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Feeding biology and resource partitioning of the Mullidae family members off the northeastern Levantine coast of Turkey

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Abstract

The introduction of invasive exotic species can have strong ecological impacts on the native biota, with direct consequences for commercial fisheries. Feeding ecology studies are among the primary sources for improving predictions related to community structures, for example, by revealing potential competitive interactions between native and invasive species. We compared the stomach contents and studied diet overlaps among a native (Mullus barbatus) and two invasive (Upeneus moluccensis and U. pori) mullid species, collected off the coasts of the northeastern Levantine where invasive mullids have been part of the ecosystem for more than half a century. We also assessed the effect of sex, sampling period, depth and size on stomach contents. Schoener’s index indicated significant diet overlaps between U. moluccensis–U. pori and U. moluccensis–M. barbatus. Diets of U. pori and M. barbatus did not significantly overlap, which was explained by their differing depth preferences. Assessment of stomach contents showed that Crustacea, specifically Decapoda, was the main prey group across the studied mullid species. Polychaeta was also of high importance in the diet of the native M. barbatus, but not for the two invasive Upeneus species. A trophic level analysis revealed the two invasive mullids to have a higher trophic level than the native species (U. moluccensis: 3.58, U. pori: 3.55 versus M. barbatus: 3.38). The lack of a clear separation in habitat and diet preferences documented here between native and invasive mullids may pose a risk for the persistence of the economically valuable native M. barbatus in the Mediterranean Sea.

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Data availability

The datasets generated and analysed during the current study are available from the corresponding author on request.

Code availability

All analyses were completed in R and the code can be provided from the corresponding author if requested.

References

  • Arndt E, Givan O, Edelist D, Sonin O, Belmaker J (2018) Shifts in eastern Mediterranean fish communities: abundance changes, trait overlap, and possible competition between native and non-native species. Fishes 3(19):1–15. https://doi.org/10.3390/fishes3020019

    Article  Google Scholar 

  • Arslan M, Işmen A (2014) Age, growth, reproduction and feeding of Mullus barbatus in Saros Bay (North Aegean Sea). J Black Sea/medit Environ 20(3):184–199

    Google Scholar 

  • Azzuro E, Soto S, Garofalo G, Maynou F (2013) Fistularia commersonii in the Mediterranean Sea: invasion history and distribution modelling based on presence-only records. Biol Invasions 15(5):977–990. https://doi.org/10.1007/s10530-012-0344-4

    Article  Google Scholar 

  • Baker R, Buckland A, Sheaves M (2014) Fish gut content analysis: robust measures of diet composition. Fish Fish 15(1):170–177. https://doi.org/10.1111/faf.12026

    Article  Google Scholar 

  • Bariche M, Letourneur Y, Harmelin-Vivien M (2004) Temporal fluctuations and settlement patterns of native and Lessepsian herbivorous fishes on the Lebanese coast (Eastern Mediterranean). Env Biol Fish 70:81–90. https://doi.org/10.1023/B:EBFI.0000022928.15148.75

    Article  Google Scholar 

  • Bautista-Vega AA, Letourneur Y, Harmelin-Vivien M, Salen-Picard C (2008) Difference in diet and size-related trophic level in two sympatric fish species the red mullets Mullus barbatus and Mullus surmuletus in the Gulf of Lions (north-west Mediterranean Sea). J Fish Biol 73:2402–2420. https://doi.org/10.1111/j.1095-8649.2008.02093.x

    Article  Google Scholar 

  • Ben-Tuvia A (1966) Red sea fishes recently found in the Mediterranean. Copeia 1966(2):254. https://doi.org/10.2307/1441133

    Article  Google Scholar 

  • Ben-Yami M, Glaser T (1974) The invasion of Saurida undosquamis (Richardson) into the Levant basin-an example of biological effect of interoceanic canals. Fish Bull 72(2):359–373

