Academic Scientific JournalsDistinctive morphological variation of saccular otoliths in relation to hermaphroditism type in Sarpa salpa and Serranus scriba (Teleostei: Perciformes) from the Mediterranean Sea in Bizerte, Tunisia
DOI:
https://doi.org/10.26881/oahs-2024.3.05Keywords:
bilateral asymmetry, elliptical Fourier descriptors, protandrous hermaphrodite, sagitta shape and size, synchronous hermaphroditeAbstract
This study aimed to describe and compare the morphological characteristics of saccular otoliths (sagittae) in the protandrous hermaphrodite Sarpa salpa and the synchronous hermaphrodite Serranus scriba collected from the Bizerte site located in northwestern Tunisia, and to examine the effect of hermaphroditism type on the otolith shape and size at the inter- and intraspecific levels, using elliptical Fourier analysis. At the interspecific level, a significant bilateral asymmetry in shape was observed between the left and right otoliths. At the intraspecific level, a significant bilateral asymmetry in shape was detected between the left and right otoliths only in S. scriba. Discriminant function analysis (DFA) produced two separate main groups corresponding to the two species, and intrasexually differentiated between left and right otoliths in S. salpa. In addition, a significant bilateral asymmetry was found in Lo, Wo, Ao, and Po in S. salpa and in Po only in synchronous S. scriba. Thus, protandrous hermaphroditism did not affect otolith shape in S. salpa, but showed an apparent bilateral asymmetry in otolith size. However, synchronous hermaphroditism exhibited a significant bilateral asymmetry in otolith shape and Po only in S. scriba. The causes of this significant inter- and intraspecific bilateral asymmetry observed in otolith shape and size were discussed.
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Abdulsamad, S. M. S. (2017). Comparison of some morphological characteristics of three sparid fishes (Perciformes: Sparidae) otoliths (Sagitta) from Shatt Al-Arab River, Basrah (southern Iraq). Mesopotamia Environmental Journal, 3(4), 33–40.
Allsop, D. J., & West, S. A. (2003). Constant relative age and size at sex change for sequentially hermaphroditic fish. Journal of Evolutionary Biology, 16(5), 921–929. https://doi. org/10.1046/j.1420-9101.2003.00590.x PMID:14635907.
Alós, J., Palmer, M., Balle, S., Grau, A. M., & Morales-Nin, B. (2010). Individual growth pattern and variability in Serranus scriba: A Bayesian analysis. ICES Journal of Marine Science, 67(3), 502–512. https://doi.org/10.1093/icesjms/fsp265.
Al-Rasady, I. H., Jawad, L. A., Al-Mamry, J. M., Al-Mamari, H. M., Al-Yarubi, M. M., & Al-Mamary, D. S. (2010). Fluctuating asymmetry in the otolith length and width of Rhynchorhamphus georgi (Valenciennes, 1846) (Family: Hemiramphidae) collected from the Sea of Oman. Annals de Museo Civico de Saint-Naturale de Ferrara, 13, 85–89.
Bakkari, W., Mejri, M., Ben Mohamed, S., Chalah, A., Quignard, J.-P., & Trabelsi, M. (2020). Shape and symmetry in the otolith of two different species Mullus barbatus and Mullus surmuletus (Actinopterygii: Perciformes: Mullidae) in Tunisian waters. Acta Ichthyologica et Piscatoria, 50(2), 151–159. https://doi.org/10.3750/AIEP/02760.
Bani, A., Poursaeid, S., & Tuset, V. M. (2013). Comparative morphology of the sagittal otolith in three species of south Caspian gobies. Journal of Fish Biology, 82(4), 1321– 1332. https://doi.org/10.1111/jfb.12073 PMID:23557309.
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.
Barhoumi, M., Khoufi, W., Kalai, S., Ouerhani, A., Essayed, S., Zaier, G., Jaziri, H., Ben Meriem, S., & 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(7), 1725– 1732. https://doi.org/10.1017/S0025315417001308.
Bauchot, M. L. (1987). Serranidae. In W. Fischer, M. L. Bauchot, & M. Schneider (Eds.), Fiches FAO d’identification des espèces pour les besoins de la pêche, (Révision 1), Mediterranée et Mer Noire (Zone de Pêche 37) (Vol. 2, pp. 1301–1319). FAO.
Bauchot, M.-L., & Hureau, J.-C. (1990). Sparidae. In J. C. Quero, J. C. Hureau, C. Karrer, A. Post & L Saldanha (Eds.), Checklist of the fishes of the eastern tropical Atlantic (CLOFETA) (Vol. 2, pp. 790–812). UNESCO.
