Morphometric variation of Spicara flexuosum Rafinesque, 1810 (Teleostei: Sparidae) inhabiting the Sea of Marmara, the Aegean and the Mediterranean Coast of Türkiye

Black Sea and the Mediterranean fish resources are important bio reservoirs in the world. The Mediterranean Sea, considered to be one of the important semi-enclosed bodies of water, contains 4% of the marine fish species biodiversity of the world (Keskin et al. 2011). Considering Black Sea fauna, a total of 161 species was present in the Turkish Black Sea and approximately 62.73% of the fish species was of Atlanto-Mediterranean origin (Keskin 2010). Spicara spp. (picarels) are members of the Sparidae family groups and are small to medium-sized fish (Froese & Pauly 2022). These family groups are an essential component of the Mediterranean as well as the Black Sea bioresources. Spicara flexuosum is observed in the eastern Atlantic, Mediterranean, and Black Sea (Salekhova 1979, Tortonose 1986, Golani et al. 2006). Spicara flexuosum (Rafinesque, 1810) (previously known as Spicara flexuosa in the literature) is now genetically identified (Şalcıoğlu et al. 2021) and has been renamed S. flexuosum in the FishBase (Froese & Pauly 2022).

Variations in the growth and development of fish caused by environmental factors lead to differences in body shape even within the same genus and species (Mejri et al. 2012, Firmat et al. 2012). Species identification and differentiation and stock structure are useful for developing management strategies and will conserve biodiversity associated with species, subspecies, and stocks (Turan et al. 2005, Cadrin et al. 2014). Identifying the intra- and interspecific differences of fish by using morphometric traits with variable life history characteristics is quite important for understanding population dynamics and evaluating sustainable resources (Turan et al. 2005, Siddik et al. 2016).

The morphometric characters of fish species are influenced by genotype and environmental factors. Moreover, identification of stock with pronounced phenotypic and genetic differentiation among fish populations within a species serves to facilitate managing the stock separately, to determine stock-wise population abundance, and to accomplish the objectives of fisheries stock assessment by modelling (Rawat et al. 2017). Moreover, morphometric characters are considered to be phenetic characters (characters of adaptive variation) and habitat variables directly influence the phenotype of an organism (Vidalis et al. 1997, Bears et al. 2008, Pigliucci 2005). Intra-specific variation in fish morphology is quite an important concept for an understanding of the response of organisms to environmental challenges across fish populations (Shuai et al. 2018).

Morphometric analyses were previously available and used for inter- and intra-specific differentiation of fish species in the literature, such as Pomatomus saltatrix from the Aegean, Black Sea, and the Mediterranean (Turan et al. 2006) and the Sea of Marmara (Bal et al. 2021) and the three Scorpena species from the Aegean, Black, Mediterranean and the Marmara Sea (Yedier & Bostancı 2021). Different metric and meristic characters and their relative distributions were also observed for phylogenetic determination and taxonomy of freshwater fishes for Luciobarbus barbulus in the Persian Gulf Basin (Khaefi et al. 2017, Khaefi et al. 2018), three Gourami species in Indonesia (Perdana et al. 2021) and some marine fish species, such as Chromis chromis (Aydın & Öztürk 2021) Sciaena umbra (Aydın & Bodur 2021) in the Black Sea.

Meristic and morphometric studies were previously observed (Vasilieva & Salekhova 1983, Rizkalla 1996) in the literature about the species Spicara. Some studies were about biology, growth, nutrition (Soykan et al. 2010), while others involved length-weight relationships (İşmen et al. 2007, Soykan et al. 2010, Dalgıç et al. 2021, Şalcıoğlu & Sönmez 2022), the sexual dimorphism of Spicara flexuosum (Karadurmuş et al. 2022) and morphological identification of Spicara flexuosum and Spicara maena (Minos et al. 2013, Кuzminova & Мartemyanova 2020).

Some morphometric characters and population characteristics of Spicara flexuosum species were previously evaluated in the literature; however, none of the studies covered the intraspecific distribution of S. flexuosum species from coastal areas of Türkiye to identify morphometric characteristics of each stock in the five different locations (Istanbul, Yalova (Armutlu), Izmir, Mersin, and Antalya). This study aims to evaluate the morphometric data based on the distribution of S. flexuosum sampling from Turkish coastal waters for fisheries management purposes.

