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Health and reproduction of red mullet, Mullus barbatus, in the western Mediterranean Sea

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Abstract

The reproductive and general health of exploited fish stocks is an essential element of sustainable and profitable fisheries. The main purpose of this study was to assess the relationships between reproduction and two important parameters of fish health (parasitism and energy reserves) in female specimens of red mullet, Mullus barbatus, from the western Mediterranean Sea. We present new data for this species on (i) the prevalence and intensity of infection by metazoan parasites; (ii) the total lipid content in muscle and gonads as a measure of condition and (iii) fecundity and egg quality as a measure of their reproductive capacity. The results show that M. barbatus is a batch spawner with an income breeding strategy, an asynchronous development of oocytes and indeterminate fecundity. The results also indicate that the three most abundant and prevalent parasites significantly affect the condition and reproduction of M. barbatus. Specifically, the digenean, Opecoeloides furcatus, causes a reduction in the female’s energy reserves, while the nematodes, Hysterothylacium fabri and H. aduncum, produce a rise in egg production but impair egg quality. These implications of the relationships between parasitism, fish health and fish reproduction should be taken into consideration in the assessment and management of exploited species.

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References

  • Adams, S. M., 1999. Ecological role of lipids in the health and success of fish populations. In Arts, M. T. & B. C. Wainnmann (eds), Lipids in Freshwater Ecosystems. Springer, New York: 132–153.

    Chapter  Google Scholar 

  • Alonso-Fernández, A., A. C. Vallejo, F. Saborido-Rey, H. Murua & E. A. Trippel, 2009. Fecundity estimation of Atlantic cod (Gadus morhua) and haddock (Melanogrammus aeglefinus) of Georges Bank: application of the autodiametric method. Fisheries Research 99: 47–54.

    Article  Google Scholar 

  • Anastasopoulou, A. & F. Saborido-Rey, 2011. Reproductive ecology of Mullus barbatus in eastern Mediterranean Sea. In Book of Abstracts of the Fish Reproduction and Fisheries (FRESH) Final Conference, 16–20 May 2011, Vigo. http://freshcost.quadralia.net/fresh-final-conference/.

  • Aydın, M. & U. Karadurmuş, 2013. An investigation on age, growth and biological characteristics of red mullet (Mullus barbatus ponticus, Essipov, 1927) in the Eastern Black Sea. Iranian Journal of Fisheries Sciences 12: 277–288.

    Google Scholar 

  • Bagamian, K. H., D. C. Heins & J. A. Baker, 2004. Body condition and reproductive capacity of three-spined stickleback infected with the cestode Schistocephalus solidus. Journal of Fish Biology 64: 1568–1576.

    Article  Google Scholar 

  • Barret, J. A., 1986. Host-parasite interactions and systematics. In Stone, A. R. & D. L. Hawksworth (eds), Coevolution and Systematics. Oxford University Press Inc., Oxford: 1–17.

    Google Scholar 

  • Bean, M. G. & T. H. Bonner, 2009. Impact of Bothriocephalus acheilognathi (Cestoda: Pseudophyllidea) on Cyprinella lutrensis condition and reproduction. Journal of Freshwater Ecology 24: 383–391.

    Article  Google Scholar 

  • Benjamini, Y. & Y. Hochberg, 1995. Controlling the false discovery rate: a practical and powerful approach to multiple testing. Journal of the Royal Statistical Society 57: 289–300.

    Google Scholar 

  • Birkeland, C. & P. K. Dayton, 2005. The importance in fishery management of leaving the big ones. Trends in Ecology and Evolution 20: 356–358.

    Article  PubMed  Google Scholar 

  • Bizsel, K. C., 1987. Seasonal variations in the diel diet of the red mullets (Mullus barbatus L.) in the northern Sicilian Basin. Middle East Technical University, 87 pp.

  • Bray, R. A., D. I. Gibson & A. Jones, 2008. Keys to the Trematoda, Vol. 3. CAB International, Wallingford, 848 pp.

  • Brown-Peterson, N. J., D. M. Wyanski, F. Saborido-Rey, B. J. Macewicz & S. K. Lowerre-Barbieri, 2011. A standardized terminology for describing reproductive development in fishes. Marine and Coastal Fisheries 3: 52–70.