Bellassoued, K., Hamza, A., Abdelmouleh, A., Makni, F. A., Pelt, J. V., & Abdelfattah, E. (2012). Toxicity assessment of dreamfish Sarpa salpa from the Gulf of Gabes (Tunisia, Eastern Mediterranean Sea). Journal of Food, Agriculture and Environment, 10(2), 1308–1313.
Ben Labidi, M., Mejri, M., Shahin, A. A. B., Quignard, J. P., Trabelsi, M., & Ben Faleh, A. R. (2020a). Otolith fluctuating asymmetry in Boops boops (Actinopterygii, Sparidae) from two marine stations (Bizerte and Kelibia) in Tunisian waters. Journal of the Marine Biological Association of the United Kingdom, 100(7), 1135–1146. https://doi.org/10.1017/S0025315420001022.
Ben Labidi, M., Mejri, M., Shahin, A. A. B., Quignard, J. P., Trabelsi, M., & Ben Faleh, A. R. (2020b). Stock discrimination of the bogue Boops boops (Actinopterygii, Sparidae) form two Tunisian Marine Stations using the otolith shape. Acta Ichthyologica et Piscatoria, 50(42), 413–422. https://doi.org/10.3750/AIEP/02978.
Ben Mohamed, S., Mejri, M., Ben Faleh, A., Allaya, H., Jmil, I., Rebaya, M., Chalh, A., Quignard, J. P., & 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, 507–516. https://doi.org/10.21411/CBM.A.873DBD51.
Ben Mohamed, S., Mejri, M., Chalh, A., Shahin, A. A. B., Quignard, J.-P., Trabelsi, M., & Ben Faleh, A. (2023). Distinct inter and intrapopulation variation in the otolith shape and size of Mullus barbatus (Actinopterygii: Mullidae) from the Bizerte and Ghar El Melh lagoons in Tunisian waters. Marine Biology Research, 19(4–5), 234–248. https://doi.org/10.1080/17451000.2023.2203503.
Bianchi, G., Carpenter, K. E., Roux, J.-P., Molloy, F. J., Boyer, D., & Boyer, H. J. (1999). FAO species identification guide for fishery purposes. Field guide to the living marine resources of Namibia. FAO.
Bose, A. P. H., Zimmermann, H., Winkler, G., Kaufmann, A., Strohmeier, T., Koblmüller, S., & Sefc, K. M. (2020). Congruent geographic variation in saccular otolith shape across multiple species of African cichlids. Scientific Reports, 10, 12820. https://doi.org/10.1038/s41598-020-69701-9 PMID:32733082.
Bouderbala, K., Yemmen, C., & Bahri, S. (2019). Biodiversity and ecology of metazoan parasites of Serranus scriba and Serranus cabrilla (Serranidae) from two coastal localities in Tunisia. Cahiers de Biologie Marine, 60, 517–525. https:// doi.org/10.21411/CBM.A.FFADA8CF.
Boukef Ben Omrane, I., Béjaoui, B., Bel Hassan, M., Mraouna, R., Got, P., Harzallah, A., & ELBour, M. (2012). Spatial distribution and decay rates of coliforms in the sediments and water column of the Bizerte lagoon. Life and Environment, 62(1), 29–36.
Box, G. E. P., & Cox, D. R. (1964). An analysis of transformations. Journal of the Royal Statistical Society. Series B, Statistical Methodology, 26(2), 211–243. https://doi. org/10.1111/j.2517-6161.1964.tb00553.x.
Bremm, C. Q., & Schulz, U. H. (2014). Otolith atlas of fish of the Sinos River. Brazilian Journal of Biology, 74(2), 274–282. https://doi.org/10.1590/1519-6984.11612 PMID:25166311.
Butler, E. C., Childs, A.-R., Milner, M. V., Farthing, M. W., Duncan, M. I., Winkler, A. C., & Potts, W. M. (2021). Do contemporary age-growth models overlook life-history complexities in protandrous fishes? A case study on the large protandrous polynemid, the giant African threadfin Polydactylus quadrifilis. Fisheries Research, 233, 105770. https://doi.org/10.1016/j.fishres.2020.105770.
Campana, S. E. (1999). Chemistry and composition of fish otoliths: Pathways, mechanisms and applications. Marine Ecology Progress Series, 188, 263–297. https://doi. org/10.3354/meps188263.
Cañás, L., Stransky, C., Schlickeisen, J., Sampedro, M. P., & Fariña, A. C. (2012). Use of the otolith shape analysis in stock identification of anglerfish (Lophius piscatorius) in the Northeast Atlantic. ICES Journal of Marine Science, 69(2), 250–256. https://doi.org/10.1093/icesjms/fss006.
