Hostname: page-component-848d4c4894-cjp7w Total loading time: 0 Render date: 2024-06-26T17:32:41.892Z Has data issue: false hasContentIssue false

Discrimination of Diplodus vulgaris (Actinopterygii, Sparidae) stock from two Tunisian lagoons using otolith shape analysis

Published online by Cambridge University Press:  30 September 2021

Maissa Khedher*
Affiliation:
Laboratory of Ecology, Biology and Physiology of Aquatic Organisms (LR/18/ES/41), Faculty of Sciences of Tunis, University of Tunis El Manar, Tunis, Tunisia
Marwa Mejri
Affiliation:
Laboratory of Ecology, Biology and Physiology of Aquatic Organisms (LR/18/ES/41), Faculty of Sciences of Tunis, University of Tunis El Manar, Tunis, Tunisia
Adel A. Basyouny Shahin
Affiliation:
Department of Zoology, Faculty of Science, Minia University, El Minia, Egypt
Jean-Pierre Quiganrd
Affiliation:
Laboratoire d'ichtyologie, Université Montpellier П, P1. E. Bataillon, Case 102, 34095Montpellier, France
Monia Trabelsi
Affiliation:
Laboratory of Ecology, Biology and Physiology of Aquatic Organisms (LR/18/ES/41), Faculty of Sciences of Tunis, University of Tunis El Manar, Tunis, Tunisia
Abderraouf Ben Faleh
Affiliation:
Laboratory of Ecology, Biology and Physiology of Aquatic Organisms (LR/18/ES/41), Faculty of Sciences of Tunis, University of Tunis El Manar, Tunis, Tunisia
*
Author for correspondence: Maissa Khedher, E-mail: khedher.maissa@gmail.com

Abstract

Saccular otolith shape and size were analysed for the first time in 120 adult individuals of D. vulgaris collected from two localities, the Bizerte and Ghar El Melh lagoons (north-east Tunisia). The objectives were (1) to examine the specific inter- and intra-individual variation in the otolith shape using elliptical Fourier analysis combined with measures of length (LO), width (WO) and area (AO); (2) to use the otolith shape and size analysis as a phenotypic-based approach to discriminate the stock structure of this species in the two localities to investigate whether they represent two separate stocks to inform on appropriate management procedures; and (3) to test for biases resulting from potential fluctuating asymmetry (FA) in the otolith size on the discrimination of stock structure. Discriminant function analysis performed with the normalized elliptical Fourier descriptors coefficients showed statistically significant differences (P < 0.0001) in the otolith contour shape, i.e. asymmetry, either between the left and right sides or between the same sides (left-left and right-right) within and among individuals of the two localities. Besides, a significant asymmetry (P < 0.05) was found in WO and AO among individuals within the Bizerte locality and in WO only within the Ghar El Melh locality. Moreover, significant FA was observed in the otolith size parameters among individuals of the two localities. This significant asymmetry detected in the otolith shape, as well as in the size due to FA, within and among individuals of D. vulgaris collected from the Bizerte and Ghar El Melh localities confirms that the two stocks could be discriminated from each other and should be managed separately. This asymmetry is discussed in light of the instability of development caused either by environmental stress associated with the variation in water temperature, salinity, depth, feeding conditions and pollutants that have led to abnormalities in the development of individuals or by the presence of poor living conditions for the larvae resulting from unfavourable environments.

