Hostname: page-component-cd9895bd7-gxg78 Total loading time: 0 Render date: 2024-12-19T08:22:12.237Z Has data issue: false hasContentIssue false
  • English
  • Français

Integrating Anisakis spp. parasites data and host genetic structure in the frame of a holistic approach for stock identification of selected Mediterranean Sea fish species

Published online by Cambridge University Press:  22 August 2014

S. MATTIUCCI ,
R. CIMMARUTA ,
P. CIPRIANI ,
P. ABAUNZA ,
B. BELLISARIO  and
G. NASCETTI
S. MATTIUCCI*
Affiliation:
Department of Public Health and Infectious Diseases, Section of Parasitology, ‘Sapienza University of Rome’, Rome, Italy
R. CIMMARUTA
Affiliation:
Department of Ecological and Biological Sciences, Tuscia University, Viterbo, Italy
P. CIPRIANI
Affiliation:
Department of Public Health and Infectious Diseases, Section of Parasitology, ‘Sapienza University of Rome’, Rome, Italy Department of Ecological and Biological Sciences, Tuscia University, Viterbo, Italy
P. ABAUNZA
Affiliation:
Instituto Español de Oceaonografía, Oceanographic Centre of Santander, Santander, Spain
B. BELLISARIO
Affiliation:
Department of Ecological and Biological Sciences, Tuscia University, Viterbo, Italy
G. NASCETTI
Affiliation:
Department of Ecological and Biological Sciences, Tuscia University, Viterbo, Italy
*
* Corresponding author: Department of Public Health and Infectious Diseases, Section of Parasitology, Sapienza University of Rome, P.le Aldo Moro, 5 00185 Rome, Italy. E-mail: [email protected]
Get access Rights & Permissions [Opens in a new window]

Summary

The unique environment of the Mediterranean Sea makes fish stock assessment a major challenge. Stock identification of Mediterranean fisheries has been based mostly from data on biology, morphometrics, artificial tags, otolith shape and fish genetics, with less effort on the use of parasites as biomarkers. Here we use some case studies comparing Mediterranean vs Atlantic fish stocks in a multidisciplinary framework. The generalized Procrustes Rotation (PR) was used to assess the association between host genetics and larval Anisakis spp. datasets on demersal (hake) and pelagic (horse mackerel, swordfish) species. When discordant results emerged, they were due to the different features of the data. While fish population genetics can detect changes over an evolutionary timescale, providing indications on the cohesive action of gene flow, parasites are more suitable biomarkers when considering fish stocks over smaller temporal and spatial scales, hence giving information of fish movements over their lifespan. Future studies on the phylogeographic analysis of parasites suitable as biomarkers, and that of their fish host, performed on the same genes, will represent a further tool to be included in multidisciplinary studies on fish stock structure.

Keywords

Mediterranean Seabiological tagsAnisakisfish genetic structuregenetic/molecular markersstock identity
Type
Fisheries
Information
Parasitology , Volume 142 , Special Issue 1: Parasites in fisheries and mariculture , January 2015 , pp. 90 - 108
Check for updates
Copyright
Copyright © Cambridge University Press 2014 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

REFERENCES

Abaunza, P., Gordo, L., Karlou-Riga, C., Murta, A., Eltink, A. T. G. W., Garcia Santamaria, M. T., Zimmermann, C., Hammer, C., Lucio, P., Iversen, S. A., Molloy, J. and Gallo, E. (2003). Growth and reproduction of horse mackerel, Trachurus trachurus (Carangidae). Review of Fish Biology and Fisheries 13, 27–61.CrossRefGoogle Scholar
Abaunza, P., Murta, A. G., Campbell, N., Cimmaruta, R., Comesana, A. S., Dahle, G., Garcia Santamaria, M. T., Gordo, L. S., Iversen, S. A., MacKenzie, K., Magoulas, A., Mattiucci, S., Molloy, J., Nascetti, G., Pinto, A. L., Quinta, R., Ramos, P., Sanjuan, A., Santos, A. T., Stransky, C. and Zimmermann, C. (2008 a). Stock identity of horse mackerel (Trachurus trachurus) in the Northeast Atlantic and Mediterranean Sea: integrating the results from different stock identification approaches. Fisheries Research 89, 196–209.CrossRefGoogle Scholar
