Turkish Journal of Zoology Turk J Zool (2015) 39: 917-924 http://journals.tubitak.gov.tr/zoology/ © TÜBİTAK Research Article doi:10.3906/zoo-1408-57

Preliminary report of a biometric analysis of greater pipefish Syngnathus acus Linnaeus, 1758 for the western Black Sea

Taner YILDIZ*, Uğur UZER, Firdes Saadet KARAKULAK Department of Fisheries Technology, Faculty of Fisheries, İstanbul University, Laleli, İstanbul, Turkey

Received: 22.08.2014 Accepted/Published Online: 27.02.2015 Printed: 30.09.2015

Abstract: The main objective of this study was to analyze the differences and similarities in morphometric characteristics among specimens of greater pipefishSyngnathus acus Linnaeus, 1758 that were collected and described based on data from bottom-trawl surveys and commercial trawl fisheries in the western Black Sea between September 2010 and October 2011. A total of 280 specimens were analyzed, of which 191 were female and 89 were male. Female individuals ranged from 15.6 to 33.8 cm in total length, whereas male individuals ranged from 16.6 to 39.2 cm. For the biometric analysis, 14 morphometric characteristics were analyzed. The females and males were found to differ in maximum body height, maximum body width, and head length (P < 0.05). The length–length equations for overall converted body lengths of fish were linear. The morphometric characteristics were strongly positively correlated except for head length / total length and snout width / head length (P < 0.05). The length–weight relationship of this species was described by the following equation: TW (g) = 0.0001 × TL3.415 (cm). Relationships between the characteristics were defined separately for both sexes.

Key words: Biometry, length–length, greater pipefish, Syngnathus acus, western Black Sea

1. Introduction and are a common bycatch. This species is not of concern Morphometric and meristic features are used primarily on the IUCN Red List presently, but it is likely to become to study relationships among stocks, such as stock endangered in the future. membership, the spatial distribution of stocks, and the Although a few ichthyological studies have focused phylogeny of stocks (Coyle, 1997; Turan, 2004). According on pipefish morphometrics (Cakić et al., 2002; Mwale, to Begg et al. (1999), phenotypic markers may be more 2005; Gürkan, 2008; Gürkan and Taşkavak, 2012), there applicable for studying short-term, environmentally is currently no information on the greater pipefish’s (S. induced variation, which is perhaps more applicable for acus) morphological structure in the Turkish waters of fisheries management. Ibanez-Aguirre et al. (2006) also the Black Sea. The purpose of this study was to analyze noted that it is of vital importance to identify the study morphological variation of S. acus among different population to understand its dynamics. locations along the western Black Sea coasts of Turkey. There are 300 species of pipefishes in 35 genera, and their taxonomy is in urgent need of revision (www. 2. Materials and methods zoonetics.com). The Mediterranean basin has 9 species A total of 280 individuals of S. acus were collected from that belong to the genus Syngnathus (Dawson, 1986); 6 bottom-trawl surveys and commercial bottom-trawl species are distributed in the Black Sea (Bilecenoğlu et catches in the western Black Sea. Surveys were carried al., 2002; Gürkan and Çulha, 2008). Syngnathus acus can out in 2 different seasons (spring and autumn) and at 3 be found in coastal and estuarine waters to depths of 90 locations. In total, 39 stations were sampled between m or more on sandy, muddy, and rough bottoms; it is September 2010 and October 2011. Specimens were relatively common among algal and eelgrass habitats captured using a 20-mm stretch cod-end mesh size, at (Dawson, 1986). Pipefishes, like most other syngnathids, a depth of 10–100 m. The study area was divided into 3 are characterized by restricted distributions, low mobility, sublocations considering local differences (Figure 1). small home ranges, and low fecundity (Vincent, 1996). The body parts were measured following standard Although they have no commercial importance in fisheries, anatomical landmarks (Cakić et al., 2002; Gürkan, they are threatened by incidental capture in fishing gears 2008). The landmarks include the following: total length

* Correspondence: [email protected] 917 YILDIZ et al. / Turk J Zool

Figure 1. Sampling stations.

