Reproductive Biology of Pink Cuttlefish Sepia Orbignyana in the Aegean Sea (Eastern Mediterranean)
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Turkish Journal of Zoology Turk J Zool (2013) 37: 576-581 http://journals.tubitak.gov.tr/zoology/ © TÜBİTAK Research Article doi:10.3906/zoo-1209-22 Reproductive biology of pink cuttlefish Sepia orbignyana in the Aegean Sea (eastern Mediterranean) Derya DURSUN, Elizabeth Grace Tunka ERONAT*, Meryem AKALİN, Mehmet Alp SALMAN Faculty of Fisheries, Ege University, Bornova, İzmir, Turkey Received: 19.09.2012 Accepted: 17.04.2013 Published Online: 12.08.2013 Printed: 06.09.2013 Abstract: Some aspects of the reproductive biology of Sepia orbignyana, such as fecundity, spawning strategies, and gonad histology, have been studied in 1048 specimens (538 males and 510 females) caught during trawl surveys from May 2008 to April 2009 in the Aegean Sea. The length at 50% maturity was estimated as 50 mm for males and 70 mm for females. The smallest mature female had a mantle length (ML) of 36 mm; the smallest mature male had a 32-mm ML. The total egg counts (potential fecundity) in females of 60–84 mm in ML varied between 201 and 1532. The spermatophore counts in mature males (ML = 42–67 mm) were between 68–1055, with a mean of 485. Key words: Reproductive biology, pink cuttlefish, S. orbignyana, Aegean Sea 1. Introduction 2. Materials and methods Sepia orbignyana Ferussac, 1826 inhabits the eastern Samples were collected onboard commercial vessels Atlantic Ocean from 55°N to 17°S and occurs throughout during daytime by bottom trawl (44-mm mesh size in the Mediterranean Sea between depths of 15 to 570 m, cod-end) on sandy and muddy bottoms at depths of 150, and mostly between 50 and 250 m. S. orbignyana, which is 350, and 550 m in the Aegean Sea (eastern Mediterranean often mistaken for S. elegans, occurs mainly on sandy and Sea). Samplings were carried out monthly from May 2008 sandy–muddy bottoms (Jereb and Roper, 2005). to April 2009 (Figure 1). The duration of each haul was 1 h, Research on Mediterranean cephalopods had shown and towing speed varied between 2.2 and 2.5 knots. that S. orbignyana is one of the most common species in The entire cephalopod catch was preserved in 4% the area (D’Onghia et al., 1991; Belcari and Sartor, 1993; formalin solution onboard. A total of 1048 S. orbignyana D’Onghia et al., 1996; Salman et al., 1997). As part of their individuals (538 males and 510 females) were collected. The dorsal mantle lengths (MLs) were measured within 1 work regarding cephalopod fishery in both the Aegean Sea mm, total body weights (TWs) within 0.01 g, and gonad and the eastern Mediterranean Sea, Salman and Katağan weights (GWs) within 0.0001 g of precision. Specimens (2004) reported that S. orbignyana is the most abundant were examined under microscope after dissection. A cephalopod bycatch species from depths of 100–200 m. In maturity stage was assigned visually using a universal European countries it is consumed fresh or frozen (Jereb maturity scale adapted for cuttlefish by Arkhipkin and Roper, 2005). (1992). Gonadosomatic indices (GSIs) of both sexes were Unlike common cuttlefish Sepia officinalis, data on the calculated for each sampling period (GSI = (GW/TW) × reproductive biology of S. orbignyana are scarce (Hastie 100) (Gabr et al., 1998). Subadult and adult large female et al., 2009). The species has been studied in the western cuttlefishes were then dissected and the ovary and oviducts Mediterranean Sea (Mangold-Wirz, 1963), but not in the were excised; out of 26, 4 were stage II, 5 were stage III, 5 eastern part of this water body, which is different in many were stage IV, and 12 were stage V. Potential fecundity (PF) oceanographic and biological aspects (Sonin et al., 2007). of females was calculated as the sum of the oocytes in the The aim of this study is to describe different aspects ovary plus the eggs in the oviduct. Since the fixated stage V of the species’ reproductive biology such as fecundity, oviduct eggs were torn during counting in the laboratory, spawning strategies, and gonad histology, which knowledge true potential fecundity could not be estimated. To get is necessary for sustainable management of its stocks. true totals of oviduct eggs, the unfixated mature stage V * Correspondence: [email protected] 576 DURSUN et al. / Turk J Zool 38.2°N 38.0°N 37.8°N 37.6°N 26.6°E 27.0°E 27.4°E Figure 1. Sampling stations (A: 150 m; B: 350 m; C: 550 m). female specimen oviducts were dissected and oviductal 3.2. Bathymetric