Comparative feeding habits of the invasive non-indigenous devil firefish Pterois miles and the indigenous scorpionfishes Scorpaena porcus, Scorpaena scrofa, and Scorpaena notata on the southwest coast of Türkiye, eastern Mediterranean


Published: Dec 3, 2024
Keywords:
stomach content diet marine invasion Scorpionfish lionfish
FIKRET ÖNDES
https://orcid.org/0000-0002-9522-7050
UĞUR ÖZDEN
VAHIT ALAN
ERHAN IRMAK
HARUN GÜÇLÜSOY
Abstract

The feeding habits of the invasive alien devil firefish (Pterois miles) and the indigenous scorpaenids Scorpaena porcus, Scorpaena scrofa, and Scorpaena notata in the eastern Mediterranean Sea were investigated based on stomach content analysis. Furthermore, we examined whether these confamiliar species feed upon similar prey. Specimens were captured by professional fishers using trammel nets on the southwestern coast of Türkiye in the winter and summer of 2021. A total of 608 stomachs (286 P. miles, 112 S. porcus, 136 S. scrofa, and 74 S. notata) were investigated. The results demonstrate that the diet of P. miles included a total of 45 taxa, with 33 identified at the species level (27 indigenous, 6 non-indigenous), while those of the three congeneric scorpaenids included a total of 46 taxa and 37 identified species (30 indigenous, 7 non-indigenous). For P. miles, the highest index of relative importance (%IRI) values were determined for fish in both seasons (83.44% in winter, 93.82% in summer), with the damselfish Chromis chromis being the most preferred species. S. scrofa fed mainly on fish in winter and cephalopods in summer, whereas the diets of S. porcus and S. notata included mainly crustaceans in both seasons. In winter, P. miles exhibited a higher percentage of empty stomachs, demonstrating a significant difference in the vacuity index in different sampling seasons, while other scorpaenids did not exhibit statistically significant differences. This study also provides the northernmost record of the non-indigenous crab species Gonioinfradens giardi and the second record of the squat lobster Dactylonida curvimana in Türkiye. It also provides new reports of rarely observed fish species for the eastern Mediterranean, including Bellottia apoda and Odondebuenia balearica.

Article Details
  • Section
  • Research Article
Downloads
Download data is not yet available.
References
Acero, P.A., Bustos-Montes, D., Pabón Quintero, P., Polo-Silva, C.J., Muñoz, A.S., 2019. Feeding habits of Pterois volitans: A real threat to Caribbean Coral Reef Biodiversity. Makowski, C., Finkl, C. (Eds). In: Impacts of invasive species on coastal environments. Coastal Research Library, Springer, Switzerland.
Agostino, D.D., Jimenez, C., Reader, T., Hadjioannou, L., Heyworth, S. et al., 2020. Behavioural traits and feeding ecology of Mediterranean lionfish and naiveté of native species to lionfish predation. Marine Ecology Progress Series, 638, 123-135.
Albins, M.A., Hixon, M.A., 2008. Invasive Indo-Pacific lionfish Pterois volitans reduce recruitment of Atlantic coral-reef fishes. Marine Ecology Progress Series, 367, 233-238.
Albins, M.A., 2013. Effects of invasive Pacific red lionfish Pterois volitans versus a native predator on Bahamian coral- reef fish communities. Biological Invasions, 15, 29-43.
Albins, M.A., Hixon, M.A., 2013. Worst case scenario: potential long-term effects of invasive predatory lionfish (Pterois volitans) on Atlantic and Caribbean coral-reef communities. Environmental Biology of Fishes, 96, 1151-1157.
Anonymous, 2014. Regulation (EU) No. 1143/2014 of the European Parliament and of the Council on the prevention and management of the introduction and spread of invasive alien species. Official Journal of the European Union L 317, 4 November 2014, 35-55.
Avşar, D., 2016. Balıkçılık biyolojisi ve popülasyon dinamiği. Akademisyen Kitabevi, Ankara, 289 pp (In Turkish).
Bariche, M. 2012. Field identification guide to the living marine resources of the Eastern and Southern Mediterranean. FAO Species Identification Guide for Fishery Purposes. Rome, 610 pp.