Capoccioni, F., Costa, C., Aguzzi, J., Menesatti, P., Lombarte, A., & 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(1), 1–7. https://doi.org/10.1016/j.jembe.2010.11.011.
Cardinale, M., Doering-Arjes, P., Kastowsky, M., & 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(2), 158–167. https://doi.org/10.1139/f03-151.
Chang, M. Y., & Geffen, A. J. (2013). Taxonomic and geographic influences on fish otolith microchemistry. Fish and Fisheries, 14(4), 458–492. https://doi.org/10.1111/j.1467- 2979.2012.00482.x.
Chevaldonne, P. (1990). Ciguatera and the saupe, Sarpa salpa (L.), in the Mediterranean: A possible misinterpretation. Journal of Fish Biology, 37(3), 503–504. https://doi. org/10.1111/j.1095-8649.1990.tb05883.x.
Colorni, A., & Diamant, A. (2014). Infectious diseases of warmwater fish in marine and brackish waters. In P. T. K. Woo & D. W. Bruno (Eds.), Diseases and disorders of finfish in cage culture (2nd ed., pp. 155–192). CABI Publishing., https://doi.org/10.1079/9781780642079.0155.
Dehghani, M., Kamrani, E., Salarpouri, A., & Sharifian, S. (2016). Otolith dimensions (length, width), otolith weight and fish length of Sardinella sindensis (Day, 1878), as index for environmental studies, Persian Gulf, Iran. Marine Biodiversity Records, 9, 44–50. https://doi.org/10.1186/s41200-016-0039-0.
Dellali, M., Romeo, M., Gnassia-Barelli, M., & 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, 131–144. https://doi.org/10.1023/B:WATE.0000036801.64830.e9.
Deng, X., Wagner, H.-J., & Popper, A. N. (2013). Interspecific variations of inner ear structure in the deep-sea fish family melamphaidae. Anatomical Record (Hoboken, N.J.), 296(7), 1064–1082. https://doi.org/10.1002/ar.22703 PMID:23625740.
Díaz-Gil, C., Palmer, M., Catalán, I. A., Alós, J., Fuiman, L. A., García, E., del Mar Gil, M., Grau, A., Kang, A., Maneja, R. H., Mohan, J. A., Morro, B., Schaffler, J. J., Buttay, L., Riera-Batle, I., Tolosa, B., & Morales-Nin, B. (2015). Otolith fluctuating asymmetry: A misconception of its biological relevance? ICES Journal of Marine Science, 72(7), 2079–2089. https://doi.org/10.1093/icesjms/fsv067.
Echreshavi, S., Esmaeili, H. R., Teimori, A., & Safaie, M. (2021). Otolith morphology: a hidden tool in the taxonomic study of goatfishes (Teleostei: Perciformes: Mullidae). Zoological Studies (Taipei, Taiwan), 60, e36. https://doi.org/10.6620/ZS.2021.60-36 PMID:34966457.
Elsdon, T. S., Wells, B. K., Campana, S. E., Gillanders, B. M., Jones, C. M., Limburg, K. E., Secor, D. H., Thorrold, S. R., & Walther, B. D. (2008). Otolith chemistry to describe movements and life-history parameters of fishes: Hypotheses, assumptions, limitations and inferences. Oceanography and Marine Biology - an Annual Review, 46, 297–330. https://doi.org/10.1201/9781420065756.ch7.
Fashandi, A., Valinassab, T., Kaymaram, F., & Fatemi, S. M. R. (2019). Morphometric parameters of the sagitta otolith among four carangids species in the Persian Gulf. Iranian Journal of Fisheries Sciences, 18(3), 547–561. https://doi.org/10.22092/ijfs.2018.116983.
Ferri, J., Bartulin, K., & Škeljo, F. (2018). Variability of otolith morphology and morphometry in eight juvenile fish species in the coastal eastern Adriatic. Ribarstvo, 76(3), 91–98. https://doi.org/10.2478/cjf-2018-0012.
Fischer, W., & Petersen, C. W. (1987). The evolution of sexual patterns in the Sea basses. Bioscience, 37(7), 482–490. https://doi.org/10.2307/1310420.
Francis, R. I. C., & Campana, S. E. (2004). Inferring age from otolith measurements: A review and a new approach. Canadian Journal of Fisheries and Aquatic Sciences, 61(7), 1269–1284. https://doi.org/10.1139/f04-063.
Gargouri Ben Abdallah, L., Antar, R., & Maamouri, F. (2011). Diversity of the digenean fauna in sparid fishes from the Lagoon of Bizerte in Tunisia. Acta Parasitologica, 56, 34–39. https://doi.org/10.2478/s11686-011-0007-0.
