Intra- and interspecific variability among congeneric Pagellus otoliths.
Journal
Scientific reports
ISSN: 2045-2322
Titre abrégé: Sci Rep
Pays: England
ID NLM: 101563288
Informations de publication
Date de publication:
11 08 2021
11 08 2021
Historique:
received:
07
05
2021
accepted:
29
07
2021
entrez:
12
8
2021
pubmed:
13
8
2021
medline:
13
8
2021
Statut:
epublish
Résumé
Otolith features are useful tools for studying taxonomy, ecology, paleontology, and fish biology since they represent a permanent record of life history. Nevertheless, the functional morphology of otoliths remains an open research question that is useful to completely understand their eco-morphology. This study aims to deepen the knowledge of intra- and interspecific variation in sagitta morphology in three congeneric seabreams, to understand how such variability could be related to the lifestyles of each species. Therefore, the sagittae (n = 161) of 24 Pagellus bogaraveo, 24 Pagellus acarne, and 37 Pagellus erythrinus specimens, collected from the south Tyrrhenian Sea, were analyzed using scanning electron microscopy and a stereomicroscope to assess morphometric features, variability between otolith pairs and the external crystalline structure the of sulcus acusticus. Statistical analysis demonstrated that, between the species, variability in sagittal otolith rostral length growth and sulcus acusticus features, correlated with increased fish total length and body weight. Moreover, slight differences between otolith pairs were detected in P. acarne and P. erythrinus (P < 0.05). The results confirm changes in otolith morphometry and morphology between different congeneric species and populations of the same species from different habitats.
Identifiants
pubmed: 34381131
doi: 10.1038/s41598-021-95814-w
pii: 10.1038/s41598-021-95814-w
pmc: PMC8357811
doi:
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
16315Informations de copyright
© 2021. The Author(s).
Références
Tuset, V. M., Lombarte, A. & Assis, C. A. Otolith atlas for the western Mediterranean, north and central eastern Atlantic. Sci. Mar. 72, 7–198 (2008).
doi: 10.3989/scimar.2008.72s1199
Schulz-Mirbach, T., Ladich, F., Plath, M. & Heß, M. Enigmatic ear stones: What we know about the functional role and evolution of fish otoliths. Biol. Rev. 94, 457–482 (2019).
pubmed: 30239135
doi: 10.1111/brv.12463
Cermeño, P., Morales-Nin, B. & Uriarte, A. Juvenile European anchovy otolith microstructure. Sci. Mar. 70, 553–557 (2006).
doi: 10.3989/scimar.2006.70n3553
Chaine, J. & Duvergier, J. Recherches sur les otolithes des poisons. Etude déscriptive et comparative de la sagitta des téléostéens. Act Soc Linn 86, 1–254 (1934).
Chaine, J. & Duvergier, J. Recherches sur les otolithes des poisons. Etude déscriptive et comparative de la sagitta des téléostéens. Act Soc Linn 92, 3–133 (1942).
Nolf, D. Otolithi Piscium. Handbook of Paleoichthyology, Vol. 10. (1985).
Volpedo, A. & Echeverría, D. D. Catálogo y claves de otolitos para la identificación de peces del mar Argentino. (2000).
Tuset, V. M. et al. Testing otolith morphology for measuring marine fish biodiversity. Mar. Freshw. Res. 67, 1037–1048 (2016).
doi: 10.1071/MF15052
Nolf, D., de Potter, H. & Lafond-Grellety, J. Hommage à Joseph Chaine et Jean Duvergier: Diversité et variabilité des otolithes des poissons. Palaeo Publishing and Library vzw. (Palaeo Publishing and Library vzw, 2009).
Chaine, J. Recherches sur les otolithes des poisons. Étude descriptive et comparative de la sagitta des Téléostéens. Actes Soc. Linn. Bord 89, 5–252 (1937).
