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Ecology of the Atlantic black skipjack Euthynnus alletteratus (Osteichthyes: Scombridae) in the western Mediterranean Sea inferred by parasitological analysis

Published online by Cambridge University Press:  13 May 2016

SALVATORE MELE Open the ORCID record for SALVATORE MELE [Opens in a new window] ,
M. GRAZIA PENNINO ,
M. CRISTINA PIRAS ,
DAVID MACÍAS ,
M. JOSÉ GÓMEZ-VIVES ,
FRANCISCO ALEMANY ,
FRANCISCO E. MONTERO ,
GIOVANNI GARIPPA  and
PAOLO MERELLA Open the ORCID record for PAOLO MERELLA [Opens in a new window]
SALVATORE MELE*
Affiliation:
Parassitologia e Malattie Parassitarie, Dipartimento di Medicina Veterinaria, Università di Sassari, via Vienna 2, 07100 Sassari, Italy
M. GRAZIA PENNINO
Affiliation:
Statistical Modeling Ecology Group (SMEG), Departament de Estadística i Investigació Operativa, Universitat de València, C/ Doctor Moliner 50, 46100 Burjassot, Spain
M. CRISTINA PIRAS
Affiliation:
Parassitologia e Malattie Parassitarie, Dipartimento di Medicina Veterinaria, Università di Sassari, via Vienna 2, 07100 Sassari, Italy
DAVID MACÍAS
Affiliation:
Centro Oceanográfico de Málaga, Instituto Español de Oceanografía, Puerto Pesquero s/n, 29640 Fuengirola, Spain
M. JOSÉ GÓMEZ-VIVES
Affiliation:
Centro Oceanográfico de Málaga, Instituto Español de Oceanografía, Puerto Pesquero s/n, 29640 Fuengirola, Spain
FRANCISCO ALEMANY
Affiliation:
Centre Oceanogràfic de les Balears, Instituto Español de Oceanografía, Moll de Ponent s/n, 07015 Palma, Spain
FRANCISCO E. MONTERO
Affiliation:
Unidad de Zoología Marina, Institut Cavanilles de Biodiversitat i Biologia Evolutiva, Parc Científic, Universitat de València, C/ Catedrático José Beltrán 2, 46980 Paterna, Spain
GIOVANNI GARIPPA
Affiliation:
Parassitologia e Malattie Parassitarie, Dipartimento di Medicina Veterinaria, Università di Sassari, via Vienna 2, 07100 Sassari, Italy
PAOLO MERELLA
Affiliation:
Parassitologia e Malattie Parassitarie, Dipartimento di Medicina Veterinaria, Università di Sassari, via Vienna 2, 07100 Sassari, Italy
*
*Corresponding author: Parassitologia e Malattie Parassitarie, Dipartimento di Medicina Veterinaria, Università di Sassari, via Vienna 2, 07100 Sassari, Italy. Tel: 0039 079 229 456. Fax: 0039 079 229 464. E-mail: smele@uniss.it
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Summary

Between 2008 and 2011, the head of 150 Euthynnus alletteratus (Osteichthyes: Scombridae) caught inshore off the southeastern Iberian coast (western Mediterranean Sea) were examined for parasites. Two monogeneans, four didymozoid trematodes and four copepods were found. Parasite abundance showed a positive relationship with the annual sea surface temperature, except for Pseudocycnus appendiculatus, but negative with the sea depth (Capsala manteri, Neonematobothrium cf. kawakawa and Caligus bonito). Prevalences and mean abundances differed significantly among sampling areas, except for C. manteri, Oesophagocystis sp. 2 and Ceratocolax euthynni, and sampling years (Melanocystis cf. kawakawa, N.cf. kawakawa, P. appendiculatus and Unicolax collateralis). Results indicate that the parasite abundances of E. alletteratus in the western Mediterranean Sea depend mainly on regional environmental variables, which can show interannual variations. The presence of pelagic parasites, i.e. didymozoids and P. appendiculatus, could indicate that E. alletteratus migrates between inshore and offshore pelagic domains. The different parasite faunas reported in E. alletteratus populations from the western Atlantic Ocean and the Mediterranean Sea appear to point out the geographical host isolation. These results suggest that E. alletteratus inhabiting the western Mediterranean Sea performs inshore-offshore small-scale migrations, and not transoceanic migrations between the western Atlantic Ocean and Mediterranean Sea.