(TL), total weight (TW), maximum body height (BH), 0.01 millimeter) on the right side of the pipefish. The maximum body width (BW), length of pectoral fin (PFL), specimens were weighed using a digital balance to the length of dorsal fin base (DFL), height of dorsal fin (HD), nearest 0.01 g. The sex of the specimens could easily be head length (HL), occipital height of head (OHH), mouth determined macroscopically. height (MH), mouth width (MW), eye diameter (ED), A linear regression of various body parts against the snout length (SL), snout depth (SD), and snout width total length and head length was carried out using the (SW). The 14 morphometric characteristics are explained least-squares method. Thorpe (1976) noted that only in Figure 2. To ensure standardization, all measurements morphometric data could be statistically adjusted to were performed by the same person using calipers (nearest permit the comparative analysis of shape independent of

Figure 2. Diagram of morphometric measurements of pipefishes.

918 YILDIZ et al. / Turk J Zool size in variations in the size of fish from different locations. BW, PFL, DFL, HD, and HL relative to the TL, and the Thus, to minimize the influence of size differences on OHH, MH, MW, ED, SW, SL, and SD relative to the HL the subsequent results, the original measurements of (Table 1). The coefficients of variation (CVs) indicated the morphometric characteristics were standardized. Six highest variability in the SW / HL ratio (CV = 23.0% for morphometric characteristics were expressed as % TL males, 20.1% for females), whereas the lowest variability and 7 as % HL. This technique is commonly used in was noted in the HL / TL ratio (CV = 7.2% for male, 6.8% ichthyological studies. Morphometric characteristics were for female). Differences between females and males were analyzed by ANOVA followed by Holm–Bonferroni’s post found in the maximum body height, maximum body hoc test (Sokal and Rohlf, 1981) for all possible pairwise width, and head length as a result of Bonferroni’s test (P comparisons from different locations and between sexes. < 0.05). The length–weight relationship was calculated with the The comparisons of the morphometric characteristics equation W = aLb, where W is the weight (g), L is the total of S. acus between different locations are given in Table length (cm), a is the intercept, and b is the slope (Ricker, 2. There were significant differences in 10 morphometric 1975). Lengths and weights were log-transformed, and the characteristics (Holm–Bonferroni’s test). The specimens resulting linear relationship was fitted by the least-squares of location 1 were morphologically different from the regression. To ensure the quality of the linear regression, individuals of location 2 in the BH, BW, PFL, DFL, MH, the coefficient of determination (r2) was used. Data were and SW characters. The specimens of location 1 were analyzed using SPSS 16.0. morphologically different from the individuals of location 3 in the BW, PFL, OHH, SD, SL, and SW characters. The 3. Results specimens of location 2 were morphologically different Of the 280 specimens, 191 were females (68.2%) and from the individuals of location 3 in the HL, OHH, SD, SL, 89 were males (31.8%). The lengths and weights of S. and SW characters. acus ranged from 156 to 392 mm and from 1 to 16.66 The estimated parameters of the length–length g, respectively. The morphology of the sampled fish was relationships as well as the coefficients of correlation (r) described as the relative body proportions of the BH, are presented in Table 3. The morphometric characteristics

Table 1. Morphometric characteristics of S. acus caught in the western Black Sea during the period from September 2010 to October 2011.

Morphometric Females Males characters Min. Max. Mean ± SD Min. Max. Mean ± SD P TL (mm) 156 338 270.59 ± 29.45 166 392 264.06 ± 29.42 0.055 % TL BH 1.24 4.65 3.37 ± 0.51 1.91 4.44 2.80 ± 0.46 0.000* BW 1.63 3.86 3.01 ± 0.43 1.49 3.76 2.68 ± 0.39 0.000* PFL 0.97 2.53 1.80 ± 0.33 1.01 2.67 1.78 ± 0.30 0.545 DFL 6.48 14.76 10.53 ± 1.12 6.15 12.83 10.50 ± 1.26 0.832 HD 1.19 3.46 2.58 ± 0.43 1.29 3.58 2.63 ± 0.47 0.408 HL 12.87 19.09 15.69 ± 1.07 10.10 18.37 15.06 ± 1.09 0.000* % HL OHH 11.83 30.42 16.52 ± 2.30 12.13 24.32 16.78 ± 2.02 0.412 MH 6.60 14.46 8.98 ± 1.36 5.49 12.58 9.24 ± 1.27 0.099 MW 2.25 5.04 3.43 ± 0.56 1.71 4.99 3.51 ± 0.64 0.296 ED 5.45 16.19 9.25 ± 1.69 6.78 14.06 9.61 ± 1.66 0.095 SW 1.85 5.03 3.23 ± 0.65 1.68 5.48 3.26 ± 0.75 0.129 SL 40.53 73.63 55.99 ± 5.40 43.01 68.24 54.56 ± 5.27 0.193 SD 4.19 11.91 6.55 ± 0.90 4.68 10.97 6.69 ± 0.90 0.238