    Article  Google Scholar 

  • Bush, A. O., K. D. Lafferty, J. M. Lotz & A. W. Shostak, 1997. Parasitology meets ecology on its own terms: Margolis et al. Revisited. Journal of Parasitology 83: 575–583.

    Article  CAS  PubMed  Google Scholar 

  • Carreras-Aubets, M., F. E. Montero, F. Padrós, S. Crespo & M. Carrassón, 2011. Parasites and hystopathology of Mullus barbatus and Citharus linguatula (Pisces) from two sites in the NW Mediterranean with different degrees of pollution. Scientia Marina 75: 369–378.

    Google Scholar 

  • Carreras-Aubets, M., F. E. Montero, A. Kostadinova & M. Carrassón, 2012. Parasite communities in the red mullet, Mullus barbatus L., respond to small-scale variation in the levels of polychlorinated biphenyls in the Western Mediterranean. Marine Pollution Bulletin 64: 1853–1860.

    Article  CAS  PubMed  Google Scholar 

  • Chérif, M., M. M. Ben Amor, S. Selmi, H. Gharbi, H. Missaoui & C. Capapé, 2011. Food and feeding habits of the red mullet, Mullus barbatus (Actinopterygii: Perciformes: Mullidae), off the northern Tunisian coast (central Mediterranean). Acta Ichthyologica Et Piscatoria 41: 109–116.

    Article  Google Scholar 

  • Desbrosses, P., 1935. Contribution a la connaissance de la biologie du rouget-barbet en Atlantique nord. Revue des Travaux de l’Institut des Pêches Maritimes IV 3: 249–270.

    Google Scholar 

  • Domínguez-Petit, R., F. Saborido-Rey & I. Medina, 2010. Changes of proximate composition, energy storage and condition of European hake (Merluccius merluccius, L. 1758) through the spawning season. Fisheries Research 104: 73–82.

    Article  Google Scholar 

  • Durieux, E. D. H., R. Galois, M.-L. Bégout, P. Sasal & F. Lagardère, 2007. Temporal changes in lipid condition and parasitic infection by digenean metacercariae of young-of-year common sole Solea solea (L.) in an Atlantic nursery ground (Bay of Biscay, France). Journal of Sea Research 57: 162–170.

    Article  Google Scholar 

  • Esposito, V., F. Andaloro, D. Bianca, A. Natalotto, T. Romeo, G. Scotti & L. Castriota, 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. Marine Biology Research 10: 167–178.

    Article  Google Scholar 

  • FAO/General Fisheries Commission for the Mediterranean, 2012. Report of the Fourteenth Session of the Scientific Advisory Committee, Sofia 20–24 Feb 2012. FAO Fisheries and Aquaculture Report No. 1001. FAO, Rome, 200 pp. http://www.fao.org/docrep/015/i2702b/i2702b.pdf.

  • Ferrer-Maza, D., J. Lloret, M. Muñoz, E. Faliex, S. Vila & P. Sasal, 2014. Parasitism, condition and reproduction of the European hake (Merluccius merluccius) in the northwestern Mediterranean Sea. ICES Journal of Marine Science 71: 1088–1099.

    Article  Google Scholar 

  • Fischer, W., M. Schneider & M. L. Bauchot, 1987. Fiches FAO d’identification des espèces pour les besoins de la peche. Mediterranée et Mer Noire. Zone de peche 37. Volume II: Vertébrés. Fiches FAO d’identification des espèces pour les besoins de la peche. FAO, Rome, 769 pp.

  • Fogelman, R. M., A. M. Kuris & A. S. Grutter, 2009. Parasitic castration of a vertebrate: Effect of the cymothoid isopod, Anilocra apogonae, on the five-lined cardinalfish, Cheilodipterus quinquelineatus. International Journal for Parasitology 39: 577–583.

    Article  PubMed  Google Scholar 

  • Francová, K. & M. Ondračková, 2013. Overwinter body condition, mortality and parasite infection in two size classes of 0+ year juvenile European bitterling Rhodeus amarus. Journal of Fish Biology 82: 555–568.

    Article  PubMed  Google Scholar 

  • Ganias, K., 2013. Determining the indeterminate: evolving concepts and methods on the assessment of the fecundity pattern of fishes. Fisheries Research 138: 23–30.

