The Reproductive Biology of the Great Pipefish Syngnathus Acus (Family: Syngnathidae) in the Aegean Sea

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North-Western Journal of Zoology Vol. 5, No. 1, 2009, pp.179-190 P-ISSN: 1584-9074, E-ISSN: 1843-5629 Article No.: 051118

The reproductive biology of the Great Pipefish Syngnathus acus (Family: Syngnathidae) in the Aegean Sea

Sule GURKAN, Ertan TASKAVAK* and Belgin HOSSUCU

Ege University, Faculty of Fisheries, 35100 Bornova-İzmir, Tureky. * Corresponding author: E. Taşkavak, Tel: 00 90 232 3884000/1943; FAX: 00 90 232 3686714; E mail: [email protected]

Abstract. With the aim of determining the reproductive characteristics and mating periods specific to Syngnathus acus, a study was carried out from December 2001 to November 2002 in the Camalti Lagoon (Izmir Bay, Aegean Sea). Study material consisted of 605 individuals that were captured using a beach seine in areas with vegetation. 43% (n=261) of the captured individuals were female, 25% (n=154) were male and 31% (n=190) were juveniles that were not sexually mature. The female-male ratio was 1:0.58. Mean total length values in females and males were 113.1 and 111.4 mm, respectively. The abundance of females carrying oocytes and of pregnant males of the species was observed between March-August 2002, coinciding with the period of relatively warmer water temperatures in that year. Gonadosomatic index (GSI %) analyses of females found that the reproductive period was between March- September. The relationship of egg/embryo number with total length in pregnant males and the total length-batch fecundity relation in females was statistically insignificant. We found that there were three groups of oocytes in the ovaries of females. Average oocyte diameter varied between 0.4-1.8 mm (developing 0.4-0.5mm, 0.7-0.8mm and 1-1.8mm hydrated oocyte group); thus, there were three spawning events during a year. The ratios of annual fecundity (mean: 65) and partial fecundity (mean: 28) data support this result (three spawning a year). Average hydrated oocyte number of females was 28, average egg number in the pouch of a male was 24, and average embryo number was 31. Average egg diameter in pregnant males was 1.42 mm (min:1, max:1.85); average length value of pre-larva and post-larvae was 8.91 mm (min:3, max:14.29) and 13.29 mm (min: 9.71 max:15.29).

Key words: Great Pipefish, Syngnathus acus, Reproductive biology, Syngnathidae, Aegean Sea

Introduction suitable for nutrition and sheltering (Polard 1984, Howard & Koehn 1985, Gurkan 2004). The genus Syngnathus, family Syngnathidae, Unlike other fish groups, members of is represented by five species (Syngnathus the family Syngnathidae have an unusual acus, S. typhle, S. abaster, S. tenurostris and S. reproduction strategy (Lyons & Dunne phylegon) in the Aegean coasts of Turkey 2005). In Syngnathus and Hippocampus ge- (Bilecenoğlu et al. 2002). Pipefish have a nus, males carry the eggs transferred from long and thin body structure, covered with females in their brood pouches (Wilson et bony scales, and are frequently dispersed in al. 2003, Monterio et al. 2005). In many pipe- lagoon areas which host sea-grass beds fish species, males carry eggs on the basis of

©NwjZ, Oradea, Romania, 2009 North-West J Zool, 5, 2009 www.herp-or.uv.ro/nwjz Oradea, Romania 180 Gurkan, S. et al. the capacity of their brood pouches duction biology of the species are insuffi- (Gasparini & Teixeira 1999); some of them cient. carry the eggs that are transferred from The purpose of this study is to deter- females in their abdomens by adhering mine sex ratio, reproduction time, number them in a special way, as in Nerophis genus of eggs and larva in the brood pouch of (Margonski 1990, Monterio et al. 2001, pregnant males, annual and batch fecundity Lyons & Dunne 2005). Polygamy is quite of females, so as to detect fecundity-length normal for many pipefish species and fe- relation and spawning number per year. males may involve in polygamy continuously or successively (Berglund 1989, Vincent et al.1992, McCoy et al. 2001). For Materials and methods

