Between 2009 and 2013, the head region of 102 juveniles of Atlantic bluefin tuna (Thunnus thynnus L.) caught in four nursery areas of the Mediterranean Sea (Balearic Sea, Ionian Sea, Ligurian Sea and Tyrrhenian Sea) were analysed for parasites. Eleven parasite species were found: Capsala magronum, C. onchidiocotyle, C. paucispinosa, Nasicola klawei, Hexostoma thynni, Didymocystis sp. 2 (sensu Rodríguez-Marín et al., 2008), Didymosulcus sp. 2 (sensu Rodríguez-Marín et al. 2008), Didymosulcus wedli, Didymozoon pretiosus, Nematobothriinae gen. sp. and Wedlia sp. The prevalence of some food-borne parasites (Didymocystis sp. 2, D. pretiosus, Nematobothriinae gen. sp. and Wedlia sp.) had significant differences between localities (p ≤ 0.05). The results showed that the parasite fauna of juvenile tunas is not homogenously distributed in the Mediterranean Sea: parasite assemblages differed between hosts from the Balearic, Ionian, Ligurian, and Tyrrhenian seas, suggesting parasites as possible tags to identify the different tuna populations from the corresponding nursery areas.Postprint0,000

Culurgioni J.

Culurgioni, J.

Garibaldi F.

Garibaldi, F.

Macías-López, A.D. (Ángel David)

Palacio-Abella J.

Rodriguez-Marin, E. (Enrique)

Rodríguez-Llanos, J.

English

Between 2009 and 2013, the head region of 102 juveniles of Atlantic bluefin tuna (Thunnus thynnus L.) caught in four nursery areas of the Mediterranean Sea (Balearic Sea, Ionian Sea, Ligurian Sea and Tyrrhenian Sea) were analysed for parasites. Eleven parasite species were found: Capsala magronum, C. onchidiocotyle, C. paucispinosa, Nasicola klawei, Hexostoma thynni, Didymocystis sp. 2 (sensu Rodríguez-Marín et al., 2008), Didymosulcus sp. 2 (sensu Rodríguez-Marín et al. 2008), Didymosulcus wedli, Didymozoon pretiosus, Nematobothriinae gen. sp. and Wedlia sp. The prevalence of some food-borne parasites (Didymocystis sp. 2, D. pretiosus, Nematobothriinae gen. sp. and Wedlia sp.) had significant differences between localities (p ≤ 0.05). The results showed that the parasite fauna of juvenile tunas is not homogenously distributed in the Mediterranean Sea: parasite assemblages differed between hosts from the Balearic, Ionian, Ligurian, and Tyrrhenian seas, suggesting parasites as possible tags to identify the different tuna populations from the corresponding nursery areas.0,000

Garibaldi, F. (Fulvio)