Gauldie, R. W., & Jones, J. B. (2000). Stocks, or geographically separated populations of the New Zealand orange roughy, Hoplostethus atlanticus, in relation to parasite infestation, growth rate, and otolith shape. Bulletin of Marine Science, 67(3), 949–971.
Gauldie, R. W., & Crampton, J. S. (2002). An ecomorphological explanation of individual variability in the shape of the fish otolith: Comparison of the otolith of Hoplostethus atlanticus with other species by depth. Journal of Fish Biology, 60(5), 1204–1240. https://doi.org/10.1111/j.1095-8649.2002.tb01715.x.
Gonçalves, J. M. S., Bentes, L., Lino, P. G., Ribeiro, J., Canario, A. V. M., & Erzini, K. (1997). Weight-length relationships for selected fish species of the small-scale demersal fisheries of the south and South-West coast of Portugal. Fisheries Research, 30(3), 253–256. https://doi.org/10.1016/S0165-7836(96)00569-3.
Harzallah, A. (2002). Etat actuel et évolution de l’exploitation halieutique des lagunes (Bizerte). Institut National des Sciences et Technologies de la Mer.
Homayuni, H., Marjani, M., & Mousavi-Sabet, H. (2013). Descriptive key to the otoliths of three Sardinella species (Pisces, Clupeidae) from the northern Oman Sea. AACL Bioflux, 6(3): 211–221.
Jadot, C., Ovidio, M., & Voss, J. (2002). Diel activity of Sarpa salpa (Sparidae) by ultrasonic telemetry in a Posidonia oceanica meadow of Corsica (Mediterranean sea). Aquatic Living Resources, 15(6), 343–350. https://doi.org/10.1016/S0990-7440(02)01193-2.
Jadot, C., Donnay, A., Acolas, M., Cornet, Y., & Bégout-Anras, M. (2006). Activity patterns, home-range size, and habitat utilization of Sarpa salpa (Teleostei: Sparidae) in the Mediterranean Sea. ICES Journal of Marine Science, 63(1), 128–139. https://doi.org/10.1016/j.icesjms.2005.06.010.
Jamila, H., Mouldi, B., & Moncef, G. (2016). Assessment of the water quality of Bizerte lagoon of Tunisia by use of statistical analyses. Hydrology: Current Research, 7(2), 237– 245. https://doi.org/10.4172/2157-7587.1000237.
Javor, B., Lo, N., & Vetter, R. (2011). Otolith morphometrics and population structure of Pacific sardine (Sardinops sagax) along the west coast of North America. Fishery Bulletin, 109(4), 402–415.
Jawad, L. A., & Sadighzadeh, Z. (2013). Otolith mass asymmetry in the mugilid fish, Liza klunzingeri (Day, 1888) collected from Persian Gulf near Bandar Abbas. Anales de Biología, 35, 105–107. https://doi.org/10.6018/analesbio.0.35.16.
Jawad, L., Gnohossou, P., & Tossou, G. A. (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, 9–20. https://doi.org/10.6018/analesbio.42.02.
Jawad, L., & Mahé, K. (2022). Fluctuating asymmetry in asteriscii otoliths of common carp (Cyprinus carpio) collected from three localities in Iraqi rivers linked to environmental factors. Fishes, 7(2), 91–102. https://doi.org/10.3390/fishes7020091.
Kaouèche, M., Bahri-Sfar, L., Hammami, I., & Hassine, O. K. B. (2017). Morphometric variations in white seabream Diplodus sargus (Linnaeus, 1758) populations along the Tunisian coast. Oceanologia, 59, 129–138. https://doi.org/10.1016/j.oceano.2016.10.003.
Khedher, M., Mejri, M., Shahin, A. A. B., Quiganrd, J. P., Trabelsi, M., & Ben Faleh, A. (2021). Discrimination of Diplodus vulgaris (Actinopterygii, Sparidae) stock from two Tunisian lagoons using the otolith shape analysis. Journal of the Marine Biological Association of the United Kingdom, 101(4), 743–751. https://doi.org/10.1017/S0025315421000667.
Krysl, P., Hawkins, A. D., Schilt, C., & Cranford, T. W. (2012). Angular oscillation of solid scatterers in response to progressive planar acoustic waves: Do fish otoliths rock? PLoS One, 7(8), e42591. https://doi.org/10.1371/journal.pone.0042591 PMID:22912710.
Lemberget, T., & McCormick, M. I. (2009). Replenishment success linked to fluctuating asymmetry in larval fish. Oecologia, 159(1), 83–93. https://doi.org/10.1007/s00442- 008-1212-x PMID:18982353.
