Population structure of the chub mackerel (Scomber colias) in the North-east Atlantic inferred from otolith shape and body morphometrics
A. A. Muniz A B , A. Moura A , R. Triay-Portella C , C. Moreira A , P. T. Santos A B and A. T. Correia A D EA Centro Interdisciplinar de Investigação Marinha e Ambiental (CIIMAR/CIMAR), Terminal de Cruzeiros do Porto de Leixões, Avenida General Norton de Matos S/N, 4450-208 Matosinhos, Portugal.
B Faculdade de Ciências da Universidade do Porto (FCUP), Rua Campo Alegre S/N, 4169-007 Porto, Portugal.
C Universidad de Las Palmas de Gran Canaria (ULPGC), Calle Juan de Quesada 30, E-35001 Las Palmas de Gran Canaria, Las Palmas, Spain.
D Faculdade de Ciências da Saúde da Universidade Fernando Pessoa (FCS/UFP), Rua Carlos Maia 296, 4200-150 Porto, Portugal.
E Corresponding author. Email: atcorreia.ciimar@gmail.com
Marine and Freshwater Research - https://doi.org/10.1071/MF19389
Submitted: 18 December 2019 Accepted: 15 June 2020 Published online: 13 August 2020
Abstract
The Atlantic chub mackerel (Scomber colias) is an important commercial fish species of the North-east Atlantic. Two-year-old individuals collected between January and April of 2018 at six sampling locations (45 fish per site) of the North-east Atlantic (Azores, Madeira, Canaries and mainland Portugal – Matosinhos, Sesimbra and Portimão) were used for body morphometrics and otolith-shape analyses. Data were analysed by univariate and multivariate statistics. Re-classification success using shape analyses and body morphometrics showed an overall rate of 51 and 74% respectively. Regional differences regarding the otolith-shape analyses suggested a single stock, not necessarily homogenous, with a discrete separation of two main groups (oceanic islands and mainland Portugal). However, body morphometrics showed a more detailed separation in two main groups (Canaries and the others, but with a slight differentiation between fish from Azores-Madeira and mainland Portugal). Moreover, joint analyses gave an overall re-classification success of 82% and allowed a more comprehensive scenario, showing the existence of three main groups (Canaries, Azores-Madeira and mainland Portugal). Regional differences are probably related with different oceanographic conditions influencing the feeding regime and fish growth. The hereby data suggest that S. colias caught in the North-east Atlantic are different population units, and we recommend a fishery management at a finer regional scale.
Additional keywords: fisheries, natural tags, Scombridae, stock delineation.
References
Allaya, H., Hattour, A., Hajjej, G., and Trabelsi, M. (2013). Biologic characteristics of Scomber japonicus (Houttuyn, 1782) in Tunisian waters (central Mediterranean Sea). African Journal of Biotechnology 12, 3040–3048.Allaya, H., Ben Faleh, A., Rebaya, M., Zrelli, S., Hajjej, G., Hattour, A., Quignard, J., and Trabelsi, M. (2016). Identification of Atlantic chub mackerel Scomber colias population through the analysis of body shape in Tunisian waters. Cahiers de Biologie Marine 57, 195–207.
Azevedo, M., Silva, A., Gaspar, M., Silva, C., Murta, A., Moura, T., Santos, M., Stratoudakis, Y., Prista, N., Martins, M., Soares, E., Figueiredo, I., Moreno, A., Pereira, J., Pereira, B., Farias, I., Lagarto, N., and Chaves, C. (2012). ‘Avaliação Inicial do Estado Ambiental das Populações de Peixes e Moluscos Explorados Comercialmente na ZEE Continental Portuguesa: Descritor da Directiva Quadro (DQEM).’ (Instituto Nacional de Recursos Biologicos, I.P., Ministério da Agricultura, Mar, Ambiente e Ordenamento do Território: Lisboa, Portugal.)
