Revista Cienfica, FCV-LUZ / Vol. XXXV Recibido: 03/10/2024 Aceptado: 11/01/2025 Publicado: 23/03/2025 hps://doi.org/10.52973/rcfcv-e35526 UNIVERSIDAD DEL ZULIA Serbiluz Sistema de Servicios Bibliotecarios y de Información Biblioteca Digital Repositorio Académico 1 of 7 Analysis of mineral and heavy metals in fish otoliths in theTigris River, Turkey Análisis de minerales y metales pesados en otolitos de peces del río Tigris, Turquía Muhammed Yaşar Dörtbudak 1 , Hikmet Dinç 2 , Serbest Bilici 3 * ¹Harran University, Veterinary Faculty, Department of Fisheries and Diseases, Sanlıurfa, Turkey. ²Gaziantep Islamic Science and Technology University, School of Medicine, Pharmacology Department, Gaziantep, Turkey. ³Şırnak University, Faculty of Agriculture, Department of Animal Science, Şırnak, Turkey. *Corresponding author: serbestbilici@hotmail.com.tr - serbestbilici@gmail.com ABSTRACT Rising polluon levels pose significant threats to fisheries. By analysing the different components of fish body structures, the interacons that occur in response to environmental changes can be beer understood. Otoliths are structures in the inner ears of fish and record environmental changes that fish are exposed to throughout their lifes. Recent studies have shown that fish otoliths provide informaon on the accumulaon of mineral and heavy metal in the environment. The accumulaon of mineral and heavy metal in fish otoliths can be an important indicator for understanding environmental interacons and ulmately assessing the sustainability of fishery resources. In this study, 62 samples of Acanthobrama marmid, Alburnus mossulensis, Paracapoeta trua, Capoeta umbla, Carassius gibelio, Chondrostoma regium, Cyprinion kais, Cyprinion macrostomum, Luciobarbus mystaceus and Planiliza abu were obtained from fishermen in the Tigris River. The presence of Co, Cr, Cu, Fe, Mn, Ni, Pb and Zn were analysed by inducvely couple plasma opcal emission apectrometry (ICP-OES) in the otoliths. The average levels of heavy metals residues in the otoliths were determined as Co>Cr>Cu>Fe>Mn>Ni>Pb and Zn. The minerals Ca, K, Mg, Na and P were found to be stascally significant among fish species (P<0.05). According to Tukey HSD mulple comparison test, the highest values of Ca, K and Na were found in P. abu and Mg in C. gibelio. The data can be used as a reference for the evaluaon of the accumulaon of mineral and heavy metal in fish otoliths in terms of fishery management and environmental protecon, and can be compared with the data from studies in different fisheries. Key words: Otolith; heavy metals; minerals in fish; Tigris river RESUMEN Los niveles crecientes de contaminación plantean amenazas significavas para la pesca. Al analizar los diferentes componentes de las estructuras corporales de los peces, se pueden comprender mejor las interacciones que ocurren en respuesta a los cambios ambientales. Los otolitos son estructuras en los oídos internos de los peces y registran los cambios ambientales a los que están expuestos los estos a lo largo de su vida. Estudios recientes han demostrado que los otolitos de los peces brindan información sobre la acumulación de minerales y metales pesados en el ambiente. La acumulación de minerales y metales pesados en los otolitos de los peces puede ser un indicador importante para comprender las interacciones ambientales y, en úlma instancia, evaluar la sostenibilidad de los recursos pesqueros. En este estudio, se obtuvieron 62 muestras de Acanthobrama marmid, Alburnus mossulensis, Paracapoeta trua, Capoeta umbla, Carassius gibelio, Chondrostoma regium, Cyprinion kais, Cyprinion macrostomum, Luciobarbus mystaceus y Planiliza abu de pescadores en el río Tigris. La presencia de Co, Cr, Cu, Fe, Mn, Ni, Pb y Zn se analizó mediante espectrometría de emisión ópca de plasma inducvamente acoplado (ICP-OES) en los otolitos. Los niveles promedio de residuos de metales pesados en los otolitos se determinaron como Co>Cr>Cu>Fe>Mn>Ni>Pb y Zn. Se encontró que los minerales Ca, K, Mg, Na y P eran estadíscamente significavos entre especies de peces (P<0,05). Según la prueba de comparación múlple de Tukey HSD, los valores más altos de Ca, K y Na se encontraron en P. abu y de Mg en C. gibelio. Los datos se pueden ulizar como referencia para la evaluación de la acumulación de minerales y metales pesados en los otolitos de peces en términos de gesón de la pesca y protección ambiental, y se pueden comparar con los datos de estudios de diferentes pesquerías. Palabras clave: Otolitos; metales pesados; minerales en peces; río Tigris