Repositorio Institucional Digital del IEO

SCRS/2014/149 Collect. Vol. Sci. Pap. ICCAT, 71(3): 1456-1461 (2015)  CAN THE PARASITES OF THE HEAD OF JUVENILE THUNNUS THYNNUS L. HELP TO IDENTIFY ITS NURSERY AREAS IN THE MEDITERRANEAN SEA?  Javier Rodríguez-Llanos1, José Palacio-Abella1, Jacopo Culurgioni2, Salvatore Mele3, David Macías4, Fulvio Garibaldi5, Enrique Rodríguez-Marín6, Nicola Sanna2, Samantha Garau2, Paolo Merella3, Giovanni Garippa3, Francisco E. Montero1, Piero Addis2,7   SUMMARY  Between 2009 and 2013, the head region of 102 juveniles of Atlantic bluefin tuna (Thunnus thynnus L.) caught in four nursery areas of the Mediterranean Sea (Balearic Sea, Ionian Sea, Ligurian Sea and Tyrrhenian Sea) were analysed for parasites. Eleven parasite species were found: Capsala magronum, C. onchidiocotyle, C. paucispinosa, Nasicola klawei, Hexostoma thynni, Didymocystis sp. 2 (sensu Rodríguez-Marín et al., 2008), Didymosulcus sp. 2 (sensu Rodríguez-Marín et al. 2008), Didymosulcus wedli, Didymozoon pretiosus, Nematobothriinae gen. sp. and Wedlia sp. The prevalence of some food-borne parasites (Didymocystis sp. 2, D. pretiosus, Nematobothriinae gen. sp. and Wedlia sp.) had significant differences between localities (p ≤ 0.05). The results showed that the parasite fauna of juvenile tunas is not homogenously distributed in the Mediterranean Sea: parasite assemblages differed between hosts from the Balearic, Ionian, Ligurian, and Tyrrhenian seas, suggesting parasites as possible tags to identify the different tuna populations from the corresponding nursery areas.  RÉSUMÉ  Entre 2009 et 2013, la région céphalique de 102 juvéniles de thon rouge de l'Atlantique (Thunnus thynnus L.), capturés dans quatre zones de nourricerie de la Méditerranée (mer des Baléares, mer Ionienne, mer de Ligure et mer Tyrrhénienne), a été analysée afin de détecter des parasites. Onze espèces de parasite ont été observées : Capsala magronum, C. onchidiocotyle, C. paucispinosa, Nasicola klawei, Hexostoma thynni, Didymocystis sp. 2 (Rodríguez-Marín et al., 2008), Didymosulcus sp. 2 (Rodríguez-Marín et al. 2008), Didymosulcus wedli, Didymozoon pretiosus, Nematobothriinae gen. sp. et Wedlia sp. La prévalence de certains parasites d'origine alimentaire (Didymocystis sp. 2, D. pretiosus, Nematobothriinae gen. sp. et Wedlia sp.) présentait des différences significative d'un lieu à l'autre (p ≤ 0,05). Les résultats indiquaient que la faune parasitaire des juvéniles de thons n'est pas distribuée de manière homogène dans la mer Méditerranée. Les assemblages parasitaires différaient entre les hôtes des mers des Baléares, Ionienne, de Ligure et Tyrrhénienne, ce qui donne à penser que les parasites pourraient servir de marques permettant d'identifier les différentes populations de thons provenant des zones de nourricerie correspondantes.  RESUMEN  Entre 2009 y 2013, se analizó la región craneal de 102 juveniles de atún rojo del Atlántico (Thunnus thynnus L.) capturados en cuatro zonas de cría del Mediterráneo (mar Balear, mar Jónico, mar de Liguria y mar Tirreno) en busca de parásitos. Se hallaron onces especies de parásitos: Capsala magronum, C. onchidiocotyle, C. paucispinosa, Nasicola klawei, Hexostoma thynni, Didymocystis sp. 2 (sensu Rodríguez-Marín et al., 2008), Didymosulcus sp. 2 (sensu Rodríguez-Marín et al. 2008), Didymosulcus wedli, Didymozoon pretiosus, Nematobothriinae gen. sp. y Wedlia sp. La prevalencia de algunos parásitos transmitidos por los alimentos (Didymocystis sp. 2, D. pretiosus, Nematobothriinae gen. sp. and Wedlia sp.) presentaba diferencias significativas entre localidades (p ≤ 0.05). Los resultados demostraron que la fauna de parásitos de los túnidos juveniles no se distribuye homogéneamente en el Mediterráneo: los 1Unidad de Zoología Marina, Institut Cavanilles de Biodiversitat i Biologia Evolutiva, Universitat de València, C/ Catedrático J. Beltrán 2, 46980 Paterna, Spain. 