*Significantly different at P < 0.05.

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Table 2. Holm–Bonferroni’s post hoc test for all possible pairwise comparisons of the morphometric characteristics of S. acus from different locations.

Body height (BH) Body width (BW) 1 2 3 1 2 3 1 — 0.000* 0.057 — 0.000* 0.006* 2 0.000* — 0.140 0.000* — 0.066 3 0.057 0.140 — 0.006* 0.066 — Head length (HL) Pectoral fin length (PFL) 1 2 3 1 2 3 1 — 1.000 0.085 — 0.001* 0.005* 2 1.000 — 0.011* 0.001* — 0.828 3 0.085 0.011* — 0.005* 0.828 — Dorsal fin length (DFL) Occipital height of head (OHH) 1 2 3 1 2 3 1 — 0.029* 0.107 — 1.000 0.000* 2 0.029* — 1.000 1.000 — 0.000* 3 0.107 1.000 — 0.000* 0.000* — Snout depth (SD) Mouth height (MH) 1 2 3 1 2 3 1 — 0.235 0.024* — 0.000* 0.570 2 0.235 — 0.000* 0.000* — 0.246 3 0.024* 0.000* — 0.570 0.240 — Snout length (SL) Snout width (SW) 1 2 3 1 2 3 1 — 0.231 0.000* — 0.000* 0.000* 2 0.231 — 0.005* 0.000* — 0.000* 3 0.000* 0.005* — 0.000* 0.000* —

*Significantly different at P < 0.05. were strongly positively correlated except for HL / TL and TW = 0.0001TL3.415 (r2 = 0.898, n = 280). The slope of the SW / HL (P < 0.05). The best fit for the length–length regression line was significantly different from 3.00, thus relationships was recorded between BH and TL (r = 0.440). indicating allometric growth (P < 0.05). The equation for The lowest correlation coefficient value was found between female individuals is TW = 0.00006TL3.553 (r2 = 0.911, n = MW and HL (r = 0.093). 191) and the equation for male individuals is The relationship between total length (cm) and total TW = 0.0002TL3.154 (r2 = 0.882, n = 89). weight (g) was highly significant (P < 0.001) (Figure 3). Positive allometric growth was observed for all sexes. 4. Discussion There were no significant differences (P > 0.05) between The TL–TW relationship of S. acus in the western Black Sea the slopes (b) of the TL–TW relationship for females displayed positive allometry. The parameters of the TL– and males as a result of ANOVA; thus, the TL–TW TW relationship of this study and previous studies’ results relationship with the sexes combined was expressed as are indicated in Table 4. TL–TW relationship parameters

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Table 3. Length–length relationships for S. acus in the western Black Sea.

y variable x variable R intercept slope 95% Clslope F ln (102 × HL / TL) ln TL 0.025 14.109 0.016 –0.0215 to 0.0545 0.181 ln (102 × BH / TL) ln TL 0.440 0.065 0.693 0.608 to 0.778 66.813* ln (102 × BW / TL) ln TL 0.370 0.176 0.500 0.425 to 0.575 44.067* ln (102 × PFL / TL) ln TL 0.233 0.214 0.378 0.283 to 0.473 15.948* ln (102 × DFL / TL) ln TL 0.114 5.420 0.118 0.057 to 0.179 3.681* ln (102 × HD / TL) ln TL 0.276 0.209 0.448 0.354 to 0.542 22.908* ln (102 × OHH / HL) ln HL 0.255 38.549 –0.229 –0.281 to –0.177 19.350* ln (102 × MH / HL) ln HL 0.263 24.463 –0.270 –0.329 to –0.211 20.662* ln (102 × MW / HL) ln HL 0.093 2.235 0.113 0.040 to 0.186 2.401* ln (10 2× ED / HL) ln HL 0.196 23.155 –0.248 –0.322 to –0.174 11.140* ln (102 × SW / HL) ln HL 0.004 3.097 0.006 –0.092 to 0.104 0.004 ln (102 × SL / HL) ln HL 0.136 81.780 –0.105 –0.151 to –0.059 5.162* ln (102 × SD / HL) ln HL 0.291 17.557 –0.266 –0.318 to -0.214 25.694*