Type
Research Article
Copyright
Copyright © The Author(s), 2021. Published by Cambridge University Press on behalf of Marine Biological Association of the United Kingdom

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

Abaunza, P, Murta, AG, Campbell, N, Cimmaruta, R, Comesaña, AS, Dahle, G, García-Santamaría, MT, Gordo, LS, Iversen, SA, MacKenzie, K, Magoulas, A, Mattiucci, S, Moloy, J, Nascetti, G, Pinto, AL, Quinta, R, Ramos, P, Sanjuan, A, Santos, AT, Stransky, C and Zimmermann, C (2008) 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, 196209.CrossRefGoogle Scholar
Al-Mamry, JM, Jawad, L and Ambuali, A (2011) Fluctuating asymmetry in the otolith length and width of adult Indian mackerel Rastrelliger kanagurta (Cuvier, 1817) collected from Muscat waters at the Sea of Oman. Journal of Black Sea/Mediterranean Environment 17, 254259.Google Scholar
Anonymous (2006) Annuaires statistiques des produits de la pêche en Tunisie. Direction Gênêrale de la pêche et de l'Aquaculture du Ministêre de l'Agriculture á Tunis.Google Scholar
Barhoumi, B (2014) Biosurveillance de la pollution de la lagune de Bizerte (Tunisie) par l'analyse comparée des niveaux de contamination et de l’écotoxicité des sédiments et du biote. Thèse de Doctorat. Université de Bordeaux, France.Google Scholar
Barhoumi, M, Khoufi, W, Kalai, S, Ouerhani, A, Essayed, S, Zaier, G, Jaziri, H, Ben Meriem, S and Fehri-Bedoui, R (2018) The use of Fourier analysis as a tool for Oblada melanura (Linnaeus, 1758) stock unit separation in the south central Mediterranean Sea. Journal of the Marine Biological Association of the United Kingdom 98, 17251732.CrossRefGoogle Scholar
Begg, GA and Brown, RW (2000) Stock identification of haddock Melanogrammus aeglefinus on Georges Bank based on otolith shape analysis. Transactions of the American Fisheries Society 129, 935945.2.3.CO;2>CrossRefGoogle Scholar
Béjaoui, B, Harzallah, A, Moussa, M, Chapelle, A and Solidoro, C (2008) Analysis of hydrobiological pattern in the Bizerte lagoon (Tunisia). Estuarine, Coastal and Shelf Science 80, 121129.CrossRefGoogle Scholar
Béjaoui, B, Ferjani, D, Zaaboub, N, Chapelle, A and Moussa, M (2010) Caractérisation hydrobiologique saisonnière de la lagune de Bizerte (Tunisie). Journal of Water Science 23, 215232.Google Scholar
Ben Labidi, M, Mejri, M, Shahin, AAB, Quignard, JP, Trabelsi, M and Ben Faleh, AR (2020 a) Stock discrimination of the bogue Boops boops (Actinopterygii, Sparidae) form two Tunisian marine lagoons using the otolith shape. Acta Ictyologica et Piscatoria 50, 413422.CrossRefGoogle Scholar
Ben Labidi, M, Mejri, M, Shahin, AAB, Quignard, JP, Trabelsi, M and Ben Faleh, AR (2020 b) Otolith fluctuating asymmetry in Boops boops (Actinopterygii, Sparidae) from two marine lagoons (Bizerte and Kelibia) in Tunisian waters. Journal of the Marine Biological Association of the United Kingdom 100, 11351146.CrossRefGoogle Scholar
Ben Mohamed, S, Mejri, M, Ben Faleh, A, Allaya, H, Jmil, I, Rebaya, M, Chalh, A, Quignard, JP and Trabelsi, M (2019) Otolith shape as a valuable tool to evaluate the stock structure of Mullus barbatus from two Tunisian lagoons (Boughrara and El Biban). Cahiers de Biologie Marine 60, 507516.Google Scholar
Benzinou, A, Carbini, S, Nasreddine, K, Elleboode, R and Mahé, K (2013) Discriminating stocks of striped red mullet (Mullus surmuletus) in the northwest European seas using three automatic shape classification methods. Fisheries Research 143, 153160.CrossRefGoogle Scholar