2Dipartimento di Scienze della Vita e dell’Ambiente, Università di Cagliari, Italy. 3Parassitologia e Malattie Parassitarie, Dipartimento di Medicina Veterinaria, Università di Sassari, via Vienna 2, 08020 Sassari, Italy. 4Centro Oceanográfico de Málaga, Instituto Español de Oceanografía, Pto Pesquero s/n, 29640, Fuengirola. 5Dipartimento di Scienze della Terra, dell'Ambiente e della Vita, Università di Genova, Corso Europa 26, 16132 Genova, Italy. 6Centro Oceanográfico de Santander, Instituto Español de Oceanografía, Promontorio San Martín s/n, 39004 Santander, Spain. 7Corresponding author: Dipartimento di Scienze della Vita e dell’Ambiente, Università di Cagliari, Italy, Via Fiorelli, 1, 09126. Cagliari, Italy Phone:00390706758082, Fax:00390706758022, E-mail: addisp@unica.it 1456                                                      conjuntos de parásitos diferían entre los anfitriones de los mares Balear, Jónico, de Liguria y Tirreno, lo que sugiere que los parásitos podrían ser posibles marcas para identificar las diferentes poblaciones de túnidos de las correspondientes zonas de cría.   KEYWORDS   Parasites assemblages, Juvenile, Biological tags, Atlantic bluefin tuna, Nursery areas  Introduction  The Atlantic bluefin tuna (BFT), Thunnus thynnus, is a pelagic fish inhabiting the Atlantic Ocean and the Mediterranean Sea. It represents one of the most economically important fish in Atlantic Ocean and Mediterranean Sea, which sustains important recreational and commercial fisheries as well as the capture-based tuna aquaculture industry (Milatou and Megalofonou 2014). At present, the Atlantic bluefin tuna is still considered overexploited and it is included in a multiannual recovery plan by International Commission for the Conservation of Atlantic Tuna (ICCAT), which is the responsible for the management of this fisheries.  Parasites have been used with success to point out differences between host populations and/or to study migrations of several fish species (Mackenzie and Abaunza 2014). The analysis of parasite assemblages throughout the whole area of the host distribution has been demonstrated to be useful to follow the migrations of tunas in the Atlantic (Lardeaux 1982, MacKenzie 1983) and Pacific Ocean (Lester et al., 1985, Jones 1991). However, no extensive studies have done on the parasite fauna of T. thynnus (MacKenzie 1983). Walters (1980) analysed the parasite data of T. thynnus from different areas of Atlantic Ocean suggesting the usefulness of Nasicola klawei and Euryphorus brachypterus to discriminate tunas from western and eastern Atlantic Ocean. Rodríguez-Marín et al. (2008) studied the parasite populations of juvenile bluefin tuna from the Gulf of Biscay suggesting that some direct life cycle parasites (monogeneans, protozoans and crustaceans) and most the food-borne parasites found in the head region would be useful to characterize tuna from this area. Culurgioni et al. (2014) reported differences in the parasite populations of smaller and larger sized tunas from the Mediterranean Sea, suggesting the school of large size bluefin tuna include specimens resident in the Mediterranean Sea and belonging from the Atlantic Ocean. Currently, the parasite fauna of young-of-the-year (YOY) tuna is unknown. The current study describes the metazoan parasite assemblages of the head of young-of-the-year T. thynnus from the Mediterranean Sea.   1. Materials and methods  Between 2009 and 2013, a total of 102 T. thynnus, caught in four locality of the Mediterranean Sea were examined for parasites: 41 specimens were collected from the Balearic Sea (length fork, LF = 22-40 cm), 21 from the Ionian Sea (LF=21-41 cm), 20 from the Ligurian Sea (LF =21-40 cm), and 20 from the Tyrrhenian Sea (LF=21-41 cm).  