Revista Cienfica, FCV-LUZ / Vol. XXXV UNIVERSIDAD DEL ZULIA Serbiluz Sistema de Servicios Bibliotecarios y de Información Biblioteca Digital Repositorio Académico INTRODUCTION Otoliths are calcified structures located inside the inner ear cavity of teleost fish and form part of the organs that provide hearing and sense of balance [1 ,2]. Otolith is a type of calcium carbonate biomineral that grows in the inner ear of teleost fish. There are three pairs of otoliths: asteriscus, lapillus and sagia. Asteriscus are the most commonly used otoliths in Cypriniformes fish species such as carp. For these species, the asteriscus is the largest of the three otolith pairs [3 ,4]. Compared to muscle and visceral data, otoliths stands out more by showing clear diurnal increments that can record accurate informaon over years, seasons, months and even down to a single day [5 , 6]. The elements deposited in otolith growth layers cannot be modified, absorbed or reconstuted [7 ,8]. Otoliths grow connuously throughout a fish’s life as a result of the deposion of calcium carbonate crystals on a matrix of proteins. During this deposion, elements from the resident waters pass through the gills into the bloodstream and are contained in the calcium carbonate protein cage of the otolith. The chemical composion of the otolith is thought to depend primarily on the environmental condions of the water body in which the fish live, although it is not directly related to ambient water chemistry, primarily due to the effects of physiological processes [9 , 10]. In parcular, the uptake of metals is usually proporonal to calcium (Ca), which inhibits uptake at high relave concentraons [1 , 11 , 12]. Otolith trace metals (i.e. metals other than Ca, Na and Sr) constute only 1% of the total otolith mass [13]. The otolith mainly contains calcium and protein carbonates, which connue to be stored with increasing age but are not reused by physiological processes [14 , 15 , 16]. Otolith chemical composion can represent a reliable natural label of the environment in which the organism lives. The mechanism of otolith uptake of trace elements is not fully understood due to the complex behavior of different metals and the fact that incorporaon between metals varies greatly [17]. Moreover, the bio-mineralizaon process is a funcon of different biological and environmental factors [9 , 18 , 19 , 20 , 21 , 22] and may be physiological differences or species-specific ontogenics [9 , 17 , 21 , 23 , 24 , 25 , 26 , 27]. Although the study of elements ranging from water to carbonate structure is complex, it is undeniable that the chemical analysis of otoliths is a valuable tool used to idenfy individuals from different regions and thus obtain informaon on habitat use [22 , 28 , 29]. The majority of metal contaminaon studies in fish have so far focused on soſt ssues (such as liver, kidney, gills and muscle), which are known to be target organs for metal accumulaon. Less data are available on calcareous ssues as an indicator of metal contaminaon. However, in these ssues, several metals are incorporated during calcificaon; some of them (e.g. Pb) are of high importance during acidificaon processes [30 , 31]. Fish samples in freshwater systems are considered one of the most decisive factors for the esmaon of trace metals polluon potenal [32 , 33 , 34]. Therefore, many studies on heavy metal accumulaon in fish have been conducted and published [34 , 35 , 36 , 37 , 38]. Planiliza abu, A. marmid, A. mossulensis, C. kais, C. macrostomum, P. trua, C. umbla, C. gibelio and L. mystaceus fish are widely consumed as food by the people living in our study area [39]. In this study, otoliths in fish were used as the main research subject because they accumulate heavy metals that cause environmental polluon and are