Introduction
Labridae is a large family with eight species living in the Black Sea (Keskin, Reference Keskin2010), 20 species along the Turkish coasts (Bilecenoğlu et al., Reference Bilecenoğlu, Kaya, Cihangir and Çiçek2014) and 594 species around the world (Parenti & Randall, Reference Parenti and Randall2011). Labrids, or wrasses, are small territorial marine fishes inhabiting algal and rocky inshore areas (Costello, Reference Costello1991). The species of the labrid genus Symphodus are found at depths of 1–50 m, inhabiting eelgrass beds and rocky areas in the Mediterranean, Eastern Atlantic and Black Sea. Sexual dimorphism and sex reversal can be seen in some species of Symphodus (Whitehead et al., Reference Whitehead, Bauchot, Hureau, Nielsen and Tortonese1986). However, it was reported that sex reversal does not occur in Symphodus cinereus (Bonnaterre, 1788) (Remacle, Reference Remacle1970). Symphodus cinereus generally aggregates in eelgrass beds and littoral areas, but these fish are occasionally found on soft bottoms (1–20 m); they are frequently present in lagoons and estuaries with abundant vegetation and detritus. They feed on small gastropods, isopods, amphipods, shrimps and bivalves. The males guard the females during spawning in built nests (Whitehead et al., Reference Whitehead, Bauchot, Hureau, Nielsen and Tortonese1986). The males of the genus Symphodus, which build and guard nests, defend their territory against other species and protect demersal eggs until hatching, expend significant energy on reproduction (Warner & Lejeune, Reference Warner and Lejeune1985; Taborsky, Reference Taborsky1998). The wrasse is not considered a commercial fish in the Black Sea. It is generally caught and discarded by small-scale commercial fisheries. As a result, similarly to many other non-commercial species, insufficient information is available about the biology of S. cinereus. The first study reporting the general characteristics of the species was conducted in the Mediterranean by Quignard & Pras (Reference Quignard, Pras, Whitehead, Bauchot, Hureau, Nielsen and Tortonese1986). Subsequently, Ghorbel-Ouannes & Bouain (Reference Ghorbel-Ouannes and Bouain2001) reported age and growth characteristics and Ghorbel-Ouannes et al. (Reference Ghorbel-Ouannes, Jarboui and Bouain2007) reported the reproductive biology of the species from the Gulf of Gabes (Tunisia). Apart from these studies, information about the growth characteristics of S. cinereus is limited. The present study is the first detailed study conducted in the south-eastern Black Sea with the aim of revealing basic biological parameters such as the sex ratio, growth properties, age distribution, spawning period, fecundity, condition factor and length-weight relationship (LWR) of S. cinereus. It is expected that the findings will fill an important gap in the literature and provide a better understanding of the life history of this species.
Materials and methods
Fish sampling
Samples were obtained from fishermen engaged in commercial fishing. A total of 384 specimens (164 male and 220 female) of S. cinereus were collected between June 2015 and May 2016 with trammel nets of 36-mm and 40-mm mesh size settled at depths of 10–40 m off the coast of Rize, Turkey, in the south-eastern Black Sea (Figure 1). The collected samples were carried to the laboratory and length (accuracy of 0.1 cm), total weight (accuracy of 0.001 g) and gonad weight (accuracy of 0.001 g) were measured. The specimens were dissected and sagittal otoliths were removed.
Study area.
Length-weight relationship (LWR)
The LWR of the samples was determined by applying the formula W = aLb (Ricker, Reference Ricker1975), where L is total length (cm), a is the intercept, b is the slope and W is total weight (g). The degree of association between variables was computed with r 2 values (King, Reference King1995) (Figure 2). The variation of the b value from b = 3 (isometric growth) was tested with the one-sample t-test, and Pauly's t-test was used for comparisons of the differences of slope values from b = 3 (Pauly, Reference Pauly1984).
Length-weight relationships by sex of Symphodus cinereus.
Age determination
For age determination, the otoliths of the 384 collected fish were removed and cleaned of blood and tissues, and then they were stored in Eppendorf tubes containing 96% alcohol. Age was determined by counting the number of opaque and transparent parts with the help of light reflected on the sagittal otoliths. Otoliths were imaged with a Nikon SMZ1000 stereomicroscope connected to a Nikon SMZ1000 digital camera with magnification from 0.8× to 8.0× (Figure 3). Ages were determined by a single reader.
