The subtropical rayed pearl oyster
Since pearl oyster farming benefits the food and ornamental industries as well as pearl production, it offers significant economic potential due to the valuable species used in rearing (Baqueiro & Castagna 1988; Gervis & Sims 1992; Urban 2000; Sahin et al. 2006; Hernandez-Olalde et al. 2007). The annual market value of pearl culture was 3–5 billion dollars by the year 2000 (Saucedo et al. 2001). The pearl oyster culture industry is not dependent on a large capital (Lodeiros et al. 2002). However, the reason behind the failure in breeding is the lack of knowledge about the species biology and larvae production (Choi & Chang 2003; Gosling 2003; Gribben et al. 2004; Hwang 2007; Wada et al. 1995).
This is the first study on the reproduction activity and the condition index of rayed pearl oysters in this area. The objective of this study is to provide a detailed explanation of the reproductive cycle of pearl oysters in Izmir Bay by analyzing the condition index, meat yield, the gonad index and their correlation with temperature, salinity and chlorophyll
The coast of Karantina Island (38°22′44″N, 26°47′12″E), located in the western part of Izmir Bay (Turkey), was selected as a study area between February 2013 and January 2014 (Fig. 1). Pearl oyster samples were collected from sandy, muddy and stony habitats.
Figure 1
Geographical location of the sampling area (Izmir Bay, Karantina Island, Turkey)

Pearl oysters (n = 30) were collected monthly by divers in the sea at a depth ranging from 3 to 5 m. The length of each individual was measured along its dorsoventral axis. The length of shells was measured with a digital caliper (sensitivity of 0.01 mm). The total fresh weight was measured with an accuracy of 0.001 g.
Temperature, salinity and chlorophyll
Oyster shells were opened using a shell opener and the gonad section was separated with a scalpel. The gonadal tissue was fixed in Davidson's solution for 24 h (Shaw & Battle 1957), and then stored in 10% formalin (Lillie 1965). Samples were subsequently dehydrated with alcohol and xylene series, embedded in paraffin (Histowax, Leica), sectioned to a thickness of 5 μm with a microtome and stained with haematoxylin and 0.5% eosin (Howard & Smith 1983). The obtained sections were examined under a light microscope. The gonadal stages were determined by modifying the number of gametogenic cycles specified by Tranter (1958).
Female and male reproductive cells are not visible. Only connective tissue is observed (Fig. 2a).
Figure 2
Gonadal stages of
a – Stage 0: Inactive; b – Stage 1: Development in male individuals (Fw: Follicular wall, Sd: Spermatid, Sg: Spermatogonia, St: Spermatocyte; c – Stage 1: Development in female individuals (Po: Previtellogenic oocyte, Vo: Vitellogenic oocyte); d – Stage 2: Maturity in male individuals (St: Spermatocyte, Sd: Spermatid, Sz: Spermatozoa, Fw: Follicular wall), e – Stage 2: Maturity in female individuals (Mo: Mature oocyte, Vo: Vitellogenic oocyte, Fw: Follicular wall); f – Stage 3: Spawning in male individuals (Sd: Spermatid, Sz: Spermatozoa, Fw: Follicular wall); g – Stage 3: Spawning in female individuals (Mo: Mature oocyte, Fl: Follicular lumen); h – Stage 4: Spent in males (Fw: Follicular wall, Rsz: Residual spermatozoa, C: Cytolysis, Ct: Connective tissue); i – Stage 4: Spent in females (Fw: Follicular wall, Ro: Residual oogonia, C: Cytolysis)