a marker to reveal the level of polluon. MATERIAL AND METHODS Heavy metal analysis in otoliths 62 fish of different species were collected from fishermen working in the Tigris River. The asterisk otoliths were removed, cleaned and stored dry in labeled boxes. Otoliths were removed from fish with plasc tweezers and stored in dry plasc boles [40]. For analysis, otolith samples (right and leſt pairs) were weighed with the And Hr-250 Low Precision Balance and placed in 15 mL tubes. They were placed in a hot water bath for complete dissoluon. When the samples were completely dissolved and no parcles remained, they were topped up to 15 mL with dislled water. Aſter dissoluon of all samples was complete, Otolith samples were analyzed twice for Co, Cr, Cu, Fe, Mn, Ni, Pb and Zn using a inducvely coupled plasma opcal emission spectrometer Perkin Elmer Opma 5300 DV ICP/OES, a fast mul-element technique with dynamic linear range and moderate detecon limits [41]. Heavy metal concentraons were expressed as μg g-1 as wet weight of ssue. Absorpon wavelength: 267.716 nm for Cr; 228.616 nm for Co; 327.393 nm for Cu; 238.204 nm for Fe; 257.610 nm for Mn; 231.604 nm for Ni; 220.353 nm for Pb and 206.200 nm for Zn. Digeson and analycal procedures were controlled by analysis of standard reference material (DORM-2 and DOLT-3 Naonal Research Council Canada, Oawa, Ontario, Canada). Stascal analysis SPSS v.23 (IBM Corp, USA) package program was used for all analyses [42]. Shapiro-Wilk and Levene’s test were used for normal distribuon and homogeneity assumpons, respecvely (P>0.05). Differences between sexes according to the related element within the species were analyzed by independent t-test. One-way analysis of variance was applied to invesgate whether there was a difference between the species in terms of the elements examined, and Tukey HSD mulple comparison test was used for species with significant differences between groups (P<0.05). For each species, a Pearson correlaon matrix was created between the elements analyzed. Data were presented as minimum, maximum, mean, standard error and analyzed at P<0.05 level. The results obtained were stascally expressed as mean, standard deviaon and P values were calculated using ANOVA analysis of variance [43]. RESULTS AND DISCUSION For the Brond-snout Chondrostoma regium, there was a stascally significant difference between the sexes in terms of Ca, Mg and P (P<0.05), while no significant difference was found between the other elements (P>0.05). In all three elements, the values of male individuals were significantly higher than female individuals. For the Tigris scraper Capoeta umbla, there was a stascally significant difference between the sexes in terms of Ca, Mg and Na (P<0.05), while there was no significant difference between 2 of 7

Analysis of mineral and heavy metals in fish otoliths / Yaşar et al. UNIVERSIDAD DEL ZULIA Serbiluz Sistema de Servicios Bibliotecarios y de Información Biblioteca Digital Repositorio Académico the other elements (P>0.05). In all three elements, the values of female individuals were significantly higher than male individuals (P<0.05). There was no significant difference between the sexes for the elements examined in other species (P>0.05). There was a stascally significant difference between fish species for Ca, K, Mg, Na and P (P<0.05) (TABLE I) (FIG. 1). When the highest and lowest differences between species were evaluated according to Tukey HSD mulple comparison test. In terms of Ca, the Abu mullet (Planiliza abu) (16,690.00 ± 726,97 a) had the highest value, and the Tigris bream (Acanthobrama marmid) (1,873.2 ± 190.61 d), the Mossul bleak (Alburnus mossulensis) (1,334.48 ± 216.36 d), the Kais kingfish (Cyprinion kais) (1,063.56 ± 139.61 d) and the Tigris kingfish (Cyprinion macrostomum) (1,463.42 ± 195.68 d) they did not have significant stascal differences and showed the lowest values. In terms of K, the Abu mullet (Planiliza abu) (27.29 ± 1.393 a) had the highest value, while the Tigris bream (Acanthobrama marmid) (2.15 ± 0.19 c), the Mossul bleak (Alburnus mossulensis) (2.36 ± 0.49 c), the Kais kingfish (Cyprinion kais) (1.04 ± 0.24 c), the Tigris kingfish (Cyprinion macrostomum) (2.02 ± 0.35 c), the Long thorn scratcher (Paracapoeta trua) (3.53 ± 0.38 c) and the Tigris scraper (Capoeta umbla) (3.94 ± 0.87 c) they didn’t show stascally significant differences and had the lowest values. In terms of Mg, the Prussian carp (Carassius gibelio) (9.46 ± 1.66 a) had the highest value, while the Kais kingfish (Cyprinion kais) (0.47 ± 0.14 c) and the Tigris kingfish (Cyprinion macrostomum) (0.86 ± 0.17 c) had the lowest values and without significant stacal differences between them. In terms of Na, the Abu mullet (Planiliza abu) (80.58 ± 3.10 a) had the highest value, while the Tigris bream (Acanthobrama marmid) (3.39 ± 0.30 c), the Mossul bleak (Alburnus mossulensis) (3.66 ± 0.84 c), the Kais kingfish (Cyprinion kais) (1.39 ± 0.33 c), the Tigris kingfish (Cyprinion macrostomum) (2.56 ± 0.44 c) and the Long thorn scratcher (Paracapoeta trua) (7.03 ± 0.84 c) had the lowest values and they did not show significant stascal differences between them. In terms of P, the Abu mullet (Planiliza abu) (3.06 ± 0.08 a) had the highest value and the Kais kingfish (Cyprinion kais) (0.83 ± 0.11 d) had the lowest value. TABLE I. Average mineral concentraons according to fish species in theTigris River Species n Ca (Mean ± Sh) mg kg-1 K (Mean ± Sh) mg kg-1 Mg (Mean ± Sh) mg kg-1 Na (Mean ± Sh) mg kg-1 P (Mean ± Sh) mg kg-1 Acanthobrama marmid 5 1873.20±190.61 d 2.15±0.19c 1.81 ± 0.18 bc 3.39 ± 0.30 c 1.07 ± 0.09 cd Alburnus mossulensis 4 1334.48±216.36d 2.36 ± 0.49 c 1.33 ± 0.33 bc 3.66 ± 0.84 c 1.07 ± 0.14 cd Carassius gibelio 7 5560.43±983.44 b 9.29 ± 1.83 b 9.46 ± 1.66 a 16.61 ± 2.95 b 2.88 ± 0.38 ab Cyprinion kais 5 1063.56± 139.61 d 1.04 ± 0.24 c 0.47 ± 0.14 c 1.39 ± 0.33 c 0.825 ± 0.11 d Cyprinion macrostomum 6 1463.42± 195.68 d 2.02 ± 0.35 c 0.86 ± 0.17 c 2.56 ± 0.44 c 1.17 ± 0.18 cd Chondrostoma regium 6 4146.67±1207.58 bc 4.86 ± 1.45 bc 2.53 ± 0.69 bc 7.28 ± 2.23 bc 1.88±0.48 abcd Paracapoeta trua 11 2940.09±325.34 bc 3.53 ± 0.38 c 3.03 ± 0.37 bc 7.03 ± 0.84 c 1.51±0.13 bcd Capoeta umbla 6 2959.50±602.67 bc 3.94 ± 0.87 c 2.54 ± 0.68 bc 8.19 ± 2.09 bc 1.76±0.30 abcd Planiliza abu 5 16690.00±726.97 a 27.29 ± 1.39 a - 80.58 ± 3.10 a 3.06 ± 0.08 a Luciobarbus mystaceus 7 3739.29±566.25 bc 5.65 ± 1.45 bc 5.27 ± 1.41 ab 10.15±2.55 bc 2.52 ± 0.51 abc P-value 62 0.000*** 0.000*** 0.000*** 0.000*** 0.000*** n: number of individuals, Ca: Calcium, K: Potassium, Mg: Magnesium Na: Sodium P: Phosphate. FIGURE 1. Average mineral values by fish species in theTigris River 3 of 7

Revista Cienfica, FCV-LUZ / Vol. XXXV UNIVERSIDAD DEL ZULIA Serbiluz Sistema de Servicios Bibliotecarios y de Información Biblioteca Digital Repositorio Académico For the Brond-snout Chondrostoma regium according to the results of Pearson correlaon analysis, Ca, K, Mg, Na and P elements had stascally strong correlaon with each other (lowest correlaon 0.94) (P<0.05), while these elements had low correlaon with Zn (P>0.05) (TABLE II). TABLE II. Correlaon table of the Brond-snout Chondrostoma Regium. Elements Ca K Mg Na P K r 0.986 p 0.000*** n 6 Mg r 0.994 0.995 p 0.000*** 0.000*** n 6 6 Na r 0.942 0.983 0.962 p 0.004** 0.000*** 0.002** n 6 6 6 P r 0.989 0.991 0.993 0.971 p 0.000*** 0.000*** 0.000*** 0.001** n 6 6 6 6 Zn r -0.306 -0.154 -0.242 0.023 -0.206 p 0.556 0.771 0.643 0.965 0.696 n 6 6 6 6 6 For the Tigris kingfish Cyprinion macrostomum according to the results of Pearson correlaon analysis, Ca, K, Mg, Na and P elements were stascally strongly correlated with each other (except Ca-K correlaon) (lowest correlaon 0.742) (P<0.05) (TABLE III). TABLE III. Correlaon table of the Tigris kingfish Cyprinion macrostomum. Ca K Mg Na K r 0.742 p 0.091 n 6 Mg r 0.826 0.95 p 0.043* 0.003** n 6 6 Na r 0.848 0.968 0.994 p 0.032* 0.001** 0.000*** n 6 6 6 P r 0.837 0.903 0.979 0.972 p 0.037* 0.013* 0.000*** 0.001** n 6 6 6 6 For the Kais kingfish Cyprinion kais; according to the results of Pearson correlaon analysis, Ca, K, Mg, Na and P elements had a stascally strong relaonship with each other (the lowest correlaon was 0.927 for Na-P pair) (P<0.05) (TABLE IV). 4 of 7