Bacha, M., Jemaa, S., Hamitouche, A., Rabhi, K., and Amara, R. (2014). Population structure of the European anchovy, Engraulis encrasicolus, in the SW Mediterranean Sea, and the Atlantic Ocean: evidence from otolith shape analysis. ICES Journal of Marine Science 71, 2429–2435.
| Population structure of the European anchovy, Engraulis encrasicolus, in the SW Mediterranean Sea, and the Atlantic Ocean: evidence from otolith shape analysis.Crossref | GoogleScholarGoogle Scholar |
Burke, N., Brophy, D., and King, P. A. (2008). Shape analysis of otolith annuli in Atlantic herring (Clupea harengus): a new method for tracking fish populations. Fisheries Research 91, 133–143.
| Shape analysis of otolith annuli in Atlantic herring (Clupea harengus): a new method for tracking fish populations.Crossref | GoogleScholarGoogle Scholar |
Cabral, H. N., Marques, J. F., Rego, A. L., Catarino, A. I., Figueiredo, J., and Garcia, J. (2003). Genetic and morphological variation of Synaptura lusitanica Capello, 1868, along the Portuguese coast. Journal of Sea Research 50, 167–175.
| Genetic and morphological variation of Synaptura lusitanica Capello, 1868, along the Portuguese coast.Crossref | GoogleScholarGoogle Scholar |
Caldeira, R. M. A., and Sangrà, P. (2012). Complex geophysical wake flows. Ocean Dynamics 62, 683–700.
| Complex geophysical wake flows.Crossref | GoogleScholarGoogle Scholar |
Caldeira, R. M. A., Groom, S., Miller, P., Pilgrim, D., and Nezlin, N. P. (2002). Sea-surface signatures of the island mass effect phenomena around Madeira Island, Northeast Atlantic. Remote Sensing of Environment 80, 336–360.
| Sea-surface signatures of the island mass effect phenomena around Madeira Island, Northeast Atlantic.Crossref | GoogleScholarGoogle Scholar |
Campana, S. E., and Casselman, J. M. (1993). Stock discrimination using otolith shape analysis. Canadian Journal of Fisheries and Aquatic Sciences 50, 1062–1083.
| Stock discrimination using otolith shape analysis.Crossref | GoogleScholarGoogle Scholar |
Campana, S. E., Chouinard, G. A., Hanson, J. M., Fréchet, A., and Brattey, J. (2000). Otolith elemental fingerprints as biological tracers of fish stocks. Fisheries Research 46, 343–357.
| Otolith elemental fingerprints as biological tracers of fish stocks.Crossref | GoogleScholarGoogle Scholar |
Cardinale, M., Doering-Arjes, P., Kastowsky, M., and Mosegaard, H. (2004). Effects of sex, stock, and environment on the shape of known-age Atlantic cod (Gadus morhua) otoliths. Canadian Journal of Fisheries and Aquatic Sciences 61, 158–167.
| Effects of sex, stock, and environment on the shape of known-age Atlantic cod (Gadus morhua) otoliths.Crossref | GoogleScholarGoogle Scholar |
Carvalho, N., Perrota, R. G., and Isidro, E. J. (2002). Age, growth and maturity in the chub mackerel (Scomber japonicus Houttuyn, 1782) from the Azores. Arquipélago. Ciências Biológicas e Marinhas 19A, 93–99.
Castro, J. J. (1993). Feeding ecology of chub mackerel Scomber japonicus in the Canary Islands area. South African Journal of Marine Science 13, 323–328.
| Feeding ecology of chub mackerel Scomber japonicus in the Canary Islands area.Crossref | GoogleScholarGoogle Scholar |
Castro-Hernández, J. J., and Santana-Ortega, A. T. (2000). ‘Synopsis of Biological Data on the Chub Mackerel (Scomber japonicus, 1782).’ FAO Fisheries Synopsis, no. 157. (FAO: Roma, Italy.)
Catanese, G., Manchado, M., and Infante, C. (2010). Evolutionary relatedness of mackerels of the genus Scomber based on complete mitochondrial genomes: strong support to the recognition of Atlantic Scomber colias and Pacific Scomber japonicus as distinct species. Gene 452, 35–43.
| Evolutionary relatedness of mackerels of the genus Scomber based on complete mitochondrial genomes: strong support to the recognition of Atlantic Scomber colias and Pacific Scomber japonicus as distinct species.Crossref | GoogleScholarGoogle Scholar | 20035845PubMed |
Chlaida, M., Laurent, V., Kifani, S., Benazzou, T., Jaziri, H., and Planes, S. (2009). Evidence of a genetic cline for Sardina pilchardus along the northwest African coast. ICES Journal of Marine Science 66, 264–271.
| Evidence of a genetic cline for Sardina pilchardus along the northwest African coast.Crossref | GoogleScholarGoogle Scholar |
Collette, B. B. (1986). Scombridae. In ‘Fish of the North-eastern Atlantic and the Mediterranean’. (Eds P. J. P. Whitehead, M. L. Bauchot, J. C. Hureau, J. Nielsen, and E. Tortonese.) pp. 981–997. (UNESCO: Paris.)
