Abstract
Reliable and detailed knowledge regarding the relationship between otolith size and the size of fish is important for fisheries management and for ecological studies on predicting fish size and on predator–prey interactions. Therefore, these relationships are estimated for three sprat (genus Clupeonella) species, including C. caspia, C. engrauliformis and C. grimmi from the Caspian Sea. The relative size and mass of the otoliths corrected for body size and mass were also estimated for the three sprat species. After biometry of collected specimens, the Sagittal otoliths were extracted from the cranium of collected specimens and photographed. Photos were used to estimate length and width of otoliths. The results revealed significant relationships between otolith length and width vs. fish length and otolith mass vs. body mass in all three species (r2 > 0.5). The higher coefficient of determination (r2) for relationships between total length (fish) – Otolith length and width was concluded in comparison with relationships between fish mass and otolith mass in the studied sprat species. Otoliths of C. grimmi showed the highest relative length and were significantly (P < 0.05) heavier than sagittal otoliths of two other sprat species. There is no previous report on size–mass relationships between fish and otolith measurements among the three studied sprat species. These estimated equations can be used in back-calculation studies, especially for these three sprats as the dominant prey for piscivorous predators such as Caspian seals and sturgeons, in their habitats.
Introduction
The most abundant fishes in the Caspian Sea are three small clupeids, the Caspian tyulka (Clupeonella caspia Svetovidov, 1941), the Anchovy sprat (Clupeonella engrauliformis (Borodin, 1904)) and Southern Caspian sprat (Clupeonella grimmi Kessler, 1877) (IFO 2022). These sprat species are endemic to the Caspian Sea and to the lower parts of its affluent rivers, such as the Terek and the Ural (Kottelat & Freyhof 2007). Clupeonella species make up a large proportion of the Caspian Seal's (Pusa caspica) diet (Kosarev & Yablonskaya 1994) and are also preyed upon by Caspian Sea sturgeons such as the Beluga sturgeon (Huso huso) (Hashemian 1996). Clupeids also play an important ecological role in the food chain of the Caspian Sea as planktivorous species (Mamedov 2006). Finally, sprats are targeted by the fisheries industry and the annual catch exceeded 20,000 tons during 2016–2021 (IFO 2022), accounting for more than 80% of the total catch in the Caspian Sea (Salmanov 1999, Ivanov 2000).
Overexploitation of fish stocks and the expansion of the invasive ctenophore, Mnemiopsis leidyi and their strong food competition and direct consumption of fish larvae and eggs, led to major declines in total biomass and catch of Clupeonella spp. in the Caspian Sea (Daskalov & Mamedov 2007, Aliasghari et al. 2017). Since 1999, total landings of the three mentioned sprat species in Iran have declined from 95,000 to 20,138 tons in 2021 (IFO 2022). Because these species are small-bodied, they are mainly used in the local fishmeal industry, but are also sold smoked, salted, canned in sauce and oil for human consumption (Alavi-Yeganeh et al. 2017). C. caspia dominates the catch in Iran, followed by C. engrauliformis and C. grimmi (Parafkandeh Haghighi & Kaymaram 2012, Janbaz et al. 2021). Their sustainable management is vital to the fisheries and ecosystem health of the Caspian Sea.
Otoliths are small calcified structures in the inner ears of all teleost fishes, and they function as balance, movement and direction indicators, but also play a role in the hearing of fish. Their shape is species-specific (Tuset et al. 2003) and is therefore used in taxonomic studies (Kumar et al. 2012, Rivera Felix et al. 2013). In ecological studies, otoliths are used to examine the diet of many piscivorous predators. Otoliths found in the digestive system are useful for identifying prey (Furlani et al. 2007). Also, by establishing relationships between fish length and otolith size as well as between fish mass and otolith mass, it is possible to back-calculate the sizes and the biomass of fish consumed by predators (Harvey et al. 2000, Zan et al. 2015, Aneesh-Kumar et al. 2017). In fisheries management, the length of a fish can be verified by the relationship between otolith length and total length of a fish when the age determined from the otolith lies outside expected values (Echeverria 1987). Accordingly, several studies have estimated such relationships for different fish species (Audai et al. 2019, Khanali et al. 2021, Bhuiya & Siddique 2022, Khandan Barani & Alavi-Yeganeh 2024).
Despite the high ecological and economical importance of sprats in the Caspian Sea, related information is limited. This study aimed to characterize the relationships between otolith metrics (length, width and mass) and fish size (total length and total mass) in three sprat species of the Caspian Sea. Such knowledge would be valuable for the study of the feeding habits of predators and for related future ecological as well as fisheries management research in the area.