this reason, the females which continuously The sampling area was the Camalti Lagoon, located produce hydrated eggs tend to mate near the old mouth of the Gediz River (Fig. 1). The frequently due to their ovary structure benthic structure of this area is sandy, and the pebb- (Gasparini & Teixeira 1999). ly and seagrass vegetation (generally represented by Cymadocea uluavecea) is scarce. During the researches The Syngnathidae family typically carried out between December 2001 and November shows sexual role reversal (Rosenqvist 2002, a total of 605 Syngnathus acus individuals were 1993): the Syngnathus females depositing captured with beach seine (120 cm x 1200 cm), by their eggs in the brood pouch of the male searching the base for 15 minutes. The samplings (Berglund et al. 1988, Vincent et al. 1995, were carried out in areas with a water depth of less than 1.5 m starting from the coast. The captured Kvarnemo & Simmons 2004). This was samples were kept in solutions containing 10% observed also in Syngnathus acus males formalin for laboratory analysis. Fishes were (Gurkan 2004). After mating, the female has identified based on Whitehead et al. (1986). For the no further role (Berglund et al. 1986a,b, total length measurement of individuals (mm) we Ahnesjö 1992). The incubation period of the used a fish measuring board, while weight measure- ments were done with a scale having 0.01 gram eggs in the brood pouch of males varies sensitivity. We used t-test (Sumbuloglu & Sumbu- according to species (Lyons & Dune 2005). loglu 1993) in our search for statistical difference In the sympatric species S. typhle, this between male and female total length values. In period lasts 35-58 days depending on water order to study its effects on species abundance, temperature (Ahnesjö 1995). No relevant surface water temperature was measured with a WTW 340i/SET thermometer. literature is available for S. acus. The sex of captured individuals was identified In Turkey, information about the eco- by the pouch in males (Vincent et al. 1995), while logy, morphometric features, reproduction males without pouch and females were dissected on and nutrition of Syngnathus acus, Syngnathus their ventral part out to the anus, and gonads were typhle and Nerophis ophidion were provided analyzed in microscopic and macroscopic terms. The specimens with incomplete gonad development by Gurkan (2004). Gurkan & Taskavak were considered as immature. In addition to this, for (2007) provided the information on length- determining whether there is a statistical difference weight relationships for syngnathid fishes in sex condition of the species according to months, a of the Aegean Sea, Turkey. In addition, χ2 (chi-square) test was used (Sumbuloglu & Sumbu- Coker et al. (2001) carried out a pre-study loglu 1993). For gonadosomatic index, ovary weights of 107 on reproduction biology of S. acus species in females were taken and monthly gonadosomatic Izmir Bay. However, the studies on repro- index (GSI) values were calculated with the GSI: [Go-

North-West J Zool, 5, 2009 Reproductive Biology of Great Pipefish Syngnathus acus 181

Figure 1. Map showing the location of sampling sites.

