Rabbitfish or spinefoots (Siganidae) are distributed in the Western Indian Ocean, in several localities in East Africa and from the Red Sea to the eastern Mediterranean via the Suez Canal. They are represented by 29 species all over the world (Froese & Pauly 2019), which occur in shallow waters, usually in protected areas, generally in schools of 50 to several hundred individuals grazing on algae (Froese & Pauly 2019). The marbled spinefoot
As the marbled spinefoot is a commercial fish species, it is one of the target species for small scale fishermen in the southern coast of Turkey. Due to its flavor, it is also an important species for recreational anglers. The capture-based Siganidae production was estimated at 86.229 tons in 2015 from the Eastern and Western Indian Ocean, the Mediterranean Sea and the Western Central Pacific (Fisheries and aquaculture software 2019). Although this is of global and regional importance to the fisheries economy, there are no official landing data for Turkey.
There have been many studies on the growth, mortality and yield per recruit of the spinefoot in the Red Sea (El-Gammal 1988; El-Ganainy 2002; Mehanna & Abdallah 2002). In addition, different biological aspects were investigated, including age, growth, mortality, and yield per recruit of
The current study was carried out to determine the annual reproductive cycle of
Fish samples were collected monthly, 20 fish each month, from small-scale (trammel nets) and recreational (angling and pot fishery) fisheries in Gökova Bay, the southern Aegean Sea, between July 2017 and June 2018 (Fig. 1). The total length (TL) was measured in the natural body position to the nearest millimeter. The total weight (W) and weight of gonads (Wg) were measured to the nearest 0.01 g, and sex was determined after the dissection of a specimen. The spawning season was established based on monthly variation in the gonadosomatic index (GSI, %), using the equation GSI = [Wg / (W − Wg)] × 100, where Wg is the weight of gonads (g) and W is the total weight (g) of the fish (Ricker 1975). Sex and maturity were determined based on macroscopic analysis of gonads. Maturity stages were assigned using Gunderson’s (1993) five-stage classification system: stage I = immature, stage II = resting, stage III = developing, stage IV = mature, and stage V = spent. Histological examination was carried out to determine seasonal changes in the gonads. A total of 240 gonad samples were histologically examined. Gonadal tissue samples were fixed in 10% formalin buffered solution for 24 h. They were dehydrated through a graded series of ethanol, cleared in xylene, embedded in paraffin, and sectioned in a Leica 2125 rotary microtome at a thickness of 5 μm. Sections were stained with haematoxylin and eosin (Luna 1982; Bancroft & Stevens 1996) and then examined under an Olympus JX31 light microscope. Samples were photographed by an Olympus E330 digital camera.
Sampling locations (indicated by black dots) to determine the ovarian histology in the marbled spinefoot from Gökova Bay, the southern Aegean Sea
The length of female fish varied from 10.8 to 26.1 cm, with a mean length of 18.7 ± 0.2 cm. Furthermore, the weight of females was in the range of 14.98–293.42 g, with a mean weight of 91.1 ± 2.93 g. The length–weight relationship was W = 0.0065L3.25 (R2 = 0.956), indicating positive allometric growth (t-test,
Length–weight relationship for female marbled spinefoot from the southern Aegean Sea
GSI values began to increase in May, peaked in June and gradually decreased in July, indicating that the spawning season was in early summer. Furthermore, the minimum value was recorded in September, while from September to early May the trend was almost stable (Fig. 3).
Monthly gonadosomatic index (GSI) for females of the marbled spinefoot
Stage I (immature): Samples identified as immature were observed in December and January with an average weight of 112.72 g. The color of ovaries was dirty yellowish-red and gonads were very small and thinly structured.
Stage II (resting): During the sampling process in February and March, ovaries of females were clearly visible with the naked eye. Female ovaries began to have a granular, symmetrical, light pink or transparent structure.
Stage III (developing): Sex can be easily determined with the naked eye. This stage was observed in April, May and June. Eggs had a pinkish and granular structure.
Stage IV (mature): Samples obtained in July included ovaries that filled the medio-dorsal part of the whole body (Fig. 4). Ovaries were orange or pink and surrounded with developed veins. Eggs were composed of big and mature cells.
Mature (stage IV) female marbled spinefoot sampled from the southern Aegean Sea
Stage V (spent): This phase continued from August to November. Ovaries were flaccid, vascularized, salmon pink, oocytes were smaller with the presence of hyaline spaces. The fourth stage was defined as the peak time of matured eggs in July. Spawned females were observed between August and November. Gonads were in the resting phase until December–January and immature individuals were observed starting from January. February and March were considered to be the period when eggs become mature (Table 1).
Monthly changes in the sexual maturity stages of
Years | Months | Sexual maturity stages |
---|---|---|
2017 | February | II |
March | II | |
April | III | |
May | III | |
June | III | |
July | IV | |
August | V | |
September | V | |
October | V | |
November | V | |
December | I | |
2018 | January | I |
The ovarian cycle of
Six-month ovarian cycle of
Six-month ovarian cycle of
Ovarian cells were observed on the edges of the ovarian lamellae. Cells were colorless, with spherical or ellipsoidal shapes. They contained basophilic and homogeneous cytoplasm (Fig. 7A). A membrane-bound yolk sphere was found between cortical alveoli in the peripheral ooplasm. Its location cells was more central compared to the perinuclear space. Egg yolk vesicles lined up around the cytoplasm (Fig. 7B).