Material and methods
Specimens were collected by local fishing boats around Babolsar port (36°44′N; 52°63′E) in the winters of 2022 and 2023 from depths of 60–100 m (Fig. 1). The salinity range in the fishing area is 11–12 ppt, and the mesh size of lantern nets on fishing boats was 7 mm. Species identification was carried out using the identification key of Coad (2017) and individuals were preserved (Formalin 4%) for later measurements. We measured total length of fish specimens with a caliper to the nearest 0.01 mm and fish mass (FM) to the nearest 0.1 g using a digital balance in a total of 360 specimens of the three species (C. caspia: 116 specimens; C. engrauliformis: 120 specimens; C. grimmi: 124 specimens). The sizes of collected specimens covered almost the entire catchable size range reported by fisheries in the southern Caspian Sea (Alavi-Yeganeh et al. 2017). Sagittal otoliths were extracted through a transverse incision made in the back of the cranium. Then the otoliths were washed with a 1% NaOH solution for 2 min (Kinacigil et al. 2000) and stored in vials after drying. Photos were taken from the right sagittal otoliths of all three species using a scanning electron microscope. Digimizer ver. 5.7.2 software was used to estimate the dimensions of otoliths, including length and width (to the nearest 0.01 mm) (Firouzi et al. 2020). Otolith masses were measured using a digital balance (to the nearest 0.1 mg).
The location of the sampling area; Babolsar port on the southern coast of the Caspian Sea
Citation: Animal Taxonomy and Ecology 70, 3; 10.1556/1777.2024.12668
Otolith length was defined as the maximum distance from the midpoint of the rostrum through the primordium to the posterior edge. Otolith width was defined as the longest distance perpendicular to the length passing through the primordium (Khanali et al. 2021) (Fig. 2). The difference between the right and left sagittal otoliths was tested using a paired t-test. No significant differences were found between the left and right otoliths in length, width and mass (Student's t-tests, P > 0.05). Therefore, measurements taken on the right otoliths were used for further analysis. Extreme outliers (less than one percent of the data) were removed from the analysis by inspection of related plots to ensure that malformed otoliths or fish specimens and mistakes during measurements do not bias the results. We used a linear regression approach to establish the relationship between the length of the fish and the length and width of the otolith, as well as between the mass of the fish and the mass of the otolith. Relative otolith lengths and masses were estimated for species using two formulas (otolith length*100)/total length and (otolith mass*1000)/fish mass, respectively. We used one-way ANOVAs to compare relative otolith lengths and weights among species. Statistical analyses were carried out using SPSS ver. 16.
Scanning electron microscope image of the inner view of the right sagittal otolith of Clupeonella caspia, caught in the Caspian Sea. Otolith width (OWI) and otolith length (OL) are indicated
Citation: Animal Taxonomy and Ecology 70, 3; 10.1556/1777.2024.12668
Results
The total length and weight of specimens ranged from 84 to 141 mm and 4.71–17.59 g for C. caspia, 105–156 mm and 7.83–20.76 g for C. engrauliformis and 107–155 mm and 6.14–20.93 g for C. grimmi. Dimensions and relative length and weight of otoliths are presented in Table 1. Absolute Relative length and weight of otoliths in C. grimmi were both significantly higher than in the other two sprat species (all P < 0.05). Absolute values of otolith length, width and mass indicated larger and heavier otolithes in C. grimmi (Table 1, Fig. 3). The comparison of the relative length of otoliths among sprat species revealed longest otoliths in C. grimmi, followed by C. caspia (Pairwise comparison; C. grimmi vs. C. caspia: P < 0.001), while C. engrauliformis exhibited the shortest otoliths (C. caspia vs. C. engrauliformis: P < 0.001). Relative otolith weight was also largest in C. grimmi, while there was no difference between the other two species (C. grimmi vs. C. caspia: P < 0.001; C. grimmi vs. C. engrauliformis: P < 0.001; C. caspia vs. C. engrauliformis: P = 0.74). The estimated relationships between otolith dimensions and fish size revealed significant positive correlations with high coefficients of determination (all r2 > 0.5; Table 2, Fig. 3).
