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Turkish Journal of Zoology Turk J Zool(2015) 39: 917-924© TÜBİTAKdoi:10.3906/zoo-1408-57

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

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

* Correspondence: yldztnr@istanbul.edu.tr

1. IntroductionMorphometric and meristic features are used primarily to study relationships among stocks, such as stock membership, the spatial distribution of stocks, and the phylogeny of stocks (Coyle, 1997; Turan, 2004). According to Begg et al. (1999), phenotypic markers may be more applicable for studying short-term, environmentally induced variation, which is perhaps more applicable for fisheries management. Ibanez-Aguirre et al. (2006) also noted that it is of vital importance to identify the study population to understand its dynamics.

There are 300 species of pipefishes in 35 genera, and their taxonomy is in urgent need of revision (www.zoonetics.com). The Mediterranean basin has 9 species that belong to the genus Syngnathus (Dawson, 1986); 6 species are distributed in the Black Sea (Bilecenoğlu et al., 2002; Gürkan and Çulha, 2008). Syngnathus acus can be found in coastal and estuarine waters to depths of 90 m or more on sandy, muddy, and rough bottoms; it is relatively common among algal and eelgrass habitats (Dawson, 1986). Pipefishes, like most other syngnathids, are characterized by restricted distributions, low mobility, small home ranges, and low fecundity (Vincent, 1996). Although they have no commercial importance in fisheries, they are threatened by incidental capture in fishing gears

and are a common bycatch. This species is not of concern on the IUCN Red List presently, but it is likely to become endangered in the future.

Although a few ichthyological studies have focused on pipefish morphometrics (Cakić et al., 2002; Mwale, 2005; Gürkan, 2008; Gürkan and Taşkavak, 2012), there is currently no information on the greater pipefish’s (S. acus) morphological structure in the Turkish waters of the Black Sea. The purpose of this study was to analyze morphological variation of S. acus among different locations along the western Black Sea coasts of Turkey.

2. Materials and methodsA total of 280 individuals of S. acus were collected from bottom-trawl surveys and commercial bottom-trawl catches in the western Black Sea. Surveys were carried out in 2 different seasons (spring and autumn) and at 3 locations. In total, 39 stations were sampled between September 2010 and October 2011. Specimens were captured using a 20-mm stretch cod-end mesh size, at a depth of 10–100 m. The study area was divided into 3 sublocations considering local differences (Figure 1).

The body parts were measured following standard anatomical landmarks (Cakić et al., 2002; Gürkan, 2008). The landmarks include the following: total length

Abstract: The main objective of this study was to analyze the differences and similarities in morphometric characteristics among specimens of greater pipefish Syngnathus 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

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

Research Article

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(TL), total weight (TW), maximum body height (BH), maximum body width (BW), length of pectoral fin (PFL), length of dorsal fin base (DFL), height of dorsal fin (HD), head length (HL), occipital height of head (OHH), mouth height (MH), mouth width (MW), eye diameter (ED), snout length (SL), snout depth (SD), and snout width (SW). The 14 morphometric characteristics are explained in Figure 2. To ensure standardization, all measurements were performed by the same person using calipers (nearest

0.01 millimeter) on the right side of the pipefish. The specimens were weighed using a digital balance to the nearest 0.01 g. The sex of the specimens could easily be determined macroscopically.

A linear regression of various body parts against the total length and head length was carried out using the least-squares method. Thorpe (1976) noted that only morphometric data could be statistically adjusted to permit the comparative analysis of shape independent of

Figure 1. Sampling stations.

Figure 2. Diagram of morphometric measurements of pipefishes.

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size in variations in the size of fish from different locations. Thus, to minimize the influence of size differences on the subsequent results, the original measurements of morphometric characteristics were standardized. Six morphometric characteristics were expressed as % TL and 7 as % HL. This technique is commonly used in ichthyological studies. Morphometric characteristics were analyzed by ANOVA followed by Holm–Bonferroni’s post hoc test (Sokal and Rohlf, 1981) for all possible pairwise comparisons from different locations and between sexes.

The length–weight relationship was calculated with the equation W = aLb, where W is the weight (g), L is the total length (cm), a is the intercept, and b is the slope (Ricker, 1975). Lengths and weights were log-transformed, and the resulting linear relationship was fitted by the least-squares regression. To ensure the quality of the linear regression, the coefficient of determination (r2) was used. Data were analyzed using SPSS 16.0.

3. ResultsOf the 280 specimens, 191 were females (68.2%) and 89 were males (31.8%). The lengths and weights of S. acus ranged from 156 to 392 mm and from 1 to 16.66 g, respectively. The morphology of the sampled fish was described as the relative body proportions of the BH,

BW, PFL, DFL, HD, and HL relative to the TL, and the OHH, MH, MW, ED, SW, SL, and SD relative to the HL (Table 1). The coefficients of variation (CVs) indicated the highest variability in the SW / HL ratio (CV = 23.0% for males, 20.1% for females), whereas the lowest variability was noted in the HL / TL ratio (CV = 7.2% for male, 6.8% for female). Differences between females and males were found in the maximum body height, maximum body width, and head length as a result of Bonferroni’s test (P < 0.05).