    Google Scholar 

  • Beukema JJ (1997) Caloric values of marine invertebrates with an emphasis on the soft parts of marine bivalves. Oceanogr Mar Biol Ann Rev 35:387–412

    Google Scholar 

  • Bilecenoğlu M, Kaya M, Cihangir B, Çiçek E (2014) An updated checklist of the marine fishes of Turkey. Turk J Zool 38(6):901–929. https://doi.org/10.3906/zoo-1405-60

    Article  Google Scholar 

  • Boudraa I, Derbal F, Kara MH (2018) Feeding habits of the red mullet, Mullus barbatus (Mullidae) of eastern coasts of Algeria. Vie Et Milieu 68:213–220

    Google Scholar 

  • Bozzano A, Recasens L, Sartor P (1997) Diet of the European hake Merluccius merluccius Pisces Merluciidae in the Western Mediterranean Gulf of Lions. Sci Mar 61(1):1–8

    Google Scholar 

  • Brawn VM, Peer DL, Bentley RJ (1968) Caloric content of the standing crop of benthic epibenthic of St Margaret’s Bay Nova Scotia. J Fish Res Bd Canada 25(9):1803–1811. https://doi.org/10.1139/f68-166

    Article  Google Scholar 

  • Buckland A, Baker R, Loneragan N, Sheaves M (2017) Standardising fish stomach content analysis: the importance of prey condition. Fish Res 196:126–140. https://doi.org/10.1016/j.fishres.2017.08.003

    Article  Google Scholar 

  • Cartes JE, Brey T, Sorbe JC, Maynou F (2002) Comparing production-biomass ratios of benthos and suprabenthos in macrofaunal marine crustaceans. Can J Fish Aquat Sci 59:1616–1625. https://doi.org/10.1139/F02-130

    Article  Google Scholar 

  • Chérif M, Zarrad R, Gharbi H, Missaoui H, Jarboui O (2007) Some biological parameters of the red mullet Mullus barbatus L 1758 from the Gulf of Tunis. Acta Adriat 48(2):131–44

    Google Scholar 

  • Chérif M, Ben Amor MM, Selmi S, Gharbi H, Missaoui H, Capapé C (2011) Food and feeding habits of the red mullet, Mullus barbatus (Actinopterygii: Perciformes: Mullidae), off the Northern Tunisian coast (Central Mediterranean). Acta Ichthyol Piscat 41(2):109–116. https://doi.org/10.3750/AIP2011.41.2.06

    Article  Google Scholar 

  • Christensen V, Pauly D (1992) ECOPATH II - a software for balancing steady-state ecosystem models and calculating network characteristics. Ecological Modelling 61:169–185. https://doi.org/10.1016/0304-3800(92)90016-8

    Article  Google Scholar 

  • Çelik Ö, Torcu H (2000) Investigations on the biology of red mullet (Mullus barbatus Linnaeus, 1758) in Edremit Bay Aegean Sea Turkey. Turk J Vet Anim Sci 24:287–295

    Google Scholar 

  • Çınar ME, Bilecenoğlu M, Öztürk B, Can A (2006) New records of alien species on the Levantine coast of Turkey. Aquat Invasions 1(2):84–90. https://doi.org/10.3391/ai.2006.1.2.6

    Article  Google Scholar 

  • Çiçek E (2015) Age, growth and mortality parameters of Mullus barbatus Linnaeus, 1758 (Perciformes: Mullidae) in Iskenderun Bay, northeastern Mediterranean. Iran J Ichthyol 2(4):262–269

    Google Scholar 

  • Dalyan C (2020) The commercial and discard catch rates of the trawl fishery in the Iskenderun ay (northeastern Levantine Sea). Trak Univ J Nat Sci 21:123–129. https://doi.org/10.23902/trkjnat.773435

    Article  Google Scholar 

  • Demestre M, Sánchez P, Abelló P (2000) Demersal fish assemblages and habitat characteristics on the continental shelf and upper slope of the north-western Mediterranean. J Mar Biol Ass UK 80:981–988. https://doi.org/10.1017/S0025315400003040