A sagittal otolith of 5-year-old Symphodus cinereus.
Growth
Size frequency
The monthly size frequency distributions of female and male specimens were calculated at class intervals of 0.5 cm for total length. The Kolmogorov–Smirnov two-sample test was applied to analyse size frequency distributions for females and males and t-tests were used to compare mean total lengths between females and males. The χ2 test was used to calculate the sex ratio and data were recorded as male:female ratios. Deviations from 1:1 were tested using χ2 analysis (Dagnelie, Reference Dagnelie1991).
Growth model
The von Bertalanffy growth equation was used to calculate growth in both weight and length (King, Reference King1995; Sparre & Venema, Reference Sparre and Venema1998). The age-length relationship is expressed as L t = L ∞[1–e–k (t–t0)], as explained in the Ford–Walford method of Sparre & Venema (Reference Sparre and Venema1992). In this formula, t represents time (or age), L t represents length at age t (cm), L ∞ represents the asymptotic average length (cm), k is the growth rate parameter (year–1) and t 0 is the theoretical age when the fish would have been at zero total length. The growth performance index (Φ’) was calculated as Φ’ = log(K) + 2log(L ∞) for comparisons of growth performance (Pauly & Munro, Reference Pauly and Munro1984).
Condition factor (K)
To compare the conditions of sampled fish from different periods or locations, a single LWR for all fish from all periods and locations was used to estimate aLb. The index was calculated as K = W/aLb, where K is Le Cren's condition factor, W is the gutted weight (g), L is the total length (cm) and a and b are constants of the model (Le Cren, Reference Le Cren1951).
Gonad maturity, spawning time and fecundity
Sex was recorded for all specimens and the wet weight of the gonads and liver were obtained to the nearest 0.01 g. Monthly values of the gonadosomatic index (GSI), calculated as GSI = W gonad/W fish × 100, were obtained for both females and males (Avşar, Reference Avşar2005). In this equation, W gonad is gonad weight (g) and W fish is body weight (g). According to their macroscopic characteristics, the ovarian tissues of the fish were categorized as belonging to one of the following five maturity stages (Hostetter & Munroe, Reference Hostetter and Munroe1993): 5, spent; 4, spawning; 3, ripe; 2, developing; 1, resting. A total of 11 mature ovaries (4th stage) were used for evaluations of fecundity. Mature ovaries were placed in plastic cups of 50 ml and Gilson's fluid solution was added to cover the ovaries. Samples were then shaken at intervals for 15 days and the eggs separated from the membranes. Total fecundity was calculated according to Ismen (Reference Ismen1995) using log-transformed fecundity and length data as follows: Log(F) = a + b × log(TL), where a and b are the slope of the regression line, TL is total length (cm) and F is total fecundity.
Results
Composition by sex and sex ratio
A total of 384 grey wrasse (220 female and 164 male) were sampled between June 2015 and May 2016. Total length ranged between 8.2–16.4 cm (mean: 12.4 ± 0.06 cm) for all individuals; it was 10–16.4 cm (mean: 12.4 ± 0.10 cm) for male fish and 8.2–15.8 cm (mean: 12.46 ± 0.06 cm) for female fish (Figure 4). Total weight ranged between 8.51–77.49 g (mean: 35.28 ± 0.65 g) for all individuals; it was 15.54–77.49 g (mean: 35.57 ± 0.010 g) for males and 8.51–70.2 g (mean: 35.07 ± 0.086 g) for females. There were no significant differences in size frequency distributions between females and males (Kolmogorov–Smirnov two-sample test: d = 0.699, P < 0.001). The overall sex ratio (male:female) was 1.34:1, differing significantly from the expected value of 1:1 (χ2 = 8.167, P > 0.05) according to the results of the χ2 test. Numbers of S. cinereus specimens collected per month by sex are shown in Table 1. No female specimens were identified in December.
Length-frequency distribution by sex of Symphodus cinereus.
