Reproductive Cycle of the Traditionally Exploited Sea Cucumber Holothuria Tubulosa (Holothuroidea: Aspidochirotida) in Pagasitikos Gulf, Western Aegean Sea, Greece

Turkish Journal of Zoology Turk J Zool (2014) 38: 306-315 http://journals.tubitak.gov.tr/zoology/ © TÜBİTAK Research Article doi:10.3906/zoo-1302-31 Reproductive cycle of the traditionally exploited sea cucumber Holothuria tubulosa (Holothuroidea: Aspidochirotida) in Pagasitikos Gulf, western Aegean Sea, Greece 1,2, 1 1 Georgios KAZANIDIS *, Alexios LOLAS , Dimitris VAFIDIS 1 Department of Ichthyology and Aquatic Environment, School of Agricultural Sciences, University of Thessaly, Nea Ionia, Magnesia, Greece 2 Current address: Oceanlab, University of Aberdeen, Newburgh, Aberdeenshire, UK Received: 15.02.2013 Accepted: 17.12.2013 Published Online: 21.03.2014 Printed: 18.04.2014 Abstract: The reproductive cycle of the traditionally exploited sea cucumber Holothuria tubulosa was investigated in the Pagasitikos Gulf (39°18′457″N, 23°05′869″E) from June 2007 to July 2008. The study examined the microscopic characteristics of the gonads and was based on maturity index (MI) and oocytes’ size-frequency distribution. The reproductive cycle was found to be synchronous between sexes, following an annual pattern. The minimum MI values were recorded in December and January, marking the onset of the reproductive cycle. During the spring, MI increased due to gamete development and proliferation. Mature specimens were prominent in summer while spawning occurred between July and September. The maximum MI values were recorded in mid-autumn, when most specimens were at the postspawning stage. The oocytes’ size-frequency distribution showed analogous seasonal variability. The present findings are crucial for establishing an efficient management strategy for this commercial and ecosystem-engineering species, since its exploitation in Greek waters has not been under official control for more than a century. The authors propose a seasonal ban on the exploitation of the species from July to September and a minimum individual drained weight limit of 250 g. Key words: Histology, maturity index, gametogenesis, spawning, eastern Mediterranean 1. Introduction Herndl, 1991; Coulon and Jangoux, 1993) and converts Holothuria tubulosa Gmelin, 1788 is a species of sea detritus in nitrogenous compounds, thus enhancing cucumber with a Mediterranean distribution (Borrero- primary productivity (Işgören-Emiroğlu and Günay, Pérez et al., 2009), recorded in various habitats but usually 2007). found in the seagrass meadows of Posidonia oceanica The most comprehensive study on H. tubulosa (Gustato et al., 1982; Bulteel et al., 1992). During the last 2 reproductive biology was carried out in the Adriatic Sea, decades, specimens harvested in Turkish regions have been focusing on the temporal distribution of maturity stages exported as a frozen or dried product to Far East countries (Despalatović et al., 2004), contrary to a number of other (Aydin, 2008; Aydin et al., 2011; Sicuro and Levine, 2011), regions across the Mediterranean, where information where they are regarded as a gastronomic delicacy (Sicuro has been provided through the use of lower-precision et al., 2012) and a source of pharmaceutical compounds techniques like gonad index (Bulteel et al., 1992; Kazanidis (Bordbar et al., 2011). In Greece, H. tubulosa is harvested et al., 2010). However, life-history information acquired by hand or by using hooks and has been utilized as bait in using state-of-the-art techniques is a prerequisite for the longline fisheries for more than a century (Antoniadou and efficient management of natural resources. Vafidis, 2011). In Greek regions, this kind of exploitation The aim of the present study was to elucidate the is not under official control, and preliminary studies reproductive cycle of H. tubulosa in the Pagasitikos Gulf have suggested its contribution to low stocks of natural through the histological examination of its gonads, focusing populations (Antoniadou and Vafidis, 2011). This is of on the temporal allocation of the spawning period, as well high concern, as H. tubulosa is considered an ecosystem- as to provide an indication regarding the environmental engineering species, mainly because of its contribution to conditions involved in the release of the gametes. Up to the bioturbation of the sediments by its feeding behavior now, parameters such as temperature (e.g., Conand, 1993; (Meysman et al., 2006; MacTavish et al., 2012); it stabilizes Chao et al., 1995), photoperiod (e.g., Ramofafia et al., the bacterial community in the sediment (Amon and 2000; Muthiga, 2006), phytoplankton blooms (e.g., Chao * Correspondence: [email protected] 306 KAZANIDIS et al. / Turk J Zool et al., 1995), or lunar cycle (e.g., Purwati and Luong-van, 1753 and patches of rocks, dominated by communities 2003) have been suggested as potential spawning cues for of photophilic algae (Lolas and Vafidis, 2013). The soft temperate and tropical holothurian species. Eventually, it sediment consists mainly