    Article  Google Scholar 

  • Dolbeth M, Martinho F, Leitão R, Cabral H, Pardal M (2008) Feeding patterns of the dominant benthic and demersal fish community in a temperate estuary. J Fish Biol 72:2500–2517. https://doi.org/10.1111/j.1095-8649.2008.01856.x

    Article  Google Scholar 

  • Edelist D, Rilov G, Golani D, Carlton JT, Spanier E (2013) Restructuring the sea: profound shifts in the world’s most invaded marine ecosystem. Divers Distrib 19:69–77. https://doi.org/10.1111/ddi.12002

    Article  Google Scholar 

  • Edelist D (2014) New length-weight relationships and Lmax values for fishes from the Southeastern Mediterranean Sea. J Appl Ichthyol 30:521–526. https://doi.org/10.1111/j.1439-0426.2012.02060.x

    Article  Google Scholar 

  • El-Drawany MA (2013) Some biological aspects of the Por’s goatfish (Family: Mullidae) from Tripoli cost of Libya. Egypt J Aquat Res 39:261–266. https://doi.org/10.1016/j.ejar.2013.11.003

    Article  Google Scholar 

  • Esposito V, Andaloro F, Bianca D, Natalotto A, Romeo T, Scotti G, Castriota L (2014) Diet and prey selectivity of the red mullet, Mullus barbatus (Pisces: Mullidae), from the southern Tyrrhenian Sea: the role of the surf zone as a feeding ground. Mar Biol Res 10(2):167–178. https://doi.org/10.1080/17451000.2013.797585

    Article  Google Scholar 

  • Fanelli E, Azzurro E, Bariche M, Cartes JE, Maynou F (2015) Depicting the novel Eastern Mediterranean food web: a stable isotopes study following Lessepsian fish invasion. Biol Invasions 17:2163–2178. https://doi.org/10.1007/s10530-015-0868-5

    Article  Google Scholar 

  • Froese R, Pauly D (2021, May 5), FishBase, World Wide Web electronic publication, www.fishbase.org.

  • Galil BS (2007) Loss or gain? Invasive aliens and biodiversity in the Mediterranean Sea. Mar Pollut Bull 55(7–9):314–322. https://doi.org/10.1016/j.marpolbul.2006.11.008

    Article  CAS  PubMed  Google Scholar 

  • Garofalo G, Bel Hassen M, Jarboui O et al. (2008) Preliminary results on spatial distribution of abundance indices, nursery and spawning areas of Merluccius merluccius and Mullus barbatus in the central Mediterranean. MedSudMed Technical Documents, GCP/RER/ITA/MSM-TD-19, Rome, pp 24

  • Gancitano V, Badalucco C, Cusumano S, Gancitano S, Giusto GB, Ingrande G, Knittweis L, Sinacori G, Rizzo P (2012) Age cohort analysis of red mullet, Mullus barbatus (L., 1758) (Pisces: Mullidae), in the Strait of Sicily (GSA 15 &16). Biol Mar Mediterr 19(1):208–209

    Google Scholar 

  • Golani D (1994) Niche separation between colonizing and indigenous goatfish (Mullidae) along the Mediterranean coast of Israel. J Fish Biol 45:503–513. https://doi.org/10.1111/j.1095-8649.1994.tb01332.x

    Article  Google Scholar 

  • Golani D, Galil B (1991) Trophic relationships of colonizing and indigenous goatfishes (Mullidae) in the eastern Mediterranean with special emphasis on decapod crustaceans. Hydrobiologia 218:27–33

    Article  Google Scholar 

  • Golani D (2010) Colonization of the Mediterranean by red sea fishes via the Suez Canal-Lessepsian migration. In: Golani D, Appelbaum-Golani B (eds) Fish invasions of the Mediterranean Sea: change and renewal. Pensoft publishers, Sofia-Moscow, pp 145-188