Başçınar, N.S., Sağlam, H., 2009. Feeding habits of black scorpionfish Scorpaena porcus, in the South-Eastern Black Sea. Turkish Journal of Fisheries and Aquatic Sciences, 9 (1), 99-103.
Batjakas, I.E., Evangelopoulos, A., Giannou, M., Pappou, S., Papanikola, E. et al., 2023. Lionfish diet composition at three study sites in the Aegean Sea: an invasive generalist? Fishes, 8 (6), 314.
Bonanno, G., 2016. Alien species: to remove or not to remove? That is the question. Environmental Science & Policy, 59, 67-73.
Bradai, M.N., Bouain, A., 1990. Régime alimentaire de Scorpaena porcus et de S. scrofa (Teleostei, Scorpaenidae) du Golfe de Gabès, Tunisie. Cybium, 14 (3), 207-216.
Castriota, L., Falautano, M., Finoia, M.G., Consoli, P., Peda, C. et al., 2012. Trophic relationships among scorpaeniform fishes associated with gas platforms. Helgoland Marine Research, 66, 401-411.
Chartosia, N., Anastasiadis, D., Bazairi, H., Crocetta, F., Deidun, A. et al., 2018. New Mediterranean biodiversity records. Mediterranean Marine Science, 19 (2), 398-415.
Compaire, J.C., Casademont, P., Cabrera, R., Gómez-Cama, C., Soriguer, M.C., 2018. Feeding of Scorpaena porcus (Scorpaenidae) in intertidal rock pools in the Gulf of Cadiz (NE Atlantic). Journal of the Marine Biological Association of the United Kingdom, 98 (4), 845-853.
Corsini-Foka, M., Pancucci-Papadopoulou, M.A., 2012. Inventory of Crustacea Decapoda and Stomatopoda from Rhodes Island (Eastern Mediterranean Sea), with emphasis on rare and newly recorded species. Journal of Biological Research, 18, 359.
Çinar, M.E., Bilecenoğlu, M., Yokeş, M.B., Öztürk, B., Taşkin, E. et al., 2021. Current status (as of end of 2020) of marine alien species in Turkey. PLoS One, 16 (5), e0251086.
Dahl, K.A., Patterson III, W.F., 2014. Habitat-specific density and diet of rapidly expanding invasive red lionfish, Pterois volitans, populations in the northern Gulf of Mexico. PloS one, 9 (8), e105852.
David, P., Thebault, E., Anneville, O., Duyck, P. F., Chapuis, E. et al., 2017. Impacts of invasive species on food webs: a review of empirical data. Advances in Ecological Research, 56, 1-60.
Del Río, L., Navarro-Martínez, Z.M., Cobián-Rojas, D., Chevalier- Monteagudo, P.P., Angulo-Valdes, J.A. et al., 2023. Biology and ecology of the lionfish Pterois volitans/Pterois miles as invasive alien species: a review. Peer J, 11, e15728.
Díaz-Ferguson, E.E., Hunter, M.E., 2019. Life history, genetics, range expansion and new frontiers of the lionfish (Pterois volitans, Perciformes: Pteroidae) in Latin America. Regional Studies in Marine Science, 31, 100793.
Dimitriadis, C., Galanidi, M., Zenetos, A., Corsini-Foka, M., Giovos, I. et al., 2020. Updating the occurrences of Pterois miles in the Mediterranean Sea, with considerations on thermal boundaries and future range expansion. Mediterranean Marine Science, 21 (1), 62-69.
Eddy, C., Pitt, J., Morris Jr, J.A., Smith, S., Goodbody-Gringley, G. et al., 2016. Diet of invasive lionfish (Pterois volitans and P. miles) in Bermuda. Marine Ecology Progress Series, 558, 193-206.
Ferretti, F., Myers, R.A., Serena, F., Lotze, H.K., 2008. Loss of large predatory sharks from the Mediterranean Sea. Conservation Biology, 22 (4), 952-964.
Galanidi, M., Aissi, M., Ali, M., Bakalem, A., Bariche, M. et al., 2023. Validated inventories of non-indigenous species (NIS) for the Mediterranean Sea as tools for regional policy and patterns of NIS spread. Diversity, 15 (9), 962.