Berg, F, Almeland, OW, Skadal, J, Slotte, A, Andersson, L and Folkvord, A (2018) Genetic factors have a major effect on growth, number of vertebrae and otolith shape in Atlantic herring (Clupea harengus). PLoS ONE 13, e0190995.CrossRefGoogle Scholar
Boulajfene, W, Strogyloudi, E, Lasram, M, El Mlayah, A, Vassiliki-Angelique, C and Zouari-Tlig, S (2019) Biological and biochemical assessment in Phorcus articulatus (Lamarck 1822): contamination and seasonal effect. Environmental Monitoring and Assessment 191, 555.CrossRefGoogle ScholarPubMed
Box, GEP and Cox, DR (1964) An analysis of transformations. Journal of the Royal Statistical Society, Series B 26, 211252.Google Scholar
Brophy, D, Haynes, P, Arrizabalaga, H, Fraile, I, Fromentin, JM, Garibaldi, F, Katavic, I, Tinti, F, Karakulak, FS, Macías, D, Busawon, D, Hanke, A, Kimoto, A, Sakai, O, Deguara, S, Abid, N and Santos, MN (2016) Otolith shape variation provides a marker of stock origin for North Atlantic bluefin tuna (Thunnus thynnus). Marine and Freshwater Research 67, 10231036.CrossRefGoogle Scholar
Campana, SE (2001) Accuracy, precision and quality control in age determination, including a review of the use and abuse of age validation methods. Journal of Fish Biology 59, 197242.CrossRefGoogle Scholar
Campana, SE and Casselman, JM (1993) Stock discrimination using otolith shape analysis. Canadian Journal of Fisheries and Aquatic Sciences 50, 10621083.CrossRefGoogle Scholar
Campana, SE and Neilson, JD (1985) Microstructure of fish otoliths. Canadian Journal of Fisheries and Aquatic Sciences 42, 10141032.CrossRefGoogle Scholar
Cañás, L, Stransky, C, Schlickeisen, J, Sampedro, MP and Fariña, AC (2012) Use of the otolith shape analysis in stock identification of anglerfish (Lophius piscatorius) in the Northeast Atlantic. ICES Journal of Marine Science 69, 250256.CrossRefGoogle Scholar
Capoccioni, F, Costa, C, Aguzzi, J, Menesatti, P, Lombarte, A and Ciccotti, E (2011) Ontogenetic and environmental effects on otolith shape variability in three Mediterranean European eel (Anguilla anguilla, L.) local stocks. Journal of Experimental Marine Biology and Ecology 397, 17.CrossRefGoogle 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, 158167.CrossRefGoogle Scholar
Casselman, JM, Collins, JJ, Crossman, EJ, Ihssen, PE and Spangler, GR (1981) Lake whitefish (Coregonus clupeaformis) stocks of the Ontario waters of Lake Huron. Canadian Journal of Fisheries and Aquatic Sciences 38, 17721789.CrossRefGoogle Scholar
Chakour, A and Elouizgani, H (2018) The uses of otolith shape in discrimination of the sand sole (Solea lascaris, Risso 1810) population. Journal of Materials and Environmental Sciences 9, 31603166.Google Scholar
Dellali, M, Romeo, M, Gnassia-Barelli, M and Aïssa, P (2004) A multivariate data analysis of the clam Ruditapes decussatus as sentinel organism of the Bizerte lagoon (Tunisia). Water Air and Soil Pollution 156, 131144.CrossRefGoogle Scholar
Dhib, A, Frossard, V, Turki, S and Aleya, L (2013 a) Dynamics of harmful dinoflagellates driven by temperature and salinity in a northeastern Mediterranean lagoon. Environmental Monitoring and Assessment 185, 33693382.CrossRefGoogle Scholar
Dhib, A, Ben Brahim, M, Ziadi, B, Akrout, F, Turki, S and Aleya, L (2013 b) Factors driving the seasonal distribution of planktonic and epiphytic ciliates in a eutrophicated Mediterranean lagoon. Marine Pollution Bulletin 74, 383395.CrossRefGoogle Scholar