  • Gosline WA (1984) Structure, function, and ecology in the Goatfishes (Family Mullidae). Pac Sci 38(4):312–323

    Google Scholar 

  • Gökçe G, Saygu I, Eryaşar AR (2016) Catch composition of trawl fisheries in Mersin Bay with emphasis on catch biodiversity. Turk J Zool 40:522–533. https://doi.org/10.3906/zoo-1505-35

    Article  CAS  Google Scholar 

  • Gücü AC, Bingel F, Avşar D, Uysal N (1994) Distribution and occurrence of Red Sea fish at the Turkish Mediterranean coast-northern Cilician basin. Acta Adriat 34(1/2):103–113

    Google Scholar 

  • Gücü AC, Ok M (2018) Lessepsian impact on the native fish stocks- the case of red mullet in GSA 24. Fish Forum. https://hdl.handle.net/11511/79134. Accessed 18 August 2021

  • Gücü AC, Ok M, Sakınan S (2010) Past and present fish fauna in the NE Levant Sea and factor facilitating the colonization by Lessepsian fishes. EastMed Technical Documents 4:88–108

    Google Scholar 

  • Hyslop EJ (1980) Stomach contents analysis-a review of methods and their application. J Fish Biol 17:411–429. https://doi.org/10.1111/j.1095-8649.1980.tb02775.x

    Article  Google Scholar 

  • Işmen A (2005) Age, growth and reproduction of the goldband goatfish, Upeneus moluccensis (Bleeker, 1855), in İskenderun Bay, the eastern Mediterranean. Turk J Zool 29(4):301–309

    Google Scholar 

  • Işmen A (2006) Growth and reproduction of Por’s Goatfish (Upeneus pori Ben-Tuvia & Golani, 1989) in Iskenderun Bay, the eastern Mediterranean. Turk J Zool 30:91–98

    Google Scholar 

  • Kaya M, Benli HA, Katağan T, Özaydın O (1999) Age, growth, sex-ratio, spawning season and food of golden banded goatfish, Upeneus moluccensis Bleeker (1855) from the Mediterranean and south Aegean Sea coasts of Turkey. Fish Res 41:317–328. https://doi.org/10.1016/S0165-7836(99)00027-2

    Article  Google Scholar 

  • Labropoulou M, Eleftheriou A (1997) The foraging ecology of two pairs of congeneric demersal fish species: importance of morphological characteristics in prey selection. J Fish Biol 50:324–340. https://doi.org/10.1111/j.1095-8649.1997.tb01361.x

    Article  Google Scholar 

  • Lefkaditou E, Abdelaty M, Bariche M et al (2011) What is the impact of Lessepsian species on the eastern Mediterranean fisheries? MEDCOAST 11:453–460

    Google Scholar 

  • Machias A, Labropoulou M (2002) Intra-specific variation in resource use by red mullet, Mullus barbatus. Estuar Coast Shelf Sci 55:565–578. https://doi.org/10.1006/ecss.2001.0924

    Article  Google Scholar 

  • Mahenna SF (2009) Growth, mortality and spawning stock biomass of striped red mullet Mullus surmuletus, in the Egyptian Mediterranean waters. Mediterr Mar Sci 10(2):5–18. https://doi.org/10.12681/mms.105

    Article  Google Scholar 

  • Mahenna SF (2018) Population dynamics of two Lessepsian migrant goatfish species; Upeneus pori and Upeneus moluccensis from the Southeastern Mediterranean, Port Said region, Egypt. In: Kallel A, Ksibi M, Ben Dhia H, Khélifi N (eds), Recent advances in environmental science from the Euro-Mediterranean and surrounding regions, 1st edn., Tunisia, pp 1659–1661

  • Mahmoud HH, Fahim RM, Srour TM, El-bermawi N, Ibrahim MA (2017) Feeding ecology of Mullus barbatus and Mullus surmuletus off the Egyptian Mediterranean coast. Int J Fish Aquat Stud 5(6):321–325