Descriptive statistics and relative distributions of all individuals with respect to some important morphometric traits are presented in Supplementary Table 1. Among all characters, the most variable characters are the head length (V.C = 17.7%), maximum body height one (V.C = 16.41%) and the eye diameter (V.C = 16.13%). The least variable characters are the standard length (V.C = 11.84 %) and the total length (V.C = 12.13%). Regarding the variation of the relative distribution of characters, the most variable ratio of the characters are HL/IO (V.C = 14.37%) and HL/ED (V.C = 13.56%) and the least variable ratio is TL/MBH1 (V.C = 7.27%). Among all characters and relative ratios of distributions, none of the results were highly variable, and these results were corroborated with each morphometric and distribution ratio character.

As stated in Supplementary Table 2, the correlation coefficients of HH/SL, HL/SL, MBH2/SL, TL/MBH1, HL/HH (> 0.700) are relatively high, and there is a strong positive relationship between the observed characters.

The mean total length of 116 specimens in this study was 14.22 ± 1.72 cm. Measurements of eight morphometric characters (Supplementary Table 3) and ratio of the some morphometric characters (Supplementary Table 4) were evaluated based on the five locations. As seen in the Supplementary Table 4, TL/MBH1 values from Izmir (4.15 cm), and Antalya (4.22 cm) were found to be greater than those in Istanbul, Yalova (Armutlu) and Mersin (3.74 – 3.93 cm), and HL/ED values from Istanbul (3.20 cm) and Yalova (Armutlu) (3.67 cm) were found to be greater than those in the Izmir, Mersin and Antalya (2.92 – 3.10 cm) populations.

3.1.

Multivariate and cluster analyses

All morphometric characters showed normality (p > 0.05) based on the Kolmogorov-Smirnov test and homogeneous variance (p > 0.05) by the Levene test. Multivariate principal components and cluster analyses were evaluated based on the eight morphometric traits and the relative ratio of some morphometric traits. Considering all morphometric characters and five location groups, significant differences were observed among all S. flexuosum populations (One–Way ANOVA, F = 276.9; p = 8.977 × 10⁻²⁷). However, significant differences were not observed between sexes (MANOVA, p = 0.234). Principal component and cluster analyses were conducted by evaluating the data of male and female individuals together.

Principal component analyses of the eight morphometric traits were 80.001% for (PCA1), 18.044% for (PCA2), 1.8096% for (PCA3) and 0.14582% for (PCA4), which resulted in 100% of the total variation. All Eigen values were positive and all of these variables have influenced the morphological variation of S. flexuosum (Table 2). Principal component loadings were evaluated based on the cut-off value of 0.3 (positive or negative) (Snoeks 2004). The highest loading characters were the head length and maximum body height 1 for PCA 1, eye diameter and interorbital distance for PCA 2, interorbital distance and maximum body height 2 and head length for PCA 3, and head height and head length for PCA 4 (Table 2).

Table 2

Principal component loadings scores, Eigen values and variance based on eight morphometric traits

	PC1	PC2	PC3	PC4
Eigenvalues	0.018318	0,00413467	0.00041466	0.00034135
Variance (%)	80.001	18.044	1.8096	0.14582
Character
HL	0.47363	0.20971	−0.54221	−0.54121
HH	0.42562	−0.095071	−0.19134	0.44293
MBH1	0.44763	−0.33877	0.22099	−0.36621
MBH2	0.38956	−0.34459	0.47519	−0.058186
SL	−7.2803E-17	5.8203E-16	−5.503E-15	5.352E-15
TL	0.32853	−0.21941	−0.22798	0.58388
ED	0.2943	0.65851	0.00334703	0.17156
IO	0.21877	0.48136	0.58547	0.055326

Principal component analyses of the relative ratio of some morphometric traits were evaluated based on the previous study for Spicara species from Minos et al. (2013) and on the results from the first principal component analysis. The principal component ratio of the morphometric traits exhibited 60.101% for (PCA 1), 28.198% for (PCA 2), 8.7805% for (PCA 3) and 2.9201% for (PCA 4) resulting in 100% of the total variation (Table 3). The most important morphometric loading characters were HL/IO and HL/ED for PCA 1, MBH2/HH and HL/IO for PCA 2, HL/ED and HH/HL for PCA 3, and HH/SL, HL/SL and TL/MBH1 for PCA 4 (Table 3). The forth principal component loadings (PCA 4) represented allometric size factor and were eliminated. HL/IO, HL/ED, MBH2/HH and HH/HL were then used for intraspecies discrimination of each groups. The classification matrix based on the discriminant function analysis showed that 94.7% of the original group were correctly classified (Table 4).