Dhib, A, Fertouna-Bellakhal, M, Turki, S and Aleya, L (2015) Harmful planktonic and epiphytic microalgae in a Mediterranean lagoon: the contribution of the macrophyte Ruppia cirrhosa to microalgae dissemination. Harmful Algae 45, 113.CrossRefGoogle Scholar
EL-Maremie, H, Abdalnabi, AS and El-Mor, M (2015) Feeding habits of the common two banded sea bream, Diplodus vulgaris (Geoffroy Saint–Hilaire, 1817) (Teleostei: Sparidae) in Ain El-Ghazala, Eastern Libya. International Journal of Bioassays 4, 39523957.Google Scholar
El-Regal, MA, Jawad, L, Mehanna, S and Ahmad, Y (2016) Fluctuating asymmetry in the otolith of two parrotfish species, Chlorurus sordidus (Forsskål, 1775) and Hipposcarus harid (Forsskål, 1775) from Hurghada, Red Sea coast of Egypt. International Journal of Marine Science 6, 15.Google Scholar
Fernandez-Jover, D and Sanchez-Jerez, P (2015) Comparison of diet and otolith growth of juvenile wild fish communities at fish farms and natural habitats. ICES Journal of Marine Science 72, 916929.CrossRefGoogle Scholar
Ferri, J, Bartulin, K and Škeljo, F (2018) Variability of otolith morphology and morphometry in eight juvenile fish species in the coastal eastern Adriatic. Croatian Journal of Fisheries 76, 9198.CrossRefGoogle Scholar
Geladakis, G, Somarakis, S and Koumoundouros, G (2021) Differences in otolith shape and fluctuating-asymmetry between reared and wild gilthead seabream (Sparus aurata Linnaeus, 1758). Journal of Fish Biology 98, 277286.CrossRefGoogle Scholar
Hadj Taieb, A, Ghorbel, M, Ben Hadj Hamida, N and Jarboui, O (2013) Reproductive biology, age and growth of the two-banded seabream Diplodus vulgaris (Pisces: Sparidae) in the Gulf of Gabes, Tunisia. Journal of the Marine Biological Association of the United Kingdom 93, 14151421.CrossRefGoogle Scholar
Helling, K, Hausmann, S, Clarke, A and Scherer, H (2003) Experimentally induced motion sickness in fish: possible role of the otolith organs. Acta Otolaryngolica 123, 488492.CrossRefGoogle ScholarPubMed
Hüssy, K (2008) Otolith shape in juvenile cod (Gadus morhua): ontogenetic and environmental effects. Journal of Experimental Marine Biology and Ecology 364, 3541.CrossRefGoogle Scholar
Ider, D, Ramdane, Z, Mahe, K, Dufour, JL, Bacha, M and Amara, R (2017) Use of otolith-shape analysis for stock discrimination of Boops boops along the Algerian coast (southwestern Mediterranean Sea). African Journal of Marine Science 39, 251258.CrossRefGoogle Scholar
Jawad, LA and Al-Sadighzadeh, Z (2013) Otolith mass asymmetry in the mugilid fish, Liza klunzingeri (Day, 1888) collected from Persian Gulf near Bandar Abbas. Anales de Biologia 35, 105107.Google Scholar
Jawad, L, Sadighzadeh, Z and Al-Mamary, D (2012 a) Fluctuating asymmetry in the otolith length, width and thickness in two pelagic fish species collected from the Persian Gulf near Bandar Abbas. Annales, Series Historia Naturalis Archives 22, 8388.Google Scholar
Jawad, L, Al-Mamry, J and Al-Mamary, D (2012 b) Fluctuating asymmetry in the otolith dimensions of Lutjanus bengalensis (Lutjanidae) collected from Muscat coast on the sea of Oman. Biological Journal of Armenia 64, 117121.Google Scholar
Jawad, L, Gnohossou, P and Tossou, GA (2020) Bilateral asymmetry in the mass and size of otolith of two cichlid species collected from Lake Ahémé and Porto-Novo Lagoon (Bénin, West Africa). Anales de Biología 42, 920.CrossRefGoogle Scholar