    Article  Google Scholar 

  • Gibson, D. I., A. Jones & R. A. Bray, 2002. Keys to the Trematoda, Vol. 1. CAB International, Wallingford, 544 pp.

  • Guidelli, G., W. L. G. Tavechio, R. M. Takemoto & G. C. Pavanelli, 2011. Relative condition factor and parasitism in anostomid fishes from the floodplain of the Upper Paraná River, Brazil. Veterinary Parasitology 177: 145–151.

    Article  PubMed  Google Scholar 

  • Houston, A. I., P. A. Stephens, I. L. Boyd, K. C. Harding & J. M. McNamara, 2006. Capital or income breeding? A theoretical model of female reproductive strategies. Behavioral Ecology 18: 241–250.

    Article  Google Scholar 

  • Jones, A., R. A. Bray & D. I. Gibson, 2005. Keys to the Trematoda, Vol. 2. CAB International, Wallingford, 768 pp.

  • Khan, R. A. & D. Lacey, 1986. Effect of concurrent infections of Lernaeocera Branchialis (Copepoda) and Trypanosoma murmanensis (Protozoa) on Atlantic cod, Gadus morhua. Journal of Wildlife Diseases 22: 201–208.

    Article  CAS  PubMed  Google Scholar 

  • Kokokiris, L., A. Stamoulis, N. Monokrousos & S. Doulgeraki, 2014. Oocytes development, maturity classification, maturity size and spawning season of the red mullet (Mullus barbatus barbatus Linnaeus, 1758). Journal of Applied Ichthyology 30: 20–27.

    Article  Google Scholar 

  • Lloret, J., M. Demestre & J. Sánchez-Pardo, 2007. Lipid reserves of red mullet (Mullus barbatus) during pre-spawning in the northwestern Mediterranean. Scientia Marina 71: 269–277.

    Article  Google Scholar 

  • Lloret, J., E. Faliex, G. E. Shulman, J. A. Raga, P. Sasal, M. Muñoz, M. Casadevall, A. E. Ahuir-Baraja, F. E. Montero, A. Repullés-Albelda, M. Cardinale, H. J. Rätz, S. Vila & D. Ferrer-Maza, 2012a. Fish health and fisheries, implications for stock assessment and management: the mediterranean example. Reviews in Fisheries Science 20: 165–180.

    Article  Google Scholar 

  • Lloret, J., R. Galzin, L. Gil de Sola, A. Souplet & M. Demestre, 2005. Habitat related differences in lipid reserves of some exploited fish species in the north-western Mediterranean continental shelf. Journal of Fish Biology 67: 51–65.

    Article  Google Scholar 

  • Lloret, J., M. Muñoz & M. Casadevall, 2012b. Threats posed by artisanal fisheries to the reproduction of coastal fish species in a Mediterranean marine protected area. Estuarine, Coastal and Shelf Science 113: 133–140.

    Article  Google Scholar 

  • Lloret, J., G. Shulman & R. M. Love, 2014. Condition and Health Indicators of Exploited Marine Fishes. Wiley Blackwell, Oxford, 262 pp.

  • Lowerre-Barbieri, S. K. & L. R. Barbieri, 1993. A new method of oocyte separation and preservation for fish reproduction studies. Fishery Bulletin 91: 165–170.

    Google Scholar 

  • Lowerre-Barbieri, S. K., N. J. Brown-Peterson, H. Murua, J. Tomkiewicz, D. M. Wyanski & F. Saborido-Rey, 2011. Emerging issues and methodological advances in fisheries reproductive biology. Marine and Coastal Fisheries 3: 32–51.

    Article  Google Scholar 

  • Martínez-Vicaria, A., J. Martín-Sánchez, P. Illescas, A. M. Lara, M. Jiménez-Albarrán & A. Valero, 2000. The occurrence of two opecoeliid digeneans in Mullus barbatus and M. surmuletus from the Spanish south-eastern Mediterranean. Journal of Helminthology 74: 161–164.

    PubMed  Google Scholar 

  • McBride, R. S., S. Somarakis, G. R. Fitzhugh, A. Albert, N. A. Yaragina, M. J. Wuenschel, A. Alonso-Fernández & G. Basilone, 2013. Energy acquisition and allocation to egg production in relation to fish reproductive strategies. Fish and Fisheries. doi:10.1111/faf.12043.