Dimensions of otoliths and relative otolith lengths and weights in three sprat species from the Caspian Sea. Letters in the superscript indicate homogeneous subsets in case of relative otolith length and relative otolith weight
| Species | Otolith length (mm) (Mean ± SD) | Otolith width (mm) (Mean ± SD) | Otolith weight (mg) (Mean ± SD) | Relative otolith length (Mean ± SD) | Relative otolith mass (Mean ± SD) |
| Clupeonella caspia | 2.12 ± 0.32 | 1.38 ± 0.21 | 1.0 ± 0.51 | 1.78 ± 0.12b | 0.09 ± 0.03a |
| Clupeonella engrauliformis | 2.28 ± 0.18 | 1.51 ± 0.11 | 1.4 ± 0.28 | 1.61 ± 0.08a | 0.09 ± 0.02a |
| Clupeonella grimmi | 2.46 ± 0.20 | 1.69 ± 0.11 | 1.97 ± 0.44 | 1.85 ± 0.12c | 0.16 ± 0.03b |
The relationship between fish total length vs. otolith length, total fish length vs. otolith width, and fish mass vs. otolith mass observed in C. caspia (a), C. engrauliformis (b) and C. grimmi (c)
Citation: Animal Taxonomy and Ecology 70, 3; 10.1556/1777.2024.12668
Descriptive statistics and estimated parameters of the relationships between fish length and otolith length as well as between fish weight and otolith mass in three Clupeonella species from the Caspian Sea. a: intercept; b: slope; CI: confidence interval; r2: coefficient of determination; FW: (fish weight); FL: (fish length); OL: (otolith length); OW (otolith width); OM: (otolith mass)
| Species | Equation | a | b | 95% CI of b | r2 |
| Clupeonella caspia Svetovidov, 1941 | FL = a + b OL | 30.98 | 41.50 | 37.79–45.21 | 0.812 |
| FL = a + b OW | 32.17 | 62.52 | 57.33–67.72 | 0.833 | |
| FW = a + b OM | 4.57 | 6300.08 | 5481.01–7119.15 | 0.679 | |
| Clupeonella engrauliformis (Borodin 1904) | FL = a + b OL | 27.68 | 50.17 | 42.67–57.67 | 0.613 |
| FL = a + b OW | 38.85 | 67.74 | 56.47–79.01 | 0.566 | |
| FW = a + b OM | 3.17 | 8581.08 | 6969.50–10192.67 | 0.505 | |
| Clupeonella grimmi Kessler, 1877 | FL = a + b OL | 20.85 | 45.23 | 38.13–52.33 | 0.594 |
| FL = a + b OW | 9.26 | 72.39 | 59.37–85.41 | 0.560 | |
| FW = a + b OM | 1.23 | 5732.63 | 4782.11–6683.14 | 0.547 |
Discussion
Information on the relationship between fish length and otolith size provides a baseline for trophic studies, so that the establishment of this correlation constitutes the first step of most dietary studies on piscivorous fishes and other predators like marine mammals and seabirds (Zijlstra 1995, Ross et al. 2005, Battaglia et al. 2015, Gimenez et al. 2017, Byrd et al. 2020). In this study, we observed strong correlations between measures of fish and otolith size. The relationship between fish weight and otolith mass turned out to be weaker than between fish length and otolith length across the three studied species. Variation in the thickness of otoliths, especially in the lower ridge of the sulcus acusticus groove, which could largely affect the weight of otoliths within individuals, is likely to have contributed to the observed lower correlation between fish weight and otolith weight. The relationship between otolith width and fish length was similarly strong, as that between otolith length and fish length, but the use of the latter is recommendable. Otolith length is easier to measure accurately because this dimension is larger, so that the measurement error is relatively smaller, but also because the bulgy shape of the otolith causes this axis to lie more parallel to the underground during photography. Our data, thus, suggest that otolith length is best used for the estimation of the body size of Clupeonella specimens.
Lombarte and Cruz (2007) compared the otolith weight of 134 species from the north-western Mediterranean Sea and they detected a positive relationship between sagittal otolith size and the depth of their habitat, ranging as deep as 750 m. They presumed the reasons related to endogenous causes are more important rather than exogenous factors in this relationship. Accordingly, in this study, we observed the largest relative otolith weight and lengths in C. grimmi, which is known to inhabit deeper waters in the Caspian Sea compared to the other two studied sprat species (Aliasghari et al. 2017, Coad 2017).
There are many factors that can affect otolith size and weight, including environmental conditions, such as the acidity of water (Di Franco et al. 2019) and water temperature (Lombarte & Lleonart 1993). In addition, fish sex, age and growth condition can also influence otolith size (Strelcheck et al. 2003). Although we did not consider these factors here, the relationships estimated in this study provide fundamental information for further ecological and fisheries management studies.
Acknowledgments
We would like to thank Dr. Hashem Khandan Barani for his assistance during laboratory work.
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