Table 3

Principal component loadings scores, Eigen values and variance based on the relative ratio of each morphometric trait

	PC1	PC2	PC3	PC4
Eigenvalues	0.00373899	0.00175425	0.00546240	0.000181664
Variance (%)	60.101	28.198	8.7805	2.9201
Character
HL/SL	−0.063376	0.016927	0.050071	0.3927
HH/SL	0.21956	−0.090208	−0.21436	0.39744
HH/HL	0.1363	0.28853	0.55127	0.23751
MBH2/SL	0.027696	0.22781	−0.13991	0.24869
TL/MBH1	−0.25438	−0.2234	0.3019	−0.60892
HL/ED	0.54835	0.039031	0.60801	−0.030984
MBH2/HH	0.2144	0.81048	−0.27264	−0.38802
HL/IO	0.71907	−0.38488	−0.30481	−0.21743

Table 4

Classification matrix (percentage) based on the discriminant function analysis of five S. flexuosum populations from Turkish coastal waters

Population	Predicted group membership
	Istanbul	Yalova	Mersin	Izmir	Antalya
Istanbul	100	-	-	-	-
Yalova	-	96.2	-	-	-
Mersin	-	-	99.0		-
Izmir	-	3.8	-	100	3.5
Antalya	-	-	1.00	-	96.5

Hierarchical clustering analyses based on the eight morphometric characters with Euclidean distance method indicated that (Fig. 3), [Izmir, Mersin, Antalya]; and [Istanbul, Yalova] populations were clustered around each other. This result was also supported by the Principal Component Analysis (Fig. 4). The minimum Euclidian distance was found between Mersin-Izmir populations.

Figure 3

Figure 4

Morphometric characters of fish species are an important resource to measure and distinguish the intraspecific variation of different stocks (Turan et al. 2005, Cadrin et al. 2014). In this study, the intraspecific discrimination of Spicara flexuosum inhabiting the Istanbul, Yalova (Armutlu), Izmir, Mersin and Antalya populations was performed based on the PCA and cluster-based morphometric results.

Considering measurements of the mean total length values of S. flexuosum, all individuals within the range of length group 11.04 to 17.27 cm similar to other studies of S. flexuosum from France (14 cm), (Bauchot 1987); Izmir Bay (Türkiye) (9.20 – 15.5 cm) (Mater et al. 2001); Portugal (10 – 19.2 cm) (Borges et al. 2003); and Crimea in the Black Sea (7.1 – 19.2 cm) (Melnikova & Kuzminova 2022) and Ordu in the Black Sea (11.5 – 23.5 cm) (Karadurmuş et al. (2022). Parameters of the morphometric regression revealed that correlation coefficient values (R²) of the TL/MBH1 are found to be greater than 0.800, similar to the findings in the study of S. flexuosom in Egyptian coastal waters (Rizkalla 1996) (BD/TL) > 0.900. Similar to this study, significant correlation of the morphological data was also found between the standard length and body depth of Spicara flexuosum in Turan (2011).