nad weight (g) / body weight (g)]* 100 formula mm); “a” is the intersection point of the line in y axis (Cample & Able 1998). Fecundity was calculated by and “b” is the constant that gives the grade. gravimetric method (Hunter et al. 1985). The abundances of females carrying hydrated For annual fecundity, oocytes in III (corticol eggs, pregnant males (the ones whose pouch is filled alveoli), IV (vitellogenetic), V (maturing) and VI. with larvae or egg) and the males with empty (mature) development phases were evaluated pouches were evaluated separately in each month (Begovac & Wallace 1987). Phase I (oogonia) and (no individuals were observed in January, February phase II (primer oocyte) oocytes were considered as and September). the eggs of the next year and were not evaluated. For partial fecundity, only hydrated eggs from phase VI were evaluated and considered in spawn- Results ing number calculations (annual fecundity/ partial fecundity). In addition, egg/embryo number in pouch of According to the results obtained, 261 males was recorded and amount of multiple (43%) of 605 individuals were females, 154 spawning of female was determined. Oocyte (25%) were males, and 190 (31%) were diameters (long diameter), pr-e and post-larvae immature. The mean female:male adult sex lengths were measured using a binocular microscope ratio of captured specimens was 1:0.58. A having micrometric ocular with 10×4 magnification. To analyze the relationship between total length- significant difference was found between hydrated oocyte (O) in females and egg/embryo (E) the abundance of sexes according to the numbers in males, regression analysis was used expected values (χ2=14.84, p<0.05). (y=a+b x). In this equation, “y” refers to egg/embryo We found total length values of im- or larvae number and “x” refers to total length (TL, mature individuals between 39-118 mm;

North-West J Zool, 5, 2009 182 Gurkan, S. et al. total length values of mature males as 61- (56%). Generally, the abundances of males 235 mm and total length of mature females with empty pouches, pregnant males and between 69-256 mm. We consider that hydrated-oocyte carrying females are con- minimal sexual maturity length was 69 mm sistent with each other. The results obtained in females and 61 mm in males (Table 1). from egg-carrying mature pipefish accord- In the monthly captures of S. acus in ing to average surface water temperatures Camalti Lagoon, no immature pipefish were are given in Figure 4. observed in February, March and April. According to these results, an increase in Thus, this result may give an idea that this water temperature increased the frequency species reaches sexual maturity in relatively of hydrated-oocyte carrying females and smaller size groups, i.e., relatively smaller pregnant males. Peak months during which age groups which were not taken into pregnant males were present were July consideration in this study (Fig. 2). (55%), March (46%) and May (26%). Simi- Frequency of hydrated-oocyte carrying larly, the females are outnumbered between females, pregnant males, and males with March-August, with highest peak in May empty pouches according to months are (56%). Within this reproductive period, given in Figure 3. average water temperature values vary Regarding the number of mature between 16–23.4 ºC. In addition, the number pipefish according to months, females with of fish decreased with temperature drop in hydrated oocytes were observed in March- average surface water (December, January August, with May having the highest value and February).

Table 1. Total length, total weight, Gonadosomatic index values and sex ratio evaluation in the captured Syngnathus acus female, male (with pouch, pregnant ones) and immature individuals. N: sample size, M: Mean; TL: total length in mm; W: weight in g.; GSI: Gonadosomatic index values; SD: Standard deviation SE: Standard errors) by months.

FEMALE Months N M TL±SD M W±SD N GSI(%)±SE ♀:♂ December 27 115.44±18.64 0.77±0.76 14 0.86±0.09 0.37 January 6 103.33±14.28 0.48±0.25 3 1.27±0.19 0.50 February 7 134±60.26 2.50±4.80 0 - 0.33 March 8 117.38±16.66 0.78±0.34 6 10.24±0.66 1.38 April 11 123.55±12.94 1.20±0.64 3 10.53±2.00 0.55 May 25 123.24±8.74 1.11±0.32 15 12.91±1.52 0.76 June 9 125.33±12.76 1.08±0.25 3 6.68±2.14 1 July 28 103.25±24.75 0.64±0.58 16 5.80±0.92 0.39 August 60 99.62±12.84 1.14±5.50 10 3.86±1.16 0.43 September 5 135.60±39.98 1.41±1.72 1 2.13 0.40 October 17 131.00±39.99 1.38±1.96 7 1.82±0.24 0.82 November 59 109.42±20.33 0.64±0.85 29 1.93±0.22 0.82 TOTAL 261 112.17±23.86 0.79±1.18 107 4.94±0.49 0.58 (Range) (69.00–256.00) (0.03-12.29)

North-West J Zool, 5, 2009 Reproductive Biology of Great Pipefish Syngnathus acus 183