Keywords

Scombridaeparasite CopepodaDidymozoidaeMonogeneamigration
Type
Research Article
Information
Parasitology , Volume 143 , Issue 10 , September 2016 , pp. 1330 - 1339
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Copyright
Copyright © Cambridge University Press 2016 

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References

REFERENCES

Abe, N. and Okamoto, M. (2015). Molecular characterization of muscle-parasitizing didymozoid from a chub mackerel, Scomber japonicus . Acta Parasitologica 60, 557–562.CrossRefGoogle ScholarPubMed
Álvarez, I., Rodríguez, J. M., Catalán, I. A., Hidalgo, M., Álvarez-Berastegui, D., Balbín, R., Aparicio-González, A. and Alemany, F. (2015). Larval fish assemblage structure in the surface layer of the northwestern Mediterranean under contrasting oceanographic scenarios. Journal of Plankton Research 37, 834–850.CrossRefGoogle Scholar
Álvarez-Berastegui, D., Ciannelli, L., Aparicio-Gonzalez, A., Reglero, P., Hidalgo, M., López-Jurado, J., Tintoré, J. and Alemany, F. (2014). Spatial scale, means and gradients of hydrographic variables define pelagic seascapes of bluefin and bullet tuna spawning distribution. PLoS ONE 9, e109338.CrossRefGoogle ScholarPubMed
Alves, D. R. and Luque, J. L. (2006). Ecologia das comunidades de metazoários parasitos de cinco espécies de escombrídeos (Perciformes: Scombridae) do litoral do estado do Rio de Janeiro, Brasil. Revista Brasileira de Parasitologia Veterinária 15, 167–181.Google Scholar
Anderson, G. R. and Barker, S. C. (1993). Species differentiation in the Didymozoidae (Digenea): restriction fragment length differences in internal transcribed spacer and 5·8S ribosomal DNA. International Journal for Parasitology 23, 133–136.CrossRefGoogle ScholarPubMed
Bowles, J., Hope, M., Tiu, W. U., Liu, S. X. and McManus, D. P. (1993). Nuclear and mitochondrial genetic markers highly conserved between Chinese and Philippine Schistosoma japonicum . Acta Tropica 55, 217–229.CrossRefGoogle ScholarPubMed
Bush, A. O., Lafferty, K. D., Lotz, J. M. and Shostak, A. W. (1997). Parasitology meets ecology on its own terms: Margolis et al. revisited. Journal of Parasitology 83, 575–583.CrossRefGoogle Scholar
Bussiéras, J. (1972). Les Monogènes Capsalinae parasites des thons de l'Atlantique tropical oriental. Annales de Parasitologie Humaine et Comparée 47, 29–49.CrossRefGoogle Scholar
Carbonell, E., Massutí, E., Castro, J. J. and Garcıá, R. M. (1999). Parasitism of dolphinfishes, Coryphaena hippurus, and Coryphaena equiselis, in the western Mediterranean (Balearic Islands) and central-eastern Atlantic (Canary Islands). Scientia Marina 63, 343–354.CrossRefGoogle Scholar
Catarci, C. (2004). World tuna markets. In GLOBEFISH Research Programme (ed. FAO), v. 74. FAO, Rome, Italy. ISSN 1014–9546.Google Scholar
Chambers, C. B. and Cribb, T. H. (2006). Phylogeny, evolution and biogeography of the Quadrifoliovariinae Yamaguti, 1965 (Digenea: Lecithasteridae). Systematic Parasitology 63, 61–82.CrossRefGoogle ScholarPubMed
Chisholm, L. A. and Whittington, I. D. (2007). Review of the Capsalinae (Monogenea: Capsalidae). Zootaxa 1559, 1–30.CrossRefGoogle Scholar
Collette, B. B. and Nauen, C. E. (1983). FAO species catalogue, v. 2. Scombrids of the world. FAO Fisheries Synopsis 125, 1–137.Google Scholar
Cressey, R. and Cressey, H. B. (1980). Parasitic copepods of mackerel and tuna-like fishes (Scombridae) of the world. Smithsonian Contributions to Zoology 311, 1–186.Google Scholar
Cressey, R. F., Collette, B. B. and Russo, J. L. (1983). Copepods and scombrid fishes: a study in host-parasite relationships. Fishery Bulletin 81, 227–265.Google Scholar
Culurgioni, J., Mele, S., Merella, P., Addis, P., Figus, V., Cau, A., Karakulak, F. S. and Garippa, G. (2014). Metazoan gill parasites of the Atlantic bluefin tuna Thunnus thynnus (Linnaeus) (Osteichthyes: Scombridae) from the Mediterranean and their possible use as biological tags. Folia Parasitologica 61, 148–156.CrossRefGoogle ScholarPubMed