Abaunza, P., Murta, A. G., Campbell, N., Cimmaruta, R., Comesana, A. S., Dahle, G., Gallo, E., Garcia Santamaria, M. T., Gordo, L. S., Iversen, S. A., MacKenzie, K., Magoulas, A., Mattiucci, S., Molloy, J., Nascetti, G., Pinto, A. L., Quinta, R., Ramos, P., Ruggi, A., Sanjuan, A., Santos, A. T., Stransky, C. and Zimmerman, C. (2008 b). Considerations on sampling strategies for an holistic approach to stock identification: the example of the HOMSIR project. Fisheries Research 89, 104–113.Google Scholar
Abaunza, P., Gordo, L., García Santamaría, M. T., Iversen, S. A., Murta, A. G. and Gallo, E. (2008 c). Life history parameters as an important basis for the initial recognition of stock management units in horse mackerel (Trachurus trachurus). Fisheries Research 89, 167–180.Google Scholar
Alegria-Hernandez, V. (1986). Catch per unit effort as an index of sardine, Sardina pilchardus (Walb.) distribution changes along the eastern Adriatic. FAO Fisheries Report 345, 127–136.Google Scholar
Alvarado Bremer, J. R., Mejutoc, J., Gómez-Márquezd, J., Boánd, F., Carpinterod, P., Rodríguez, J. M., Viñase, J., Greig, T. W. and Elyg, B. (2005 a). Hierarchical analyses of genetic variation of samples from breeding and feeding grounds confirm the genetic partitioning of northwest Atlantic and South Atlantic populations of swordfish (Xiphias gladius L.). Journal of Experimental Marine Biology and Ecology 327, 167–182.Google Scholar
Alvarado Bremer, J. R., Viñasa, J., Mejutoc, J., Elyd, B. and Plae, C. (2005 b). Comparative phylogeography of Atlantic bluefin tuna and swordfish: the combined effects of vicariance, secondary contact, introgression, and population expansion on the regional phylogenies of two highly migratory pelagic fishes. Molecular Phylogenetics and Evolution 36, 169–187.Google Scholar
Alvarado Bremer, J. R., Hinton, M. G. and Grieg, T. W. (2006). Evidence of spatial genetic heterogeneity in Pacific swordfish (Xiphias gladius) revealed by the analysis of ldh-A sequences. Bulletin of Marine Science 79, 493–503.Google Scholar
Bahri-Sfar, L., Lemaire, C., Hassine, B. and Bonhomme, F. (2000). Fragmentation of sea bass populations in the western and eastern Mediterranean as revealed by microsatellite polymorphism. Proceedings of the Royal Society of London Series B – Biological Sciences 267, 929–935.Google Scholar
Balbuena, J. A., Miguez-Lozano, R. and Blasco-Costa, I. (2013). PACo: a novel Procrustes application to cophylogenetic analysis. PLOS ONE 8, e61048.CrossRefGoogle Scholar
Baldwin, R. E., Rew, M. B., Johansson, M. L., Banks, M. A. and Jacobson, K. C. (2011). Population structure of three species of Anisakis nematodes recovered from Pacific sardines (Sardinopsis sagax) distributed throughout the California Current System. Journal of Parasitology 97, 545–554.Google Scholar
Bargelloni, L., Alarcon, J. A., Alvarez, M. C., Penzo, E., Magoulas, A., Reis, C. and Patarnello, T. (2003). Discord in the family Sparidae (Teleostei): divergent phylogeographical patterns across the Atlantic–Mediterranean divide. Journal of Evolutionary Biology 16, 1149–1158.Google Scholar
Bargelloni, L., Alarcon, J. A., Alvarez, M. C., Penzo, E., Magoulas, A., Reis, C. and Patarnello, T. (2005). The Atlantic-Mediterranean transition: discordant genetic patterns in two seabream species, Diplodus puntazzo (Cetti) and Diplodus sargus (L.). Molecular Phylogenetic and Evolution 36, 523–535.Google Scholar
Begg, G. and Waldman, J. R. (1999). An holistic approach to fish stock identification. Fisheries Research 43, 35–44.Google Scholar