Number of specimens by sex and combined sexes collected per month of S. cinereus in the south-eastern Black Sea
Length-weight relationship (LWR)
The LWR was calculated for a total of 384 specimens including 220 females and 164 males. The exponent (b) of the LWR was estimated to be 3.1821 for females and 3.2596 for males. The parameters of the LWR for each sex are shown in Figure 2. The relationship for males was W = 0.009L3.2596 (r 2 = 0.9174, P < 0.005) and that for females was W = 0.0011L3.1821 (r 2 = 0.9012, P < 0.005).
According to Froese (Reference Froese2006), if b = 3, it demonstrates that the specimens have an isometric growth. If b > 3, fish are heavier and have positive allometric growth. If b < 3, fish are thinner with increasing length, showing a negative allometric growth. Both males and females showed positive allometric growth.
Age composition
Age determination was successfully accomplished for a total of 384 grey wrasse otoliths (164 male and 220 female specimens). Table 2 shows the age-length key for both females and males. Ages ranged between 0 and 5 for females and between 0 and 4 for males. It was concluded that the dominant age group was 2 years for females (34.54%) and 1 year for males (40.24%). In the samples, individuals were found to be mostly between 1 and 2 years of age for both females (68.63%) and males (68.29%) (Figure 5).
Age composition of males and females of Symphodus cinereus.
Age–length key of males and female of Symphodus cinereus in the south-eastern Black Sea
Growth model
With the von Bertalanffy growth model, the asymptotic length (L ∞) of males was found to be greater than that of females with estimated L ∞ values of 17.23 cm for males and 16.46 cm for females. On the other hand, the growth rate, k, of females was estimated to be higher than that of males. The k values were estimated as 0.296 year–1 for females and 0.272 year–1 for males. The growth performance index, Φ’, derived from the growth model was 1.37 for females and 2.67 for males. These results showed that male grey wrasses had better growth performance than females (Table 3).
Von Bertalanffy growth parameters and size of Symphodus cinereus in the south-eastern Black Sea
L ∞, asymptotic total length (cm); k, growth rate (year-1); Φ´, growth performance index.
Condition factor
Mean seasonal K values are shown in Figure 6 according to the sexes. While the highest condition (K) value was calculated in spring, the lowest value was determined in winter for both sexes. The highest mean K value in the spring was 1.06 for females, whereas it was calculated as 1.03 for males. The lowest mean K value in winter was determined as 0.98 for females and 0.93 for males.
Seasonal condition factor (K) values of all S. cinereus in south-east Black Sea.
Gonad maturity, spawning time and fecundity
Monthly fluctuations of the GSI for female, male and all sampled S. cinereus individuals are shown in Figure 7. The data revealed monthly changes in the GSI and maturity stages of male and female specimens, and the annual spawning season of this population began in March and ended in June. Stage 1 was observed between September and December for males, whereas stage 4 was seen between March and June for both sexes (Figures 8 and 9). The spent stage was observed for females between May and August. In males, the final stage was observed between June and September (Figure 8). Fecundity varied between 1375 and 5493 eggs/individual (mean: 2868.11 ± 36–59.69 eggs), and the relationship between egg production and total length was highly statistically significant (P < 0.0001) (Figure 10).
Monthly gonadosomatic index (GSI) of females, males and all individuals.
Percentage rates of monthly gonad stage (1, immature; 2, developing; 3, mature; 4, spawning; 5, spent) of males of Symphodus cinereus.
Percentage rates of monthly gonad stage (1, immature; 2, developing; 3, mature; 4, spawning; 5, spent) of females of Symphodus cinereus.
Fecundity and total length relationships of Symphodus cinereus in south-east Black Sea.
Discussion
Length-weight relationship (LWR)
In Table 4, the findings of other relevant studies in the literature are given. Altın et al. (Reference Altin, Ayyildiz, Kale and Alver2015) estimated LWR values from a wide range of lengths (1.5–15.8 cm); they reported the maximum length to be 15.8 cm. In the present study, on the other hand, an individual with a length of 16.4 cm was identified and the smallest obtained specimen was 8.2 cm. The b values in these previous studies are similar to the b value obtained in the present work. In addition, the values of the allometric coefficient ‘b’ found in our study agree with the expected range (2.5–3.5) reported by Froese (Reference Froese2006) for teleost fishes. Both in the literature and in this study, b values were calculated as b > 3, meaning that S. cinereus showed positive allometric growth in all studies. Factors such as feeding habits, maturity, health, habitat, season (Tesch, Reference Tesch and Ricker1968) and differences in the environment (Froese, Reference Froese2006) can affect LWR values.