    Google Scholar 

  • Muñoz, M., C. Dimitriadis, M. Casadevall, S. Vila, E. Delgado, J. Lloret & F. Saborido-Rey, 2010. Female reproductive biology of the bluemouth Helicolenus dactylopterus dactylopterus: spawning and fecundity. Journal of Fish Biology 77: 2423–2442.

    Article  PubMed  Google Scholar 

  • Murua, H. & L. Motos, 2006. Reproductive strategy and spawning activity of the European hake Merluccius merluccius (L.) in the Bay of Biscay. Journal of Fish Biology 69: 1288–1303.

    Article  Google Scholar 

  • Murua, H. & F. Saborido-Rey, 2003. Female reproductive strategies of marine fish species of the North Atlantic. Journal of Northwest Atlantic Fishery Science 33: 23–31.

    Article  Google Scholar 

  • Murua, H., G. Kraus, F. Saborido-Rey, P. R. Witthames, A. Thorsen & S. Junquera, 2003. Procedures to estimate fecundity of marine fish species in relation to their reproductive strategy. Journal of Northwest Atlantic Fishery Science 33: 33–54.

    Article  Google Scholar 

  • Naidenova, N. N. & V. M. Nikolaeva, 1968. Nematode fauna of some benthic fish of the Mediterranean Basin. Biologiya Morya 14: 63–82.

    Google Scholar 

  • Ondracková, M., K. Francová, M. Dávidová, M. Polacik & P. Jurajda, 2010. Condition status and parasite infection of Neogobius kessleri and N. melanostomus (Gobiidae) in their native and non-native area of distribution of the Danube River. Ecological Research 25: 857–866.

    Article  Google Scholar 

  • Petter, A. J., C. Lèbre & B. M. Radujkovic, 1984. Nematode parasites of osteichthyen fish of the southern Adriatic. Acta Adriatica 25: 205–221.

    Google Scholar 

  • Petter, A. J. & C. Maillard, 1987. Ascarids of fishes from Western Mediterranean sea. Bulletin du Muséum National d’Histoire Naturelle. Section A, Zoologie, Biologie et Écologie Animales 9: 773–798.

    Google Scholar 

  • Petter, A. J. & C. Maillard, 1988. Larval Ascarids parasites of fishes from western Mediterranean sea. Bulletin du Muséum National d’Histoire Naturelle. Section A, Zoologie, Biologie et Écologie Animales Muséum national d’histoire naturelle 10: 347–369.

    Google Scholar 

  • Ramdane, Z., J. P. Trilles, K. Mahé & R. Amara, 2013. Metazoan ectoparasites of two teleost fish, Boops boops (L.) and Mullus barbatus barbatus L. from Algerian coast: diversity, parasitological index and impact of parasitism. Cybium 37: 59–66.

    Google Scholar 

  • Reiczigel, J. & L. Rózsa, 2005. Quantitative Parasitology 3.0. Budapest. Distributed by the authors. Available at http://www.zoologia.hu/qp/qp.html.

  • Rijnsdorp, A. D. & P. R. Witthames, 2005. Ecology of reproduction. In Gibson, R. N. (ed.), Flatfishes: Biology and Exploitation. Fish and Aquatic Resources Series 9. Blackwell Science, Oxford: 68–93.

    Chapter  Google Scholar 

  • Roncarati, A., G. Brambilla, A. Meluzzi, A. L. Iamiceli, R. Fanelli, I. Moret, A. Ubaldi, R. Miniero, F. Sirri, P. Melotti & A. di Domenico, 2012. Fatty acid profile and proximate composition of fillets from Engraulis encrasicholus, Mullus barbatus, Merluccius merluccius and Sarda sarda caught in Tyrrhenian, Adriatic and Ionian seas. Journal of Applied Ichthyology 28: 545–552.

    Article  CAS  Google Scholar 

  • Rózsa, L., J. Reiczigel & G. Majoros, 2000. Quantifying parasites in samples of hosts. Journal of Parasitology 86: 228–232.

    Article  PubMed  Google Scholar 

  • Saborido-Rey, F., O. S. Kjesbu & A. Thorsen, 2003. Buoyancy of Atlantic cod larvae in relation to developmental stage and maternal influences. Journal of Plankton Research 25: 291–307.