Bembo, D. G., Carvalho, G. R., Snow, M., Cingolani, N. and Pitcher, T. J. (1995). Stock discrimination among European anchovies, Engraulis encrasicolus, by means of PCR-amplified mitochondrial DNA analysis. Fishery Bulletin 94, 31–40.Google Scholar
Bembo, D. G., Carvalho, G. R., Cingolani, N., Arneri, E., Giannetti, G. and Pitcher, T. J. (1996 a). Allozymic and morphometric evidence for two stocks of the European anchovy Engraulis encrasicolus in Adriatic waters. Marine Biology 126, 529–538.Google Scholar
Bembo, D. G., Carvalho, G. R., Cingolani, N. and Pitcher, T. J. (1996 b). Electrophoretic analysis of stock structure in northern Mediterranean anchovies, Engraulis encrasicolus . ICES Journal of Marine Science 53, 115–128.Google Scholar
Berland, B. (1961). Nematodes from some Norwegian marine fishes. Sarsia 2, 1–50.Google Scholar
Cacaud, P. (2005). Fisheries laws and regulations in the Mediterranean: a comparative study. Studies and Reviews/General Fisheries Commission for the Mediterranean 7, 40.Google Scholar
Caddy, J. F. (1995). Cephalopod and demersal finfish stocks: some statistical trends and biological interactions. In Squid 94 Venice, Proceedings of the Third International Cephalopod Trade Conference, Agra Europe, London, UK.Google Scholar
Charrier, G., Chenel, T., Durand, J. D., Girard, M., Quiniou, L. and Laroche, J. (2006). Discrepancies in phylogeographical patterns of two European anglerfishes (Lophius budegassa and Lophius piscatorius). Molecular Phylogenetics and Evolution 38, 742–754.Google Scholar
Chow, S. and Takeyama, H. (2000). Nuclear and mitochondrial DNA analyses reveal four genetically separated breeding units of the swordfish (Xiphias gladius). Journal of Fish Biology 56, 1087–1098.Google Scholar
Chow, S., Okamoto, H., Uozumi, Y., Takeuchi, Y. and Takeyama, H. (1997). Genetic stock structure of the swordfish (Xiphias gladius) inferred by PCR–RFLP analysis of the mitochondrial DNA control region. Marine Biology 127, 359–367.Google Scholar
Chow, S., Clarke, S., Nakadate, M. and Okazaki, M. (2007). Boundary between the north and south Atlantic populations of the swordfish (Xiphias gladius) inferred by a single nucleotide polymorphism at calmodulin gene intron. Marine Biology 152, 87–93.Google Scholar
Cimmaruta, R., Iaconelli, M., Nascetti, G. and Bullini, L. (1998). Diversità genetica in popolazioni di grandi pelagici del Mediterraneo. Biologia Marina Mediterranea 5, 300–310.Google Scholar
Cimmaruta, R., Bondanelli, P. and Nascetti, G. (2005). Genetic structure and environmental heterogeneity in the European hake (Merluccius merluccius). Molecular Ecology 14, 2577–2591.Google Scholar
Cimmaruta, R., Bondanelli, P., Ruggi, A. and Nascetti, G. (2008). Genetic structure and temporal stability in the horse mackerel (Trachurus trachurus). Fisheries Research 89, 114–121.CrossRefGoogle Scholar
Comesaña, A. S., Martinez-Areal, M. T. and Sanjuan, A. (2008). Genetic variation in the mitochondrial DNA control region among horse mackerel (Trachurus trachurus) from the Atlantic and Mediterranean areas. Fisheries Research 89, 122–131.Google Scholar
Cowen, R. K. and Sponaugle, S. (2009). Larval dispersal and marine population connectivity. Annual Review of Marine Science 1, 443–466.Google Scholar
Cowen, R. K., Lwiza, K. M. M., Sponaugle, S., Paris, C. B. and Olson, D. B. (2000). Connectivity of marine populations: open or closed? Science 287, 857–859.Google Scholar
Cowen, R. K., Paris, C. B. and Srinivasan, A. (2006). Scaling of connectivity in marine populations. Science 311, 522–527.Google Scholar
Criscione, C. D. and Blouin, M. S. (2007). Parasite phylogeographical congruence with salmon host evolutionary units: implications for salmon conservation. Molecular Ecology 16, 993–1005.Google Scholar
Criscione, C. D., Cooper, B. and Blouin, M. S. (2006). Parasite genotypes identify source populations of migratory fish more accurately than fish genotypes. Ecology 87, 823–828.Google Scholar