LWR parameters for Symphodus cinereus estimated from other areas
Age and growth
The predicted age range in this study was up to 5 years for females and 4 years for males. According to Quignard & Pras (Reference Quignard, Pras, Whitehead, Bauchot, Hureau, Nielsen and Tortonese1986), 6 years was the maximum age, whereas it was 4 years in the lagoon of Thau (Quignard, Reference Quignard1966). According to Bach (Reference Bach1985), females reach 11.9 cm in total length and males reach 13.6 cm. In Tunisia, females reach a maximum age of 5 years at 10.8 cm in total length and males reach 6 years at 12 cm in total length (Ouannes Ghorbel & Bouain, 2001). Quignard (Reference Quignard1966) and Bach (Reference Bach1985) reported that males as well as females reached the age of 4 years with respective total lengths of 15 and 14 cm in the lagoon of Thau. These differences between ages are likely related to differences in the lengths of sampled fish. Fish growth rate potential of fish may also vary with the environment as a result of changes in food density and water temperature (Tyler, Reference Tyler1998). A limited number of studies have provided relevant sex-based data for this species, as shown in Table 5. In the present study, the L ∞ value of male individuals was higher than that of females. Pauly (Reference Pauly1978) and Ghorbel-Ouannes & Bouain (Reference Ghorbel-Ouannes and Bouain2001), however, estimated the L ∞ values of females to be higher than those of males along the Mediterranean. Ghorbel-Ouannes & Bouain (2001) and Quignard (Reference Quignard1966) reported that, at a given age, males are always larger than females. This may be due to differences in oxygen consumption and different rates of maintenance metabolism of the two sexes (Pauly, Reference Pauly1994; Landa et al., Reference Landa, Pérez and Pin˜eiro2002). In addition, the L ∞ values reported by other studies as shown in Table 5 were smaller than the values calculated in the present work. The k value found here was smaller than that estimated by Kalinina (Reference Kalinina1963), but it was similar to the values previously reported by Pauly (Reference Pauly1978) and Ghorbel-Ouannes & Bouain (Reference Ghorbel-Ouannes and Bouain2001). Considering the relationships that exist between the various parameters that constitute the growth equation together with their dependence on age, Zivkov et al. (Reference Zivkov, Trichkova and Raikova-Petrova1999) suggested that it would be more meaningful to use mean lengths in such comparisons. This is reflected in the larger length distribution obtained in the present study (Table 5). Similarly, k values are affected by the time period of sampling as well as the geographic region, and differences may be observed as a result of length and age distributions, as well as different biotic (e.g. presence of predators, prey availability or genetic variations) and abiotic factors (e.g. temperature, salinity levels or habitat structures) (Bilgin et al., Reference Bilgin, Taşçı and Bal2014). Among all studies of S. cinereus published to date in which the von Bertalanffy model was utilized in one of its possible forms, estimated values of t 0 have tended to be non-zero and negative (Table 5). This suggests that the von Bertalanffy model is not capable of providing accurate descriptions of growth for this species in the earliest stages of life (Pajuelo & Lorenzo, Reference Pajuelo and Lorenzo2011). Negative t 0 values are frequently observed for demersal fish species that experience rapid spurts of growth in the first year of life with slower rates of growth in subsequent years (Dwyer et al., Reference Dwyer, Stephen and Campana2003; Amaral & Cabral, Reference Amaral and Cabral2004; Teixeira et al., Reference Teixeira, Batista and Cabral2010). The growth performance index (Φ’) is applicable for the assessment of growth under a variety of environmental conditions (Pauly, Reference Pauly1991). The present results for Φ’ were comparatively higher than the values reported from previous research. Moreover, Ghorbel-Ouannes & Bouain (Reference Ghorbel-Ouannes and Bouain2001) found higher Φ’ values for male fish than females, similar to the present results, while Pauly (Reference Pauly1978) reported higher Φ’ values for females. Weatherley & Gill (Reference Weatherly and Gill1987) reported that water temperature had a direct effect on fish growth by affecting the physiology of fish.