The comparisons of the morphometric characteristics of S. acus between different locations are given in Table 2. There were significant differences in 10 morphometric characteristics (Holm–Bonferroni’s test). The specimens of location 1 were morphologically different from the individuals of location 2 in the BH, BW, PFL, DFL, MH, and SW characters. The specimens of location 1 were morphologically different from the individuals of location 3 in the BW, PFL, OHH, SD, SL, and SW characters. The specimens of location 2 were morphologically different from the individuals of location 3 in the HL, OHH, SD, SL, and SW characters.

The estimated parameters of the length–length relationships as well as the coefficients of correlation (r) 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.

Morphometriccharacters

Females MalesMin. Max. Mean ± SD Min. Max. Mean ± SD P

TL (mm) 156 338 270.59 ± 29.45 166 392 264.06 ± 29.42 0.055% TLBH 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 0.545DFL 6.48 14.76 10.53 ± 1.12 6.15 12.83 10.50 ± 1.26 0.832HD 1.19 3.46 2.58 ± 0.43 1.29 3.58 2.63 ± 0.47 0.408HL 12.87 19.09 15.69 ± 1.07 10.10 18.37 15.06 ± 1.09 0.000*% HLOHH 11.83 30.42 16.52 ± 2.30 12.13 24.32 16.78 ± 2.02 0.412MH 6.60 14.46 8.98 ± 1.36 5.49 12.58 9.24 ± 1.27 0.099MW 2.25 5.04 3.43 ± 0.56 1.71 4.99 3.51 ± 0.64 0.296ED 5.45 16.19 9.25 ± 1.69 6.78 14.06 9.61 ± 1.66 0.095SW 1.85 5.03 3.23 ± 0.65 1.68 5.48 3.26 ± 0.75 0.129SL 40.53 73.63 55.99 ± 5.40 43.01 68.24 54.56 ± 5.27 0.193SD 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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were strongly positively correlated except for HL / TL and SW / HL (P < 0.05). The best fit for the length–length relationships was recorded between BH and TL (r = 0.440). The lowest correlation coefficient value was found between MW and HL (r = 0.093).

The relationship between total length (cm) and total weight (g) was highly significant (P < 0.001) (Figure 3). Positive allometric growth was observed for all sexes. There were no significant differences (P > 0.05) between the slopes (b) of the TL–TW relationship for females and males as a result of ANOVA; thus, the TL–TW relationship with the sexes combined was expressed as

TW = 0.0001TL3.415 (r2 = 0.898, n = 280). The slope of the regression line was significantly different from 3.00, thus indicating allometric growth (P < 0.05). The equation for female individuals is TW = 0.00006TL3.553 (r2 = 0.911, n = 191) and the equation for male individuals is TW = 0.0002TL3.154 (r2 = 0.882, n = 89).

4. DiscussionThe TL–TW relationship of S. acus in the western Black Sea displayed positive allometry. The parameters of the TL–TW relationship of this study and previous studies’ results are indicated in Table 4. TL–TW relationship parameters

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.

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from the Black Sea, eastern Mediterranean Sea (Koutrakis and Tsikliras, 2003; Gürkan and Taşkavak, 2007; Gürkan et al., 2010), central Mediterranean Sea (Dulčić and Glamuzina, 2006), and Arade Estuary (Portugal) (Veiga et al., 2009) show that there is no significant difference (P > 0.05). However, we found that the TL–TW relationships are significantly different (P < 0.05) in the Black Sea, South Africa (Harrison, 2001), and the western Mediterranean (Valle et al., 2003). These observed differences could be due to the sampling procedure, seasonal and regional effects, changes in water temperature, salinity, sex, depth, breeding season, and food availability (Tesch, 1971; Wootton, 1992).

In this study, we found the morphometric characteristics were strongly positively correlated, with the exception of HL / TL and SW / HL (P < 0.05). Mwale (2005) indicated that the morphological characters were positively correlated to standard length (r2 > 70%) for the European and South African S. acus populations.

Syngnathid species consume mainly planktonic and benthic crustaceans (Brook, 1977; Bell and Harmelin-Vivien, 1983; Franzoi et al., 1993; Vizzini and Mazzola, 2004). Kendrick and Hyndes (2005) reported that syngnathid species with long snouts (>0.5 mm of the head length) tend to consume relatively mobile prey, whereas species with short snouts feed more commonly on less mobile prey, such as amphipods, harpacticoid copepods, and polychaetes. Moreover, for the southwestern Australian population, the snout length is 0.43–0.59 times greater than the head length (Kendrick and Hyndes, 2005). The results of the present study confirm this proportion (0.51–0.57 times the HL). In addition, S. acus ingests harpacticoid copepods in the shallow waters of the Black Sea; in particular, Euterpina acutifrons was the dominant prey item (Gürkan and Aydın-Uncumusaoğlu, 2012).