Volpedo, A. & DianaEcheverría, D. Ecomorphological patterns of the sagitta in fish on the continental shelf off Argentine. Fish. Res. 60, 551–560 (2003).
doi: 10.1016/S0165-7836(02)00170-4
Amorim, M. C. P., Stratoudakis, Y. & Hawkins, A. D. Sound production during competitive feeding in the grey gurnard. J. Fish Biol. 65, 182–194 (2004).
doi: 10.1111/j.0022-1112.2004.00443.x
Cardinale, M., Doering-Arjes, P., Kastowsky, M. & Mosegaard, H. Effects of sex, stock, and environment on the shape of known-age Atlantic cod (Gadus morhua) otoliths. Can. J. Fish. Aquat. Sci. 61, 158–167 (2004).
doi: 10.1139/f03-151
Capoccioni, F. et al. Ontogenetic and environmental effects on otolith shape variability in three Mediterranean European eel (Anguilla anguilla, L.) local stocks. J. Exp. Mar. Biol. Ecol. 397, 1–7 (2011).
doi: 10.1016/j.jembe.2010.11.011
Lombarte, A. & Cruz, A. Otolith size trends in marine fish communities from different depth strata. J. Fish Biol. 71, 53–76 (2007).
doi: 10.1111/j.1095-8649.2007.01465.x
Torres, G. J., Lombarte, A. & Morales-Nin, B. Sagittal otolith size and shape variability to identify geographical intraspecific differences in three species of the genus Merluccius. J. Mar. Biol. Assoc. U. K. 80, 333–342 (2000).
doi: 10.1017/S0025315499001915
Mahé, K., Evano, H., Mille, T., Muths, D. & Bourjea, J. Otolith shape as a valuable tool to evaluate the stock structure of swordfish Xiphias gladius in the Indian Ocean. Afr. J. Mar. Sci. 38, 457–464 (2016).
doi: 10.2989/1814232X.2016.1224205
Morat, F., Letourneur, Y., Nérini, D., Banaru, D. & Batjakas, I. E. Discrimination of red mullet populations (Teleostean, Mullidae) along multi-spatial and ontogenetic scales within the Mediterranean basin on the basis of otolith shape analysis. Aquat. Living Resour. 25, 27–39 (2012).
doi: 10.1051/alr/2011151
Truman, C. N., Chung, M. T. & Shores, D. Ecogeochemistry potential in deep time biodiversity illustrated using a modern deep-water case study. Philos. Trans. R. Soc. B Biol. Sci. 371, 20150223 (2016).
doi: 10.1098/rstb.2015.0223
Lombarte, A. & Tuset, V. M. Chapter3- Morfometría de otolitos. in Métodos de estudios con otolitos: principios y aplicaciones/ Métodos de estudos com otólitos: princípios e aplicações (eds. Volpedo, A. V. & Vaz-dos-Santos, A. M.) 31 (2015).
Murta, A. G. Morphological variation of horse mackerel (Trachurus trachurus) in the Iberian and North African Atlantic: Implications for stock identification. ICES J. Mar. Sci. 57, 1240–1248 (2000).
doi: 10.1006/jmsc.2000.0810
Bolles, K. L. & Begg, G. A. Distinction between silver hake (Merluccius bilinearis) stocks in U.S. waters of the northwest Atlantic based on whole otolith morphometrics. Fish. Bull. 98, 451–462 (2000).
Montanini, S., Stagioni, M., Valdrè, G., Tommasini, S. & Vallisneri, M. Intra-specific and inter-specific variability of the sulcus acusticus of sagittal otoliths in two gurnard species (Scorpaeniformes, Triglidae). Fish. Res. 161, 93–101 (2015).
doi: 10.1016/j.fishres.2014.07.003
Spedicato, M. T. et al. Geographical distribution, abundance and some population characteristics of the species of the genus Pagellus (Osteichthyes: Perciformes) in different areas of the Mediterranean. Sci. Mar. 66, 65–82 (2002).
doi: 10.3989/scimar.2002.66s265
Di Maio, F. et al. Age structure of spawners of the axillary seabream, Pagellus acarne (Risso, 1827), in the central Mediterranean Sea (Strait of Sicily). Reg. Stud. Mar. Sci. 34, 101082 (2020).
