Otolith phenotypic analysis for the endemic Anatolian fish species, Caucasian bleak Alburnus escherichii Steindachner, 1897 (Teleostei, Leuciscidae), from Selevir Reservoir, Akarçay Basin, Turkey

Otolith phenotypic variability was analyzed in the Caucasian bleak (Alburnus escherichii) from the Selevir Reservoir in Turkey. Utricular (lapillus) and lagenar (asteriscus) otoliths were removed, while distinguishing between left and right otoliths. All otoliths were photographed on the distal (for asterisci) and dorsal surface (for lapilli) using a Leica DF295 digital camera. Otolith morphometrics were measured to the nearest 0.001 mm using Leica Imaging Software. Linear and nonlinear (power) models were applied to determine the relationships between otolith measurements and total length of fish individuals. Two length classes (Class I: 6.7–10.9 cm L_t; Class II: 11.0–15.0 cm L_t) were established to analyze the shape of otoliths. The Form Factor, Circularity, Roundness, Rectangularity, Aspect Ratio and Ellipticity were used to analyze the shape of otoliths. A standardized model was used to remove the effect of size on otolith measurements. Multivariate analysis was performed to detect differences in otolith shape variation. The results of discriminant function analysis showed that 79.9% of A. escherichii specimens were correctly classified by length classes. In this study, intraspecific variation of asteriscus and lapillus otoliths in A. escherichii is reported for the first time. The results of this study provide the first comprehensive data on otolith shape analysis and the relationship between otolith morphometrics and total length in the Caucasian bleak.

Conclusion

The data presented here indicate that the stages of gonadal development affect the shape of otoliths. To this end, further research will be needed on environmental factors, genetic patterns, and the relationship at the individual level between microchemical composition, which carriers information on fish life history, and shapes of otoliths.

Conflicts of interest

The authors declare that there is no conflict of interest.

Acknowledgements

This research did not receive any specific funding. The authors would like to thank Dr. Ali İmamoğlu for the sampling area map, Enes Hançer for preparing figures of otoliths and local fishermen for sampling.