El-Haweet, A. E., Sabry, E. and Mohamed, H. (2013). Fishery and population characteristics of Euthynnus alletteratus (Rafinesque 1810) in the eastern coast of Alexandria, Egypt. Turkish Journal of Fisheries and Aquatic Sciences 13, 629–638.CrossRefGoogle Scholar
Falautano, M., Castriota, M. G., Finoia, M. G. and Andaloro, F. (2007). Feeding ecology of little tunny Euthynnus alletteratus in the central Mediterranean Sea. Journal of the Marine Biological Association of the United Kingdom 87, 999–1005.CrossRefGoogle Scholar
FAO (2014). FishStatJ: Universal Software for Fishery Statistical Time Series. FAO Fisheries and Aquaculture Department, Statistics and Information Service, Rome, Italy.Google Scholar
Gaykov, V. Z. and Bokhanov, D. V. (2008). The biological characteristic of Atlantic black skipjack (Euthynnus alletteratus) of the eastern Atlantic Ocean. Collective Volume of Scientifics Papers ICCAT 62, 1610–1628.Google Scholar
Georgieva, S., Selbach, C., Faltýnková, A., Soldánová, M., Sures, B., Skírnisson, K. and Kostadinova, A. (2013). New cryptic species of the ‘revolutum’ group of Echinostoma (Digenea: Echinostomatidae) revealed by molecular and morphological data. Parasites and Vectors 6, 64.CrossRefGoogle ScholarPubMed
Hayward, C. J., Aiken, H. M. and Nowak, B. F. (2008). Epizootics of metazoan gill parasites did not threaten feasibility of farming southern bluefin tuna (Thunnus maccoyii) in a trial extending over summer months. Veterinary Parasitology 154, 122–128.CrossRefGoogle ScholarPubMed
Hendrix, S. S. (1994). Marine Flora and Fauna of the Eastern United States. Platyhelminthes: Monogenea. NOAA Technical Report NMFS series 121. U.S. Department of Commerce, Seattle, Washington, USA.Google Scholar
Hillis, D. M. and Bull, J. J. (1993). An empirical test of bootstrapping as a method for assessing confidence in phylogenetic analysis. Systematic Biology 42, 182–192.CrossRefGoogle Scholar
Jones, J. B. (1991). Movements of albacore tuna (Thunnus alalunga) in the South Pacific: evidence from parasites. Marine Biology 111, 1–9.CrossRefGoogle Scholar
Justo, M. C. N. and Kohn, A. (2015). Diversity of Monogenoidea parasitizing scombrid fishes from Rio de Janeiro coast, Brazil. Check List 11, 1628.CrossRefGoogle Scholar
Lester, R. J. G., Barnes, A. and Habib, G. (1985). Parasites of skipjack tuna, Katsuwonus pelamis: fishery implications. Fishery Bulletin (US) 83, 343–356.Google Scholar
Lin, C. and Ho, S. (2006). Four species of Unicolax Cressey and Cressey, 1980 (Copepoda: Bomolochidae) parasitic on marine fishes of Taiwan. Zoological Studies 45, 339–356.Google Scholar
Madhavi, R. and Ram, B. K. (2000). Community structure of helminth parasites of the tuna, Euthynnus affinis, from the Visakhapatnam coast, Bay of Bengal. Journal of Helminthology 74, 337–342.CrossRefGoogle ScholarPubMed
Manooch, C. S., Mason, D. L. and Nelson, R. S. (1985). Foods of little tunny Euthynnus alletteratus collected along the southeastern and Gulf coasts of the United States. Bulletin of the Japanese Society of Scientific Fisheries 51, 1207–1218.CrossRefGoogle Scholar
Mateu, P., Nardi, V., Fraija-Fernández, N., Mattiucci, S., de Sola, L. G., Raga, J. A., Fernández, M. and Aznar, F. J. (2015). The role of lantern fish (Myctophidae) in the life-cycle of cetacean parasites from western Mediterranean waters. Deep-Sea Research Part 1. 95, 115–121.CrossRefGoogle Scholar
Mele, S., Merella, P., Macías, D., Gómez, M. J., Garippa, G. and Alemany, F. (2010). Metazoan gill parasites of wild albacore Thunnus alalunga (Bonaterre, 1788) from the Balearic Sea (western Mediterranean) and their use as biological tags. Fisheries Research 10, 305–310.CrossRefGoogle Scholar
Mele, S., Macías, D., Gómez, M. J., Garippa, G., Alemany, F. and Merella, P. (2012). Metazoan parasites on the gills of the skipjack tuna Katsuwonus pelamis (Osteichthyes: Scombridae) from the Alboran Sea (western Mediterranean Sea). Diseases of Aquatic Organisms 97, 219–225.CrossRefGoogle ScholarPubMed