The heads of fish were excised, stored individually in plastic bags and frozen at –20 °C. Subsequently the samples were defrosted and examined for parasites according to Mele et al., (2012). The following literature was used for species identification: for monogeneans, Palombi (1949) and Chisholm and Whittington (2007); and for didymozoids Yamaguti (1970) and Pozdnyakov and Gibson (2008).  The prevalence of infection and mean abundance of each parasite species was calculated according to Bush et al. (1997). Confidence intervals of prevalence and mean abundance were assessed with the Sterne's exact method and the bias-corrected and accelerated Efron-Tibshirani bootstrap, respectively, using the free software Quantitative Parasitology 3.0 (Reiczigel and Rózsa 2005). Levels of infection of each parasite species were calculated according to locality. Differences between the parasite infections of the host groups were evaluated using the Fisher exact test for prevalence and the Welsh bootstrap t-test for mean abundance (Reiczigel and Rózsa 2005). Multivariate analyses were carried out on the data of the parasites that showed significant difference of prevalence and mean abundance between at least one pair of localities, using R-software (see Mele et al., 2012). Hierarchical cluster analysis of prevalence and mean abundance were performed on a Bray-Curtis similarity matrix to identify possible differences between the examined localities.      1457 2. Results  Eleven parasite species/taxa were found in the head region of juvenile bluefin tuna from the Mediterranean Sea (Table 1). Most of the parasites were didymozoid trematodes belonging to six species: Didymocystis sp. 2 (sensu Rodríguez–Marín et al., 2008), Didymosulcus sp. 2 (sensu Rodríguez–Marín et al., 2008), D. wedli (Ariola, 1902), Didymozoon pretiosus (Ariola, 1902), Nematobothriinae gen. sp. and Wedlia sp. Five monogenean species were found: Capsala magronum (Ishii, 1936), C. onchidiocotyle (Setti, 1899), C. paucispinosa (Mamaev, 1968), Hexostoma thynni (Delaroche, 1811), and Nasicola klawei (Stunkard, 1962). The parasite assemblage of bluefin tuna from the Ionian Sea was the highest parasite richness (9 species), followed by bluefin tuna from the Tyrrhenian (8), Balearic (7) and Ligurian seas (4). H. thynni was the dominant species in the Balearic Sea, Didymosulcus sp. 2 in the Ionian and Ligurian seas, and Wedlia sp. in the Tyrrhenian Sea.  The prevalence of four parasites (Didymosulcus sp. 2, D. pretiosus, Nematobothriinae gen. sp. and Wedlia sp.) showed differences between localities (Table 1). The prevalence of Didymosulcus sp. 2 and D. pretiosus was higher in bluefin tuna from the Ionian Sea than bluefin tuna from the remaining areas (p < 0.05). The prevalence of Nematobothriinae gen. sp. and Wedlia sp. was higher in BFT from the Ionian and Tyrrhenian seas than bluefin tuna from the Balearic and Ligurian seas. The mean abundance of Didymosulcus sp. 2 and D. pretiosus was higher in bluefin tuna from the Ionian Sea than bluefin tuna from the other localities. The mean abundance of Wedlia sp. was higher in fish from Tyrrhenian Sea than bluefin tuna from the Ligurian Sea. The cluster analysis of prevalence and mean abundance (Figure 1) of the parasite assemblages showed that bluefin tuna from Ligurian Sea and Balearic Sea had the lowest level of dissimilarity, whereas bluefin tuna from the Ionian Sea were the most dissimilar.   