Crosetti, D., Nelson, W. S. and Avise, J. C. (1994). Pronounced genetic structure of mitochondrial DNA among populations of the circumglobally distributed grey mullet (Mugil cephalus). Journal of Fish Biology 44, 47–58.Google Scholar
Cross, M. A., Collins, C., Campbell, N., Watts, P. C., Chubb, J. C., Cunningham, C. O., Hatfield, E. M. C. and MacKenzie, K. (2007). Levels of intra-host and temporal sequence variation in a large CO1 subunit from Anisakis simplex sensu stricto (Rudolphi, 1809) (Nematoda: Anisakidae): implications for fisheries managements. Molecular Biology 151, 695–702.Google Scholar
Ehrhardt, N. M. (1992). Age and growth of swordfish, Xiphias gladius, in the Northwestern Atlantic. Bulletin of Marine Science 50, 292–301.Google Scholar
Fernandes, P. G. and Cook, R. M. (2013). Reversal of fish stock decline in the Northeast Atlantic. Current Biology 23, 1432–1437.Google Scholar
Ferrer-Castelló, E., Raga, J. A. and Aznar, F. J. (2007). Parasites as fish population tags and pseudoreplication problems: the case of striped red mullet Mullus surmuletus in the Spanish Mediterranean. Journal of Helminthology 81, 169–178.Google Scholar
Food and Agriculture Organization. (1999). Aquaculture Production Statistics 1988–1997. Fisheries Circular No. 815 Rev. 11, FAO, Rome, Italy.Google Scholar
Froese, R. and Pauly, D. (eds.) (2014). FishBase. World Wide Web Electronic Publication. Available at: www.fishbase.org, version (01/2014).Google Scholar
Gačić, M., Schroeder, K., Civitarese, G., Vetrano, A. and Eusebi Borzelli, G. L. (2012). On the relationship among the Adriatic-Ionian bimodal Oscillating System (BiOS), the Eastern Mediterranean salinity variations and Western Mediterranean thermohaline cell. Ocean Science Discussion 9, 2561–2580.Google Scholar
Galarza, J. A., Carreras-Carbonell, J., Macpherson, E., Pascual, M., Roque, S., Turner, G. F. and Rico, C. (2009). The influence of oceanographic fronts and early-life-history traits on connectivity among littoral fish species. Proceedings of the National Academy of Sciences USA 106, 1473–1478.Google Scholar
Garcia, A., Mattiucci, S., Damiano, S., Santos, M. N. and Nascetti, G. (2011). Metazoan parasites of swordfish, Xiphias gladius (Pisces: Xiphiidae) from the Atlantic Ocean: implications for host stock identification. ICES Journal of Marine Science 68, 175–182.Google Scholar
Gelman, A. and Hill, J. (2007). Data Analysis Using Regression and Multilevel/Hierarchical Models. Cambridge University Press, Cambridge, UK.Google Scholar
GFCM (2012). General Fisheries Commission for the Mediterranean (GFCM). Scientific Advisory Committee on Stock Assessment.Google Scholar
Gordo, L. S., Costa, A., Abaunza, P., Lucio, P., Eltink, A. T. G. W. and Figueiredo, I. (2008). Determinate versus indeterminate fecundity in horse mackerel. Fisheries Research 89, 181–185.Google Scholar
ICES (2013). Advice 2013. North Sea. Horse mackerel (Trachurus trachurus) in Divisions IIIa, IVb,c, and VIId (North Sea stock). http://www.ices.dk/sites/pub/Publication%20Reports/Advice/2013/2013/hom-nsea.pdf.Google Scholar
Kasapidis, P. and Magoulas, A. (2008). Development and application of microsatellite markers to address the population structure of the horse mackerel Trachurus trachurus . Fisheries Research 89, 132–134.Google Scholar
Kasapidis, P., Mejuto, J., Tserpes, G., Antoniou, A., Garcia-Cortes, B., Peristeraki, P., Oikioonomaki, K., Kotoulas, G. and Magoulas, A. (2007). Genetic structure of swordfish (Xiphias gladius) stocks in the Atlantic using microsatellite DNA analysis. Collective Volume of Scientific Papers ICCAT 61, 89–98.Google Scholar
Klimpel, S., Kleinertz, S. and Palm, H. W. (2008). Distribution of parasites from red mullets (Mullus surmuletus L., Mullidae) in the North Sea and Mediterranean Sea. Bulletin of Fish Biology 10, 25–38.Google Scholar