Descriptive statistics and variation coefficient of each morphometric character of S. flexuosum showed that most variable characters are the head length, maximum body height one and the eye diameter. Karadurmuş et al. (2022) investigated sexual dimorphism and some morphometric characters of S. flexuosum along the coast of the Black Sea. It was found that eye diameter (V.C. 9.17% for females and V.C. 6.17% for males) was the most variable character for both females and males, similar to the results in the current study (V.C. 16.13%). However unlike the results of the current study of the variation of the head length (V.C 17.7%), little variation was observed of the head length of Spicara flexuosum specimens in the Black Sea region (Karadurmuş et al. 2022) for males (V.C 2.62%) and females (V.C. 3.20%). This result could be related to the different sampling locations and the time of the sampling. Head- and eye-related morphological differences have been previously observed according to habitat differences (physical characteristics of each habitat, e.g. water temperature, current, also chemical characteristics, e.g. O₂, water clarity (Shuai et al. 2018) and also by feeding behaviour and diet conditions between different fish populations from the Eastern Atlantic and the Mediterranean (Palma & Andrade 2002). Different head morphology exhibited by different populations of the same species indicated the utilisation of different ecological niches (Hyndes et al. 1997). According to Chiba et al. (2009), many morphological characters were evolved in Sparidae family members as a result of adaptive radiation of various habitats, and this concept was important the evolution and distribution of Sparid members, including Spicara species. Several studies from the literature revealed that eye diameter, head length and body depth characteristics were the most variable characteristics and distinctions of fish stocks both among Spicara maena and S. flexuosum (Кuzminova & Мartemyanova 2020) Scorpaena spp. (Yedier and Bostancı 2021), Sparids (Palma & Andrade 2002, Delariva & Agostinho 2001) and intraspecific variation of fish species Pomatomus saltatrix (Bal et al. 2021), African freshwater fish (Turan et al. 2005), and European anchovy (Khan et al. 2022).

The results from this study indicated that the most important ratio of the morphometric characters from PCA were HL/IO and HL/ED for PCA 1, MBH2/HH and HL/IO for PCA 2, and HL/ED and HH/HL for PCA 3. Similar to Minos et al. (2013), no significant morphometric differences results were observed between the sexes of the same species in this study. Similar to current study result, HH/HL was also found to be an informative characteristic for interspecies discrimination of two species of Spicara (Spicara maena and Spicara flexuosa) as previously stated by Minos et al. (2013) and Кuzminova & Мartemyanova (2020). HL, ED, IO, MBH1 and MBH2 values were also found to be informative characteristics of different stocks of Spicara smaris whose populations absent from significant gender differences in the North Aegean Sea (Vidalis et al. 1997).

Finally, current results from morphometric analysis indicate the existence of two morphologically differentiated groups of Spicara flexuosum. First group composed of Istanbul and Yalova (from Marmara Sea) and the second one consisted of Izmir, Mersin and Antalya (Aegean and Mediterranean Sea) populations whose distances were almost proportional to the geographical distances between the sampling localities. Thus, the results obtained from this study could be related to the differences in the environmental conditions, such as temperature, pH, turbidity, habitat (Wimberger 1992, Turan et al. 2005, Crow et al. 2007, Shuai et al. 2018) spawning sites, and homing behaviour (Danancher & Garcia-Vazquez 2011), as previously observed in the literature.

The Turkish Strait System, specifically the Dardanelles Strait, could have been instrumental in the observed differentiation. Significant hydrographical differences, in particular physical barriers (currents, water velocity and temperature) (Zheng et al. 2001, Shuai et al. 2018) between the Marmara, the Aegean and the Eastern Mediterranean seas could have an influence on the morphological variation and distribution of this fish species. Overall, fish functional morphological traits were understood to be influenced by physical properties of water, such as flow and temperature within fresh water (Chapman et al. 2015, Shuai et al. 2018) and salinity differences among marine water habitat (Winans 1984, Vidalis et al. 1997, Erdoğan et al. 2009). The spatial distribution of fish species was previously investigated in different fish species populations in three different seas in Turkish coastal waters, and most of the studies reported that species from the Black Sea populations were separated from the Marmara, Aegean and the Mediterranean Sea (Turan et al. 2006, Yedier & Bostancı 2021, Bal et al. 2021).

The results from this study indicated that Izmir, Mersin, Antalya on the one hand; and Istanbul, Yalova populations on the other, were clustered and more closely related to each other. Geographical isolation of each sub group from the Marmara (Istanbul, Yalova), the Aegean (Izmir) and the Mediterranean (Mersin, Antalya) was also observed among these samples within the morphometric results. As a result of this, these populations might be considered as separate stocks for fisheries management purposes. Regarding morphometric characteristics, the head length, eye diameter, and interorbital distance were determined to be promising tools for the population structure of S. flexuosum (both female and male individuals) along the Turkish coast. Further morphometric traits related to the tail and the caudal peduncle should be necessary tools for morphometric studies for the fisheries management purposes for this genus.