Lord, C., Morat, F., Lecomte-Finiger, R., & Keith, P. (2012). Otolith shape analysis for three Sicyopterus (Teleostei: Gobioidei: Sicydiinae) species from New Caledonia and Vanuatu. Environmental Biology of Fishes, 93, 209–222. https://doi.org/10.1007/s10641-011-9907-y.
Lychakov, D. V., & Rebane, Y. T. (2005). Fish otolith mass asymmetry: Morphometry and influence on acoustic functionality. Hearing Research, 201(1–2), 55–69. https:// doi.org/10.1016/j.heares.2004.08.017 PMID:15721561.
Mahé, K. (2019). Sources de Variation de la Forme des Otolithes: Implications Pour la Discrimination des Stocks de Poissons. Ph.D. Thesis, Université du Littoral Côte d’Opale, Boulogne-sur-mer, France.
Mahé, K., Gourtay, C., Defruit, G., Chantre, C., de Pontual, H., Amara, R., Claireaux, G., Audet, C., Zambonino-Infante, J. L., & Ernande, B. (2019). Do environmental conditions (temperature and food composition) affect otolith shape during fish early-juvenile phase? An experimental approach applied to European Seabass (Dicentrarchus labrax). Journal of Experimental Marine Biology and Ecology, 521, 151239. https://doi.org/10.1016/j.jembe.2019.151239.
Mahé, K., MacKenzie, K., Ider, D., Massaro, A., Hamed, O., Jurado-Ruzafa, A., Gonçalves, P., Anastasopoulou, A., Jadaud, A., Mytilineou, C., Randon, M., Elleboode, R., Morell, A., Ramdane, Z., Smith, J., Bekaert, K., Amara, R., de Pontual, H., & Ernande, B. (2021). Directional bilateral asymmetry in fish otolith: A potential tool to evaluate stock boundaries? Symmetry, 13(6), 987–1000. https://doi.org/10.3390/sym13060987.
Mejri, M., Trojette, M., Ben Alaya, H., Ben Faleh, A., Jmil, I., Chalh, A., Quignard, J. P., & 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(2), 153–161. https://doi.org/10.3750/AIEP/02376.
Mejri, M., Trojette, M., Jmil, I., Ben Faleh, A. R., Chalh, A., Quignard, J. P., & 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, 1–7. https://doi.org/10.21411/CBM.A.4738CCD6.
Mejri, M., Bakkari, W., Tazarki, M., Mili, S., Chalh, A., Shahin, A. A. B., Quignard, J.-P., Trabelsi, M., & Ben Faleh, A. (2022a). Discriminant geographic variation of saccular otolith shape and size in the common Pandora, Pagellus erythrinus (Sparidae) across the Gulf of Gabes, Tunisia. Journal of Ichthyology, 62, 1053–1066. https://doi.org/10.1134/S0032945222060169.
Mejri, M., Bakkari, W., Allagui, F., Rebaya, M., Jmil, I., Mili, S., Shahin, A. A. B., Quignard, J.-P., Trabelsi, M., & Ben Faleh, A. (2022b). Interspecific and intersexual variability of the sagitta otolith shape between Liza aurata and Chelon ramada (Mugiliformes: Mugilidae) inhabiting the Boughrara lagoon, Tunisia. Thalassas: An International Journal of Marine Sciences, 38(2), 1357–1369. https://doi. org/10.1007/s41208-022-00460-2.
Méndez Villamil, M., Lorenzo, J. M., Pajuelo, J. G., Ramos, A., & Coca, J. (2002). Aspects of the history of the salema, Sarpa salpa (Pisces, Sparidae), off the Canarian Arcipelago (centraleast Atlantic). Environmental Biology of Fishes, 63, 183–192. https://doi.org/10.1023/A:1014216000459.
Meynier, L., Stockin, K. A., Bando, M. K. H., & Duignan, P. J. (2008). Stomach contents of common dolphin (Delphinus sp.) from New Zealand waters. New Zealand Journal of Marine and Freshwater Research, 42(2), 257–268. https://doi.org/10.1080/00288330809509952.
Munday, P. L., Hodges, A. L., Choat, J. H., & Gust, N. (2004). Sexspecific growth effects in protogynous hermaphrodites. Canadian Journal of Fisheries and Aquatic Sciences, 61(3), 323–327. https://doi.org/10.1139/f04-057.
Neofitou, N. (2016). Waste feed from fish farms of the Eastern Mediterranean and attraction of wild fish. Universal Journal of Geoscience, 4(5), 112–115. https://doi.org/10.13189/ujg.2016.040503.