Jmil, I, Ben Faleh, A, Rebaya, M, Allaya, H, Ben Mohamed, S, Trojette, M, Chalh, A, Quignard, JP and Trabelsi, M (2019) Otolith shape analysis as a tool for stock discrimination of Liza aurata from two Tunisian lagoons (Boughrara and El Biban). Cahiers de Biologie Marine 60, 167174.Google Scholar
Kaoueche, M (2019) Parasitological, morphometric and genetic characterization of two Sparidae species: Diplodus sargus and Diplodus vulgaris along Tunisian coasts. Journal of Aquaculture and Marine Biology 8, 114115.CrossRefGoogle Scholar
Kaouèche, M, Bahri-Sfar, L, Hammami, I and Hassine, OKB (2017) Morphometric variations in white seabream Diplodus sargus (Linneus, 1758) populations along the Tunisian coast. Oceanologia 59, 129138.CrossRefGoogle Scholar
Khedher, M and Fatnassi, M (2018) Relationships between fish length otolith size of Diplodus vulgaris from Boughrara and El Bibane lagoons (Southeastern Tunisia). Research and Reviews: Journal of Zoological Sciences 6, 4350.Google Scholar
Khedhri, I, Afli, A and Aleya, L (2017) Structuring factors of the spatio-temporal variability of macrozoobenthos assemblages in a southern Mediterranean lagoon: how useful for bioindication is a multi-biotic indices approach? Marine Pollution Bulletin 114, 515527.CrossRefGoogle Scholar
Khemiri, S, Gaamour, A, Ben Abdallah, L and Fezzani, S (2018) The use of otolith shape to determine stock structure of Engraulis encrasicolus along the Tunisian coast. Hydrobiologia 821, 7382.CrossRefGoogle Scholar
Kontaş, S, Bostanci, D, Yedіer, S, Kurucu, G and Polat, N (2018) Investigation of fluctuating asymmetry in the four otolith characters of Merlangius merlangus collected from Middle Black Sea. Turkish Journal of Maritime and Marine Sciences 4, 128138.Google Scholar
Lombarte, A and Lleonart, J (1993) Otolith size changes related with body growth, habitat depth and temperature. Environmental Biology of Fishes 37, 297306.CrossRefGoogle Scholar
Lord, C, Morat, F, Lecomte-Finiger, R and Keith, P (2012) Otolith shape analysis for three Sicyopterus (Teleostei: Gobioidei: Sicydiinae) species from New Caledonia and Vanuatu. Environmental Biology of Fishes 93, 209222.CrossRefGoogle Scholar
Louiz, I, Kinani, S, Gouze, M-E, Ben-Attia, M, Menif, D, Bouchonnet, S, Porcher, JM, Ben-Hassine, OK and Aït-Aïssa, S (2008) Monitoring of dioxin-like, estrogenic and anti-androgenic activities in sediments of the Bizerte lagoon (Tunisia) by means of in vitro cell-based bioassays: contribution of low concentrations of polynuclear aromatic 329.-hydrocarbons (PAHs). Science of the Total Environment 402, 318329.CrossRefGoogle Scholar
Lychakov, DV and Rebane, YT (2005) Fish otolith mass asymmetry: morphometry and influence on acoustic functionality. Hearing Research 201, 5569.CrossRefGoogle ScholarPubMed
Mahé, K, Evano, H, Mille, T and Bourjea, J (2014) Otolith shape as a valuable tool to evaluate the stock structure of swordfish (Xiphias gladius) in the Indian Ocean. Indian Ocean Tuna Commission WPB 12, 112.Google Scholar
Mahé, K, Ider, D, Massaro, A, Hamed, O, Alba, J, Patricia, G, Aiketerini, A, Angelique, J, Chryssi, M, Romain, E, Zohir, R, Mahmoud, B, Rachid, A, Hélène, DP and Bruno, E (2019) Directional bilateral asymmetry in otolith morphology may affect fish stock discrimination based on otolith shape analysis. ICES Journal of Marine Science 76, 232243.CrossRefGoogle 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, 4352.CrossRefGoogle Scholar
Martin, GB and Wuenschel, MJ (2006) Effect of temperature and salinity on otolith element incorporation in juvenile gray snapper Lutjanus griseus. Marine Ecology Progress Series 324, 229239.CrossRefGoogle Scholar