Table 1. (Continued)

MALES Male (Total) Pregnant male Pouchs male Months N M TL±SD M W±SD N M TL±SD N M TL±SD December 10 111.90±9.57 0.68±0.15 0 - 7 113.0±11.43 January 3 107.33±14.19 0.48±0.20 0 - 0 - February 2 179.5±71.42 4.18±4.53 0 - 0 - March 11 108.91±12.89 0.62±0.37 5 104.0±18.09 5 105.40±5.13 April 6 114.0±15.74 1.01±0.59 1 102.0±0.0 3 113.67±17.95 May 19 125.37±10.11 1.28±0.38 10 124.70±10.31 1 111.0±0.0 June 9 132.33±7.76 1.38±0.30 0 - 3 133.0±10.44 July 11 111.18±26.10 0.81±0.59 6 105.50±18.09 0 - August 26 99.04±18.33 0.49±0.30 5 103.80±9.93 5 104.6±5.37 September 2 131.50±30.41 1.13±0.73 0 - 0 - October 14 106.50±8.79 0.60±0.19 0 - 2 110.5±2.12 November 41 111.93±22.07 0.78±1.28 0 - 4 108.5±3.42 TOTAL 154 112.96±21.39 0.85±0.93 27 112.26±2.89 30 111.57±2.08 (Range) (61.00–235.00) (0.09-8.66) (93–142) (97–140)

IMMATURE Months N M TL±SD M W±SD December 11 93.91±8.95 0.33±0.12 January 7 93.29±6.37 0.31±0.08 February 0 - - March 3 88.67±4.16 0.24±0.03 April 0 - - May 12 57.83±11.59 0.09±0.05 June 35 75.0±9.66 0.18±0.09 July 59 75.17±10.17 0.17±0.07 August 24 81.29±11.84 0.23±0.10 September 6 81.67±9.83 0.19±0.05 October 13 94.15±13.01 0.36±0.18 November 20 100.50±10.10 0.41±0.17 TOTAL 190 80.95±14.91 0.23±0.14 (Range) (39.00–118.00) (0.02-0.14)

Total length of S. acus females, males The highest GSI value in S. acus females (with pouch, pregnant ones) and immature analyzed during the whole year was individuals is given in Table 1. According to reached in May (mean 12.9) and repro- these data, mean length values of males and duction period of the species was between females are similar (t413=0.726, p>0.05). March-September 2002 (Table 1 and Fig. 5).

North-West J Zool, 5, 2009 184 Gurkan, S. et al.

4 Frequency (%) Frequency 2

0 Dec Jan Feb Mar Apr May Jun July Aug Sep Oct Nov

%Female 4,62 0,99 0,99 1,32 1,81 4,13 1,48 4,62 9,91 0,82 2,8 9,91 %Male 1,65 0,49 0,16 1,81 0,99 3,14 1,48 1,81 4,29 0,33 2,31 6,77 % Immatur e 1,81 1,15 0 0,49 0 1,98 5,78 9,75 3,96 0,99 2,14 3,3 Months

Figure 2. Frequency of mature males, mature females and juveniles in the samples according to months.

% ECF 80 d %PM 70 %MEP 60 50 40 30 MEP (%) 20 10

Frequency of ECF PM an 0

c r e eb p D Jan F A May July March June Agust Months

Figure 3. Frequency of hydrated-oocyte carrying females (ECF), pregnant males (PM), and males with empty pouches (MEP) according to months.