Knutsen, H., Jorde, P. E., André, C. and Stenseth, N. C. (2003). Fine-scaled geographical population structuring in a highly mobile marine species: the Atlantic cod. Molecular Ecology 12, 385–394.Google Scholar
Kotoulas, G., Magoulas, A., Tsimenides, N. and Zouros, E. (1995). Marked mitochondrial DNA differences between Mediterranean and Atlantic populations of the swordfish, Xiphias gladius . Molecular Ecology 4, 473–481.Google Scholar
Lemaire, C., Versini, J. J. and Bonhomme, F. (2005). Maintenance of genetic differentiation across a transition zone in the sea: discordance between nuclear and cytoplasmic markers. Journal of Evolutionary Biology 18, 70–80.Google Scholar
Lleonart, J. and Maynou, F. (2003). Fish stock assessments in the Mediterranean: state of art. Scientia Marina 67, 37–49.Google Scholar
Lundy, C., Moran, P., Rico, C., Milner, R. S. and Hewitt, G. M. (1999). Macrogeographical population differentiation in oceanic environments: a case study of European hake (Merluccius merluccius) a commercially important fish. Molecular Ecology 8, 1889–1898.Google Scholar
Lundy, C. J., Rico, C. and Hewitt, G. M. (2000). Temporal and spatial genetic variation in spawning grounds of European hake (Merluccius merluccius) in the Bay of Biscay. Molecular Ecology 9, 2067–2079.Google Scholar
MacKenzie, K., Campbell, N., Mattiucci, S., Ramos, P., Pinto, A. L. and Abaunza, P. (2008). Parasites as biological tags for stock identification of Atlantic horse mackerel Trachurus trachurus L. Fisheries Research 89, 136–145.Google Scholar
Magoulas, A., Kotoulas, G., de la Serna, J. M., De Metrio, G., Tsimenides, N. and Zouros, E. (1992). Genetic structure of swordfish (Xiphias gladius) populations of the Mediterranean and the eastern side of the Atlantic: analysis by mitochondrial DNA markers. Collective Volume of Scientific Papers ICCAT XL, 126–136.Google Scholar
Magoulas, A., Tsimenides, N. and Zouros, E. (1996). Mitochondrial DNA phylogeny and the reconstruction of the population history of a species: the case of the European anchovy (Engraulis encrasicolus). Molecular Biology and Evolution 13, 178–190.Google Scholar
Mattiangeli, V., Ryan, A. W., Galvin, P., Mork, J. and Cross, T. F. (2003). Eastern and western poor cod (Trisopterus minutus capelanus) populations in the Mediterranean Sea: evidence from allozyme and minisatellite loci. Marine Ecology 24, 247–258.Google Scholar
Mattiucci, S. and Nascetti, G. (2007). Genetic diversity and infection levels in anisakid nematodes parasitic in fish and marine mammals from Boreal and Austral hemispheres. Veterinary Parasitology 148, 43–57.Google Scholar
Mattiucci, S. and Nascetti, G. (2008). Advances and trends in the molecular systematics of Anisakid nematodes, with implications for their evolutionary ecology and host-parasite co-evolutionary processes. Advances in Parasitology 66, 47–148.CrossRefGoogle ScholarPubMed
Mattiucci, S., Nascetti, G., Cianchi, R., Paggi, L., Arduino, P., Margolis, L., Brattey, J., Webb, S. C., D'Amelio, S., Orecchia, P. and Bullini, L. (1997). Genetic and ecological data on the Anisakis simplex complex, with evidence for a new species (Nematoda: Ascaridoidea, Anisakidae). Journal of Parasitology 83, 401–416.Google Scholar
Mattiucci, S., Paggi, L., Nascetti, G., Portes Santos, C., Costa, G., Di Benedetto, A. P., Ramos, R., Argyrou, M., Cianchi, R. and Bullini, L. (2002). Genetic markers in the study of Anisakis typica (Diesing, 1860): larval identification and genetic relationships with other species of Anisakis Dujardin, 1845 (Nematoda: Anisakidae). Systematic Parasitology 51, 159–170.Google Scholar
Mattiucci, S., Abaunza, P., Ramadori, L. and Nascetti, G. (2004). Genetic identification of Anisakis larvae in European hake from Atlantic and Mediterranean waters for stock recognition. Journal of Fish Biology 65, 495–510.Google Scholar
