Determination of batch fecundity of garfish, Belone belone, in the northern Aegean Sea

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J. Black Sea/Mediterranean Environment Vol. 19, No. 3: 385 392 (2013) RESEARCH ARTICLE Determination of batch fecundity of garfish, Belone belone, in the northern Aegean Sea Tülin Çoker 1, Okan Akyol 2*, Gökçen Bilge 1 1 Faculty of Fisheries, Muğla University, 48000 Muğla, TURKEY 2 Faculty of Fisheries, Ege University, 35440 Urla, Izmir, TURKEY * Corresponding author: okan.akyol@ege.edu.tr Abstract This study reports the batch fecundity (BF) and oocyte diameters of Belone belone from the Aegean Sea (Izmir and Candarli Bays). A total of 51 female specimens of garfish were collected from January to December 2003. Oocyte diameters (n = 12140) of B. belone ranged from 0.063 to 3.5 mm, concentrating between 0.063 and 1.5 mm. The fish weight BF relationships according to both hydrated oocyte and oocyte size frequency methods were BF = - 0.3794 W + 192.22 (R 2 = 0.037) and BF = 5.165 W - 55.21 (R 2 = 0.218), respectively. Mean oocyte numbers in the ovaries were 4144 ± 604 with varied from 662 to 15962. Maximum BF was 2130 (mean: 670 ± 97) in hydrated oocytes, and 8189 (mean: 1667 ± 559) in large oocytes. There was no linear relationship between BF and fish weight according to determination coefficients. Keywords: Garfish, Belone belone, oocyte diameter, batch fecundity, Aegean Sea. Introduction The garfish, Belone belone, is distributed in the eastern Atlantic and Mediterranean Sea. Three subspecies were recognized by Collette and Parin (1986); B. belone belone in the Northeast Atlantic, occurring especially from France northwards; B. belone euxini in the Black Sea and Sea of Azov; and B. belone gracilis in the Mediterranean. The garfish is epipelagic and lives solitarily or in small groups usually near the surface. It feeds on small schooling fish (Golani et al. 2006). According to FishBase (http://www.fishbase.org/), maximum recorded length and weight of the garfish is 93 cm TL and 1300 g, respectively (Froese and Pauly 2013). 385

Russell (1976) described that the eggs of B. belone waere demersal, spherical with 3.0-3.5 mm in diameter, unsegmented yolk, membrane with filamentous and no oil globule. Spawning of large eggs, attached to vegetation and floating objects by sticky threads, occurs in coastal waters from May to June in the British Isles; February-May in Algeria, April-September in the Black Sea (Collette and Parin 1986; Golani et al. 2006). Although there are some researches on reproductive biology of garfishes in all over the world (Rosenthal and Fonds 1973; Goldberg and Pizzorno 1985; Dorman 1989, 1991; Korzelecka-Orkizs et al. 2005; Hughes and Stewart 2006), there is a gap in the Aegean Sea. There has been a unique biological study, which also defines some reproductive properties of garfish in Izmir Bay, the Aegean Sea (Uçkun et al. 2004). Recently, a new species (B. svetovidovi) of Belone was reported by Meriç and Altun (1999) for the Aegean Sea. According to our observations, B. belone and B. svetovidovi are using the same habitat for both feeding and reproductive activities in the same season (in late spring and early summer). This study reports some reproductive aspects such as oocyte numbers and diameters and determining the batch fecundity of B. belone in the Northern Aegean Sea. Materials and Methods A total of 51 female specimens of B. belone were collected from purse-seiners in northern Aegean Sea (Izmir and Çandarlı Bays) between January 2003 and December 2003 (Figure 1). Mature gonads (n=51) of female specimens [total lengths ranged from 31.1 cm (32.4 g) to 58.4 cm (256.2 g)] were obtained and fixed in 4% formaldehyde solution. Maturity was assessed according to Gunderson s (1993) scale: stage I: immature, stage II: resting, stage III: developing, stage IV: ripe and stage V: spent. However, no gonads in stage V were observed in this study. The batch fecundity (BF) was estimated by the oocyte size frequency (n=15) and the hydrated oocyte (n=36) methods (Hunter et al. 1985). According to gravimetric sampling (Holden and Raitt 1974), eggs were thoroughly washed and spread on blotting paper to dry in the air. Totally 2.0 g (± 0.1 g) oocytes from the gonads were counted in a Petri dish and their diameters were measured under a stereo microscope (10 x 1.5) with micrometric ocular (the measuring unit; 0.0625 ± 0.001 mm). Oocytes greater than 1.0 mm in diameter were assumed as large oocytes. 386