In females, hydrated oocyte amount and relation was weak. In males, the relation- TL relationship was O= 0.6391, TL–44.535 ship between egg/embryo amount and TL (n=27; r2=0.18, p=0.043 p<0.05) and the cor- was E = -0.669TL + 96.918 (n=11; r2=0.33,

North-West J Zool, 5, 2009 Reproductive Biology of Great Pipefish Syngnathus acus 185 p=0.000 p<0.05) and correlation was strong. er of females was 29±4.35 (min:2, max:84, As in hydrated oocyte-TL relationship in n:27), average egg number in pouch of females, larva that is carried in male pouch- pregnant males was 24±5.16 (min:2, max:42, TL relationship was also weak [E=0.1357– n:11), and embryo number was 34±8.80 6.2143 (n=6, r2=0.10, p=0.004 p<0.05)]. (min:2, max:81, n:11) (Fig. 8A,B,C,D). While The relation between the amount of oo- average egg diameter in pregnant males cyte transferred by the females to the pou- was 1.42 mm (min:1, max:1.85, n:14), pre- ches of the males at one time and the total larvae and post-larvae average length va- length was found to be weak [(TL=0.5784- lues were 8.91 mm (min:3, max:14.29, n: 51) 39.52, r2=0.15, p=0.044, p<0.05)] (Fig. 6). and 13.29 mm (min:9.71, max:15.29 n: 20) Oocytes smaller than 0.3 mm (diameter) respectively (Fig.8E,F). Average hydrated in an ovary were considered as belonging to oocyte diameter in females was 1.41 mm the next reproduction period. According to (min:1, max: 1.85, n=24), which is almost the this, the diameters of oocytes vary between same with the diameter of the eggs carried 0.4 and 1.8 mm. When the diameter by the males. frequency distribution of these oocytes was analyzed, three groups were distinguished (0.4–0.5mm, developing 0.7–0.8mm and 1– Discussion 1.8mm hydrated oocyte group) (Fig. 7). Accordingly, it can be accepted that this In this study, the reproductive period of species spawns three times a year. The ratio Syngnathus acus in Camalti Lagoon was bet- of annual fecundity (average: 65, min: 3, ween March-September. The reproductive max.:282, n=38) and partial fecundity (ave- seasons given for the syngnathid species rage: 28, min: 2, max.:84, n=27) data support vary between four and nine months accord- this result. Average hydrated oocyte numb- ing to regions (Froese & Pauly 2001 in Taka-

60 30 0

50 25

40 20

30 15 C

20carring (%) 10

10 5 The numbers of hydrated oocyte 0 0 Mean seawater temperature Clutc h n b y ct ov ec Ja Apr uly Brood D Fe Ma June J Sept O N March Agust Temp Months

Figure 4. Relationship between hydrated-oocyte and water temperature for each month.

North-West J Zool, 5, 2009 186 Gurkan, S. et al.

14 12 10 8 6 4

Mean GSIvalues 2 0

y ec g p Jan Apr Oct D Ma June July Au Se Nov March Months

Figure 5. Mean GSI values of females over time.

80 y = 0,5784x - 39,524 70 R2 = 0,1492 N=27 60 50 40 Batch 30 20 10 0 75 100 125 150 Total Length

Figure 6. Total length-batch fecundity relationship in females.

hashi et al. 2003). S. acus has also a repro- this period may change on the basis of ductive period similar to other syngnathid latitude and water temperature (Ano- species (Froese & Pauly 2001 in Takahashi et nymous 1956, Vincent et al. 1995, Lyons & al. 2003). While the reproductive season of Dune 2005). this species in the Mediterranean is indi- Concomitant to an increase in water cated as January-July (Anonymous 1956), temperature in Camalti Lagoon, existence of

North-West J Zool, 5, 2009 Reproductive Biology of Great Pipefish Syngnathus acus 187 hydrated-oocyte carrying females and preg- highest abundance in March-August, most- nant males also increased. Therefore, the ly in May (56%). For S. acus found in the months which pregnant males were most North Sea with colder water, males with or abundant were March (46%) May (26%) and without pouch are observed in May-July July (55%). As for females, they reached the (Vincent et al. 1995).

