Some morphometric features of congeneric pipefish species (Syngnathus abaster Risso 1826, Syngnathus acus Linnaeus, 1758) distributed in Lake Bafa (Turkey)

Pipefish are a member of the Syngnathidae family and an important component of the fish fauna, due to their tolerance to high temperature and salinity (Kornienko 2001; Hablützel, Wilson 2011) in estuarine areas and shallow coastal waters (Howard, Koehn 1985). Pipefish belong to the same family as seahorses and are widely used in many parts of the world, mainly in aquariums, ornamental items, and as a raw material in the traditional Chinese medicine in the Far East (Payne et al. 1998). Therefore, the species is threatened by excessive hunting and deterioration of their habitats. Syngnathus acus and Syngnathus abaster are among typical small and cryptic fish of epibenthic habitats with abundant vegetation (Kuiter 2000).

Syngnathus acus can be found in sandy-muddy and densely vegetated habitats of continental and estuarine areas (Dawson 1986), while S. abaster (an euryhaline form) occurs in similar habitats of the open sea, brackish and fresh waters (Movčan 1988; Kuiter 2001; Cakič et al. 2002; Hablützel, Wilson 2011). These species are included in the Least Concern (LC) category of the Red Data Book (IUCN 2016) and they are important ecological examples, because of their sex-role reversal, parental care, single or multiple spawning seasons (Franzoi et al. 1993; Taylan et al. 2018), in addition to habitat sharing with other pipefish species (Campolmi et al. 1996; Curtis, Vincent 2005; Malavasi et. 2007).

Morphometric characteristics are important details revealing the structure and properties of fish stocks (Turan 2004). The degree of morphological diversity at the species or population level is evaluated by referring to morpho-ecological results of studies relating to the genetic structure (Chan 2001; Cakič et al. 2002). Length-weight and length-length relationships are frequently used in ichthyological studies to analyze fish stocks (Ricker 1975). These parameters enable local and regional comparisons of populations and species.

Over the last decade, studies focusing on morphometric characteristics of pipefish have gathered momentum (Cakič et al. 2002; Mwale 2005; Gurkan 2008; Gurkan, Taşkavak 2012; Yildiz et al. 2015; Khrystenko et al. 2015). However, no studies have been found in relation to different coastal areas of Turkey, except for those carried out in the Aegean and Black Sea regions. The objective of this study was to determine the morphometric characteristics of the S. acus and S. abaster populations in Lake Bafa.

Lake Bafa is a natural barrier lake situated in the southeast region of the Büyük Menderes River delta, with an indented coastline. The sampling was carried out by seining in the coastal area of the Kapikiri region (37°30′N, 27°31′E-37°29′N, 27°31′E) of the lake at depths not exceeding 1–1.5 m (Fig. 1).

Figure 1

Pipefish samples were seasonally collected from the study area between November 2014 and March 2016 by seining in the coastal area at depths up to 1.5 m. Regulations of the ethical committee were followed during the capturing and processing of the fish species. The captured fish samples were transported to the laboratory in sealed vessels containing 70% ethanol. In the laboratory, total lengths of fish specimens (TL, mm) were measured using a measuring board, weights (W, g) were determined using a scale with 0.01 g sensitivity, and morphometric measurements were performed using a digital caliper with 0.001 mm sensitivity. Sexes of the pipefish specimens were macroscopically determined and the sex ratio of the captured species was calculated for the sampling area.

The total length-weight relationship of the samples was determined according to the procedure proposed by Ricker (1975). The length-weight relationship for the total body weight was calculated using the equation W = aL^b, where W is the weight (g), L is the length (TL, mm), a is the intercept, and b is the slope. The determination coefficient (R²) was used to calculate the degree of association between the variables. The parameters a and b were determined by linear regression on the (Log10) equation:

log(W)=log(a)+blog(L) $$\begin{array}{} \displaystyle log(W)=log(a)+b\,log(L) \end{array}$$

The significance of the regression was assessed by ANOVA, and the b value for each species was tested by t-test. Growth types were assigned to the values of b that are different from 3 (positive allometric if b > 3; negative allometric if b < 3; isometric if b = 3).