Galil, B.S., Froglia, C., Noel, P.Y., 2002. CIESM Atlas of Exotic Species in the Mediterranean. Volume 2: Crustaceans: decapods and stomatopods. F. Briand (Ed.), Monaco, 192 pp.
Galil, B.S., Douek, J., Gevili, R., Goren, M., Yudkovsky, Y. et al., 2018. The resurrection of Charybdis (Gonioinfradens) giardi (Nobili, 1905), newly recorded from the SE Mediterranean Sea. Zootaxa, 4370 (5), 580-590.
Garrabou, J., Gómez-Gras, D., Ledoux, J.B., Linares, C., Bensoussan, N. et al., 2019. Collaborative database to track mass mortality events in the Mediterranean Sea. Frontiers in Marine Science, 6, 707.
Golani, D., Sonin, O., 1992. New records of the Red Sea fishes, Pterois miles (Scorpaenidae) and Pteragogus pelycus (Labridae) from the eastern Mediterranean Sea. Japanese Journal of Ichthyology, 39 (2), 167-169.
Golani, D., Azzurro, E., Dulčić, J., Massutí, E., Orsi-Relini, L., 2021. Atlas of exotic fishes in the Mediterranean Sea. CIESM Publishers, Monaco, 365 pp.
Gramitto, M.E., Deval, M.C., Saygu, I., 2011. First record of two deep-water fish, Bellottia apoda and Symphurus ligulatus in the Turkish Mediterranean Sea. Cybium, 35 (1), 75-76.
Hacunda, J.S., 1981. Trophic relationships among demersal fishes in a coastal area of the gulf of Maine. Fishery Bulletin, 79 (4), 775.
Harmelin‐Vivien, M.L., Kaim‐Malka, R.A., Ledoyer, M., Jacob‐ Abraham, S.S., 1989. Food partitioning among scorpaenid fishes in Mediterranean seagrass beds. Journal of Fish Biology, 34 (5), 715-734.
Harms-Tuohy, C.A., Schizas, N.V., Appeldoorn, R.S., 2016. Use of DNA metabarcoding for stomach content analysis in the invasive lionfish Pterois volitans in Puerto Rico. Marine Ecology Progress Series, 558, 181-191.
Hernández-Garcia, V., Hernández-López, J.L., Castro-Hdez, J.J., 2002. On the reproduction of Octopus vulgaris off the coast of the Canary Islands. Fisheries Research, 57 (2), 197-203.
Hureau, J.C., Monod, T. (Εds.), 1973. Check-list of the fishes of the north-eastern Atlantic and of the Mediterranean. UNESCO, Paris.
Huth, W.L., McEvoy, D.M., Morgan, O.A., 2018. Controlling an invasive species through consumption: the case of lionfish as an impure public good. Ecological Economics, 149, 74-79.
Hyslop, E.J., 1980. Stomach contents analysis-a review of methods and their application. Journal of Fish Biology, 17 (4), 411-429.
Irmak, E., Engin, S., 2015. A newly established population of the Indian Ocean Twospot Cardinalfish, Cheilodipterus novemstriatus (Rüppell, 1838), in the Northern Levantine Sea (Osteichthyes: Apogonidae). Zoology in the Middle East, 61 (2), 186-188.
Irmak, E., Öndes, F., 2019. Occurrence of the squat lobster Munida curvimana A. Milne Edwards & Bouvier, 1894 and Colombus crab Planes minutus (Linnaeus, 1758) in Turkey. Journal of the Black Sea/Mediterranean Environment, 25 (2), 150-159.
Karhan, S.Ü., Yokeş, M.B., 2012. An earlier record of the Indo- Pacific swimming crab, Gonioinfradens paucidentatus (A. Milne-Edwards, 1861) (Decapoda, Brachyura, Portunidae) off the Mediterranean coast of Turkey. Crustaceana, 85 (1), 117-121.
Katsanevakis, S., Verriopoulos, G., 2004. Den ecology of Octopus vulgaris Cuvier, 1797, on soft sediment: availability and types of shelter. Scientia Marina, 68 (1), 147-157.
Kleitou, P., Savva, I., Kletou, D., Hall-Spencer, J.M., Antoniou, C. et al., 2019. Invasive lionfish in the Mediterranean: Low public awareness yet high stakeholder concerns. Marine Policy, 104, 66-74.