İlhan, D. Age, growth, and diet of axillary seabream, Pagellus Acarne (Actinopterygii: Perciformes: Sparidae), in the central Aegean sea. Acta Ichthyol. Piscat. 48, 329–339 (2018).
doi: 10.3750/AIEP/02454
Morato, T., Solà, E., Grós, M. P. & Menezes, G. Feeding habits of two congener species of seabreams, Pagellus bogaraveo and Pagellus acarne, off the Azores (northeastern Atlantic) during spring of 1996 and 1997. Bull. Mar. Sci. https://doi.org/10.1016/j.yhbeh.2011.02.016 (2001).
doi: 10.1016/j.yhbeh.2011.02.016
Busalacchi, B., Bottari, T., Giordano, D., Profeta, A. & Rinelli, P. Distribution and biological features of the common pandora, Pagellus erythrinus (Linnaeus, 1758), in the southern Tyrrhenian Sea (Central Mediterranean). Helgol. Mar. Res. 68, 491–501 (2014).
doi: 10.1007/s10152-014-0404-5
Fanelli, E. et al. Food partitioning and diet temporal variation in two coexisting sparids, Pagellus erythrinus and Pagellus acarne. J. Fish Biol. 78, 869–900 (2011).
pubmed: 21366579
doi: 10.1111/j.1095-8649.2011.02915.x
Savoca, S. et al. Microplastics occurrence in the Tyrrhenian waters and in the gastrointestinal tract of two congener species of seabreams. Environ. Toxicol. Pharmacol. 67, 35–41 (2019).
pubmed: 30711873
doi: 10.1016/j.etap.2019.01.011
Lorance, P. History and dynamics of the overexploitation of the blackspot sea bream (Pagellus bogaraveo) in the Bay of Biscay. ICES J. Mar. Sci. 68, 290–301 (2011).
doi: 10.1093/icesjms/fsq072
Jawad, L. A., Sabatino, G., Ibáñez, A. L., Andaloro, F. & Battaglia, P. Morphology and ontogenetic changes in otoliths of the mesopelagic fishes Ceratoscopelus maderensis (Myctophidae), Vinciguerria attenuata and V. poweriae (Phosichthyidae) from the Strait of Messina (Mediterranean Sea). Acta Zool. https://doi.org/10.1111/azo.12197 (2018).
doi: 10.1111/azo.12197
Swan, S. C. et al. Otolith chemistry: An aid to stock separation of Helicolenus dactylopterus (bluemouth) and Merluccius merluccius (European hake) in the Northeast Atlantic and Mediterranean. ICES J. Mar. Sci. 63, 504–513 (2006).
doi: 10.1016/j.icesjms.2005.08.012
Vignon, M. & Morat, F. Environmental and genetic determinant of otolith shape revealed by a non-indigenous tropical fish. Mar. Ecol. Prog. Ser. 411, 231–241 (2010).
doi: 10.3354/meps08651
Gagliano, M. & McCormick, M. I. Feeding history influences otolith shape in tropical fish. Mar. Ecol. Prog. Ser. https://doi.org/10.3354/meps278291 (2004).
doi: 10.3354/meps278291
Stransky, C., Murta, A. G., Schlickeisen, J. & Zimmermann, C. Otolith shape analysis as a tool for stock separation of horse mackerel (Trachurus trachurus) in the Northeast Atlantic and Mediterranean. Fish. Res. 89, 159–166 (2008).
doi: 10.1016/j.fishres.2007.09.017
Mejri, M. et al. Use of otolith shape to differentiate two lagoon populations of Pagellus erythrinus (Actinopterygii: Perciformes: Sparidae) in Tunisian waters. Acta Ichthyol. Piscat. 48, 153–161 (2018).
doi: 10.3750/AIEP/02376
Mejri, M. et al. Fluctuating asymmetry in the otolith shape, length, width and area of Pagellus erythrinus collected from the Gulf of Tunis. Cah. Biol. 60, 1–7 (2020).
Volpedo, A. V. & Cirelli, A. F. Otolith chemical composition as a useful tool for sciaenid stock discrimination in the south-western Atlantic. Sci. Mar. https://doi.org/10.3989/scimar.2006.70n2325 (2006).
doi: 10.3989/scimar.2006.70n2325
Rebaya, M. et al. Otolith shape discrimination of Liza ramada (Actinopterygii: Mugiliformes: Mugilidae) from marine and estuarine populations in Tunisia. Acta Ichthyol. Piscat. 47, 13–21 (2017).
doi: 10.3750/AIEP/02006
Trojette, M. et al. Stock discrimination of two insular populations of diplodus annularis (Actinopterygii: Perciformes: Sparidae) along the coast of tunisia by analysis of otolith shape. Acta Ichthyol. Piscat. 45, 363–372 (2015).