Von Bertalanffy growth parameters of grey wrasse, Symphodus cinereus. L ∞, asymptotic total length (cm); K, growth rate (year−1); Φ´, growth performance index
Growth rates vary according to the season, annual variations in growth, environmental differences and species (Brandt et al., Reference Brandt, Mason and Patrick1992; Horne et al., Reference Horne, Jech and Brandt1996; Tyler & Brandt, Reference Tyler and Brandt2001). In addition, differences between studies might arise as a result of variations in the number of samples, the sampling period and the sampling method. It is also possible that different populations of the same species or individuals of the same population may show variations in different years due to different feeding conditions (Erkoyuncu, Reference Erkoyuncu1995).
Condition factor
The condition factors of fish vary depending on growth, reproduction and seasonal food availability (Weatherley & Gill, Reference Weatherly and Gill1987). A healthy population should have high growth and survival rates and display good reproductive potential (Vassilopoulou & Haralabous, Reference Vassilopoulou and Haralabous2008). Accordingly, condition factor analysis provides information about important ecological and physiological changes in fish populations (Vassilopoulou & Haralabous, Reference Vassilopoulou and Haralabous2008). In the present study, K values increased in spring and autumn in S. cinereus, while an opposite trend was observed in winter and summer. A decrease in K values was detected during the breeding season and in summer, and it increased again in autumn after breeding. Finding that the seasonal condition pattern in the populations of S. cinereus studied here matches with the general pattern in fishes (Le Cren, 1951; Froese, Reference Froese2006) creates an interesting contribution to broaden the knowledge of its biology. These results are generally consistent with the findings of previous studies in the literature, but no research has been conducted to date regarding K values of S. cinereus.
Gonad maturity, spawning time and fecundity
The external appearance of the gonads is usually used in studies of fish reproduction. This approach is quick, but it is also the least certain. It is necessary to use histological techniques for more detailed analyses (West, Reference West1990). García-Díaz et al. (Reference Garcıa-Dıaz, Tuset, Gonza´lez and Socorro1997) reported that macroscopic classification was more practical because of its ease of application despite the lower reliability of macroscopic examinations compared with histological examinations. In the present study, reproduction was evaluated with a macroscopic observation method.
The results obtained here revealed monthly variations in the GSI values and maturity stages of both male and female S. cinereus, and the annual spawning cycle of this species in the south-eastern Black Sea, off the coast of Rize, Turkey, was found to occur between March and June. Ghorbel-Ouannes et al. (Reference Ghorbel-Ouannes, Jarboui and Bouain2007) reported that gonad maturation begins in February and ends in June for this species in Tunisia. Differences in the timing of the spawning season may arise between different geographic locations as a result of variations in environmental factors, and particularly differences in temperature and salinity ranges (Zorica et al., Reference Zorica, Sinovčić and Keč2011).
In this study, 1375–5493 eggs were identified per individual (0.309–0.723 mm in diameter) for fish ranging from 10.2–14.1 cm in length and 21.7 to 35.72 g in weight. Ouannes-Ghorbel et al. (2007) reported total lengths between 7.8–10.5 cm, with egg counts of 4304–5089 eggs/individual from among mature oocytes (0.65–0.68 mm in diameter). The beginning and end of the spawning period may occur in different months for different populations because of different ecological and climate conditions (Nikolsky, Reference Nikolsky1980).
Conclusion
In the Black Sea, S. cinereus is not caught as a target species by fishermen. The current study has reported data on the spawning season, age and growth of this species and other factors that are essential for fishery management. Consequently, this study will serve as a source of baseline data on this fish species in the Black Sea and it should be helpful for the successful management of fisheries in the future. This study is the first detailed study of this species in the Black Sea.
Acknowledgements
I am pleased to thank Dr Semih Engin for his help to identifiy Symphodus cinereus. I also thank İbrahim Çolak (a fisherman in Rize), for his great help to provide fish samples every month during the study. This study was not supported by any funding.
Author contributions
Author HO designed the study, HO wrote the first draft of the manuscript, performed and managed statistical analyses.
Financial support
This study has no financial support.
Conflict of interest
No potential conflict of interest was reported by the author.