3. Discussion  In this study eleven parasites were found in the head region of young-of-the-year T. thynnus from the Mediterranean Sea. Only Didymosulcus sp. 2 has been previously described in the YOY from the Mediterranean Sea (Culurgioni et al., 2014). Most of the parasites found, have been previously described in bluefin tuna from the Mediterranean Sea and the Atlantic Ocean. Interestingly, N. klawei, previously reported only in the Atlantic, is also present in the juvenile Mediterranean tunas (Walters 1980, Rodríguez-Marín et al. 2008, Mladineo et al., 2011, Culurgioni et al., 2014). This is the first report of Didymocystis sp. 2, Nematobothriinae gen. sp. and Wedlia sp. in bluefin tuna from the Mediterranean Sea.  The parasite fauna of YOY bluefin tuna from the Mediterranean Sea had a lower richness than larger bluefin tuna from the Mediterranean Sea (Adriatic and Sardinia seas) and the North East Atlantic Ocean (Gulf of Biscay) (Walters 1980, Rodríguez-Marín et al., 2008, Mladineo et al., 2011, Culurgioni et al,. 2014). Surprisingly, D. wedli was only found in one YOY bluefin tuna, whereas it was the dominant species everywhere in the larger tunas. Other two food-borne parasites (Copiatestes thyrsitae Crowcroft, 1948 and Didymocystis sp. 3(sensu Rodríguez-Marín et al., 2008) reported in bluefin tuna from the Atlantic Ocean did not infect YOY bluefin tuna from the four areas herein analysed. Moreover, copepod parasites, such as Caligus coryphaenae, Euryphorus brachypterus (Gerstaecker, 1853) and Pseudocycnus appendiculatus, reported in larger tuna from Sardinia Sea and the Atlantic Ocean, were not present in YOY bluefin tuna.  The comparison of the parasite populations indicates that some species (Didymosulcus sp. 2, D. pretiosus, and Wedlia sp.) had differences in prevalence and mean abundance between areas. According to the general principle to select the parasites as biological tags illustrated by MacKenzie and Abaunza (2014), these didymozoids can be considered reliable tags to follow its migrations, because: (i) they showed differences of infection levels between localities; (ii) they are permanent parasites (sensu Lester et al. 1985) and their remains are recognizable in the host tissues well after their death; and (iii) the host cannot lose them when it migrates outside the endemic area of these parasites (Lester et al. 1985). In fact, the absence of D. pretiosus, Nematobothriinae gen sp. and Wedlia sp. in fish from Ligurian Sea suggest that (i) these parasites did not infect the praise of T. thynnus in this area, (ii) and that no infected fish migrated from Tyrrhenian and Ionian seas to the Ligurian one.  The analysis of the parasite assemblages clustered tuna (Figure 1) in three groups belonging to the Ionian, Tyrrhenian and a third group that includes Balearic and Ligurian samples. This result seems to agree the general oceanographic division of the Mediterranean Sea, suggesting that tuna from Ionian Sea and Tyrrhenian Sea stay around of their breeding areas (Ionian and Tyrrhenian Sea, respectively; Alemany et al. 2010), while the Balearic one, probably migrates throughout the northernmost areas of the western Mediterranean Sea (Balearic and Ligurian seas). 1458 References  Alemany, F., Quintanilla, L., Velez-Belchí, P., García, A., Cortés, D., Rodríguez, J.M., Fernández de Puelles, M.L., González-Pola C., López-Jurado, J.L. 2010. Characterization of the spawning habitat of Atlantic Bluefin tuna and related species in the Balearic Sea (western Mediterranean Progress in Oceanography 86: 21-38.   Bush, A.O., Lafferty, K.D., Lotz, J.M., Shostak, A.W. 1997. Parasitology meets ecology on its own terms: Margolis et al. revisited. Journal of Parasitology 83: 575-583.  Chisholm, L.A., Whittington, I.D. 2007. Review of the Capsalinae (Monogenea: Capsalidae). Zootaxa 1559: 1-30.  Culurgioni, J., Mele, S., Merella, P., Addis, P., Figus, V., Cau, A., Karakulak, F.S., 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.  Jones, J.B. 1991. Movements of albacore tuna (Thunnus alalunga) in the South Pacific: evidence from parasites. Marine Biology 111: 1-9.  