Collette, B. B., and Nauen, C. E. (1983). ‘Scombrids of the World.’ FAO Fisheries Synopsis, no. 125. (FAO: Rome, Italy.)
DGRM (2018). Recursos da pesca. Série estatística, 30 A-B, version of 2017. Available at www.dgrm.mm.gov.pt [verified 29 August 2018].
Erguden, E., Öztürk, B., Erdogan, Z. A., and Turan, C. (2009). Morphologic structuring between populations of chub mackerel Scomber japonicus in the Black, Marmara, Aegean, and northeastern Mediterranean Seas. Fisheries Science 75, 129–135.
| Morphologic structuring between populations of chub mackerel Scomber japonicus in the Black, Marmara, Aegean, and northeastern Mediterranean Seas.Crossref | GoogleScholarGoogle Scholar |
European Commission (2017). The EU consumer habits. Final report. Directorate-General for Maritime Affairs and Fisheries of the European Commission, Brussels.
Feijó, D., Marçalo, A., Bento, T., Barra, J., Marujo, D., Correia, M., and Silva, P. (2018). Trends in the activity pattern, fishing yields, catch and landing composition between 2009 and 2013 from onboard observations in the Portuguese purse seine fleet. Regional Studies in Marine Science 23, 97–106.
| Trends in the activity pattern, fishing yields, catch and landing composition between 2009 and 2013 from onboard observations in the Portuguese purse seine fleet.Crossref | GoogleScholarGoogle Scholar |
Ferguson, G. J., Ward, T. M., and Gillanders, B. M. (2011). Otolith shape and elemental composition: complementary tools for stock discrimination of mulloway (Argyrosomus japonicus) in southern Australia. Fisheries Research 110, 75–83.
| Otolith shape and elemental composition: complementary tools for stock discrimination of mulloway (Argyrosomus japonicus) in southern Australia.Crossref | GoogleScholarGoogle Scholar |
Gamito, R., Teixeira, M. C., Costa, M. J., and Cabral, H. N. (2015). Are the regional fisheries’ catches changing with climate? Fisheries Research 161, 207–216.
| Are the regional fisheries’ catches changing with climate?Crossref | GoogleScholarGoogle Scholar |
Hernández-Guerra, A., Machín, F., Antoranz, A., Cisneros-Aguirre, J., Gordo, C., Marrero-Díaz, A., Martínez, A., Ratsimandresy, A. W., Rodríguez-Santana, A., Sangrá, P., López-Laazen, F., Parrilla, G., and Pelegrí, J. L. (2002). Temporal variability of mass transport in the Canary Current. Deep-sea Research Part II: Topical Studies in Oceanography 49, 3415–3426.
| Temporal variability of mass transport in the Canary Current.Crossref | GoogleScholarGoogle Scholar |
Hernández-León, S., Gómez, M., and Arístegui, J. (2007). Mesozooplankton in the Canary Current System: the coastal–ocean transition zone. Progress in Oceanography 74, 397–421.
| Mesozooplankton in the Canary Current System: the coastal–ocean transition zone.Crossref | GoogleScholarGoogle Scholar |
Hoff, N. T., Dias, J. F., Zani-Teixeira, M. L., and Correia, A. T. (2020). Spatio-temporal evaluation of the population structure of the bigtooth corvina Isopisthus parvipinnis from Southwest Atlantic Ocean using otolith shape signatures. Journal of Applied Ichthyology , .
| Spatio-temporal evaluation of the population structure of the bigtooth corvina Isopisthus parvipinnis from Southwest Atlantic Ocean using otolith shape signatures.Crossref | GoogleScholarGoogle Scholar |
ICES (2015). Report of the workshop on age reading of chub mackerel (Scomber colias) (WKARCM), Lisbon, 2–6 November 2015. ICES CM 2015\SSGEIOM:11. International Council for the Exploration of the Sea, Denmark.