40 35 30 25 20 15 % Frequency 10 5 0 0,3 0,4 0,5 0,7 0,8 0,9 1 1,1 1,2 1,4 1,5 1,7 1,8 Diameter of oocyts (mm)

Figure 7. The frequency of oocyte diameters in the female ovary (n=75).

Figure 8. A: Hydrated oocytes of a female: B,C: eggs in pouch of pregnant male; D: Embryos in pouch of pregnant male; E: Pre-larvae; F: Post-larvae.

North-West J Zool, 5, 2009 188 Gurkan, S. et al.

Sexual dimorphism is not observed in (Vincent et al. 1995), having polygamous Syngnathus acus (Vincent et al. 1995; Gurkan characteristics (Fries et al. 1895, Berglund et 2004). For this reason, the minimum total al. 1988), take part in reproduction for a few length of females and males corresponds to years after reaching sexual maturity and sexual maturity value. Minimum length they may mainly focus on reproduction values at which females and males reach rather than growing in terms of length and sexual maturity are 69 and 61 mm, res- weight. pectively. These length values are smaller The majority of studies that are carried than those of females (77 mm) and males (81 out on the reproduction ecology of pipefish mm) given by Coker et al. (2001) for Izmir focus on Nerophis ophidion and Syngnathus bay, Aegean Sea. In northern regions which typhle, species which have sexual dimorph- have colder water, sexual maturity mean ism and which show specialized mating be- length was given as 344 mm (Vincent et al. haviour (Berglund et al. 1986b, Berglund et 1995). al. 1988). According to Vincent et al. (1995), Maximum total length value detected in there is no sexual dimorphism in body our research is 256 mm for females, and 235 length of S. acus, and our study supports mm for males (Table 1). It was given as 124 this result. mm for northern Aegean Sea, while maxi- When analyzing the frequency distri- mum length value determined for eastern bution of oocyte diameters, three groups Aegean Sea was 101 mm for pooled sexes were distinguished (0.4–0.5mm, 0.7–0.8mm (Gurkan & Taskavak 2007). Maximum male developing and 1–1.8mm hydrated oocyte total length detected in waters colder (13-16 group). Accordingly, spawn frequency can oC) than the waters of our region (8-28 oC) be considered as 3. The ratios of annual fe- was 460 mm (Monterio et al. 2001, Monterio cundity and partial fecundity data approxi- et al. 2005). mately support this result. As the studies on In this study, female:male ratio of this issue are rather limited, we can not any pipefish is 1:0.58. The obtained results are make comparison in this sense. consistent with the values found by Coker Average hydrated oocyte number of et al. (2001), who found exactly the same females was 29±4.35 (min:2, max:84 and ratio, while Vincent et al. (1995) reported an n:27), average egg number in pouch of equal sex ratio. pregnant males was 24±5.16 (min:2, mak:42 The relation of egg/embryo number and n:11), and embryo number was 34±8.80 with total length in pregnant males, and (min:2 max:81, n:11). Egg/embryo number total length-batch fecundity relation of in pregnant males was maximum 400 eggs females were found to be weak. For for Syngnathus acus (Monteiro et al. 2005); Nerophis lumbriciformis (Lyons & Dunne average 49.5 (min:4 max:88) for Nerophis 2005), Syngnathus scovelli (Gasparini & lumbriciformis (Lynos & Dunne 2005); 29.5 Teixeira 1999) a very weak relation was (McLane 1955), 56-58 (Joseph 1957), 12.2 found between egg number of pregnant (Hellier 1967), 30-92 (Gasparini & Teixeria males and standard length. The reason may 1999), 296 embryo (Targett 1984) for be the fact that these short-lived fish which Syngnathus scovelli. The difference in numb- are said to live for more than one year er of eggs/embryo may stem from different