A total of 69 adult S. abaster and 107 adult S. acus samples were included in the analysis of morphometric characteristics. Immature individuals were ignored. The principles introduced by Cakič et al. (2002) were followed during the morphometric measurements. Moreover, the regression relationship (R²) of the transformation equations for morphometric characteristics and length was determined (Sokal, Rohlf 1981). The t-test was used to determine the morphometric relationships between the species. The statistical differences between the sexes were analyzed using the Chi-square test (χ²).

A total of 77 S. abaster (♀: 25; ♂: 44; immature: 8) and 134 S. acus (♀: 31; ♂: 76; immature: 27) samples were analyzed in the present study. The male-female ratios were 1:1.76 and 1:2.45, respectively. A difference was found between S. abaster (χ² = 65.757; p < 0.05) and S. acus (χ² = 116.213; p < 0.05). The total length values ranged from 55 mm to 130 mm (mean ± SD: 86.63 ± 16.77 mm) for S. abaster and from 54 mm to 125 mm (mean: 82.63 ± 16.02 mm) for S. acus. The total length-weight relationship in S. abaster and S. acus samples were calculated as follows: W = 0.00000001 TL^3.71 (R² = 0.89) (Fig. 2) and W = 0.000000007 TL^3.86 (R² = 0.85) (Fig. 3), respectively.

Figure 2

Figure 3

The relationships (linear regressions) were significant for both species (p < 0.05), with R² values greater than 0.95. The regression analysis showed that both S. abaster (mean: 3.408 ± 0.026; 95% CI) and S. acus (mean: 3.406 ± 0.028; 95% CI) had positive allometric growth.

In total, 69 adult S abaster and 107 adult S. acus samples were included in the analysis of morphometric characteristics. The results of comparative measurements of other body parts corresponding to the total length are shown in Table 1. According to the t-test results, the body depth – BD (t_0.05(206)) = 2.729 (p = 0.006), the mouth width – MW (t_0.05(210)) = 2.953 (p = 0.004) and the mouth height – MH (t_0.05(210)) = 2.652 (p = 0.008) were different among the morphometric characteristics of all samples from two species, which leads to the conclusion that the body depth of S. abaster was greater than that of S. acus and the mouth structure of S. abaster was bigger than that of S. acus.

Table 1

Morphometric features of S. abaster and S. acus occurring in Lake Bafa (M – mean; SD – standard deviation)

The regression analysis for S. abaster (Table 2) yielded the highest correlation (R² = 0.81) between the total length (TL) and the body depth (BD), while the lowest correlation (R² = 0.22) between the head length (HL) and the mouth height (MH). Therefore, the body depth explained closely the total length, but the increase in the head length (HL) could not be explained by its relationship with the mouth height (MH).

Table 2

Length-length relationship values for specimens of S. abaster and S. acus (CI – Confidence Intervals; F – observed)

In the case of S. acus, the highest correlation (R²) was determined between the total length (TL) and the head depth (HD), while the lowest one between the head length (HL) and the mouth width (MW). The correlation value suggests that the total length was explained by the head depth, as opposed to the relationship between the head length (HL) and the mouth width (MW), which fails to explain the evident increase in the head length.

Tables 3 and 4 show the comparison of the morphometric characteristics between the sexes. According to the t-test results, the difference between the body width of the sexes was statistically significant for both S. abaster (t_(0.05)(63) = 2.752; p = 0.008) and S. acus (t_(0.05)(91) = 2168; p=0.032).

Table 3

Morphometric features of sexes, Syngnathus abaster (N – sample size; M – mean; SD – standard deviation)

Table 4

Morphometric features of sexes, Syngnathus acus (N – sample size; M – mean; SD – standard deviation)

In this study, selected morphometric characteristics of S.abaster and S. acus species in Lake Bafa were investigated in relation to the species and the sex of the specimens examined. The male to female ratios for S.abaster and S. acus were determined as 1:1.76 and 1:2.45, respectively. The sex ratios were found to be higher than those reported in other studies (Vincent et al. 1995; Silva 2008; Gurkan et al. 2009). This may be due to the number of males and females carrying eggs, as well as the fact that females have a higher potential reproductive rate than males (Silva 2008).