Osman, A.G.M., Farrag, M.M., Mehanna, S.F., & Osman, Y.A. (2020). Use of otolithic morphometrics and ultrastructure for comparing between three goatfish species (family: Mullidae) from the northern Red Sea, Hurghada, Egypt. Iranian Journal of Fisheries Sciences, 19(2), 814–832. 10.22092/ijfs.2018.120044.
Paiva, R. B., Neves, A., Vieira, A. R., Sequeira, V., Vendrell, C., Costa, M. J., Peleteiro, M., & Gordo, L. S. (2014). Cystic structures in fish ovaries: More common than we think. The case study of Sarpa salpa (Sparidae). Cybium, 38(2), 158–160. https://doi.org/10.26028/cybium/2014-382-009.
Paiva, R., Neves, A., Sequeira, V., Vieira, A., Costa, M., & Gordo, L. (2018). Age, growth and reproduction of the protandrous hermaphrodite fish, Sarpa salpa, from the Portuguese continental coast. Journal of the Marine Biological Association of the United Kingdom, 98(2), 269–281. https://doi.org/10.1017/S0025315416001405.
Palacios-Fuentes, P., Landaeta, M. F., Muñoz, G., Plaza, G., & Ojeda, F. P. (2012). The effects of a parasitic copepod on the recent larval growth of a fish inhabiting rocky coasts. Parasitology Research, 111(4), 1661–1671. https://doi.org/10.1007/s00436-012-3005-8 PMID:22752746.
Palazzo, Q., Stagioni, M., Raaijmakers, S., Belleman, R. G., Prada, F., Hammel, J. U., Fermani, S., Kaandorp, J., Goffredo, S., & Falini, G. (2022). Multiscale analysis on otolith structural features reveals differences in ontogenesis and sex in Merluccius merluccius in the western Adriatic Sea. Royal Society Open Science, 9(5), 211943. https://doi.org/10.1098/rsos.211943 PMID:35620014.
Palmer, A. R. (1994). Fluctuating asymmetry analysis: a primer. In T. A. Markow (Ed.), Developmental Instability: Its Origins and Evolutionary Implications (pp. 335–364). Kluwer., https://doi.org/10.1007/978-94-011-0830-0_26.
Palmer, A. R., & Strobeck, C. (1986). Fluctuating asymmetry: Measurement, analysis, patterns. Annual Review of Ecology and Systematics, 17, 391–421. https://doi.org/10.1146/ annurev.es.17.110186.002135.
Panfili, J., Durand, J.-D., Diop, K., Gourène, B., & Simier, M. (2005). Fluctuating asymmetry in fish otoliths and heterozygosity in stressful estuarine environments (West Africa). Marine and Freshwater Research, 56(5), 505–516. https://doi.org/10.1071/MF04138.
Papaconstantinou, C., Politou, C. Y., Caragitsou, E., Stergiou, K. I., Mytilineou, E., Vassilopoulou, V., Fourtouni, A., Karkani, M., Kavadas, S., Petrakis, G., Siapatis, A., Chatzinikolaou, P., & Giagnisi, M. (1994). Investigations on the abundance and distribution of demersal stocks of primary importance in the Thermaikos Gulf and the Thracian Sea (Hellas). National Centre for Marine Research, Athens, Hellas, Technical Report, North Aegean Sea Series, 4/1994. (In Hellenic). 365p.
Pashkov, A. N., & Reshetnikov, S. I. (2012). First catch of salema Sarpa salpa (Perciformes, Sparidae) in waters of Russia. Journal of Ichthyology, 52, 566–568. https://doi. org/10.1134/S0032945212050062.
Politou, C. Y., & Papaconstantinou, C. (1995). Age and growth of comber Serranus cabrilla (L. 1785) in the Thracian Sea and the Thennaikos Gulf (Northern Greece). Rapport de la Commission International Mer Méditerranée, 1–34.
Popper, A. N., Ramcharitar, J., & Campana, S. E. (2005). Why otoliths? Insights from inner ear physiology and fisheries biology. Marine and Freshwater Research, 56(5), 497–504. https://doi.org/10.1071/MF04267.
Puentes-Granada, V., Rojas, P., Pavolini, G., Gutiérrez, F. C., & Villa, A. A. (2019). Morphology and morphometric relationships for sagitta otoliths in Lutjanus argentiventris (Pisces: Lutjanidae) and Hyporthodus acanthistius (Pisces: Serranidae) from the Colombian Pacific Ocean. Universitas Scientiarum, 24(2), 337–361. https://doi.org/10.11144/Javeriana.SC24-2.mamr.