North-West J Zool, 5, 2009 Reproductive Biology of Great Pipefish Syngnathus acus 189 carrying capacity of males, locality and differences in egg diameter. Acknowledgements. The material used in this study was gathered in the frame of the “Fishes and their While average egg diameter was 1.42 reproductive periods in Tuzla Lagoon and Urla Coasts of mm (min:1, max:1.85 and n:14) in pregnant Izmir Bay” project (Project No: 2001 SÜF 003), financially males, pre-larvae and post-larvae average funded by Ege University. We are grateful to the project staff. length values were 8.91 mm (min:3, max:14.29 and n: 51) and 13.29 mm (min: 9.71, max:15.29 and n: 20), respectively. References Average hydrated oocyte diameter in females was 1.41 mm (min: 1, max.: 1.85 and Ahnesjö, I. (1992): Consequences o male brood care; n=24), which is approximately equal to the weight and number of newborn in a sex-role diameter of eggs carried by males. reserved pipefish. Functional Ecology 6: 274-281. Ahnesjö, I. (1995): Temperature affects male and female Consequently, in this study we tried to potential reproductive rates differently in the sex- determine whole-year reproduction strategy role reversed pipefish Syngnathus typhle. Behavioral of S. acus, captured in Izmir Bay. The results Ecology 6 (2): 229-233. Anonymous (1956): Uova, larve e stadi giovanili di given above may speculate that the teleostei. Pp. 385-1064. In: Fauna e Flora del Golfo di inhabitants of cold seas reach sexual ma- Napoli. Monografia 38, Puntata 3. Stazione turity later and therefore have longer zoologica di Napoli. Italy. length. In this research, the total mean Begovac, P.C, Wallace, R. A. (1987): Ovary of the pipefish, Syngnathus scovelli. Journal of Morphology length values in males and females were 193: 117-133. 112.96 and 112.17 mm, respectively. Con- Berglund, A., Rosenqvist, G., Svensson, I. (1986a): versely, Vincent et al. (1995) reported 354 Reserved sex roles and parental energy investment in zygotes of two pipefish (Syngnathidae) species. and 344 mm in males and females for the Marine Ecology Progress Series 29: 209–215. colder water specimens of this pipefish spe- Berglund, A., Rosenqvist, G., Svensson, I. (1986b): Mate cies. The findings of two researches are in choice, fecundity and sexual dimorphism in two accordance with the argument on water pipefish species (Syngnathidae). Behavioral Ecology and Sociobiology 19: 301–307. temperature and sexual maturity age (cold Berglund, A., Rosenqvist, G., Svensson, I. (1988): water but late maturity with longer length; Multiple matings and paternal brood care in the warm water but early maturity with shorter pipefish Syngnathus typhle. Oikos 51: 184–188. Berglund, A., Rosenqvist, G., Svensson, I. (1989): Males length). Mean numbers of eggs/embryos in limit the reproductive success of females in two the male pouches and hydrated-oocyte in pipefish species. American Naturalist 133: 506-516. the females varied between months, pro- Bilecenoglu M, Taskavak, E., Mater, S., Kaya M. (2002): bably duo to influence of abiotic conditions Zootaxa 113 Check list of marine fishes of Turkey. Magnolia Press, Auckland, New Zealand. (water temperature) or/and duo to differen- Cample, B.C., Able, K.W. (1998): Life History ces in length of fish captured. The numbers Characteristics of Northern Pipefish, Syngnathus of gravid females (also high GSI values) and fuscus, in Southern New Jersey. Estuaries 21: 470– 475. pregnant males may indicate that the great Coker, T., Taskavak, E., Atabey, S., Özaydın, O., Akalın, pipefish appears to have a protracted S. (2001): Observations on the breeding biology of mating season in the Camalti Lagoon, Izmir Syngnathus acus Linnaeus 1758, in Izmir Bay. 4–6 Bay, western Aegean Sea. September 2001 XI. National Symposium on Aquatic Products, Antakya, Turkey. [in Turkish, unpublished]. Fries, B., Ekström, C.U., Sundewall, C. (1895): Lophobranchs. Pp. 661-688. In: F.A. Smith (ed.): A

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