    Google Scholar 

  • Mavruk S, Bengil F, Yeldan H, Manasirli M, Avsar D (2017) The trend of Lessepsian fish populations with an emphasis on temperature variations in Iskenderun Bay, the Northeastern Mediterranean. Fish Oceanogr 1-13. https://doi.org/10.1111/fog.12215

  • Mutlu E, Ergev MB (2012) Distribution of soft-bottom mollusks (Mollusca) in Mersin Bay (eastern Mediterranean Sea). Turk J Zool 36(4):430–446. https://doi.org/10.3906/zoo-1103-15

    Article  Google Scholar 

  • Mutlu E, Ergev MB (2013) Depth-related gradient of soft-bottom crustacean distribution along the Cilician shelf. Turk J Zool 37:262–276. https://doi.org/10.3906/zoo-1204-33

    Article  Google Scholar 

  • Oksanen J, Blanchet FG, Friendly M, Kindt R. Legendre P, McGlinn D, Minchin PR, O’Hara RB, Simpson GL, Solymos P, Stevens MHH, Szoecs E., Wagner H (2018) Vegan: Community ecology package, R Package Version 2.5–3.

  • Özvarol ZAB, Balcı BA, Gökoğlu M, Taşlı A, Kaya Y, Pehlivan M (2010) Age, growth and reproduction of Goldband Goatfish from the Gulf of Antalya. J Anim Vet Adv 9(5):939–945. https://doi.org/10.3923/javaa.2010.939.945

    Article  Google Scholar 

  • Özyurt CE, Çiçek E, Avşar D, Yeldan H, Manaşırlı M (2014) The relationship among spawning period length at first maturity and depth distribution of Mullus barbatus and Upeneus moluccensis inhabiting the Northeastern Mediterranean coast of Turkey. Int J Aquat Biol 2(4):215–222. https://doi.org/10.22034/ijab.v2i4.88

    Article  Google Scholar 

  • Pauly D (1980) On the interrelationships between natural mortality, growth parameters and mean environmental temperature in 175 fish stocks. J Cons Int Explor Mer 39(2):175–792. https://doi.org/10.1093/icesjms/39.2.175

    Article  Google Scholar 

  • Pauly D (1984) Fish population dynamics in tropical waters: a manual for use with programmable calculators. ICLARM Studies and Reviews, Philippines

  • Pinkas L, Oliphant MS, Iverson ILK (1971) Food habits of albacore, bluefin tuna, and bonito in California waters. Calif Fish Game 152:1–105

    Google Scholar 

  • Pipitone C, Badalamenti F, D’Anna G, Patti B (2000) Fish biomass increase after a four-year trawl ban in the Gulf of Castellammare (NW Sicily, Mediterranean Sea). Fish Res 48:23–30. https://doi.org/10.1016/S0165-7836(00)00114-4

    Article  Google Scholar 

  • Por FD (1978) Lessepsian Migration, the influx of Red Sea biota into the Mediterranean by way of the Suez Canal. Springer-Verlag, Berlin

    Google Scholar 

  • R Development Core Team, A Language and Environment for Statistical Computing. Vienna: R Found Stat Comput, 2021

  • Schoener TW (1970) Nonsynchronous spatial overlap of lizards in patchy habitats. Ecology 51(3):408–418

    Article  Google Scholar 

  • Sergiwa SSS, Ali RAS, Abd-Elsemeea ZM, Ali SM, Elmor MAA (2017) Food and feeding habits of the Por’s goatfish Upeneus pori (Ben-Tuvia and Golani, 1989), Mullidae, in Ain El-Ghazala Lagoon, Eastern Libya Mediterranean Sea. Int J Fisher Aquac Res 3(1):33–50

    Google Scholar 

  • Spanier E, Galil BS (1991) Lessepsian migration: a continuous biogeographical process. Endeavour 15(3):102–106. https://doi.org/10.1016/0160-9327(91)90152-2