Mattiucci, S., Abaunza, P., Damiano, S., Garcia, A., Santos, M. N. and Nascetti, G. (2007). Distribution of Anisakis larvae, identified by genetic markers, and their use for stock characterization of demersal and pelagic fish from European waters: an update. Journal of Helminthology 81, 117–127.Google Scholar
Mattiucci, S., Farina, V., Campbell, N., Mackenzie, K., Ramos, P., Pinto, A. L., Abaunza, P. and Nascetti, G. (2008). Anisakis spp. larvae (Nematoda: Anisakidae) from Atlantic horse mackerel: their genetic identification and use as biological tags for host stock identification. Fisheries Research 89, 146–151.Google Scholar
Mattiucci, S., Cipriani, P., Webb, S. C., Paoletti, M., Marcer, F., Bellisario, B., Gibson, D. I. and Nascetti, G. (2014 a). Genetic and morphological approaches distinguish the three sibling species of the Anisakis simplex species complex, with a species designation as Anisakis berlandi n. sp. for A. simplex sp. C (Nematoda: Anisakidae). Journal of Parasitology 100, 199–214.Google Scholar
Mattiucci, S., Garcia, A., Cipriani, P., Santos, M. N., Nascetti, G. and Cimmaruta, R. (2014 b). Metazoan parasite infection in the swordfish, Xiphias gladius, from the Mediterranean Sea and comparison with Atlantic populations: implications for its stock characterization. Parasite 21, 35. doi: 10.1051/parasite/2014036.Google Scholar
Milano, I., Babbucci, M., Cariani, A., Atanassova, M., Bekkevold, D., Carvalho, G. R., Espiñeira, M., Fiorentino, F., Garofalo, G., Geffen, A. J., Hansen, J. H., Helyar, S. J., Nielsen, E. E., Ogden, R., Patarnello, T., Stagioni, M., FishPopTrace Consortium, Tinti, F. and Bargelloni, L. (2014). Outlier SNP markers reveal fine-scale genetic structuring across European hake populations (Merluccius merluccius). Molecular Ecology 23, 118–135.Google Scholar
Mladineo, I., Simat, V., Miletic, J., Beck, R. and Poliack, V. (2012). Molecular identification and population dynamics of Anisakis pegreffii (Nematoda: Anisakidae Dujardin, 1845) isolated from the European anchovy (Engraulis encrasicolus L.) in the Adriatic Sea. International Journal of Food Microbiology 157, 224–227.Google Scholar
Murta, A. G., Pinto, A. L. and Abaunza, P. (2008). Stock identification of horse mackerel (Trachurus trachurus) through the analysis of body shape. Fisheries Research 89, 152–158.Google Scholar
Naciri, M., Lemaire, C., Borsa, P. and Bonhomme, F. (1999). Genetic study of the Atlantic/Mediterranean transition in sea bass (Dicentrarchus labrax). Journal of Heredity 90, 591–596.Google Scholar
Nascetti, G., Paggi, L., Orecchia, P., Smith, J. W., Mattiucci, S. and Bullini, L. (1986). Electrophoretic studies on the Anisakis simplex complex (Ascaridida: Anisakidae) from the Mediterranean and North-East Atlantic. International Journal for Parasitology 16, 633–640.Google Scholar
Nascetti, G., Abaunza, P., Mattiucci, S., Magoulas, A., Cimmaruta, R. and Bullini, L. (2000). Genetic Diversity and Parasitic Infections of European Hake (Merluccius merluccius) as Descriptors of Fishing Impact on Mediterranean and Atlantic Stocks. Final Report of the European Project GENHAKE (FAIR CT 97–3494).Google Scholar
Neilson, J., Arocha, F., Cass-Calay, S., Mejuto, J., Ortiz, M., Scott, G., Smith, C., Travassos, P., Tserpes, G. and Andrushchenko, I. (2013). The recovery of Atlantic swordfish: the comparative roles of the regional fisheries management organization and species biology. Reviews in Fisheries Science 21, 59–97.Google Scholar
Notarbartolo di Sciara, G., Agardy, T., Hyrenbach, D., Scovazzi, T. and Van Klaveren, P. (2008). The Pelagos Sanctuary for Mediterranean marine mammals. Aquatic Conservation 18, 367–391.Google Scholar
Palomera, I., Olivar, M. P., Salat, J., Sabates, A., Coll, A., Garcıa, A. and Morales-Nin, B. (2007). Small pelagic fish in the NW Mediterranean Sea: an ecological review. Progress in Oceanography 74, 377–396.Google Scholar