McCormick, MI, Ryen, CA, Munday, PL and Walker, SPW (2010) Differing mechanisms underlie sexual size-dimorphism in two populations of a sex-changing fish. PLoS ONE 5, e10616.CrossRefGoogle ScholarPubMed
McQuinn, IH (1997) Metapopulations and the Atlantic herring. Reviews in Fish Biology and Fisheries 7, 297329.CrossRefGoogle Scholar
Mejri, M, Trojette, M, Allaya, H, Ben Faleh, AR, Jmil, I, Chalh, A, Quignard, JP and Trabelsi, M (2018) Use of otolith shape to differentiate two lagoon populations of Pagellus erythrinus (Actinopterygii: Perciformes: Sparidae) in Tunisian waters. Acta Ichthyologica et Piscatoria 48, 153161.CrossRefGoogle Scholar
Mejri, M, Trojette, M, Jmil, I, Ben Faleh, AR, Chalh, A, Quignard, JP and Trabelsi, M (2020) Fluctuating asymmetry in the otolith shape, length, width and area of Pagellus erythrinus collected from the Gulf of Tunis. Cahiers de Biologie Marine 61, 17.Google Scholar
Meyer, A (1987) Phenotypic plasticity and heterochrony in Cichlasoma managuense (Pisces, Cichlidae) and their implications for speciation in cichlid fishes. Evolution 41, 13571369.Google ScholarPubMed
Mille, T, Mahé, K, Villanueva, MC, De Pontual, H and Ernande, B (2015) Sagittal otolith morphogenesis asymmetry in marine fishes. Journal of Fish Biology 87, 646663.CrossRefGoogle ScholarPubMed
Mosegaard, H and Madsen, KP (1996) Discrimination of mixed herring stocks in the North Sea using vertebral counts and otolith microstructure. ICES Council Meeting H 17, 18.Google Scholar
Mouine, N, Francour, P, Ktari, MH and Chakroun-Marzouk, N (2012) Reproductive biology of four Diplodus species Diplodus vulgaris, D. annularis, D. sargus sargus and D. puntazzo (Sparidae) in the Gulf of Tunis (central Mediterranean). Tunisia. Journal of the Marine Biological Association of the United Kingdom 92, 623631.CrossRefGoogle Scholar
Palmer, AR and Strobeck, C (1986) Fluctuating asymmetry: measurement, analysis, patterns. Annual Review of Ecology and Systematics 17, 391421.CrossRefGoogle Scholar
Panfili, J, De Pontual, H, Troadec, H and Wright, PJ (2002) Manual of Fish Sclerochronology. Brest: Ifremer-lRD coedition.Google Scholar
Panfili, J, Durand, J-D, Diop, K, Gourene, B and Simier, M (2005) Fluctuating asymmetry in fish otoliths and heterozygosity in stressful estuarine environments (West Africa). Marine and Freshwater Research 56, 505516.CrossRefGoogle Scholar
Parisi-Baradad, V, Lombarte, A, García-Ladona, E, Cabestany, J, Piera, J and Chic, O (2005) Otolith shape contour analysis using affine transformation invariant wavelet transforms and curvature scale representation. Marine and Freshwater Research 56, 795804.CrossRefGoogle Scholar
Ponton, D (2006) Is geometric morphometrics efficient for comparing otolith shape of different fish species? Journal of Morphology 267, 750757.CrossRefGoogle ScholarPubMed
Popper, AN and Lu, Z (2000) Structure-function relationships in fish otolith organs. Fisheries Research 46, 1525.CrossRefGoogle Scholar
Rebaya, M, Ben Faleh, AR, Allaya, H, Kheder, M, Trojette, M, Marsaoui, B, Fatnassi, M, Chalh, A, Quignard, JP and Trabelsi, M (2017) Otolith shape discrimination of Liza ramada (Actinopterygii: Mugiliformes: Mugilidae) from marine and estuarine populations in Tunisia. Acta Ichthyologica et Piscatoria 47, 1321.CrossRefGoogle Scholar