Figure 1. The map of the study areas Fish (gonad free) weights (W) BF relationships according to both methods were computed by linear regressions, where BF is batch fecundity (number), W is body weight (g), and a, b, c and d are constants. Means were given with standard error (± SE). Results and Discussion Oocyte diameters (n = 12140) of B. belone ranged from 0.063 to 3.5 mm, concentrating between 0.063 and 1.5 mm (Figure 2). The fish weight BF relationships according to both hydrated oocyte and oocyte size frequency methods were BF = -0.3794W + 192.22 (R 2 = 0.037) and BF = 5.165W - 55.21 (R 2 = 0.218), respectively (Figure 3). The number of oocyte in the ovaries varied from 662 to 15962 (mean: 4144 ± 604). Maximum BF was 2130 (mean: 670 ± 97) in hydrated oocytes, and 8189 (mean: 1667 ± 559) in large oocytes. There was no linear relationship between BF and fish weight according to the determination of coefficients. The garfishes are multiple-spawner fish, spawning more than once during a reproductive season. There are several batches (most probably 3, as evidenced by oocytes of different size found in different parts of the ovary) (Goldberg and Pizzorno 1985; Korzelecka-Orkizs et al. 2005). Indeed, we observed various sizes of oocytes in the present study. Occurrence of the hydrated and larger 387

oocytes throughout the sampling period indicated that the garfish was a typical batch spawner and the reproduction might be continuous during the whole year with some peaks. However, the most abundant hydrated and larger oocytes, even the largest oocyte (3.5 mm) together in the same ripe gonads, were found in May. Therefore, the peak of the spawning is determined to be May. Figure 2. Distribution of oocyte diameters in monthly samplings of B. belone 388

Figure 3. The fish weight BF relationships [(A) hydrated oocyte, n = 36; (B) oocyte size frequency, n = 15] in B. belone Collette and Parin (1986) reported that B. belone spawns from May to June in the British Isles; February-May in Algeria and April-September in the Black Sea. Dorman (1989, 1991) reported that spawning of the species occurred from early to late June for Southern Ireland, and from May to June for the Western coast of Sweden and from August to September for the Baltic Sea. Along the Dutch and German coast of the North Sea, spawning period of the garfish was primarily in May and June (Rosenthal 1970; Rosenthal and Fonds 1973). Yüce (1975) stated that the spawning season of this fish in the Sea of Marmara was extended from mid April to end of August. In the Aegean Sea, the maximal seasonal GSI values for garfish were found as winter and spring and the spawning period starts from late March and early April (Uçkun et al. 2004). 389

In the present study, the smallest reproductively active female was measured 311 mm TL and its gonad (2.3 g) contained 111 hydrated oocytes. The oocyte diameters of garfish ranged from 0.063 to 3.5 mm, concentrating between 0.063 and 1.5 mm. The largest oocyte (3.5 mm) was measured in May. However, some oocytes with 3.38 mm in diameter were also observed between March and May. Uçkun et al. (2004) reported that the oocyte diameters (n=794) of garfish from the Izmir Bay ranged from 0.4 to 4.00 mm. Yüce (1975) informed that the diameters of garfish from the Sea of Marmara were between 0.3 and 3.7 mm. Korzelecka-Orkizs et al. (2005) measured that the diameters of the smallest and the largest eggs of B. belone were 2.95 and 3.70 mm, respectively (mean: 3.27 ± 0.15) in Gulf of Gdansk (Baltic Sea, Poland). In the current study, the mean number of oocytes in ovaries were 4144 ± 604, with the range from 662 to 15962. Maximum BF was 2130 (mean: 670 ± 97) in hydrated oocytes, and 8189 (mean: 1667 ± 559) in large oocytes. Uçkun et al. (2004) calculated that the average number of oocytes was 7780 with the range from 1066 to 20446. Yüce (1975) reported that the number of oocytes of garfish from the Sea of Marmara varied from 10196 to 48903. Dorman (1991) stated that the fecundity estimates ranged from 2193 to 10804 eggs per ripe ovary. Hughes and Stewart (2006) estimated that mean BF for eastern sea garfish (Hyporhamhus australis), and for eastern river garfish (H. regularis ardelio), and for snub-nosed garfish (Arrhamphus sclerolepis) in south-eastern Australia were 1498 ± 110 (range: 98-3449); 917 ± 36 (range: 102-2268) and 716 ± 104 (range: 20-2956) ripe oocytes per female, respectively. Although, these results were found similar, differentiation from Yüce (1975) might be recognized. As he did not describe exactly which oocytes he counted. The maximal gonad weight reported by Yüce (1975) was 3350 mg (=3.35 g), whereas, there was a maximum 47.5 g gonad weight in our study. In the present study, there was no strong linear relationship between BF and fish weight due to several reasons. The eel-like body form of the garfish (we could not give fish length-bf relationship due to negative determination coefficient) and the sampled fish in the study probable partially spawn, namely, there can be some fish with full gonads. In conclusion, there is lack of studies on reproductive biology of the garfish in the Mediterranean probably due to sampling difficulties. However, the garfish is commercially important species in Turkish marine waters, and the further studies such as histological examinations, first maturity length/age, etc. are essential in order to determine the reproductive biology of the garfish for sustainable fishing. 390