Palumbi, S. R. (1994). Genetic divergence, reproductive isolation and marine speciation. Annual Review in Ecology and Systematics 25, 547–572.Google Scholar
Pannacciulli, F. G., Bishop, J. D. D. and Hawkins, S. J. (1997). Genetic structure of populations of two species of Chthamalus (Crustacea: Cirripedia) in the North-East Atlantic and Mediterranean. Marine Biology 128, 73–82.Google Scholar
Patarnello, T., Volckaert, F. M. J. and Castilho, R. (2007). Pillars of Hercules: is the Atlantic-Mediterranean transition a phylogeographical break? Molecular Ecology 16, 4426–4444.Google Scholar
Peres-Neto, P. R. and Jackson, D. A. (2001). How well do multivariate data sets match? The advantages of a Procrustean superimposition approach over the Mantel test. Oecologia 129, 169–178.Google Scholar
Pla, C., Tudela, S. and Garcia-Marin, J. L. (1996). Diversity and population structure of the European anchovy in the Mediterranean Sea. In The European Anchovy and its Environment (ed. Palomera, I. and Rubies, P.). Sciencia Marina 60, 285–286.Google Scholar
Power, A. M., Balbuena, J. A. and Raga, J. A. (2005). Parasite infracommunities as predictors of harvest location of bogue (Boops boops L.): a pilot study using statistical classifiers. Fisheries Research 72, 229–239.Google Scholar
Pujolar, J. M., Zane, L. and Congiu, L. (2012). Phylogenetic relationships and demographic histories of the Atherinidae in the Eastern Atlantic and Mediterranean Sea re-examined by Bayesian inference. Molecular Phylogenetic and Evolution 63, 857–865.Google Scholar
Quesada, H., Beynon, C. M. and Skibinski, D. O. F. (1995). A mitochondrial DNA discontinuity in the Mussel Mytilus galloprovincialis Lmk: Pleistocene Vicariance Biogeography and secondary Intergradation. Molecular Biology and Evolution 12, 521–524.Google Scholar
Quignard, J. P. (1978). La Méditerranée: creuset ichtyologique. Bollettino di Zoologia 45, 23–36.Google Scholar
R Development Core Team (2012). R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna, Austria.Google Scholar
Rello, F. J., Adroher, F. J., Benitez, R. and Valero, A. (2009). The fishing area as a possible indicator of the infection by anisakids in anchovies (Engraulis encrasicolus) from southwestern Europe. International Journal for food Microbiology 129, 277–281.Google Scholar
Riginos, C., Douglas, K. E., Jin, Y., Shanahan, D. F. and Treml, E. A. (2011). Effects of geography and life history traits on genetic differentiation in benthic marine fishes. Ecography 34, 566–575.Google Scholar
Roldan, M. I., Garcia-Marin, J. L., Utter, F. and Pla, C. (1998). Population genetic structure of European hake, Merluccius merluccius . Heredity 81, 327–334.Google Scholar
Ruggeri, P., Splendiani, A., Bonanomi, S., Arneri, E., Cingolani, N., Santojanni, A., Colella, S., Donato, F., Giovannotti, M., Caputo, V. and Barucchi, N. (2013). Searching for a stock structure in Sardina pilchardus from the Adriatic and Ionian seas using a microsatellite DNA-based approach. Scientia Marina 77, 565–574.Google Scholar
Sà-Pinto, A., Branco, M. S., Alexandrino, P. B., Fontaine, M. C. and Baird, S. J. E. (2012). Barriers to gene flow in the marine environment: insights from two common intertidal limpet species of the Atlantic and Mediterranean. PLOS ONE 7, e50330.Google Scholar
Serracca, L., Cencetti, E., Battistini, R., Rossini, I., Prearo, M., Pavoletti, E., Fioravanti, M. L., Righetti, M., Di Donfrancesco, B. and Ercolini, C. (2013). Survey on the presence of Anisakis and Hysterothylacium larvae from fishes and squids caught in Ligurian Sea. Veterinary Parasitology 196, 547–551.Google Scholar
Smith, B. L. and Alvarado-Bremer, J. R. (2010). Inferring population admixture with multiple nuclear genetic markers and Bayesian genetic clustering in Atlantic swordfish (Xiphias gladius). Collective Volume of Scientific Papers ICCAT 65, 185–190.Google Scholar