Kleitou, P., Hall-Spencer, J.M., Savva, I., Kletou, D., Hadjistylli, M. et al., 2021. The case of lionfish (Pterois miles) in the Mediterranean Sea demonstrates limitations in EU legislation to address marine biological invasions. Journal of Marine Science and Engineering, 9 (3), 325.
Kletou, D., Hall-Spencer, J.M., Kleitou, P., 2016. A lionfish (Pterois miles) invasion has begun in the Mediterranean Sea. Marine Biodiversity Records, 9, 1-7.
Koilakos, S.M., Georgatis, I., Leonardos, I., 2024. Feeding Strategies and Biological Traits of the Lessepsian Migrant Pterois miles (Bennett, 1828) in the Messenian Gulf, SW Greece. Fishes, 9 (10), 380.
Kondylatos, G., Vagenas, G., Kalaentzis, K., Mavrouleas, D., Conides, A. et al., 2023. Exploring the Structure of Static Net Fisheries in a Highly Invaded Region: The Case of Rhodes Island (Eastern Mediterranean). Sustainability, 76615, 14976.
Kondylatos, G., Theocharis, A., Mandalakis, M., Avgoustinaki, M., Karagyaurova, T. et al., 2024. The Devil Firefish Pterois miles (Bennett, 1828): Life History Traits of a Potential Fishing Resource in Rhodes (Eastern Mediterranean). Hydrobiology, 3 (1), 31-50.
Kourantidou, M., Cuthbert, R.N., Haubrock, P.J., Novoa, A., Taylor N.G. et al., 2021. Economic costs of invasive alien species in the Mediterranean basin. NeoBiota, 67, 427-458.
Loya-Cancino, K.F., Ángeles-González, L.E., Yañez-Arenas, C., Ibarra-Cerdeña, C.N., Velázquez-Abunader, I. et al., 2023. Predictions of current and potential global invasion risk in populations of lionfish (Pterois volitans and Pterois miles) under climate change scenarios. Marine Biology, 170 (3), 27.
Marshall, N.J., Cortesi, F., de Busserolles, F., Siebeck, U.E., Cheney, K.L., 2019. Colours and colour vision in reef fishes: Past, present and future research directions. Journal of Fish Biology, 95 (1), 5-38.
Mokrane, Z., Laribi, H., Touahria, N., Boufersaoui, S., Zerouali, F., 2015. Diet in relation to the tract structure and the chitinolytic activity in Scorpaena notata (Rafinesque, 1810) at the Algerian coast. Cahiers de Biologie Marine, 56, 245-252.
Morris, J.A., 2009. The biology and ecology of invasive Indo- Pacific lionfish. Ph.D. Thesis. North Carolina State University, Raleigh, NC. 168pp.
Morris, J.A., Akins, J.L., 2009. Feeding ecology of invasive lionfish (Pterois volitans) in the Bahamian archipelago. Environmental Biology of Fishes, 86, 389-398.
Morris, J.A., Akins, J.L., Barse, A., Cerino, D., Freshwater, D.W. et al., 2009. Biology and ecology of the invasive lionfishes, Pterois miles and Pterois volitans. Proceedings of the 61st Gulf Caribbean Fisheries Institute, 29, 409-414.
Morris, J.A., Whitfield, P., 2012. Biology, ecology, control and management of the invasive Indo-Pacific lionfish: An updated integrated assessment. Monograph or Serial issue. Beaufort, NC: NOAA/National Ocean Service. Center for Coastal Fisheries and Habitat Research.
Morte, S., Redon, M.J., Sanz-Brau, A., 2001. Diet of Scorpaena porcus and Scorpaena notata (Pisces: Scorpaenidae) in the western Mediterranean. Cahiers de Biologie Marine, 42 (4), 333-344.
Mouchlianitis, F.A., Kalaitzi, G., Kleitou, P., Savva, I., Kletou, D. et al., 2022. Reproductive dynamics of the invasive lionfish (Pterois miles) in the Eastern Mediterranean Sea. Journal of Fish Biology, 100 (2), 574-581.
Moullec, F., Barrier, N., Drira, S., Guilhaumon, F., Marsaleix, P. et al., 2019. An end-to-end model reveals losers and winners in a warming Mediterranean Sea. Frontiers in Marine Science, 6, 345.