According to Gürkan (2008), for S. acus in the eastern Mediterranean Sea measuring 6.1–25.6 cm TL, the females and males of this species do not differ in their morphometric characteristics. However, morphological variation was found between the sexes of Syngnathus typhle and Nerophis ophidian. Cakić et al. (2002) found

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.

y = 0.0001x 3.4152

R² = 0.8981

0

5

10

15

20

25

30

10 15 20 25 30 35 40 45

TW (g

)

TL (cm)

Figure 3. Length–weight relationship of S. acus from catches in the western Black Sea.

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significant differences in 16 out of the 18 morphometric characteristics among Syngnathus abaster caught in the Danube River (Yugoslav region), Black Sea, and Azov Sea. Movčan (1988) reported that differences in 5 out of 10 morphometric characteristics, mainly related to the head length, were observed in S. abaster caught in the Black Sea and Azov Sea. This study demonstrates the existence of morphometric variations between sexes and locations in S. acus in the western Black Sea.

The variation of morphometric characteristics in specimens from different geographical populations could be caused by differences in the genetic structure or the aquatic ecosystems from which they originated (Movčan, 1988; Cakić et al., 2002; Mwale, 2005). The major environmental variables responsible for distribution and

morphological variation are differences in both the abiotic and biotic habitat characteristics such as temperature, salinity, water depth, direction of ocean currents, substrates, and vegetation types (Wiens, 2001). Geographical distance is important in variation because it has a great influence on species dispersal and therefore on gene flow and population mixing (Gill and Kemp, 2002). The locations of this study were geographically close but significantly different from each other in several characteristics. The İstanbul Strait acts as a biological barrier limiting the distribution of certain species of both Mediterranean and Black Sea origin (Öztürk and Öztürk, 1996). The main currents in the Black Sea have a circular character and an anticlockwise direction (cyclonic currents). There are small circulations in the waters, but the circulations are of an anticyclonic

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

Lengthtype N Length range

(cm) a b r2 Region Reference

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.

Head length (HL)1 84 34.0 10.1 58.0 12.22

2 280 41.5 18.9 53.9 5.44

Snout length (SL)1 84 19.6 4.7 32.9 7.67

2 280 23.1 13.1 31.0 3.31

Snout depth (SD)1 84 2.9 0.8 4.9 0.89

2 280 2.7 1.7 4.1 0.44

Eye diameter (ED)1 84 3.9 1.3 6.4 1.18

2 280 3.9 1.3 5.5 0.72

Dorsal fin base (DFL)1 84 29.3 8.1 58.9 11.8

2 280 28.3 13.9 43.7 4.62

Source: 1 = Mwale (2005), 2 = present study.

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character (clockwise) in the coastal zones (Zaitsev, 2008). The Bosphorus eddy (in location 1) and Sakarya eddy (in location 3) are anticyclonic currents and influence the randomized distribution of eggs and population mixing. In addition, the Sakarya River discharges into the Black Sea in the town of Karasu, which changes the salinity in location 3.

The biometric characteristics of European and Black Sea S. acus population groups are given in Table 5. The results of our research on S. acus in the western Black Sea indicate that HL and SL are relatively greater than in European populations. Mwale (2005) compared the biometric characteristics of North Atlantic, South African, and European S. acus populations and found that no single characteristic could reliably separate the North Atlantic and South African populations. The overlap in range values that we observed is normal among syngnathids (Herald, 1965; Fritzsche, 1980) and 2 groups that are closely related or living in similar habitats. In addition, S. acus specimens from Europe differ from the South African specimens, as they have on average more dorsal fin rays, trunk and tail rings, and subdorsal rings. Meristic characteristics were more effective than morphometric characteristics in separating the S. acus populations. It

was noted (www.zoonetics.com) that South African and European populations were morphologically different and that segregation by visually comparing their appearance was possible, as one species was larger and had an angled head. It has repeatedly been shown that fish morphology is affected by environmental factors like diet, habitat, and predation risk (Pakkasmaa and Piironen, 2000; Kendrick and Hyndes, 2005; Eklöv and Svanbäck, 2006; Costa and Cataudella, 2007).

Morphometric measurements are widely used to identify differences between fish populations (Petrakis and Stergiou, 1995; Tzeng, 2004; Cheng et al., 2005; Buj et al., 2008; Torres et al., 2010). In addition, morphometric studies are essential to understand species variations in features, which are most likely related to habitat differences (Cavalcanti et al., 1999). For the western Black Sea, the biometric results in this paper are preliminary, and our results should be verified in future genetic studies.

AcknowledgmentThis study was supported by the Scientific Research Projects Coordination Unit of İstanbul University with 2 projects (Project Numbers: 4231 and 5381).

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