Mele, S., Pennino, M. G., Piras, M. C., Garippa, G. and Merella, P. (2014). Parasite of the head of Scomber colias (Osteichthyes: Scombridae) from the western Mediterranean Sea and their use as biological tags. Acta Parasitologica 59, 173–183.CrossRefGoogle Scholar
Mele, S., Saber, S., Gómez-Vives, M. J., Garippa, G., Alemany, F., Macías, D. and Merella, P. (2015). Metazoan parasites of the head of the bullet tuna Auxis rochei (Osteichthyes: Scombridae) from the western Mediterranean Sea. Journal of Helminthology 89, 734–739.CrossRefGoogle ScholarPubMed
Mladineo, I., Segvić, T. and Petrić, M. (2011). Do captive conditions favor shedding of parasites in the reared Atlantic bluefin tuna (Thunnus thynnus)? Parasitology International 60, 25–33.CrossRefGoogle ScholarPubMed
Muñoz, F., Pennino, M. G., Conesa, D., López-Quílez, A. and Bellido, J. M. (2013). Estimation and prediction of the spatial occurrence of fish species using Bayesian latent Gaussian models. Stochastic Environmental Research and Risk Assessment 27, 1171–1180.CrossRefGoogle Scholar
Nikolaeva, V. M. (1985). Trematodes – Didymozoidae fauna, distribution and biology. In Parasitology and Pathology of Marine Organisms of the World Ocean (ed. Hargis, W. J.), Vol. 25, pp. 67–72. NOAA Technical Report NMFS series 25. U.S. Department of Commerce, Seattle, Washington, USA.Google Scholar
Palm, H. W., Waeschenbach, A., Olson, P. D. and Littlewood, D. T. (2009). Molecular phylogeny and evolution of the Trypanorhyncha Diesing, 1863 (Platyhelminthes: Cestoda). Molecular Phylogenetics and Evolution 52, 351–367.CrossRefGoogle ScholarPubMed
Palombi, A. (1949). I trematodi d'Italia. Parte I. Trematodi monogenetici. Archivio Zoologico Italiano 34, 204–408.Google Scholar
Pozdnyakov, S. E. and Gibson, D. I. (2008). Family Didymozoidae Monticelli, 1888. In Keys to the Trematoda (ed. Bray, R. A., Gibson, D. I. and Jones, A.), Vol. 3, pp. 631–734. CABI Publishing and the Natural History Museum, Wallingford, UK.Google Scholar
R Development Core Team (2015). R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna, Austria. URL [available online at: http://www.R-project.org].Google Scholar
Reiczigel, J., Rózsa, L. and Reiczigel, A. (2013). Quantitative Parasitology (QPweb) [available online at: http://www2.univet.hu/qpweb].Google Scholar
Roos, N. C., Carvalho, A. R., Lopes, P. F. M. and Pennino, M. G. (2015). Modelling sensitive parrotfish (Labridae: Scarini) habitats along the Brazilian coast. Marine Environmental Research 110, 92–100.CrossRefGoogle ScholarPubMed
Rue, H., Martino, S. and Chopin, N. (2009). Approximate Bayesian inference for latent Gaussian models by using integrated nested Laplace approximations. Journal of the Royal Statistical Society: Series B (Statistical Methodology) 71, 319–392.CrossRefGoogle Scholar
Sharples, A. D. and Evans, C. W. (1995). Metazoan parasites of the snapper, Pagrus auratus (Bloch and Schneider, 1801), in New Zealand. 2. Site-specificity. New Zealand Journal of Marine and Freshwater Research 29, 203–211.CrossRefGoogle Scholar
Spiegelhalter, D. J., Best, N. G., Carlin, B. P. and Van Der Linde, A. (2002). Bayesian measures of model complexity and fit. Journal of the Royal Statistical Society: Series B (Statistical Methodology) 64, 583–639.CrossRefGoogle Scholar
Tamura, K., Stecher, G., Peterson, D., Filipski, A. and Kumar, S. (2013). MEGA6: molecular Evolutionary Genetics Analysis Version 6.0. Molecular Biology and Evolution 30, 2725–2729.CrossRefGoogle ScholarPubMed
Yamaguti, S. (1970). Digenetic Trematodes of Hawaiian Fishes. Keigaku Publishing Co. Tokyo.Google Scholar
Yoshida, H. O. (1979). Synopsis of Biological Data on Tunas of the Genus Euthynnus. FAO Fisheries Synopsis 122. NOAA Technical Report NMFS Circular 429. U.S. Department of Commerce, Seattle, Washington, USA.Google Scholar