References

Assis, C.A. (2003). The lagenar otoliths of teleosts: their morphology and its application in species identification, phylogeny and systematics. Journal of Fish Biology 62: 1268–1295. DOI: 10.1046/j.1095-8649.2003.00106.x.
Assis, I.O., da Silva, V.E., Souto-Vieira, D., Lozano, A.P., Volpedo, A.V. et al. (2020). Ecomorphological patterns in otoliths of tropical fishes: assessing trophic groups and depth strata preference by shape. Environmental Biology of Fishes 103 (7): 349–361. DOI: 10.1007/s10641-020-00961-0.
Bano, F. & Serajuddin, M. (2021). Sulcus and outline morphometrics of sagittal otolith variability in freshwater fragmented populations of dwarf gourami, Trichogaster lalia (Hamilton,1822). Limnologica 86: 125842. DOI: 10.1016/j.limno.2020.125842.
Basusta, A., Bal, H. & Aslan, E. (2013). Otolith biometry-total length relationships in the population of Hazar Bleak, Alburnus heckeli (Battalgil, 1943) inhabiting Lake Hazar, Elazig. Turkey. Pakistan Journal of Zoology 45(4): 1180–1182.
Bayçelebi, E., Turan, D., Kaya, C. & Freyhof, J. (2020). Alburnus nasreddini, a synonym of A. escherichii (Teleostei: Leuciscidae). Zootaxa 4894: 123–132. DOI: 10.11646/zootaxa.4894.1.7.
Bektas, Y., Aksu, I., Kaya, C., Bayçelebi, E., Küçük, F. et al. (2020). Molecular systematics and phylogeography of the genus Alburnus Rafinesque, 1820 (Teleostei, Leuciscidae) in Turkey. Mitochondrial DNA Part A 31(7): 273–284. DOI: 10.1080/24701394.2020.1791840.
Berinkey, L. (1956). The taxonomical examination of the otoliths of the Cyprinidae of Hungary. Annales Historico-Naturales Musei Nationalis Hungarici 7: 455–462.
Bostanci, D. & Polat, N. (2011). Age and growth of Alburnus tarichi (Güldenstädt, 1814): an endemic fish species of Lake Van (Turkey). Journal of Applied Ichthyology 27 (6): 1346–1349. DOI: 10.1111/j.1439-0426.2010.01468.x.
Bostanci, D., Polat, N., Kurucu, G., Yedier, S., Kontaş, S. et al. (2015). Using otolith shape and morphometry to identify four Alburnus species (A. chalcoides, A. escherichii, A. mossulensis and A. tarichi) in Turkish inland waters. Journal of Applied Ichthyology 31 (6): 1013–1022. DOI: 10.1111/jai.12860.
Bostanci, D., Türker, D., Yedier, S., Kontaş S. & Kurucu, G. (2018). Investigating the fluctuating asymmetry in the otolith characters of mediterranean horse mackerel, Trachurus mediterraneus (Steindachner 1868) inhabiting Edremit Bay, North Aegean Sea. Ordu University Journal of Science and Technology 8(1): 69–78.
Brown-Peterson, N.J., Wyanski, D.M., Saborido-Rey, F., Macewicz, B.J., & Lowerre-Barbieri, S.K. (2011). A standardized terminology for describing reproductive development in fishes. Marine and Coastal Fisheries 3(1): 52–70. DOI: 10.1080/19425120.2011.555724.
Buckland, A., Baker, R., Loneragan, N. & Sheaves, M. (2017). Standardizing fish stomach content analysis: The importance of prey condition. Fisheries Research 196: 126–140. DOI: 10.1016/j.fishres.2017.08.003.
Capoccioni, F., Costa, C., Aguzzi, J., Menesatti, P., Lombarte, A. et al. (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. DOI: 10.1016/j.jembe.2010.11.011.
Carvalho, B.M.D., Volpedo, A.V. & Fávaro, L.F. (2020). Ontogenetic and sexual variation in the sagitta otolith of Menticirrhus americanus (Teleostei; Sciaenidae) (Linnaeus, 1758) in a subtropical environment. Papéis Avulsos de Zoologia, 60: e20206009. DOI: 10.11606/1807-0205/2020.60.09.
Cerna, F., Saavedra-Nievas, J.C., Plaza-Pasten, G., Niklitschek, E. & Morales-Nin, B. (2019). Ontogenetic and intraspecific variability in otolith shape of anchoveta (Engraulis ringens) used to identify demographic units in the Pacific Southeast off Chile. Marine and Freshwater Research 70(12): 1794–1804. DOI: 10.1071/MF18278.