Purrafee Dizaj, L., Esmaeili, H. R., & Teimori, A. (2022). Comparative otolith morphology of clupeids from the Iranian brackish and marine resources (Teleostei: Clupeiformes). Acta Zoologica (Stockholm, Sweden), 103(1), 29–47. https://doi.org/10.1111/azo.12353.
Ranaldi, M. M., & Gagnon, M. M. (2008). Zinc incorporation in the otoliths of juvenile pink snapper (Pagrus auratus Forster): The influence of dietary versus waterborne sources. Journal of Experimental Marine Biology and Ecology, 360(1), 56–62. https://doi.org/10.1016/j.jembe.2008.03.013.
Rebaya, M., Ben-Faleh, A., Allaya, H., Khedher, M., Marsaoui, B., Chalh, A., Quignard, J.-P., & Trabelsi, M. (2016). Morphological variability of saccular otoliths in two populations of Liza ramada (Risso, 1810) (Mugilidae) in Tunisian lagoons (Bizerte and Ghar El Melh). Cahiers de Biologie Marine, 57, 227–234.
Reiner, F. (1996). Catálogo dos peixes do arquipélago de Cabo Verde. Publicações avulsas do IPIMAR, no. 2. Instituto Portugues de Investigacao Maritima. 339 p.
Roy, S., & Bardhan, I. (2021). The developmental variations of the sagitta otolith in the young and mature male of a hermaphrodite polynemidae fish, Eleutheronema tetradactylum (Shaw, 1804). Papéis Avulsos de Zoologia, 61, e20216178. https://doi.org/10.11606/1807-0205/2021.61.78.
Russell, B., Pollard, D., Mann, B. Q., Buxton, C. D., & Carpenter, K. E. (2014). Sarpa salpa. The IUCN red list of threatened species. Version 2015.2. Available at http://www. iucnredlist.org (Accessed 26 August 2021).
Santificetur, C., Conversani, V. R. M., Brenha-Nunes, M. R., Giaretta, M. B., Siliprandi, C. C., & Wongtschowski, C. L. D. B. R. (2017). Atlas of marine bony fish otoliths (sagittae) of Southeastern-Southern Brazil Part V: Perciformes (Sparidae, Sciaenidae, Polynemidae, Mullidae, Kyphosidae, Chaetodontidae, Mugilidae, Scaridae, Percophidae, Pinguipedidae, Blenniidae, Gobiidae, Ephippidae, Sphyraenidae, Gempylidae, Trichiuridae, Scombridae, Ariommatidae, Stromateidae, and Caproidae). Brazilian Journal of Oceanography, 65(2), 201–257. https://doi.org/10.1590/s1679-87592017131006502.
Santos, R. S., Azevedo, M. C. C., Albuquerque, C. Q., & Araújo, F. G. (2017). Different sagitta otolith morphotypes for the white mouth croaker Micropogonias furnieri in the Southwestern Atlantic coast. Fisheries Research, 195, 222– 229. https://doi.org/10.1016/j.fishres.2017.07.027.
Schulz-Mirbach, T., Ladich, F., Plath, M., & Heß, M. (2019). Enigmatic ear stones: What we know about the functional role and evolution of fish otoliths. Biological Reviews of the Cambridge Philosophical Society, 94(2), 457–482. https://doi.org/10.1111/brv.12463 PMID:30239135.
Sellami, A., & Bruslé, J. (1975). Contribution à l’étude de la sexualité de la saupe Sarpa salpa Linnaeus, 1758 (téléostéen Sparidae) des côtes de Tunisienne. Vie et Milieu, 25, 261–275.
Simoneau, M., Casselman, J. M., & 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(9), 1597–1603. https://doi.org/10.1139/z00-093.
Stergiou, K. I. (1997). The Hellenic seas: Physics, chemistry, biology, and fisheries. In A. D. Ansell, R. N. Gibson, & M. Barnes (Eds.), Oceanography and Marine Biology: An annual Review 35 (pp. 415–538). UCL Press.
Stergiou, K. I., & Motopoulos, D. K. (2001). A review of lengthweight relationships of fishes from Greek marine waters. Naga. ICLARM Quarterly, 24, 23–39.
Torres, G. J., Lombarte, A., & Morales-Nin, B. (2000). Variability of the sulcus acusticus in the sagitta otolith of the genus Merluccius (Merlucciidae). Fisheries Research, 46(1–3), 5–13. https://doi.org/10.1016/S0165-7836(00)00128-4.
Tortonese, E. (1986). Serranidae. In P. J. P. Whitehead, M.-L. Bauchot, J.-C. Hureau, J. Nielsen, & E. Tortonese (Eds.), Fishes of the north-eastern Atlantic and the Mediterranean (Vol. 2, pp. 780–792). UNESCO.