*Significantly different at P < 0.05.

30 In this study, we found the morphometric 25 characteristics were strongly positively correlated, with y = 0.0001x 3.4152 the exception of HL / TL and SW / HL (P < 0.05). Mwale 20 R² = 0.8981 (2005) indicated that the morphological characters were 2 15 positively correlated to standard length (r > 70%) for the

TW (g) European and South African S. acus populations. 10 Syngnathid species consume mainly planktonic and 5 benthic crustaceans (Brook, 1977; Bell and Harmelin- Vivien, 1983; Franzoi et al., 1993; Vizzini and Mazzola, 0 10 15 20 25 30 35 40 45 2004). Kendrick and Hyndes (2005) reported that TL (cm) syngnathid species with long snouts (>0.5 mm of the head Figure 3. Length–weight relationship of S. acus from catches in length) tend to consume relatively mobile prey, whereas the western Black Sea. species with short snouts feed more commonly on less mobile prey, such as amphipods, harpacticoid copepods, and polychaetes. Moreover, for the southwestern from the Black Sea, eastern Mediterranean Sea (Koutrakis Australian population, the snout length is 0.43–0.59 times and Tsikliras, 2003; Gürkan and Taşkavak, 2007; Gürkan greater than the head length (Kendrick and Hyndes, 2005). et al., 2010), central Mediterranean Sea (Dulčić and The results of the present study confirm this proportion Glamuzina, 2006), and Arade Estuary (Portugal) (Veiga et (0.51–0.57 times the HL). In addition, S. acus ingests al., 2009) show that there is no significant difference (P > harpacticoid copepods in the shallow waters of the Black 0.05). However, we found that the TL–TW relationships Sea; in particular, Euterpina acutifrons was the dominant are significantly different (P < 0.05) in the Black Sea, South prey item (Gürkan and Aydın-Uncumusaoğlu, 2012). Africa (Harrison, 2001), and the western Mediterranean According to Gürkan (2008), for S. acus in the (Valle et al., 2003). These observed differences could be eastern Mediterranean Sea measuring 6.1–25.6 cm TL, due to the sampling procedure, seasonal and regional the females and males of this species do not differ in their effects, changes in water temperature, salinity, sex, depth, morphometric characteristics. However, morphological breeding season, and food availability (Tesch, 1971; variation was found between the sexes of Syngnathus Wootton, 1992). typhle and Nerophis ophidian. Cakić et al. (2002) found

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Table 4. Comparison of relationships between the length and weight of S. acus from various regions of the Atlantic and Mediterranean.

Length Length range N a b r2 Region Reference type (cm)

SL 225 11.0–29.3 0.00072 2.883 0.958 Spain Valle et al. (2003)

SL 133 4.6–21.6 0.00038 3.074 0.961 South Africa Harrison (2001)

TL 22 7.6–13.9 0.00040 3.122 0.958 Croatia Dulčić and Glamuzina (2006)

TL - 7.1–34.6 0.00020 3.330 0.989 Arade Estuary, Portugal Veiga et al. (2009)

TL 5 8.3–12.4 0.0001 3.729 0.958 North Aegean Sea, Greece Koutrakis and Tsikliras (2003)

TL 570 3.3–25.6 0.00021 3.540 0.951 Aegean Sea, Turkey Gürkan and Taşkavak (2007)

TL 77 5.4–21.2 0.0003 3.256 0.912 North Aegean Sea, Turkey Gürkan et al. (2010)

TL 280 15.6–39.2 0.0001 3.415 0.898 Western Black Sea, Turkey In this study

Table 5. Morphometric characteristics (mm) among the European and Black Sea S. acus populations groups.