Dopeikar, H., Keivany, Y., & Shadkhast, M. (2015). Reproductive biology and gonad histology of the Kura Barbel, Barbus lacerta (Cyprinidae), in Bibi-Sayyedan River, Tigris basin. North-Western Journal of Zoology 11(1): 163–170.
Elliot, N.G., Haskard, K. & Koslow, J.A. (1995). Morphometric analysis of the orange roughy (Hoplostethus atlanticus) of the continental slope of southern Australia. Journal of Fish Biology 46(2): 202–220. DOI: 10.1111/j.1095-8649.1995.tb05962.x.
Elp, M., Şen, F. & Özuluğ, M. (2015). Alburnus selcuklui, a new species of Cyprinid Fish from East Anatolia, Turkey (Teleostei: Cyprinidae). Turkish Journal of Fisheries and Aquatic Sciences 15: 181–186. DOI: 10.4194/1303-2712-v15_1_20.
Firidin S., Eroglu, O. & Kutlu, I. (2017). Optimizing DNA extraction method for archived otoliths. Genetics of Aquatic Organisms 1: 57–60. DOI: 10.4194/2459-1831-v1_2_03.
Freyhof J., & Turan, D. (2019). Alburnus magnificus, a new species of bleak from the Orontes River drainage (Teleostei: Leuciscidae). Zootaxa, 4559(2): 373–383. DOI: 10.11646/zootaxa.4559.2.10.
Freyhof, J., Kaya, C., Bayçelebi, E., Geiger, M. & Turan, D. (2018). Generic assignment of Leuciscus kurui Bogutskaya from the upper Tigris drainage, and a replacement name for Alburnus kurui Mangit and Yerli (Teleostei: Leuciscidae). Zootaxa 4410(1): 113–135. DOI: 10.11646/zootaxa.4410.1.6.
Freyhof, J. (2014). Alburnus escherichii. The IUCN Red List of Threatened Species 2014: e.T19018485A19222778.https://dx.doi.org/10.2305/IUCN.UK.2014.RLTS.T19018485A19222778.en. Retrieved January 21 2021, from https://www.iucnredlist.org/.
Froese, R. & Pauly. D. (2019). FishBase. World Wide Web electronic publication. Retrieved January 21 2021, from https:// www.fishbase.org.
Gierl, C. & Reichenbacher, B. (2015). A new fossil genus of gobiiformes from the miocene characterized by a mosaic set of characters. Copeia 103: 792–805. DOI: 10.1643/CI-14-146.
Gierl, C., Liebl, D., Radek, R., Vukic, J., Esmaeili, H.R. et al. (2018). What can goby otolith morphology tell us? Cybium 42(4): 349–363. DOI: 10.26028/cybium/2018-424-006.
Gülle, İ., Küçük, F. & Güçlü, S.S. (2017). Re-description and new distribution area of an endemic anatolian fish species, Alburnus nasreddini Battalgil, 1944. Turkish Journal of Fisheries and Aquatic Sciences 17: 863–869. DOI: 10.4194/1303-2712-v17_5_02.
Grønkjaer, P. & Sand, M.K. (2003). Fluctuating asymmetry and nutritional condition of Baltic cod (Gadus morhua) larvae. Marine Biology 143: 191–197. DOI: 10.1007/s00227-003-1064-1.
Jawad, L.A., Park, J.M., Kwak, S.N. & Ligas, A. (2017). Study of the relationship between fish size and otolith size in four demersal species from the south-eastern Yellow Sea. Cahiers de Biologie Marine 58(1): 9–15. DOI: 10.21411/CBM.A.645C2013.
Keivany, Y., Ghorbani, M. & Paykan-Heyrati, F. (2017). Reproductive biology of Mossul bleak (Alburnus mossulensis) in Bibi-Sayyedan River of Tigris basin in Iran. Caspian Journal of Environmental Sciences 15(2): 135–145. DOI: 10.22124/CJES.2017.2370.
Koeberle, A.L., Arismendi, I., Crittenden, W., Di Prinzio, C., Gomez-Uchida, D. et al. (2020). Otolith shape as a classification tool for Chinook salmon (Oncorhynchus tshawytscha) discrimination in native and introduced systems. Canadian Journal of Fisheries and Aquatic Science 999: 1–17. DOI: 10.1139/cjfas-2019-0280.
La Mesa, M., Guicciardi, S., Donato, F., Riginella, E., Schiavon, L. et al. (2020). Comparative analysis of otolith morphology in icefishes (Channichthyidae) applying different statistical classification methods. Fisheries Research 230: 105668. DOI: 10.1016/j.fishres.2020.105668.
Lagardère F., Chaumillon, G., Amara, R., Heineman, G. & Lago, J.M. (1995). Recent Developments in Fish Otolith Research. Columbia: Univ. South Carolina Press.
Lleonart, J., Salat, J. & Torres, G.J. (2000). Removing allometric effects of body size in morphological analysis. Journal of Theoretical Biology 205: 85–93. DOI: 10.1006/jtbi.2000.2043.