Olguner, M.T., Tosunoğlu, Z., Ünal, V., Kök, F. 2024. Impact of invasive edible species on Mediterranean small-scale fisheries. Fish Forum 2024, 19-13 February 2024, Antalya.
Omri, N., Derbal, F., Kara, M.H., 2019. Diet of the black scorpionfish Scorpaena porcus (Scorpaenidae) of the gulf of Annaba, Algeria. Cybium, 43 (2), 179-186.
Ouakka, K., Yahyaoui, A., Mesfioui, A., El Ayoubi, S., 2017. Stomach fullness index and condition factor of European sardine (Sardina pilchardus) in the south Moroccan Atlantic coast. Aquaculture, Aquarium, Conservation & Legislation, 10 (1), 56-63.
Öndes, F., Ünal, V., 2023. The dominance of non-indigenous species in the catch composition of small-scale fisheries: A case study from the Kaş-Kekova Special Environmental Protection Area, Türkiye, Eastern Mediterranean. Acta Ichthyologica et Piscatoria, 53, 27-35.
Peake, J., Bogdanoff, A.K., Layman, C.A., Castillo, B., Reale- Munroe, K. et al., 2018. Feeding ecology of invasive lionfish (Pterois volitans and Pterois miles) in the temperate and tropical western Atlantic. Biological Invasions, 20, 2567-2597.
Phillips, E.W., Bottacini, D., Schoonhoven, A.N., Kamstra, Y.J., De Waele, H. et al., 2024. Limited effects of culling on the behavior of invasive lionfish (Pterois miles) in the Mediterranean. Journal of Fish Biology, 1-10.
Pinkas, L., 1971. Food habits of albacore, bluefin tuna, and bonito in California waters. Fishery Bulletin, 152, 1-139.
Pinnegar, J.K., 2018. Why the damselfish Chromis chromis is a key species in the Mediterranean rocky littoral–a quantitative perspective. Journal of Fish Biology, 92 (3), 851-872.
Poursanidis, D., Kalogirou, S., Azzurro, E., Parravicini, V., Bariche, M. et al., 2020. Habitat suitability, niche unfilling and the potential spread of Pterois miles in the Mediterranean Sea. Marine Pollution Bulletin, 154, 111054.
Rafrafi-Nouira, S., El Kamel-Moutalibi, O., Boumaïza, M., Reynaud, C., Capapé, C., 2016. Food and feeding habits of black scorpionfish, Scorpaena porcus (Osteichthyes: Scorpaenidae) from the northern coast of Tunisia (Central Mediterranean). Journal of Ichthyology, 56, 107-123.
Rajasilta, M., Hänninen, J., Vuorinen, I., 2014. Decreasing salinity improves the feeding conditions of the Baltic herring (Clupea harengus membras) during spring in the Bothnian Sea, northern Baltic. ICES Journal of Marine Science, 71 (5), 1148-1152.
R Core Team, 2022. R: A language and environment for statistical computing. R foundation for statistical computing, Vienna, Austria.
Samourdani, A., Ketsilis-Rinis, V., Koutsidi, M., Lazaris, A., Peristeraki, P. et al., 2024. Ecology and behaviour of the invasive lionfish Pterois miles colonizing coastal areas of the central Mediterranean. Estuarine, Coastal and Shelf Science, 108796.
Sancho, G., Kingsley-Smith, P.R., Morris, J.A., Toline, C.A., McDonough, V. et al., 2018. Invasive lionfish (Pterois volitans/ miles) feeding ecology in Biscayne National Park, Florida, USA. Biological Invasions, 20, 2343-2361.
Šantić, M., Pallaoro, A., Rađa, B., 2021. Feeding habits of Scorpaena notata (Scorpaenidae) from eastern Adriatic Sea. Cybium, 45 (3), 217-224.
Savva, I., Chartosia, N., Antoniou, C., Kleitou, P., Georgiou, A. et al., 2020. They are here to stay: the biology and ecology of lionfish (Pterois miles) in the Mediterranean Sea. Journal of Fish Biology, 97 (1), 148-162.
Schultz, E.T., 1986. Pterois volitans and Pterois miles: two valid species. Copeia, 686-690.