Rodgveller, CJ, Hutchinson, CE, Harris, JP, Vulstek, SC and Guthrie CM, III (2017) Otolith shape variability and associated body growth differences in giant grenadier, Albatrossia pectoralis. PLoS ONE 12, e0180020.CrossRefGoogle ScholarPubMed
Simoneau, M, Casselman, JM and Fortin, R (2000) Determining the effect of negative allometry (length/height relationship) on variation in otolith shape in lake trout (Salvelinus namaycush), using Fourier-series analysis. Canadian Journal of Zoology 78, 15971603.CrossRefGoogle Scholar
Stransky, C (2005) Geographic variation of golden redfish (Sebastes marinus) and deep-sea redfish (S. mentella) in the North Atlantic based on otolith shape analysis. ICES Journal of Marine Science 62, 16911698.CrossRefGoogle Scholar
Stransky, C, Baumann, H, Fevolden, S-E, Harbitz, A, Høie, H, Nedreaas, KH, Salberg, A-B and Skarstein, TH (2008) Separation of Norwegian coastal cod and Northeast Arctic cod by outer otolith shape analysis. Fisheries Research 90, 2635.CrossRefGoogle Scholar
Sunda, WG and Cai, WJ (2012) Eutrophication induced CO2-acidification of subsurface coastal waters: interactive effects of temperature, salinity, and atmospheric PCO2. Environmental Science and Technology 46, 1065110659.CrossRefGoogle Scholar
Trokovic, N, Herczeg, G, Ab Ghani, NI, Shikano, T and Merilä, J (2012) High levels of fluctuating asymmetry in isolated stickleback populations. BMC Evolutionary Biology 12, 115.CrossRefGoogle ScholarPubMed
Tsikliras, AC and Stergiou, KI (2014) Size at maturity of Mediterranean marine fishes. Reviews in Fish Biology and Fisheries 24, 219268.CrossRefGoogle Scholar
Treinen-Crespo, C, Villegas-Hernández, H, Guillén-Hernández, S, Ruiz-Zárate, and González-Salas, C (2012) Otolith shape analysis as a tool for population discrimination of the white grunt (Haemulon plumieri) stock in the northern coast of the Yucatan Peninsula, Mexico. Revista Ciencias Marinas y Costeras 4, 157168.CrossRefGoogle Scholar
Trojette, M, Ben Faleh, AR, Fatnassi, M, Marsaoui, B, Mahouachi, N, Chalh, A, Quignard, J-P and Trabelsi, M (2015) Stock discrimination of two insular populations of Diplodus annularis (Actinopterygii: Perciformes: Sparidae) along the coast of Tunisia by analysis of otolith shape. Acta Ichthyologica et Piscatoria 45, 363372.CrossRefGoogle Scholar
Turan, C (2000) Otolith shape and meristic analysis of herring (Clupea harengus) in the North-East Atlantic. Archive of Fishery and Marine Research 48, 283295.Google Scholar
Tuset, VM, Lozano, IJ, Gonzalez, JA, Pertusa, JF and Garcıa-Dıaz, MM (2003) Shape indices to identify regional differences in otolith morphology of comber, Serranus cabrilla (L., 1758). Journal of Applied Ichthyology 19, 8893.CrossRefGoogle Scholar
Van Valen, L (1962) A study of fluctuating asymmetry. Evolution 16, 17.Google Scholar
Więcaszek, B, Nowosielski, A, Dąbrowski, J, Górecka, K, Keszka, S and Strzelczak, A (2020) Fish size effect on sagittal otolith outer shape variability in round goby Neogobius melanostomus (Pallas 1814). Journal of Fish Biology 97, 15201541.CrossRefGoogle Scholar
Yedier, S, Bostancı, D, Kontaş, S, Kurucu, G and Polat, N (2018 a) Fluctuating asymmetry in otolith dimensions of Trachurus mediterraneus collected from the Middle Black Sea. Acta Biologica Turcica 31, 152159.Google Scholar
Yedier, S, Bostancı, D, Kontaş, S, Kurucu, G and Polat, N (2018 b) Comparison of otolith mass asymmetry in two different Solea solea populations in Mediterranean Sea. Ordu University Journal of Science and Technology 8, 125133.Google Scholar