Mangıt, F. & Yerli, S. (2018). Systematic evaluation of the genus Alburnus (Cyprinidae) with description of a new species. Hydrobiologia 807: 297–312. DOI: 10.1007/s10750-017-3405-y.
Mangıt, F. (2014). Morphometric and phylogenetic studies on genus Alburnus (Teleostei: Cyprinidae). PhD Thesis, Hacettepe University Graduate School of Science and Engineering.
Mapp, J., Hunter, E., Kooij, J.V.D., Songer, S. & Fisher, M. (2017). Otolith shape and size: The importance of age when determining indices for fish-stock separation. Fisheries Research 190: 43–52. DOI: 10.1016/j.fishres.2017.01.017.
Mejri, M., Trojette, M., Jmil, I., Ben Faleh, A., Chalh, A. et al. (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. DOI: 10.21411/CBM.A.4738CCD6.
Ozpicak, M. (2020). Otolith shape and characteristics as a morphological approach to the stock identification in Barbus tauricus (Cyprinidae). Journal of Ichthyology 60(4): 716–724. DOI: 10.1134/S0032945220050045.
Ozuluğ, M. & Freyhof, J. (2007). Rediagnosis of four species of Alburnus from Turkey and description of two new species (Teleostei: Cyprinidae). Ichthyological Exploration of Freshwaters 18(3): 233–246.
Park, J.M., Gaston, T.F., Riedel, R. & Williamson, J.E. (2018). Biometric relationships between body and otolith measurements in nine demersal fishes from north-eastern Tasmanian waters, Australia. Journal of Applied Ichthyology 34(4): 801–805. DOI: 10.1111/jai.13612.
Perea, S., Böhme, M., Zupancic, P., Freyhof, J., Sanda, R. et al. (2010). Phylogenetic relationships and biogeographical patterns in Circum-Mediterranean subfamily Leuciscinae (Teleostei, Cyprinidae) inferred from both mitochondrial and nuclear data. BMC Evolutionary Biology 10: 265. DOI: 10.1186/1471-2148-10-265.
Ponton, D. (2006). Is geometric morphometrics efficient for comparing otolith shape of different fish species?. Journal of Morphology 267(6): 750–757. DOI: 10.1002/jmor.10439.
Popper, A. N., Ramcharitar, J. & Campana, S.E. (2005). Why otoliths? Insights from inner ear physiology and fisheries biology. Marine and Freshwater Research 56: 497–504. DOI: 10.1071/MF04267.
Romero, M.A., Ruiz, N.S., Medina, A.I. & González, R.A. (2020). Biometric relationships between otolith and fish size of the main demersal resources of North Patagonia, Argentina. Journal of Ichthyology 60: 411–421.
Saygın, S., Özpiçak, M., Yılmaz, S. & Polat, N. (2020). Otolith shape analysis and the relationships between otolith dimensions–total length of European Bitterling, Rhodeus amarus (Cyprinidae) Sampled from Samsun Province, Turkey. Journal of Ichthyology 60: 570–577. DOI: 10.1134/S0032945220040190.
Saygın, S., Ozpiçak, M., Elp, M., Polat, N., Atici, A.A. et al. (2017). Comparative analysis of the otolith features of tarek (Alburnus tarichi (Güldenstädt, 1814)) from different lakes across Van Basin (Van, Erçek, Nazik, Aygır) (Turkey). Limnofish 3: 91–99.
Schulz-Mirbach, T. & Reichenbacher, B. (2006). Reconstruction of oligocene and neogene freshwater fish faunas–an actualistic study on cypriniform otoliths. Acta Palaeontologica Polonica 51(2): 283–304.
Škeljo, F. & Ferri, J. (2012). The use of otolith shape and morphometry for identification and size-estimation of five wrasse species in predator-prey studies. Journal of Applied Ichthyology 28(4): 524–530. DOI: 10.1111/j.1439-0426.2011.01925.x.
Souza, A.T., Soukalová, K., Děd, V., Šmejkal, M., Moraes, K. et al. (2020). Otolith shape variations between artificially stocked and autochthonous pikeperch (Sander lucioperca). Fisheries Research 231: 105708. DOI: 10.1016/j.fishres.2020.105708.
Sun, Y., Zhang, C., Tian, Y. & Watanabe, Y. (2020). Age, growth, and mortality rate of the yellow goosefish Lophius litulon (Jordan, 1902) in the Yellow Sea. Journal of Oceanology and Limnology 1–9. DOI: 10.1007/s00343-019-9216-4.