changes in cuttlefish eggs were fixated separately during trawling. All oocytes The minimum monthly average mantle length of females from the ovaries and the oviducts were counted separately was recorded in May (38.66 ± 14.39 mm), and the maximum and measured along the major axis to the nearest 0.1 was recorded in November (67.54 ± 7.55 mm). In males, mm. Spermatophores were counted in 16 mature males, the minimum monthly average mantle length occurred in and a total of 30 spermatophores were measured in each January (45.01 ± 8.86 mm) and the maximum occurred in specimen. November (60.45 ± 9.59 mm), though no monthly trend To validate our conclusions on oocyte development, was obvious (Figure 3). histological studies were used. Samples from ovaries were When the combined data of the bathymetric distribution first rinsed with water. After that, they were dehydrated in of the MLs were examined, 73.8% of the MLs at 150-m a graded ethanol series (dehydration processes started with depths were between 22 and 85 mm, and the average ML 70% alcohol and increased to a series of 96% and 100% alcohol) and then stained with Mallory’s hematoxylin and 100 eosin to reveal the start of yolk accumulation. Mallory’s hematoxylin stains the membrane and proteinaceous Fema le N = 538 90 TW = pow (ML,2.55267) * 0.000802773 structures like yolk droplets blue, and eosin stains R-squared = 0.956003 cytoplasmic structures pink (Laptikhovsky and Arkhipkin, 80 2001). The slides were examined using a CX-31 phase 70 Male N = 510 contrast microscope and photographed with an Olympus TW = pow (ML,2.30968) * 0.0019176 ) R-squared = 0.863104 DP-20 digital camera. (g 60 t gh Histological study of mature gonads with ripe eggs was 50 we impossible because of the very large size of the oocytes. l ta 40 To 3. Results 30 3.1. Cuttlefish size and weight Females were the larger sex (Figure 2); their size in 20 monthly samples varied between 22 and 90 mm ML versus 21 and 78 mm ML in males. The length–weight relations 10 2309 were estimated as TW♂ = 0.0019 ML and TW♀ = 0 2552 0.0008 ML for males and females, respectively. When 0102030405060708090100 the length–weight relationships were compared by t-test Mantle length (mm) (P > 0.05), it showed that there was a difference (ttab < tcalc) Figure 2. Length–weight relationship between the 2 sexes of S. between the sexes. orbignyana from the Aegean Sea. 577 DURSUN et al. / Turk J Zool 80 Male Female + 70 m) (m 60 th ng 50 le le nt 40 Ma 30 20 08 08 08 08 8 08 08 08 08 09 09 09 09 r- - - l- -0 - t- - - - - r- r- p ay un u g ep c ov ec an eb a p A M J J Au S O N D J F M A Figure 3. Monthly average length and standard deviation distribution of S. orbignyana in the Aegean Sea. and standard deviation was 53.47 ± 13.92. At a depth of 350 diameter (Figure 3). Oocyte growth and maturation was m, 20.1% of MLs of the specimens were between 21 and 90 asynchronous, and oocytes of 0.1–2.0 mm predominated at mm, and the average ML and standard deviation was 56.12 all maturity stages (Figure 8). There was no evidence of egg ± 13.52 mm. At a depth of 550 m, 6.1% of the specimens’ size increase with an increase in female ML (r = 0.0407), but MLs were between 25 and 82 mm (Figure 4). the sample size was too small to judge this. 3.3. Maturity Mature males had between 68 and 1055 (mean: 485) The smallest mature female was of 36 mm in ML, and the spermatophores. Spermatophore length (SpL) increased smallest mature male was of 32 mm in ML. The size at with male size (Figure 9). The calculated SpL/ML index varied between 7.7% and 12.7% (mean 10.2%). maturity (ML50) was 70 mm for MLs in females and 50 mm for MLs in males (Figure 5). Maturity increased with ML 3.5. Ovary development (Figure 6). Asynchronous oocyte development was obvious after The mean monthly female GSIs demonstrated 2 annual maturity stage I (Figures 10A and 10B). The connective peaks, in spring (May) and in autumn (November). Male tissue in the center of the gonad holds the oocytes together GSIs were similar throughout the year (Figure 7). and provides nourishment via the net of blood vessels. 3.4. Fecundity Growing oocytes lie more sparsely in the ovary. Potential fecundity of females (60–84 mm ML) varied between 201 and 1532 eggs. Mature specimens had from 4 to 4. Discussion 82 ripe eggs of 6.7–8.3 mm (average: 7.9 mm) at the largest The earlier maturation and thus the smaller size of males are in agreement with data from the Strait of Sicily by 25 Ragonese and Jereb (1991) and from the Adriatic by Bello Fema le; N= 375 20 (2001).