Stefanni, S. and Thorley, J. L. (2003). Mitochondrial DNA phylogeography reveals the existence of an evolutionary significant unit of the sand goby Pomatoschistus minutus in the Adriatic (Eastern Mediterranean). Molecular Phylogenetics and Evolution 28, 601–609.Google Scholar
Stransky, C., Murta, A. G., Schlickeisen, J. and Zimmermann, C. (2008). Otolith shape analysis as a tool for stock separation of horse mackerel (Trachurus trachurus) in the Northeast Atlantic and Mediterranean. Fisheries Research 89, 159–168.Google Scholar
Thomas, F., Verneau, O., de Meeûs, T. and Renaud, F. (1996). Parasites as to host evolutionary prints: Insights into host evolution from parasitological data. International Journal for Parasitology 26, 677–686.Google Scholar
Tinti, S., Di Nunno, C., Guarniero, I., Talenti, M., Tommasini, S., Fabbri, E. and Piccinetti, C. (2002). Mitochondrial DNA sequence variation suggests the lack of genetic heterogeneity in the Adriatic and Ionian stocks of Sardina pilchardus . Marine Biotechnology 4, 163–172.Google Scholar
Tintore, J., La Violette, P. E., Blade, I. and Cruzado, G. (1988). A study of an intense density front in the eastern Alboran sea: the Almería-Oran front. Journal of Physical Oceanography 18, 1384–1397.Google Scholar
Tserpes, G. and Tsimenides, N. (1995). Determination of age and growth of swordfish, Xiphias gladius L, 1758, in the Eastern Mediterranean using anal-fin spines. Fishery Bulletin 93, 594–602.Google Scholar
Tserpes, G., Tzanatos, E. and Peristeraki, P. (2011). Use of risk analysis for the evaluation of different management strategies for the Mediterranean swordfish. Collective Volume of Scientific Papers ICCAT 66, 1506–1514.Google Scholar
Tudela, S., Garcia-Marin, J. L. and Pla, C. (1999). Genetic structure of the European anchovy, Engraulis encrasicolus, in the North-West Mediterranean. Journal of Experimental Marine Biology and Ecology 234, 95–109.Google Scholar
Valsecchi, E., Pasolini, P., Bertozzi, M., Garoia, F., Ungaro, N., Vacchi, M., Sabelli, B. and Tinti, F. (2005). Rapid Miocene–Pliocene dispersal and evolution of Mediterranean rajid fauna as inferred by mitochondrial gene variation. Journal of Evolutionary Biology 18, 436–446.Google Scholar
Viñas, J., Pérez-Serra, A., Vidal, O., Alvarado-Bremer, J. R. and Pla, C. (2010). Genetic differentiation between eastern and western Mediterranean swordfish revealed by phylogeographic analysis of the mitochondrial DNA control region. ICES Journal of Marine Science 67, 1222–1229.Google Scholar
Waldman, J. R. (1999). The importance of comparative studies in stock analysis. Fisheries Research 43, 237–246.Google Scholar
Waldman, J. R. (2005). Definition of stocks: an evolving concept. In Stock Identification Methods – Application in Fisheries Science (ed. Cadrin, S. X., Friedland, K. D. and Waldman, J. R.) pp. 7–16. Elsevier Academic Press, Burlington, MA, USA.Google Scholar
Waples, R. S. (1998). Separating the wheat from the chaff: patterns of genetic differentiation in high gene flow species. Journal of Heredity 89, 438–450.Google Scholar
Ward, R. D., Woodwark, M. and Skibinski, D. O. F. (1994). A comparison of genetic diversity levels in marine, freshwater and anadromous fish. Journal of Fish Biology 44, 213–232.Google Scholar
Whiteman, N. K. and Parker, P. G. (2005). Using parasites to infer host population history: a new rationale for parasite conservation. Animal Conservation 8, 175–181.Google Scholar
Zardoya, R., Castilho, R., Grande, C., Favre-Krey, L., Caetano, S., Marcato, S., Krey, G. and Patarnello, T. (2004). Differential population structuring of two closely related fish species, the mackerel (Scomber scombrus) and the chub mackerel (Scomber japonicus), in the Mediterranean Sea. Molecular Ecology 13, 1785–1798.Google Scholar