Teimori, A., Motamedi, M. & Zeinali, F. (2020). Intrapopulation variation of otolith associated with ontogeny and morphological dimorphism in Hormuz tooth‐carp Aphanius hormuzensis (Teleostei: Aphaniidae). Acta Zoologica 1–15. DOI: 10.1111/azo.12332.
Tuset, V.M., Lombarte, A., Gonzalez, J.A., Pertusa, J.F. & Lorente, M. (2003). Comparative morphology of the sagittal otolith in Serranus spp. Journal of Fish Biology 63: 1491–1504.
Tuset, V.M., Olivar, M.P., Otero-Ferrer, J.L., López-Pérez, C., Hulley, P.A. et al. (2018). Morpho-functional diversity in Diaphus spp. (Pisces: Myctophidae) from the central Atlantic Ocean: Ecological and evolutionary implications. Deep Sea Research, Part I 138: 46–59. DOI: 10.1016/j.dsr.2018.07.005.
Uysal, K., Köse, E., Bülbül, M., Dönmez, M., Erdoğan, Y. et al. (2009). The comparison of heavy metal accumulation ratios of some fish species in Enne Dame Lake (Kütahya/Turkey). Environmental Monitoring and Assessment 157: 355–362. DOI: 10.1007/s10661-008-0540-y.
van der Laan, R. (2020). Freshwater Fish List. The Netherland, Twenty nineth edition. 1094.
Van Neer, W., Ervynck, A., Bolle, L. & Millner, R. (2004). Seasonality only Works in certain parts of the year: the reconstruction of fishing seasons through otolith analysis. International Journal of Osteoarchaeology 14(6): 457–474. DOI: 10.1002/oa.727.
Waessle, J.A., Lasta, C.A. & Favero, M. (2003). Otolith morphology and body size relationships for juvenile Sciaenidae in the Río de la Plata estuary (35-36 S). Scientia Marina 67: 233–240.
Więcaszek, B., Nowosielski, A., Dąbrowski, J., Górecka, K., Keszka, S. et al. (2020). Fish size effect on sagittal otolith outer shape variability in round goby Neogobius melanostomus (Pallas 1814). Journal of Fish Biology 97(5): 1520–1541. DOI: 10.1111/jfb.14521.
Wright, P.J., Panfili, J., Morales-Nin, B. & Geffen, A.J. (2002). Types of calcified structures. Otoliths. In J. Panfili, H. de Pontual, H. Troadec & P.J. Wright (Eds.), Manual of Fish Sclerochronology (pp. 31–57). Brest, France: Ifremer-lRD coedition.
Yedier, S., Bostancı, D., Kontaş, S., Kurucu, G. & Polat, N. (2018). Comparison of otolith mass asymmetry in two different Solea solea populations in Mediterranean Sea. Ordu University Journal of Science and Technology 8(1): 125–133.
Yedier, S. & Bostanci, D. (2019). Aberrant crystallization of Blackbellied angler Lophius budegassa Spinola, 1807 otoliths. Cahiers de Biologie Marine 60(4): 527–533.
Yedier, S. & Bostanci, D. (2020). Aberrant otoliths in four marine fishes from the Aegean Sea, Black Sea, and Sea of Marmara (Turkey). Regional Studies in Marine Science 34 (101011): 1–7.
Yılmaz, F., Barlas, M., Yorulmaz, B. & Özdemir, N. (2006). A taxonomical study on the inland water fishes of Muğla. Ege University Journal of Fisheries and Aquatic Sciences 23: 27–30.
Yılmaz, S., Yazıcıoğlu, O., Yazici, R. & Polat, N. (2015). Relationships between fish length and otolith size for five cyprinid species from Lake Ladik, Samsun, Turkey. Turkish Journal of Zoology 39(3): 438–446. DOI: 10.3906/zoo-1403-58.
Yılmaz, S., Emiroğlu, Ö., Aksu, S., Başkurt, S. & Polat, N. (2019). Relationships between otolith dimensions and body growth of North African Catfish Clarias gariepinus (Burchell, 1822) from the upper basin of the Sakarya River, Turkey. Croatian Journal of Fisheries 77: 57–62. DOI: 10.2478/cjf-2019-0006.
Zar, J. H. (1999). Biostatistical Analysis. New Jersey (USA), Prentice-Hall. 663.
Zhao, B., Liu, J., Song, J., Cao, L. & Dou, S. (2017). Otolith shape analysis for stock discrimination of two Collichthys genus croaker (Pieces: Sciaenidae,) from the northern Chinese coast, Chin. Chinese Journal of Oceanology and Limnology 36: 981–989. DOI: 10.1007/s00343-018-7082-0.