of sand fractions and silt, could prove a difficult task to determine which of these with large amounts of detritus that provide a favorable environmental factors is the key driver to this behavior environment for the establishment and development of (Olive, 1995). the sea cucumbers (Mercier et al., 1999, 2000). Since no official regulation exists regarding the Samples were collected between June 2007 and July exploitation of the species in Greece, information on the 2008 on a monthly or semimonthly basis via scuba diving, reproductive cycle of H. tubulosa will be crucial in the reaching a total of 15 samplings. In each sampling event, development of a potential conservation strategy within 20–25 specimens were collected from the soft sediment, the regions of the Greek Exclusive Economic Zone. in depths of up to 10 m, while the seawater temperature was recorded with a Seabird SBE 19Plus CTD instrument 2. Materials and methods (measurement range: –5 to +35 ± 0.0074 °C). The body The present survey took place in the Pagasitikos Gulf, size at first maturity was calculated in terms of the drained which is located in the central-western region of the Aegean weight of the individuals (DW50), according to Conand Sea (Figure 1). It is a semienclosed shallow water basin (1981). After dissection, the gonads from each individual (mean depth is 69 m) in which the water masses are cold were fixed in 10% seawater formalin and preserved and homogeneous in winter (12.6 °C) and highly stratified afterwards in 70% ethanol pending further analysis. in the summer (27.5 °C) (Petihakis et al., 2005). In the The histological examination was carried out using sampling area (Kato Gatzea: 39°18′457″N, 23°05′869″E), the hematoxylin-eosin regressive staining method, the bottom consists mainly of a soft substratum with a accompanied by the use of a light microscope and a digital sparse meadow of the seagrass Zostera marina Linnaeus, camera. From each female, the diameter of 60 oocytes 39° 24’ N 39° 18’ N Kato Gatzea 39° 12’ N 22° 48’ E 23° 00’ E 23° 12’ E Figure 1. Map of the study area with the sampling location. 307 KAZANIDIS et al. / Turk J Zool whose nuclei could be observed was recorded (Doyle onset of the reproductive cycle. The growing stage (II) was et al., 2012) and the values were grouped in 20-µm size observed between March and May, with slight differences classes (Despalatović et al., 2004). The null hypothesis between sexes, thus contributing to the increase in MI of no significant differences in oocyte diameter between values over the spring months. The presence of individuals the samplings and between the seasons was tested using in the mature stage (III) was prevalent over the summer one-way ANOVA, while individual group differences were period (June–August) for both sexes. Individuals in the assessed by Fisher’s LSD procedure. The homogeneity of spawning stage (IV) were present from July to September, variances was tested (Levene test) and, whenever necessary, with slight differences in frequency between the sexes. The the log transformation log (x + 1) was used (Zar, 1996). spawning period was followed by a short postspawning Microscopic features (i.e. type of gametes present in period (V) in October and November, which in turn led the lumen, presence of connective tissue) were used to to the highest values of the MI during the autumn months, assign the individuals to 1 of the 5 developmental stages designating the end of the reproductive cycle. described for H. tubulosa by Despalatović et al. (2004): The variation in the values of oocyte diameters was recovery stage (I), growing stage (II), mature stage (III), significantly different between the samplings 14,7545(F = spawning stage (IV), and postspawning stage (V). The 1718.06, P < 0.0001), as well as between the seasons (F3,7556 relative percentage of the developmental stages at each = 3856.96, P < 0.0001), while the post hoc analysis by sampling was used in the estimation of the maturity index Fisher’s LSD procedure classified the seasons in 4 different (MI) for males and females using the following equation: groups in the increasing order of winter < spring < autumn < summer (Figure 5) The oocytes’ size frequency distribution showed a 5 i⋅n well-marked seasonal pattern (Figure 6; Table 1). During ∑ i December and January, small previtellogenic oocytes with MI = i=1 , a diameter of up to 40 µm were abundant. As oogenesis N progressed during the spring months, a wide spectrum of sizes ranging from 40 to 140 µm was recorded. During where i = developmental stage, n = number of individuals i the summer months, the allocation of the size spectrum in developmental stage i, and N = total number of showed a clear shift towards the upper size classes (up individuals in the sample (Yoshida, 1952). to 200 µm). In spawning and postspawning stages, the presence of oocytes in the upper size classes was reduced 3. Results and the vast majority of relict oocytes were found in the From the microscopic examination of the gonads from size classes of 120 and 140 µm.

Load more