First development phase of ovarian cells; A – chromatin-nuclear period, B – chromatin-nuclear period, perinuclear period;
Ovarian cells were surrounded by a series of theca and granulosa cells, which form a follicle from the early stage of the perinuclear phase transition (Fig. 8A). The basal membrane was present within these two cell groups. The follicle was surrounded externally by a series of epithelial cells and internally by zona radiata, which formed the corion.
Components of ovarian cells; A – post-vitellogenesis period, B, C – perinuclear period, Pa – perinuclear area, Kr – chromatin, N – nucleus, Nu – nucleolus, Te – theca cells, Gr – granulosa cells, Zr – zona radiata, F – follicle
In the progressive/upcoming stages of the perinuclear phase, the chromatin material became dense, enclosed within the nucleus wall and the number of nucleoli increased (Fig. 8B). The number of nucleoli reached 16 units. The dimensions of these nucleoli did not vary as much as they did in the chromatin-nuclear phase and they were more or less the same (Fig. 8C).
At the beginning of this phase, the entrance of vitelline globes into the ovum was observed at the cytoplasm periphery. This phase was very rarely observed in ovarian cells, which is related to the short duration of this period. This is yolk phase I, which is the first stage of vitellogenesis (Fig. 9A).
First stage of the second development phase, early vitellogenesis; yolk phase I; A: cortical alveoli phase, B: accumulated vitellin globules around the nucleus observed during the period of cortical alveoli; Ka: cortical alveoli, Zr: zona radiata;
It was observed at the beginning of this phase that vitelline globes entered into the cytoplasm periphery. This phase was rarely determined in ovarian cells, which was associated with its very short duration. This is yolk phase I of the first part of early vitellogenesis (Fig. 9A).
During this phase, vitelline globules grew quickly and accumulated around the nucleus (Fig. 9B). The size of vitelline globules increased between the nucleus and zona radiata, which resulted in the granular form of the cytoplasm. Zona radiata became clear and visible in this phase.
During this phase, which is known as a germinal vesicle or a nucleus migration stage, fat droplets (Fig. 10A) began to accumulate around the germinal vesicle. Fat globules located in this zone began to form fat droplets due to the deformation of the nucleus (Fig. 10B). After accumulation of fat droplets, it was observed that the germinal vesicle and those droplets moved to the animal pole of the ovarian cell (Fig. 10C).
Maturing phase of ovarian cells; A – accumulated fat globules around the nucleus, B – fat globules come together and form fat droplets, C – movement of the germinal vesicle into the animal pole O – oil droplets, Vg – vitelline globules;
Ovaries were hydrated and grew in size after this stage. The ovarian follicle covering the ovarian cell became thinner and the ovary became very large, occupying almost the entire abdominal cavity. Mature oocytes were observed in May–July.
The marbled spinefoot
This study describes the annual gonadal development and the gonadal cycle of
A six-month ovarian cycle was observed in June and July. While the ovarian cells of both the first and second development phase were determined in this period, only the first development phase and mitotic ovarian cells were observed during the other months. It was found that the results of this study and of the previous studies on the reproduction biology of spinefoots show some discrepancies. Ben Tuvia et al. (1966) reported the occurrence of mature females in the southeastern Mediterranean waters between July and November. Amin et al. (1985) stated that the gonadal development of the species starts earlier in the Jeddah part of the Red Sea compared to the Eastern Mediterranean. In fact, the results of Amin (1985), obtained based on various samples collected in the Red Sea, revealed that gonadal maturity was achieved in three months (January–March) and spawning lasted approximately seven months (March–September). This result may be attributed to water temperature, which is higher in the Red Sea than in the Eastern Mediterranean. Ben Tuvia (1985) reported that the spawning season for the species lasts from July to August. According to Hussein (1986), the spawning season of this species in the Mediterranean coast is between July and September. On the other hand, Golani (1990) reported that the spawning season on the Israeli Mediterranean coast lasts from May to August.
In addition to studies from other parts of the Mediterranean Sea, some works included information on the reproductive biology of the species from the Turkish coast. Akşıray et al. (1954) observed that the marbled spinefoot spread to the southern Aegean Sea from the Mediterranean coast and its spawning season lasted from early to mid-summer. Torcu et al. (1994) reported the reproduction season of the species in the Mediterranean between April and August. Results of the histological analysis conducted in our study (Table 1) revealed that the marbled spinefoot in the southern Aegean Sea reproduces in June. Furthermore, the reproduction period of the species was determined by Yeldan and Avşar (2000) as July and August. The difference between our study and the study by Yeldan and Avşar (2000) is not only attributed to water temperature, but may also be due to feeding habit, stomach fullness of the examined individuals and the sampling method.
Research on the histology of
Histological studies of gonads in the Siganidae family were performed for only three species. Particularly evident is the lack of studies focusing on the spawning season and gonadal development of invasive