    Article  Google Scholar 

  • Stergiou KI (1989) Multivariate analysis and trends of the Greek Fishery. Fishbyte 7(2):4–7

    Google Scholar 

  • Stergiou KI, Christou ED, Georgopoylos D, Zenetos A, Souvermezoglou C (1997) The Hellenic Seas: physics, chemistry, biology and fisheries. Oceanogr Mar Biol: Ann Rev 35:415–538

    Google Scholar 

  • Stergiou K, Karpouzi VS (2002) Feeding habits and trophic levels of Mediterranean fish. Rev Fish Biol Fisher 11:217–254. https://doi.org/10.1023/A:1020556722822

    Article  Google Scholar 

  • Torcu H (1994) The investigations of the Indo-Pacific fish species living on the coasts of the Mediterranean and Aegean Sea, biology and ecology of Upeneus moluccensis (Bleeker, 1855) - Saurida undosquamis (Richardson, 1848). Dissertation, Selçuk University Institute of Science.

  • Tyler AV (1973) Caloric values of some North Atlantic invertebrates. Mar Biol 19:258–261. https://doi.org/10.1007/BF02097146

    Article  Google Scholar 

  • Uiblein F (2007) Goatfishes (Mullidae) as indicators in tropical and temperate coastal habitat monitoring and management. Mar Biol Res 3(5):275–288. https://doi.org/10.1080/17451000701687129

    Article  Google Scholar 

  • Vassilopoulou V, Papaconstantinou C (1993) Feeding habits of red mullet (Mullus barbatus) in a gulf in western Greece. Fish Res 16(1):69–83. https://doi.org/10.1016/0165-7836(93)90110-S

    Article  Google Scholar 

  • Vassilopoulou V, Papaconstantinou C, Christides G (2001) Food segregation of sympatric Mullus barbatus and Mullus surmuletus in the Aegean Sea. Isr J Zool 47(3):201–211. https://doi.org/10.1560/9NAK-73CF-34QC-NJ71

    Article  Google Scholar 

  • Wallace RK, Ramsey JS (1983) Reliability in measuring diet overlap. Can J Fish Aquat Sci 40:347–351. https://doi.org/10.1139/f83-050

    Article  Google Scholar 

  • Yapıcı S, Filiz H (2019) Biological aspects of two coexisting indigenous and non-indigenous fish species in the Aegean Sea: Pagellus erythrinus vs. Nemipterus randalli. Mediterr Mar Sci 20(3):594–602. https://doi.org/10.12681/mms.19658

    Article  Google Scholar 

  • Yemişken E, Dalyan C, Eryılmaz L (2014) Catch and discard fish species of trawl fisheries in the Iskenderun Bay (Northeastern Mediterranean) with emphasis on Lessepsian and chondricthyan species. Mediterr Mar Sci 15(2):380–389. https://doi.org/10.12681/mms.538

    Article  Google Scholar 

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Acknowledgements

The authors would like to thank Dr. Onur Gönülal and Bikem Kesici for their help during samplings, and Dr. Nedim Tüzün for his help and suggestions for statistical analyses and grammatical corrections.

Funding

This study was funded by the Scientific Research Fund of the Istanbul University, project no. 49576.

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  1. Galip Dede Cad, Nakkas Cikmazi No: 3, Beyoglu, Istanbul, Turkey

    Suna Tüzün

  2. Faculty of Science, Department of Biology, Division of Hydrobiology, Istanbul University, 34452, Istanbul, Turkey

    Cem Dalyan & Lütfiye Eryılmaz

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  1. Suna Tüzün
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Tüzün, S., Dalyan, C. & Eryılmaz, L. Feeding biology and resource partitioning of the Mullidae family members off the northeastern Levantine coast of Turkey. Environ Biol Fish 104, 1629–1642 (2021). https://doi.org/10.1007/s10641-021-01190-9

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