Lardeaux, F. 1982. Étude de la structure des populations d’albacores (Thunnus albacares) dans l’Atlantique tropical par l’analyse des chiffres d’infestations parasitaire. Col. Vol. Sci. Pap. ICCAT 17: 68-74.  Lester, R.J.G., Barnes, A., Habib, G. 1985. Parasites of skipjack tuna, Katsuwonus pelamis: fishery implications. Fishery Bulletin NOAA 83: 343-356.  MacKenzie, K. 1983. The selection of parasites for use as biological tags in population studies of bluefin tuna. Col. Vol. Sci. Pap. ICCAT 18: 834–838.  MacKenzie, K., Abaunza, P. 2014. Parasites as Biological Tags (Chapter Ten). Stock Identification Methods (Second Edition). Applications in Fishery Science 185-203.  Mele, S., Macías, D., Gómez, M.J., Garippa, G., Alemany, F., 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.  Mladineo, I., Šegvic, T., Petric, M. 2011. Do captive conditions favor shedding of parasites in the reared Atlantic Bluefin tuna (Thunnus thynnus)? Parasitology International 60, 25–33.  Palombi, A., 1949. I Trematodi d’Italia. Parte I. Trematodi monogenetici. Archivio Zoologico Italiano 34, 204-408.  Pozdnyakov, S.E., Gibson D.I. 2008: Family Didymozoidae Monticelli, 1888. R.A. Bray, A. Jones and D.I. Gibson (Eds.), Keys to the Trematoda. Vol. 3. CABi, Wallingford, 631–734.  ReicziGeL J., RózsA. L. 2005: Quantitative Parasitology 3.0. Budapest. Distributed by the authors.  Rodríguez-Marín, E., Barreiro, S., Montero, F.E., Carbonell, E. 2008. Looking for skin and gill parasites as biological tags for Atlantic bluefin tuna (Thunnus thynnus). Aquatic Living Resources 21: 365-371.  Walters V. 1980: Ectoparasites of eastern and western Atlantic Bluefin tuna. Col. Vol. Sci. Pap. ICCAT 9: 491–498.  Yamaguti S. 1970: Digenetic Trematodes of Hawaiian Fishes. Interscience Publishers, New York, 436 pp. 1459 Table 1. Prevalence and mean abundance of parasites of juvenile Thunnus thynnus from the Mediterranean Sea, 95% confident interval given in parenthesis. Bal., Balearic Sea; Ion., Ionian Sea; Lig., Ligurian Sea; Tyr., Tyrrhenian Sea. Uppercase letters, significant P-value<0.05.   Parasite     Prevalence (%)     Mean abundance   Bal Ion Lig Tyr Bal Ion Lig Tyr Capsala magronum 25 (12-40) 34 (15-57) 10 (2-32) 30 (12-55) 0.5 (0.2-0.9) 0.3 (0.1-0.5) 0.25 (0-0.9) 0.5 (0.2-1.0) Capsala onchidyocotile - 5 (1-24) - - - 0.1 (0.0-0.1) - - Capsala paucispinosa - 5 (1-24) - 10 (2-32) - 0.1 (0.0-0.1) - 0.1 (0.0-0.2) Nasicola klawei - - - 5 (1-25) - - - 0.1 (0-0.2) Hexostoma thynni 42 (26-58) 33 (15-57) 30 (12-55) 35 (16-60) 0.8 (0.5-1.3) 0.4 (0.2-0.7) 0.4 (0.1-0.6) 0.5 (0.2-0.8) Didymocystis sp.2 17 (8-32) 18 (8-33) - 5 (1-25) 0.6 (0.2-1.5) 0.6 (0.2-1.4) - 0.1 (0.0-0.3) Didymosulcus sp.2 8 (2-20)a 72 (48-89)abc 25 (9-50)bd -cd 0.5 (0.1-1.4)a 2.1 (1.3-3.8)ab 0.5 (0.2-1.0)b - Didymosulcus wedli - - 5 (1-25) - - - 0.1 (0.0-0.2) - Didymozoon pretiosus 12 (5-27)a 77 (53-92)abc -b 20 (6 -44)c 0.4 (0.1-0.9)a 1.6 (1.0-2.4)abc -b  0.4 (0.1-1.1)c Nematobothriinae gen. sp. 3 (1-13)ab  19 (6-42)a -c 25 (9-50)bc 0.02 (0.0-0.1) 0.2 (0.1-0.3) - 0.3 (0.1-0.4) Wedlia sp. 18 (8-33)ab 34 (15-57)c -acd 45 (24-69)bd 0.4 (0.2-0.9) 1.1 (0.4-2.4) -a 0.8 (0.4-1.3)a 1460  Figure 1. Cluster dendrogram (group-average linkage method) of the parasites of the head of the young-of-the-year Thunnus thynnus from the Mediterranean Sea using a Bray-Curtis (B) dissimilarity indices based on prevalence. 1461 

Can the parasites of the head of juvenile Thunnus thynnus help to identify its nursery areas in the Mediterranean Sea?

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Can the parasites of the head of juvenile Thunnus thynnus help to identify its nursery areas in the Mediterranean Sea?

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