doi: 10.3750/AIP2015.45.4.04
Bostanci, D. et al. Sagittal Otolith Morphology of Sharpsnout Seabream Diplodus puntazzo (Walbaum, 1792) in the Aegean Sea. Int. J. Morphol. https://doi.org/10.4067/s0717-95022016000200012 (2016).
doi: 10.4067/s0717-95022016000200012
Bird, J. L., Eppler, D. T. & Checkley, D. M. Comparisons of herring otoliths using Fourier series shape analysis. Can. J. Fish. Aquat. Sci. https://doi.org/10.1139/f86-152 (1986).
doi: 10.1139/f86-152
Zhang, C. et al. Population structure of Japanese Spanish mackerel Scomberomorus niphonius in the Bohai Sea, the Yellow Sea and the East China Sea: evidence from random forests based on otolith features. Fish. Sci. https://doi.org/10.1007/s12562-016-0968-x (2016).
doi: 10.1007/s12562-016-0968-x
Buran, B. N., Deng, X. & Popper, A. N. Structural variation in the inner ears of four deep-sea elopomorph fishes. J. Morphol. https://doi.org/10.1002/jmor.10355 (2005).
doi: 10.1002/jmor.10355
pubmed: 15986409
Kéver, L., Colleye, O., Herrel, A., Romans, P. & Parmentier, E. Hearing capacities and otolith size in two ophidiiform species (Ophidion rochei and Carapus acus). J. Exp. Biol. https://doi.org/10.1242/jeb.105254 (2014).
doi: 10.1242/jeb.105254
pubmed: 25520383
Paxton, J. R. Fish otoliths: Do sizes correlate with taxonomic group, habitat and/or luminescence?. Philos. Trans. R. Soc. B Biol. Sci. https://doi.org/10.1098/rstb.2000.0688 (2000).
doi: 10.1098/rstb.2000.0688
Torres, G. J., Lombarte, A. & Morales-Nin, B. Variability of the sulcus acusticus in the sagittal otolith of the genus Merluccius (Merlucciidae). Fish. Res. 46, 5–13 (2000).
doi: 10.1016/S0165-7836(00)00128-4
Tuset, V. M., Lombarte, A., González, J. A., Pertusa, J. F. & Lorente, M. J. Comparative morphology of the sagittal otolith in Serranus spp. J. Fish Biol. 63, 1491–1504 (2003).
doi: 10.1111/j.1095-8649.2003.00262.x
Popper, A. N., Ramcharitar, J. & Campana, S. E. Why otoliths? Insights from inner ear physiology and fisheries biology. Mar. Freshw. Res. 56, 497–504 (2005).
doi: 10.1071/MF04267
Capillo, G. et al. Quali-quantive analysis of plastics and microfibers found in demersal species from Southern Tyrrhenian Sea (Central Mediterranean). Mar. Poll. Bull. 150, 110596 (2020)
doi: 10.1016/j.marpolbul.2019.110596
Schneider, C. A., Rasband, W. S. & Eliceiri, K. W. NIH Image to ImageJ: 25 years of image analysis. Nat. Methods 9, 671–675 (2012).
pubmed: 22930834
pmcid: 5554542
doi: 10.1038/nmeth.2089
Mangano, M. C., Kaiser, M. J., Porporato, E. M. D., Lambert, G. I. & Spanò, N. Trawling disturbance effects on the trophic ecology of two co-generic Astropectinid species. Mediterr. Mar. Sci. 16, 538–549 (2015).
doi: 10.12681/mms.1256
Libungan, L. A. & Pálsson, S. ShapeR: An R package to study otolith shape variation among fish populations. PLoS ONE 10, 1–12 (2015).
doi: 10.1371/journal.pone.0121102
Savoca, S. et al. Plastics occurrence in juveniles of Engraulis encrasicolus and Sardina pilchardus in the Southern Tyrrhenian Sea. Sci. Total Environ. 718, 137457 (2020).
pubmed: 32325618
doi: 10.1016/j.scitotenv.2020.137457
Hammer, Ø., Harper, D. A. T. & Ryan, P. D. Past: Paleontological statistics software package for education and data analysis. Palaeontol. Electron. 4, 9 (2001).