Scholar 

  • 70.

    Goosen, A. J. J. & Smale, M. J. A preliminary study of age and growth of the smoothhound shark Mustelus mustelus (Triakidae). S. Afr. J. Mar. Sci. 18, 85–91 (1997).

    Google Scholar 

  • 71.

    Belleggia, M., Figueroa, D. E., Sánchez, F. & Bremec, C. The feeding ecology of Mustelus schmitti in the southwestern Atlantic: geographic variations and dietary shifts. Environ. Biol. Fishes 95, 99–114 (2012).

    Google Scholar 

  • 72.

    Morte, S., Redon, M. J. & Sanz-Brau, A. Feeding habits of juvenile Mustelus mustelus (Carcharhiniformes, Triakidae) in the western Mediterranean. Cah. Biol. Mar. 38, 103–107 (1997).

    Google Scholar 

  • 73.

    Filiz, H. Diet composition of smooth-hound, Mustelus mustelus (Linnaeus, 1758). Aegean Sea, Turkey. 139, 81–84 (2009).

    Google Scholar 

  • 74.

    Kara, A. F., Al Hajaji, M., Ghmati, H. & Shakman, E. A. Food and feeding habits of Mustelus mustelus (linnaeus, 1758) (chondrichthyes: triakidae) along the western coast of Libya. Ann. Ser. Hist. Nat. Koper 29(2), 197–204. https://doi.org/10.19233/ASHN.2019.19 (2019).

    Article  Google Scholar 

  • 75.

    Gračan, R., Zavodnik, D., Krstinić, P., Dragičević, B. & Lazar, B. Feeding ecology and trophic segregation of two sympatric mesopredatory sharks in the heavily exploited coastal ecosystem of the Adriatic Sea. J. Fish Biol. 90, 167–184 (2017).

    PubMed  Google Scholar 

  • 76.

    Yemisken, E., Navarro, J., Forero, M. G., Megalofonou, P. & Eryilmaz, L. Trophic partitioning between abundant demersal sharks coexisting in the North Aegean Sea. J. Mar. Biol. Assoc. UK https://doi.org/10.1017/S0025315419000110 (2019).

    Article  Google Scholar 

  • 77.

    Cartes, J. E. et al. Feeding guilds of western Mediterranean demersal fish and crustaceans: An analysis based on a spring survey. Sci. Mar. 66, 209–220 (2002).

    Google Scholar 

  • 78.

    Hughes, R. N. & Elner, R. W. Foraging behaviour of a tropical crab: Calappa ocellata Holthuis feeding upon the mussel Brachidontes domingensis (Lamarck). J. Exp. Mar. Bio. Ecol. 133, 93–101 (1989).

    Google Scholar 

  • 79.

    Schoener, T. W. Field experiments on interspecific competition. Am. Nat. 122, 240–285 (1983).

    Google Scholar 

  • 80.

    Yemışken, E., Forero, M. G., Megalofonou, P., Eryilmaz, L. & Navarro, J. Feeding habits of three Batoids in the Levantine Sea (north-eastern Mediterranean Sea) based on stomach content and isotopic data. J. Mar. Biol. Assoc. UK 98(1), 89–96 (2018).

    Google Scholar 

  • 81.

    Hernández-Aguilar, S. B., Escobar-Sánchez, O., Galván-Magaña, F. & Abitia-Cárdenas, L. A. Trophic ecology of the blue shark (Prionace glauca) based on stable isotopes (δ 13C and δ 15N) and stomach content. J. Mar. Biol. Assoc. UK 96, 1403–1410 (2016).

    Google Scholar 

  • 82.

    Amariles, D. F., Navia, A. F. & Giraldo, A. Food resource partitioning of the Mustelus lunulatus and Mustelus henlei (Elasmobranchii: Carcharhiniformes). Environ. Biol. Fishes 100, 717–732 (2017).

    Google Scholar 

  • 83.

    Matich, P., Kiszka, J. J., Heithaus, M. R., Le Bourg, B. & Mourier, J. Inter-individual differences in ontogenetic trophic shifts among three marine predators. Oecologia 189, 621–636 (2019).

    ADS  PubMed  Google Scholar 

  • 84.

    Heithaus, M. R. Predator-prey and competitive interactions between sharks (order Selachii) and dolphins (suborder Odontoceti): a review. J. Zool. 253, 53–68 (2001).

    Google Scholar 

  • 85.

    Mulas, A. et al. Resource partitioning among sympatric elasmobranchs in the central-western Mediterranean continental shelf. Mar. Biol. 166, 1–16 (2019).

    Google Scholar 

  • 86.

    Colloca, F., Carpentieri, P., Balestri, E. & Ardizzone, G. Food resource partitioning in a Mediterranean demersal fish assemblage: the effect of body size and niche width. Mar. Biol. 157, 565–574 (2010).

    Google Scholar 

  • 87.

    Macpherson, E. Ecological overlap between macrourids in the western mediterranean sea. Mar. Biol. 53, 149–159 (1979).

    Google Scholar 

  • 88.

    Kousteni, V., Karachle, P. K. & Megalofonou, P. Diet and trophic level of the longnose spurdog Squalus blainville (Risso, 1826) in the deep waters of the Aegean Sea. Deep. Res. Part I Oceanogr. Res. Pap. 124, 93–102 (2017).

    ADS  Google Scholar 

  • 89.

    Barría, C., Coll, M. & Navarro, J. Unravelling the ecological role and trophic relationships of uncommon and threatened elasmobranchs in the western Mediterranean Sea. Mar. Ecol. Prog. Ser. 539, 225–240 (2015).

    ADS  Google Scholar 

  • 90.

    Valls, M., Quetglas, A., Ordines, F. & Moranta, J. Feeding ecology of demersal elasmobranchs from the shelf and slope off the Balearic Sea (western Mediterranean). Sci. Mar. 75, 633–639 (2011).

    Google Scholar 

  • 91.

    Colloca, F., Carrozzi, V., Simonetti, A. & Di Lorenzo, M. Using local ecological knowledge of fishers to reconstruct abundance trends of elasmobranch populations in the Strait of Sicily. Front. Mar. Sci. https://doi.org/10.3389/fmars.2020.00508 (2020).


  • Source: Ecology - nature.com

    Solarizing networks

    Light limitation regulates the response of autumn terrestrial carbon uptake to warming