    Article  Google Scholar 

  • Saborido-Rey, F., H. Murua, J. Tomkiewicz & S. Lowerre-Barbieri, 2010. Female reproductive strategies: an energetic balance between maturation, growth and egg production. In Wyanski, D. M. & N. J. Brown-Peterson (eds), Proceedings of the 4th Workshop on Gonadal Histology of Fishes, 16–19 June 2009, El Puerto de Santa María: 15–18. http://hdl.handle.net/10261/24937.

  • Sajiki, J., K. Takahashi, Y. Hayashi, Y. Ando, M. Kaneda & T. Hamazaki, 1992. Fatty acid composition in anchovy (Engraulis japonicus) infected with Anisakis simplex. Japanese Journal of Toxicology and Environmental Health 38: 361–365.

    Article  CAS  Google Scholar 

  • Sasal, P., E. Faliex, I. De Buron & S. Morand, 2001. Sex discriminatory effect of the acanthocephalan Acanthocephaloides propinquus on a gobid fish Gobius bucchichii. Parasite 8: 231–236.

    Article  CAS  PubMed  Google Scholar 

  • Shahidi, F., 2001. Extraction and measurement of total lipids. In Wrolstad, R. E. (ed.), Current Protocols in Food Analytical Chemistry. Wiley, New York: 1–11.

    Google Scholar 

  • Shchepkina, A. M., 1980. Lipid composition of the tissues of Engraulis encrasicholus during its annual cycle and in infection with larvae of the nematode Contracaecum aduncum. Ekologiya Morya 3: 33–39.

    Google Scholar 

  • Tirasin, E. M., A. Unluoglu & B. Cihangir, 2007. Fecundity of red mullet (Mullus barbatus L., 1758) along the Turkish coasts of the Mediterranean sea. Rapport Commission International pour l’Exploration Scientifique de la Mer Méditerranée 38: 614.

    Google Scholar 

  • Tserpes, G., F. Fiorentino, D. Levi, A. Cau, M. Murenu, A. Zamboni & C. Papaconstantinou, 2002. Distribution of Mullus barbatus and M. surmuletus (Osteichthyes: Perciformes) in the Mediterranean continental shelf: implications for management. Scientia Marina 66: 39–54.

    Article  Google Scholar 

  • Tsikliras, A. C., E. Antonopoulou & K. I. Stergiou, 2010. Spawning period of Mediterranean marine fishes. Reviews in Fish Biology and Fisheries 20: 499–538.

    Article  Google Scholar 

  • Vassilopoulou, V. & C. Papaconstantinou, 1993. Feeding habits of red mullet (Mullus barbatus) in a gulf in western Greece. Fisheries Research 16: 69–83.

    Article  Google Scholar 

  • Verhoeven, K. J. F., K. L. Simonsen & L. M. McIntyre, 2005. Implementing false discovery rate control: increasing your power. Oikos 108: 643–647.

    Article  Google Scholar 

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Acknowledgments

We are grateful to our colleagues at the University of Girona (Animal Biology-Ichthyology Research Group) for their collaboration in the laboratory work and, especially, to A. El Aoussimi for his helpful assistance during on-board fish sampling. Thanks are also given to the crew of the R/V Cornide de Saavedra (IEO, Spain) for technical and scientific support during the MEDITS GSA-06 trawl surveys. We also wish to extend our gratitude to R. A. Bray (NHM, London) for his kind help with the digenean identification and the Guest Editor and the anonymous referees for their helpful comments and suggestions on earlier drafts of the manuscript. This study was carried out within the framework of a research project (ref. CTM2009-08602) funded by the Spanish Ministry of Science and Innovation, whereby D. Ferrer-Maza benefited from a FPI predoctoral fellowship (ref. BES-2010-032618). J. Lloret benefited from a “Ramón y Cajal” research contract from the Spanish Ministry of Economy and Competitiveness.

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Ferrer-Maza, D., Muñoz, M., Lloret, J. et al. Health and reproduction of red mullet, Mullus barbatus, in the western Mediterranean Sea. Hydrobiologia 753, 189–204 (2015). https://doi.org/10.1007/s10750-015-2205-5

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