Trojette, M., Fatnassi, M., Ben Alaya, H., Mahouachi, N., Chalh, A., Quignard, J.-P., & Trabelsi, M. (2014). Applying sagitta otolith shape in the discrimination of fish populations Scorpaena porcus (Linnaeus, 1758) (Scorpaenidae) in the Tunisian coasts. Cahiers de Biologie Marine, 55(4), 499–506.
Trojette, M., Ben-Falah, A., Fatnassi, M., Marsaoui, B., Mahouachi, N., Chalh, A., Quignard, J. P., & 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(4), 363–372. https://doi.org/10.3750/AIP2015.45.4.04.
Tserpes, G., & Tsimenides, N. (2001). Age, growth and mortality of Serranus cabrilla (Linnaeus, 1785) on the Cretan shelf. Fisheries Research, 51(1), 27–34. https://doi.org/10.1016/S0165-7836(00)00237-X.
Turan, C., Oral, M., Öztürk, B., & Düzgüneş, E. (2006). Morphometrics and meristic variation between stocks of bluefish (Pomatomus saltatrix) in the Black, Marmara, Aegean and northeastern Mediterranean Seas. Fisheries Research, 79(1-2), 139–147. https://doi.org/10.1016/j. fishres.2006.01.015.
Tuset, V. M., Lombarte, A., González, J. A., Pertusa, J. F., & Lorente, M. J. (2003). Comparative morphology of the sagittae otolith in Serranus spp. Journal of Fish Biology, 63(6), 1491– 1504. https://doi.org/10.1111/j.1095-8649.2003.00262.x.
Van Valen, L. (1962). A study of fluctuating asymmetry. Evolution; International Journal of Organic Evolution, 16(2), 1–7.
Vaux, F., Rasmuson, L. K., Kautzi, L. A., Rankin, P. S., Blume, M. T. O., Lawrence, K. A., Bohn, S., & O’Malley, K. G. (2019). Sex matters: Otolith shape and genomic variation in deacon rockfish (Sebastes diaconus). Ecology and Evolution, 9(23), 13153–13173. https://doi.org/10.1002/ece3.5763 PMID:31871636.
Vignon, M., & Morat, F. (2010). Environmental and genetic determinant of otolith shape revealed by a non-indigenous tropical fish. Marine Ecology Progress Series, 411, 231–241. https://doi.org/10.3354/meps08651.
Volpedo, A., & Echeverría, D. D. (2003). Ecomorphological patterns of the sagitta in fish on the continental shelf off Argentine. Fisheries Research, 60(2–3), 551–560. https://doi.org/10.1016/S0165-7836(02)00170-4.
Walker, S. P. W., & McCormick, M. I. (2009). Fish ears are sensitive to sex change. Biology Letters, 5(1), 73–76. https://doi.org/10.1098/rsbl.2008.0555 PMID:19033133.
Walt, B. A., & Mann, B. Q. (1998). Aspects of the reproductive biology of Sarpa salpa (Pisces: Sparidae) off the east coast of South Africa. South African Journal of Zoology, 33(4), 241–248. https://doi.org/10.1080/02541858.1998.114484 78.
Yedier, S. (2021). Otolith shape analysis and relationships between total length and otolith dimensions of European barracuda, Sphyraena sphyraena in the Mediterranean Sea. Iranian Journal of Fisheries Sciences, 20(4), 1080–1096. https://doi.org/10.22092/ijfs.2021.124429.
Yedier, S., & Bostanci, D. (2021). Morphologic and morphometric comparisons of sagittal otoliths of five Scorpaena species in the Sea of Marmara, Mediterranean Sea, Aegean Sea and Black Sea. Cahiers de Biologie Marine, 62, 357–369. https://doi.org/10.21411/CBM.A.6B8915B2.
Yedier, S., & Bostanci, D. (2022). Molecular and otolith shape analyses of Scorpaena spp. in the Turkish seas. Turkish Journal of Zoology, 46(1), 78–92. https://doi.org/10.3906/zoo-2105-26.
Zorica, B., Sinovčić, G., Pallaoro, A., & Čikeš Keč, V. (2006). Reproductive biology and length–weight relationship of painted comber, Serranus scriba (Linnaeus, 1758), in the Trogir Bay area (middle-eastern Adriatic). Journal of Applied Ichthyology, 22(4), 260–263. https://doi.org/10.1111/j.1439-0426.2006.00632.x.
Zorica, B., Pallaoro, A., Sinovčić, G., & Keč, V. Č. (2010). Recent data of maximum age and length of painted comber Serranus scriba (Linnaeus, 1758) in Mediterranean Sea. Acta Adriatica, 51(2), 223–226.