Character Source N Mean Min. Max. Std. dev. 1 84 34.0 10.1 58.0 12.22 Head length (HL) 2 280 41.5 18.9 53.9 5.44 1 84 19.6 4.7 32.9 7.67 Snout length (SL) 2 280 23.1 13.1 31.0 3.31 1 84 2.9 0.8 4.9 0.89 Snout depth (SD) 2 280 2.7 1.7 4.1 0.44 1 84 3.9 1.3 6.4 1.18 Eye diameter (ED) 2 280 3.9 1.3 5.5 0.72 1 84 29.3 8.1 58.9 11.8 Dorsal fin base (DFL) 2 280 28.3 13.9 43.7 4.62

Source: 1 = Mwale (2005), 2 = present study. significant differences in 16 out of the 18 morphometric morphological variation are differences in both the abiotic characteristics among Syngnathus abaster caught in the and biotic habitat characteristics such as temperature, Danube River (Yugoslav region), Black Sea, and Azov Sea. salinity, water depth, direction of ocean currents, substrates, Movčan (1988) reported that differences in 5 out of 10 and vegetation types (Wiens, 2001). Geographical distance morphometric characteristics, mainly related to the head is important in variation because it has a great influence on length, were observed in S. abaster caught in the Black Sea species dispersal and therefore on gene flow and population and Azov Sea. This study demonstrates the existence of mixing (Gill and Kemp, 2002). The locations of this study morphometric variations between sexes and locations in were geographically close but significantly different from S. acus in the western Black Sea. each other in several characteristics. The İstanbul Strait The variation of morphometric characteristics in acts as a biological barrier limiting the distribution of specimens from different geographical populations could certain species of both Mediterranean and Black Sea origin be caused by differences in the genetic structure or the (Öztürk and Öztürk, 1996). The main currents in the aquatic ecosystems from which they originated (Movčan, Black Sea have a circular character and an anticlockwise 1988; Cakić et al., 2002; Mwale, 2005). The major direction (cyclonic currents). There are small circulations environmental variables responsible for distribution and in the waters, but the circulations are of an anticyclonic

922 YILDIZ et al. / Turk J Zool character (clockwise) in the coastal zones (Zaitsev, 2008). was noted (www.zoonetics.com) that South African and The Bosphorus eddy (in location 1) and Sakarya eddy (in European populations were morphologically different and location 3) are anticyclonic currents and influence the that segregation by visually comparing their appearance randomized distribution of eggs and population mixing. was possible, as one species was larger and had an angled In addition, the Sakarya River discharges into the Black head. It has repeatedly been shown that fish morphology Sea in the town of Karasu, which changes the salinity in is affected by environmental factors like diet, habitat, and location 3. predation risk (Pakkasmaa and Piironen, 2000; Kendrick The biometric characteristics of European and Black and Hyndes, 2005; Eklöv and Svanbäck, 2006; Costa and Sea S. acus population groups are given in Table 5. The Cataudella, 2007). results of our research on S. acus in the western Black Morphometric measurements are widely used to Sea indicate that HL and SL are relatively greater than identify differences between fish populations (Petrakis in European populations. Mwale (2005) compared the and Stergiou, 1995; Tzeng, 2004; Cheng et al., 2005; Buj et biometric characteristics of North Atlantic, South African, al., 2008; Torres et al., 2010). In addition, morphometric and European S. acus populations and found that no single studies are essential to understand species variations in characteristic could reliably separate the North Atlantic features, which are most likely related to habitat differences and South African populations. The overlap in range (Cavalcanti et al., 1999). For the western Black Sea, the values that we observed is normal among syngnathids biometric results in this paper are preliminary, and our (Herald, 1965; Fritzsche, 1980) and 2 groups that are results should be verified in future genetic studies. closely related or living in similar habitats. In addition, S. acus specimens from Europe differ from the South Acknowledgment African specimens, as they have on average more dorsal This study was supported by the Scientific Research fin rays, trunk and tail rings, and subdorsal rings. Meristic Projects Coordination Unit of İstanbul University with 2 characteristics were more effective than morphometric projects (Project Numbers: 4231 and 5381). characteristics in separating the S. acus populations. It

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