Since the early 2000s, a growing number of studies have shown that the length and weight values of the pipefish species vary depending on the region of their distribution (Table 5). The results of this study were compared with the results obtained in the studies carried out in the last decade (Gurkan, Taskavak 2007; Gurkan, Çulha 2008; Veiga et al. 2009; Gurkan et al. 2010; Keskin, Gaygusuz 2010; Altin et al. 2015; Yildiz et al.2015; Khrystenko et al. 2015; Taylan et al. 2018). The minimum length values of S. acus occurring in Lake Bafa were higher than those reported in the studies by Gurkan & Taskavak (2007), Liousia et al. (2012), and Vieria et al. (2014) and lower than those reported by Altin et al. (2015) and Yildiz et al. (2015). Similar results were also observed for S. abaster. The minimum length values obtained in this study were higher than those obtained by Veiga et al. (2009), Gurkan et al. (2010), Keskin & Gaygusuz (2010), and Ben Amor et al. (2011), and lower than those obtained by Altin et al. (2015).

Table 5

Selected studies and their results on the two species from Turkey and other parts of the world

The species S. acus and S. abaster occurring in Lake Bafa showed positive allometric growth (b > 3). The total length-weight relationship revealed that the S. abaster samples from Lake Bafa showed a lower growth rate compared to the population in the Black Sea (Cakič et al. 2002) and a higher growth rate compared to the population in the Dnieper reservoir (Khrystenko et al. 2015). The length-weight relationship in the S. acus samples showed that the growth value of the samples was lower compared to that of the Aegean (Gurkan, Taskavak 2007) and Black Sea populations (Yildiz et al. 2015). The differences in the growth values are attributable to biotic and abiotic factors (Tesch 1971). The difference between the length-weight relationships is due to the regional and seasonal changes, the sampling type and time, physicochemical parameters, sex, habitat, reproduction time, and presence of nutrients in the environment (Tesch 1971).

The difference in the body depth is the most distinct morphometric difference between S. abaster and S. acus samples (p = 0.0056; p < 0.05) – S. abaster has a greater body depth compared to S. acus. According to Dawson (1986), the body depth is an important morphological characteristic in the identification of the pipefish species. This is also evident in the macroscopic identification of two species sharing the same habitat.

In S. abaster, a high correlation was determined for the morphometric characteristics denoted as TL/BD and TL/HL (R² > 0.78 and R² > 0.81, respectively; p < 0.05). Furthermore, there are studies arguing that some differences in morphometric characters are related to the head region of the fish (Cakič et al. 2002; Khrystenko et al. 2015). The differences in the head region are regarded as an adaptation to feeding in the habitat in which the species is found (Mitrofanov 1977). Syngnathid species feed on small planktonic and benthic prey items using their pipe-like mouth structure. This adaptation of the feeding apparatus in the mouth is specialized in catching the mobile prey (Franzoi et al. 1993; Kendrick, Hyndes 2005). The same specialization applies to the lotic systems (Khrystenko et al. 2015).

Among the morphometric characteristics of S. acus, TL/HD shows higher correlation (R² > 0.59; p < 0.05). In contrast with other species, morphometric characteristics of S. acus show higher correlation with the total length. For the S. acus populations in Europe and South Africa, Mwale (2005) and Yildiz et al. (2015) interpreted the same situation in a similar manner. According to Mwale (2005), differences in the body size of S. acus are an important source of morphological variation. It can therefore be argued that a difference in any of the morphological characteristics may lead researchers to the conclusion that species adapt to the habitat in which they live.

In both species, the differences between the sexes in terms of the body width are statistically significant (p < 0.05). Morphological differences between species are regarded as a phenotypic response to the habitat structure in which they live. According to Cakič et al. (2002), the morphological differences in S. abaster result from the aquatic system from which the species originates, whereas according to Khrystenko et al. (2015), S. abaster is more adapted to lotic ecosystems rather than lentic ones in terms of the manifested morphological differences. According to Silva (2008), females are bigger than males. This results mainly from the sexual dimorphism observed in S. abaster. The morphological difference between the sexes of S. acus in Lake Bafa can be examined from the same perspective. However, no morphometric differences between the sexes were reported in the study of the S. acus population from the Aegean Sea (Gurkan 2008). The morphometric differences between the sea populations and lake populations of S. acus were attributed to the aquatic ecosystem from which the species originates.

In conclusion, the two pipefish species occurring in Lake Bafa, S. abaster and S. acus, have a shorter head length and total length compared to their sea counterparts. To summarize, this study presents important morphological results, which can be used in the precise identification of the congeneric pipefish species occurring in the lacustrine environment. Therefore, the information presented in the study will contribute to other studies focusing on similar ecosystems.