Infante, C., Blanco, E., Zuasti, E., Crespo, A., and Manchado, M. (2007). Phylogenetic differentiation between Atlantic Scomber colias and Pacific Scomber japonicus based on nuclear DNA sequences. Genetica 130, 1–8.
| Phylogenetic differentiation between Atlantic Scomber colias and Pacific Scomber japonicus based on nuclear DNA sequences.Crossref | GoogleScholarGoogle Scholar | 16897460PubMed |
IUCN (2011). Scomber colias, IUCN red list of threatened species. Available at www.iucn.org [verified 29 August 2018].
Iwata, H., and Ukai, Y. (2002). SHAPE: um pacote de programa de computador para avaliação quantitativa de formas biológicas baseada em descritores de Fourier elípticos. The Journal of Heredity 93, 384–385.
| SHAPE: um pacote de programa de computador para avaliação quantitativa de formas biológicas baseada em descritores de Fourier elípticos.Crossref | GoogleScholarGoogle Scholar | 12547931PubMed |
Jemaa, S., Bacha, M., Khalaf, G., Dessailly, D., Rabhi, K., and Amara, R. (2015). What can otolith shape analysis tell us about population structure of the European sardine, Sardina pilchardus, from Atlantic and Mediterranean waters? Journal of Sea Research 96, 11–17.
| What can otolith shape analysis tell us about population structure of the European sardine, Sardina pilchardus, from Atlantic and Mediterranean waters?Crossref | GoogleScholarGoogle Scholar |
Kaouèche, M., Bahri-Sfar, L., Hammami, I., and Ben Hassine, O. K. (2017). Morphometric variantions in white seabream Diplodus sargus (Linneus, 1758) populations along the Tunisian coast. Oceanologia 59, 129–138.
| Morphometric variantions in white seabream Diplodus sargus (Linneus, 1758) populations along the Tunisian coast.Crossref | GoogleScholarGoogle Scholar |
Kasapidis, P., Silva, A., Zampicinini, G., and Magoulas, A. (2012). Evidence for microsatellite hitchhiking selection in European sardine (Sardina pilchardus) and implications in inferring stock structure. Scientia Marina 76, 123–132.
| Evidence for microsatellite hitchhiking selection in European sardine (Sardina pilchardus) and implications in inferring stock structure.Crossref | GoogleScholarGoogle Scholar |
Kritzer, J. P., and Liu, O. R. (2013). Fishery management strategies for addressing complex spatial structure in marine fish stocks. In ‘Stock Identification Methods: Applications in Fisheries Science’. 2nd Edn. (Ed. S. X. Cadrin.) pp. 29–57. (Academic Press: USA.)
Kuhl, F. P., and Giardina, C. R. (1982). Elliptic Fourier features of a closed contour. Computer Graphics and Image Processing 18, 236–258.
| Elliptic Fourier features of a closed contour.Crossref | GoogleScholarGoogle Scholar |
Mapp, J., Hunter, E., Van Der Kooijc, J., Songer, S., and Fisher, M. (2017). Otolith shape and size: the importance of age when determining indices for fish-stock separation. Fisheries Research 190, 43–52.
| Otolith shape and size: the importance of age when determining indices for fish-stock separation.Crossref | GoogleScholarGoogle Scholar |
Martins, M. M. (2007). Growth variability in Atlantic mackerel (Scomber scombrus) and Spanish mackerel (Scomber japonicus) off Portugal. ICES Journal of Marine Science 64, 1785–1790.
| Growth variability in Atlantic mackerel (Scomber scombrus) and Spanish mackerel (Scomber japonicus) off Portugal.Crossref | GoogleScholarGoogle Scholar |
Martins, M. M., Skagen, D., Marques, V., Zwolinski, J., and Silva, A. (2013). Changes in the abundance and spatial distribution of the Atlantic chub mackerel (Scomber colias) in the pelagic ecosystem and fisheries off Portugal. Scientia Marina 77, 551–563.
| Changes in the abundance and spatial distribution of the Atlantic chub mackerel (Scomber colias) in the pelagic ecosystem and fisheries off Portugal.Crossref | GoogleScholarGoogle Scholar |
Mille, T., Ernande, B., Pontual, H., Villanueva, C., and Mahé, K. (2016). ‘Sources of Otolith Morphology Variation at the Intra-population Level: Directional Asymmetry and Diet.’ (SFI Days: Marseille, France.)