Shahrani, S.E., Shakman, E., 2015. Food and feeding habits of Scorpaena scrofa (Linnaeus 1758) in the western part of Libya. Libyan Journal of Marine Science, 14, 5-15.
Shine, C., 2007. Invasive species in an international context: IPPC, CBD, European Strategy on Invasive Alien Species and other legal instruments. EPPO bulletin, 37 (1), 103-113.
Sokal, R.R., Rohlf F.J., 1981. Biometry. The principles and practices of statistics in biological research, 2nd ed. San Francisco: W.H. Freeman.
South, J., Dick, J.T., McCard, M., Barrios-O’Neill, D., Anton, A., 2017. Predicting predatory impact of juvenile invasive lionfish (Pterois volitans) on a crustacean prey using functional response analysis: effects of temperature, habitat complexity and light regimes. Environmental Biology of Fishes, 100, 1155-1165.
Stern, N., Badreddine, A., Bitar, G., Crocetta, F., Deidun, A. et al., 2019. New Mediterranean Biodiversity Records (July 2019). Mediterranean Marine Science, 20 (2), 409-426.
Trégarot, E., Fumaroli, M., Arqué, A., Hellio, C., Maréchal, J.P., 2015. First records of the red lionfish (Pterois volitans) in Martinique, French West Indies: monitoring invasion status through visual surveys. Marine Biodiversity Records, 8, e1.
Turan, C., Ergüden, D., Gürlek, M., Yağlioğlu, D., Uyan, A. et al., 2014. First record of the Indo-Pacific lionfish Pterois miles (Bennett, 1828) (Osteichthyes: Scorpaenidae) for the Turkish marine waters. Journal of Black Sea/Mediterranean Environment, 20 (2), 158-163.
Ulman, A., Harris, H.E., Doumpas, N., Deniz Akbora, H., Mabruk, A. et al., 2021. Low pufferfish and lionfish predation in their native and invaded ranges suggests human control mechanisms may be necessary to control their Mediterranean abundances. Frontiers in Marine Science, 8, 670413.
Ulman, A., Ali, F. Z., Harris, H. E., Adel, M., Mabruk, S.A.A. et al., 2022. Lessons from the Western Atlantic lionfish invasion to inform management in the Mediterranean. Frontiers in Marine Science, 9, 865162.
Ünal, V., Tıraşın, E.M., Tosunoğlu, Z., 2022. An ecosystem approach to fisheries management for small-scale fisheries in Gökova marine protected area, Turkey: challenges encountered during the transition process.
Vasconcellos, M., Ünal, V. (Eds). Transition towards an ecosystem approach to fisheries in the Mediterranean Sea - Lessons learned through selected case studies. FAO Fisheries and Aquaculture Technical Paper No. 681. Rome, 117-136 pp.
Vagenas, G., Karachle, P.K., Oikonomou, A., Stoumboudi, M.T., Zenetos, A., 2024. Decoding the spread of non-indigenous fishes in the Mediterranean Sea. Scientific Reports, 14, 6669.
Valdez-Moreno, M., Quintal-Lizama, C., Gómez-Lozano, R., García-Rivas, M.D.C., 2012. Monitoring an alien invasion: DNA barcoding and the identification of lionfish and their prey on coral reefs of the Mexican Caribbean. PloS one, 7 (6), e36636.
Whitehead, P.J.P., Bauchot, M.L., Hureau, J.C., Nielsen, J., Tortonese, E. (Eds), 1986. Fishes of the North-eastern Atlantic and the Mediterranean. UNESCO, Paris. Vols. I-III: 1473 pp.
Zannaki, K., Corsini-Foka, M., Kampouris, T.E., Batjakas, I.E., 2019. First results on the diet of the invasive Pterois miles (Actinopterygii: Scorpaeniformes: Scorpaenidae) in the Hellenic waters. Acta Ichthyologica et Piscatoria, 49 (3), 311-317.
Zenetos, A., Albano, P.G., Garcia, E.L., Stern, N., Tsiamis, K. et al., 2022. Established non-indigenous species increased by 40% in 11 years in the Mediterranean Sea. Mediterranean Marine Science, 23 (1), 196-212.
Most read articles by the same author(s)