Kuzey Ege Denizi nde zargana balığının (Belone belone) bir defada yumurtlama miktarının belirlenmesi Özet Bu çalışma, Ege Denizi nde İzmir ve Çandarlı Körfezleri nden elde edilmiş Belone belone lerin bir defada yumurtlama miktarını (BF) ve yumurta çaplarını rapor etmektedir. Toplam 51 dişi zargana bireyi Ocak-Aralık 2003 tarihleri arasında toplanmıştır. B. belone nin yumurta çapları (n=12140) 0,063 ve 1,5 mm yoğunlukla, 0,063 den 3,5 mm ye değişmektedir. Balık ağırlığı-bf ilişkisi hem hidrate yumurta hem de yumurta büyüklüğü yöntemlerine göre sırasıyla BF = - 0.3794 W + 192.22 (R 2 = 0.037) ve BF = 5.165 W - 55.21 (R 2 = 0.218) şeklindedir. Ovaryumlarda ortalama yumurta sayısı 4144 ± 604 adettir (min. 662 maks. 15962). Maksimum BF, hidrate yumurtalar için 2130 (ortalama: 670 ± 97), büyük yumurtalar için 8189 (ortalama: 1667 ± 559) adettir. Korelasyon katsayısına göre BF ve balık ağırlığı arasında lineer bir ilişki yoktur. References Collette, B. B., Parin, N. V. (1986) Belonidae. In: Fishes of the North-eastern Atlantic and the Mediterranean. (eds. Whitehead, P. J. P., Bauchot, M.-L., Hureu, J.-C., Nielsen, J., Tortonose, E.).,Vol. II. Paris: UNESCO, pp. 604-609. Dorman, J. A. (1989) Some aspects of the biology of the garfish Belone belone (L.) from Southern Ireland. Journal of Fish Biology 35: 621-629. Dorman, J. A. (1991) Investigations into the biology of the garfish, Belone belone (L.), in Swedish waters. Journal of Fish Biology 39: 59-69. Froese, R., Pauly, D. (Eds.) (2013) FishBase. World Wide Web electronic publication. www.fishbase.org, version (02/2013). Golani, D., Öztürk, B., Başusta, N. (2006) Fishes of the Eastern Mediterranean. Turkish Marine Research Foundation, Publication No. 24, Istanbul, Turkey, 259 pp. Goldberg, S. R., Pizzorno, M. C. (1985) Notes on spawning of the fish Belone stolzmanni (Belonidae) from Peru. Pacific Science 39 (4): 367-368. Gunderson, D. R. (1993) Surveys of fisheries resources. John Wiley & Sons, Inc. N.Y., 248 pp. 391

Holden, M. J., Raitt, D. F. S. (1974) Manual of fisheries science, Part 2: Methods of resource investigation and their application. FAO Fisheries Tech. Paper No: 115, Rome, 214 pp. Hughes, J., Stewart, J. (2006) Reproductive biology of three commercially important Hemirhamphid species in South-eastern Australia. Environmental Biology of Fishes 75 (2): 237-256. Hunter, J. R., Lo, N. C. H., Leong, R. J. H. (1985) Batch fecundity in multiple spawning fishes. In: An egg production method for estimating biomass of pelagic fish, application to the northern anchovy, Engraulis mordax, (ed., R. Lasker), NOAA Technical Reports, 36: 67-77. Korzelecka-Orkizs, A., Formicki, K., Winnicki, A., Bonislawska, M., Szulc, J., Biernaczyk, M., Tanski, A., Wawrzyniak, W. (2005) Peculiarities of egg structure and embryonic development of garfish (Belone belone L.). Electronic Journal of Ichthyology 2: 42-53. Meriç, N., Altun, O. (1999) The garfish, Belone svetovidovi Collette and Parin, 1970, new to the Aegean Sea. Israel Journal of Zoology 45 (3): 423 426. Rosenthal, H. (1970) Anfütterung und wachstum der larven und jungfishe des hornhectes, Belone belone. Helgolander wis Meer 21: 320 332. Rosenthal, H., Fonds, M. (1973) Biological observations during rearing experiments with the garfish Belone belone. Marine Biology 21: 203-218. Russell, F. S. (1976) The eggs and planktonic stages of British marine fishes. Academic Press, London, 524 pp. Uçkun, D., Akalın, S., Taşkavak, E., Toğulga, M. (2004) Some biological characteristics of the garfish (Belone belone L., 1761) in Izmir Bay, Aegean Sea. Journal of Applied Ichthyology 20: 413 416. Yüce, R. (1975) Biology of garfish Belone belone (L.). Hidrobioloji Araştırma Enstitüsü Yayınları 75: 1-25. (in Turkish). Received: 07.05.2013 Accepted: 15.09.2013 392