Moreira, C., Froufe, E., Sial, A. N., Caeiro, A., Vaz-Pires, P., and Correia, A. T. (2018). Population structure of the blue jack mackerel (Trachurus picturatus) in the NE Atlantic inferred from otolith microchemistry. Fisheries Research 197, 113–122.
| Population structure of the blue jack mackerel (Trachurus picturatus) in the NE Atlantic inferred from otolith microchemistry.Crossref | GoogleScholarGoogle Scholar |
Moreira, C., Froufe, E., Vaz-Pires, P., and Correia, A. T. (2019a). Otolith shape analysis as a tool to infer the population structure of the blue jack mackerel, Trachurus picturatus, in the NE Atlantic. Fisheries Research 209, 40–48.
| Otolith shape analysis as a tool to infer the population structure of the blue jack mackerel, Trachurus picturatus, in the NE Atlantic.Crossref | GoogleScholarGoogle Scholar |
Moreira, C., Correia, A. T., Vaz-Pires, P., and Froufe, E. (2019b). Genetic diversity and population structure of the blue jack mackerel Trachurus picturatus across its western distribution. Journal of Fish Biology 94, 725–731.
| Genetic diversity and population structure of the blue jack mackerel Trachurus picturatus across its western distribution.Crossref | GoogleScholarGoogle Scholar | 30895622PubMed |
Nespereira, J. M. L., and Pajuelo, J. M. G. (1993). Determinación de la talla de primera madurez sexual y período reproductivo de la caballa (Scomber japonicus Houttuyn, 1782) de las islas Canarias. Boletín del Instituto Español de Oceanografía 9, 15–21.
Panfili, J., Pontual, H., Troadec, H., and Wright, P. (2002). ‘Manual of Sclerochronoly.’ (IFREMER-IRD Coedition: Brest, France.)
Perrotta, R. G., Madirolas, A., Viñas, M. D., Akselman, R., Guerrero, R., Sánchez, F., López, F., Castro Machado, F., and Macchi, G. (1999). La caballa (Scomber japonicus) y las condiciones ambientales en el área bonaerense de ‘El Rincón’. INIDEP Inf Téc. 26, 1–29.
Reist, J. D. (1985). An empirical evaluation of several univariate methods that adjust for size variation in morphometric data. Canadian Journal of Zoology 63, 1429–1439.
| An empirical evaluation of several univariate methods that adjust for size variation in morphometric data.Crossref | GoogleScholarGoogle Scholar |
Rodgveller, C. J., Hutchinson, C. E., Harris, J. P., Vulstek, S. C., and Guthrie, C. M. (2017). Otolith shape variability and associated body growth differences in giant grenadier, Albatrossia pectoralis. PLoS One 12, e0180020.
| Otolith shape variability and associated body growth differences in giant grenadier, Albatrossia pectoralis.Crossref | GoogleScholarGoogle Scholar | 28658326PubMed |
Rohlf, F. J., and Slice, D. (1990). Extensions of the Procrustes method for the optimal superimposition of landmarks. Systematic Zoology 39, 40–59.
| Extensions of the Procrustes method for the optimal superimposition of landmarks.Crossref | GoogleScholarGoogle Scholar |
Roldán, M. I., Perrotta, R. G., Cortey, M., and Pla, C. (2000). Molecular and morphologic approaches to discrimination of variability patterns in chub mackerel, Scomber japonicus. Journal of Experimental Marine Biology and Ecology 253, 63–74.
| Molecular and morphologic approaches to discrimination of variability patterns in chub mackerel, Scomber japonicus.Crossref | GoogleScholarGoogle Scholar | 11018237PubMed |
Santos, A. M. P., Chícharo, A., Santos, A., Moita, T., Oliveira, P. B., Peliz, A., and Ré, P. (2007). Physical-biological interactions in the life history of small pelagic fish in the western Iberia upwelling ecosystem. Progress in Oceanography 74, 192–209.
| Physical-biological interactions in the life history of small pelagic fish in the western Iberia upwelling ecosystem.Crossref | GoogleScholarGoogle Scholar |
Scoles, D. R., Collette, B. C., and Graves, J. E. (1998). Global phylogeography of mackerels of the genus Scomber. Fish Bulletin 96, 823–842.