Analysis of mineral and heavy metals in fish otoliths / Yaşar et al. UNIVERSIDAD DEL ZULIA Serbiluz Sistema de Servicios Bibliotecarios y de Información Biblioteca Digital Repositorio Académico Tablo IV. Correlaon table of the Kais kingfish Cyprinion Kais. Ca K Mg Na K r 0.966 p 0.007** n 5 Mg r 0.976 0.994 p 0.004** 0.000*** n 5 5 Na r 0.966 0.995 0.988 p 0.007** 0.000*** 0.001** n 5 5 5 P r 0.986 0.94 0.962 0.927 p 0.002* 0.017* 0.008** 0.023* n 5 5 5 5 Many internaonal studies have recognized otoliths as a new opon for monitoring toxic element accumulaon in fish [44 , 45] Many internaonal studies have been conducted to detect toxic elements in these calcareous structures of fish [17 , 40 , 46]. Campana [1] conducted research to confirm that otolith chemistry can detect differences between freshwater and marine fishes, to determine the scale of variaon in trace element concentraons between habitats, to examine links with temperature, salinity, growth and freshwater flow volumes, and to assess the role of freshwater flows for freshwater fishes that may have returned to the estuary aſter a major flood event. Previous otolith studies have shown that salinity, temperature and growth rate can affect the otolith chemistry of some marine species, but the paern varies [1]. Paral correlaons with linear, nonlinear and inverse effects could not explain a significant proporon of the variance in otolith chemistry [47 , 48]. The relaonship between otolith and water concentraons will be strongly influenced by the residence me of each fish in different parts of the estuary at different mes. Despite these potenal confounding effects, otolith Sr/Ca has proven to be an unambiguous determinant of fish movement between freshwater and estuary. Ranaldi and Gagnon [17] found differences in trace element concentraons in otoliths of fish between different sampling locaons. In our study, different species of fish from the same locaon were examined. They concluded that non-essenal metals such as Cd and Pb represent good markers of dietary/ waterborne exposure, while essenal metals such as Zn may be predominantly associated with dietary intake and therefore exposure history should be taken into account when interpreng trace metal composions in otoliths of wild fish and subsequent suscepbility to metal polluon. The use of inducvely Coupled Plasma Mass Spectrometry (ICP-MS) provides sensive spaal informaon that has the potenal to help accurate reconstrucon of the fish’s habitat. Since we used Inducvely Coupled Plasma-Opcal Emission Spectrophotometer (ICP-OES) in our study, we could not obtain some sensive informaon. Herrera-Reveles et al. [40] analyzed the otoliths of fish in Venezuela for heavy metals using Energy Dispersive X-ray spectroscopy (EDS) stabilized by scanning electron microscopy (SEM) and found that five heavy metals (Cd, Cu, Hg, Pb and Zn) were detected mostly in the outer layers of otoliths in fish from all regions. The highest values of Pb/Ca and Hg/Ca weights were observed. These results showed significant spaal variaon in otoliths, providing evidence of different Cd, Hg and Pb concentraons in the water and/or sediments of these locaons. CONCLUSION In light of the data obtained in our study through the inducvely couple plasma opcal emission apectrometry (ICP- OES), the amount of minerals detected in the otoliths of the fish summarized the situaon due to diet/water exposure in fish species living in the Tigris River and is expected to be a source for future studies. ACKNOWLEDGMENTS We are highly thankful to the HUBAP (Harran University Scienfic Research Projects Unit) for their support in this proje- ct. Project number: 18118 Conflict of interests The authors declare that they have no conflict of interests in publishing this manuscript. BIBLIOGRAPHIC REFERENCES [1] Campana SE. Chemistry and composion of fish otoliths: pathways, mechanisms and applicaons. Mar. Ecol. Prog. Ser. [Internet]. 1999; 188:263-297. doi: hps://doi.org/ c2mc46 [2] Campana SE, Thorrold SR. Otoliths, increment and ele- ments: keys to a comprehensive understanding of fish populaons? Can. J. Fish. Aquat. Sci. [Internet]. 2001; 58(1):30–38. doi: hps://doi.org/cs4ckn 5 of 7

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