Secor, D. H., Dean, J. M., and Laban, E. H. (1992). Otolith removal and preparation for microstructural examination. In ‘Otolith Microstructure Examination and Analysis’. Canadian Special Publication of Fisheries and Aquatic Sciences 117. (Eds D. K. Stevenson and S. E. Campana.) pp. 19–57. (Communication Group - Publishing: Ottawa, Canada.)
Strauss, R. E., and Bookstein, F. L. (1982). The truss: body form reconstruction in morphometrics. Systematic Zoology 31, 113–135.
| The truss: body form reconstruction in morphometrics.Crossref | GoogleScholarGoogle Scholar |
Tuset, V. M., Lozano, I. J., Gonzalez, J. A., Pertusa, J. F., and Garcia-Diaz, M. M. (2003). Shape indices to identify regional differences in otolith morphology of comber Serranus cabrilla (L., 1758). Journal of Applied Ichthyology 19, 88–93.
| Shape indices to identify regional differences in otolith morphology of comber Serranus cabrilla (L., 1758).Crossref | GoogleScholarGoogle Scholar |
Vasconcelos, J., Afonso-Dias, M., and Faria, G. (2012). Atlantic chub mackerel (Scomber colias) spawning season, size and age at first maturity in Madeira waters. Arquipélago. Ciências Biológicas e Marinhas 29, 43–51.
Vasconcelos, J., Vieira, A. R., Sequeira, V., González, J. A., Kaufmann, M., and Gordo, L. S. (2018). Identifying populations of the blue jack mackerel (Trachurus picturatus) in the Northeast Atlantic by using geometric morphometrics and otolith shape analysis. Fishery Bulletin 116, 81–92.
| Identifying populations of the blue jack mackerel (Trachurus picturatus) in the Northeast Atlantic by using geometric morphometrics and otolith shape analysis.Crossref | GoogleScholarGoogle Scholar |
Vergara-Solana, F. J., García-Rodríguez, F. J., and Cruz-Agüero, D. L. (2013). Comparing body and otolith shape for stock discrimination of Pacific sardine, Sardinops sagax Jenyns, 1842. Journal of Applied Ichthyology 29, 1241–1246.
| Comparing body and otolith shape for stock discrimination of Pacific sardine, Sardinops sagax Jenyns, 1842.Crossref | GoogleScholarGoogle Scholar |
Vignon, M., and Morat, F. (2010). Environmental and genetic determinant of otolith shape revealed by non-indigenous tropical fish. Marine Ecology Progress Series 411, 231–241.
| Environmental and genetic determinant of otolith shape revealed by non-indigenous tropical fish.Crossref | GoogleScholarGoogle Scholar |
Villamor, B., Carrera, P., Castro, J., Ramos, F., Velasco, F., Sobrino, I., Navarro, M. R., Gancedo, R., Hernandez, C., Marín, M., Blanco, M., Tornero, J., and Burgos, C. (2017). ‘The Chub Mackerel (Scomber colias) in the Atlantic Spanish Waters (ICES Divisions 8.c and 9.a): Biological, Fishery and Survey Data.’ Working Document to WGWIDE. (Instituto Español de Oceanografia.)
Volpedo, A. V., and Vaz-dos-Santos, A. M. (2015). ‘Métodos de Estudios con Otolitos: Principios y Aplicaciones/Métodos de Estudos con Otólitos: Princípios e Aplicações.’ 1st edn. edición bilingue. (Ciudad Autónoma de Buenos Aires: Argentina.) [in Spanish]
Zardoya, R., Castilho, R., Grande, C., Favre-Krey, L., Caetano, S., Marcato, S., Krey, G., and Paternello, 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.
| Differential population structuring of two closely related fish species, the mackerel (Scomber scombrus) and the chub mackerel (Scomber japonicus), in the Mediterranean Sea.Crossref | GoogleScholarGoogle Scholar | 15189203PubMed |