The first stage in males, where spermatogonia, spermatocytes and spermatids are placed in the follicle. It represents early spermatogenesis. The volume of the follicle decreases and spermatogonia turn into spermatocytes (Fig. 2b). In females, early oogenesis is observed. Previtellogenic and vitellogenic oocytes are located on the follicle wall. At this stage, vitellogenic oocytes grow along the follicle wall (Fig. 2c).
At this stage in males, centralized spermatids are transformed into spermatozoa, filling the center of the follicle. This is followed by a reduction in the number of spermatogonia around the walls of the follicle (Fig. 2d). In females, the volume of vitellogenic oocytes adhering to the follicle wall increases. Mature oocytes accumulate in the follicle lumen (Fig. 2e).
The number of spermatozoa increases in male individuals. Follicles expand. The distance between the follicles decreases (Fig. 2f). The number of mature oocytes in females increases. The follicle volume expands. Follicle walls adhere to each other (Fig. 2g).
At this stage in males, the follicle is almost empty. Few residual spermatozoa are visible. The cytolysis is observed (Fig. 2h). In females, few residual oogonia and cytolysis are visible (Fig. 2i).
The gonad index (GI) was estimated using a numerical grading system based on the maturity stages of pearl oysters (Soria et al. 2002). Based on the gonadal development, three category scores (CS) were defined as follows:
1 = Inactive (I) + Spent (VI), 2 = Development (II), 3 = Mature (III) + Spawning (IV).
The total number of individuals in each reproductive stage is multiplied by the category score and the sum is calculated. The result is divided by the total number of individuals.
The GI was calculated according to the formula presented below (Soria et al. 2002):
To analyze the CI and MY, 30 specimens of pearl oysters were processed monthly. The accompanying parameters were measured for each pearl oyster in grams (g): dry meat weight (DMW) and dry shell weight (DSW) for the condition index (CI), and wet meat weight (WMW) and total weight (TW) for meat yield (MY). The calculation of CI and MY (Walne 1976; Crosby & Gale 1990) was based on the following formulas:
The distribution of data was tested to determine their normality using the Kolmogorov–Smirnov test. Pearson's correlation analysis was applied to determine the degree of association between the environmental parameters and the gonad index, the condition index, and the meat yield. ANOVA followed by Tukey's post hoc test (Zar 1996) was used to confirm differences in the monthly condition index and meat yield. The sex ratio was analyzed using chi-square (χ2). The results were presented as means (standard deviation) and the significance level used for the test was
The average shell length and the total flesh weight of the examined pearl oysters are shown in Table 1. The length of shells measured in this study ranges from 47.79 mm to 100.85 mm (mean lengths 73.21 ± 9.46 mm). The weight of the oysters ranged between 14.02 g and 135.02 g (mean weight 54.09 ± 22.60 g).
Mean length and total fresh weight of pearl oyster samples used in the study
Months | Pearl oyster samples | Mean length | Mean weight |
---|---|---|---|
Feb. | 30 | 73.99 ± 10.67 | 52.72 ± 23.08 |
Mar. | 75.42 ± 8.99 | 60.02 ± 19.30 | |
Apr. | 75.22 ± 9.54 | 61.25 ± 22.23 | |
May | 72.03 ± 9.28 | 51.85 ± 23.03 | |
June | 73.42 ± 11.26 | 57.03 ± 29.62 | |
July | 71.10 ± 9.60 | 54.40 ± 25.43 | |
Aug. | 72.87 ± 9.71 | 56.33 ± 24.46 | |
Sept. | 74.57 ± 11.19 | 60.45 ± 29.50 | |
Oct. | 73.87 ± 6.54 | 53.41 ± 13.59 | |
Nov. | 75.22 ± 9.54 | 55.60 ± 21.98 | |
Dec. | 72.52 ± 5.91 | 49.39 ± 13.58 | |
Jan. | 68.25 ± 6.36 | 41.38 ± 12.37 |
The maximum and minimum water temperature in the region was measured as 27°C in July 2013 and 14.2°C in January 2014, respectively. The lowest salinity value of 35 PSU was recorded in May and the highest in September – 38 PSU (Fig. 3a). The highest and the lowest values of chlorophyll
Figure 3
Environmental parameters in the study area: a) temperature and salinity; b) chlorophyll

Five stages of reproduction were determined according to the cycles of gametes on histological images: inactive, development, mature, spawning, spent.
According to the evaluation of histological sections,
Figure 4
Frequency of gonad development stages in

The overall female to male ratio was 1.32:1 (χ2 test
Figure 5
Changes in the sex proportion (%) in

The GI value was calculated as 1 in March when all individuals were inactive and spent. The highest values of the GI (above 2.5) were calculated in the months of peak reproductive activity of this species (June, July, August and September): 2.8 in July, 2.9 in August and 2.8 in September (Fig. 2c). There is a strong positive correlation between the GI and temperature (
The MY and CI were calculated for pearl oysters, whose average length and weight were 73.21 ± 0.47 mm and 54.09 ± 22.60 g, respectively. The minimum MY was 19.11 ± 0.50 in October, while the maximum MY was 24.8 ± 0.66 in April (Fig. 6). The difference between the monthly mean values of the MY values was statistically significant (
Figure 6
Meat yield (%) and the condition index of pearl oysters in the study area

Gonad development is defined as changes in gonads during inactive reproductive periods, which are complex processes that occur with seasonal changes when appropriate biological and physical conditions are provided (Quintana 2005). Many studies have attempted to explain the effect of environmental parameters on gonadal development and reproduction of different species of bivalve mollusks. Some researchers reported that temperature, as an environmental parameter, has a major effect on reproduction (Behzadi et al. 1997; Choi & Chang 2003; Delgado & Camacho 2007; Wada et al. 1995; Sastry 1979). Wada et al. (1995) reported that various factors such as temperature, salinity and availability of food in the environment can affect the gametogenic cycle of bivalves, and this applies in particular to temperature.
When water temperature increased in April to 18.4°C, the reproductive cells developed rapidly and the maturation process began. During that period, spermatocytes and spermatids from reproductive cells were observed in large numbers in male individuals, while oocytes and oogonia were observed in female individuals. It was found that the spawning phase began as the water temperature increased to 20°C in May. Choi & Chang (2003) reported that oocytes develop and mature as water temperature rises and the reproductive activity of pearl oysters was observed in water with temperature above 15°C. Mature oocytes were released by pearl oysters when water temperature began to rise to 20.1°C. Choi & Chang (2003) reported that the main breeding peak activity of
As an environmental factor, salinity is often considered to a lesser extent in terms of its effects on the survival and distribution of marine organisms and their reproductive strategies (Steel & Steel 1991). Gervis and Sims (1992) reported that ovulation in pearl oysters was usually triggered by a change in environmental conditions, such as an increase or decrease in water temperature or salinity. In this study, the lowest salinity of 35 PSU was recorded in May. Derbali et al. (2009) reported that the spawning season of
In this study, spawning of
Observations of the reproductive status and temperature range in pearl oysters in different areas
Study area | Species | Temperature (min.–max °C) | Spawning periods | Spawning peak periods | Authors |
---|---|---|---|---|---|
South Korea | 13.5–28.3 | April–August | June–July | Choi & Chang 2003 | |
Tunisia | 12–30 | May–December | July–November | Derbali et al. 2009 | |
Iran | – | February–April | summer | Karami et al. 2014 | |
Tunisia | 12–27 | – | June | Zouari & Zaouali 1994 | |
Columbia | 24.7–27.5 | December–June and October | January–March and October | Urban 2000 | |
Bahrain | 15–30 | May–December | August–September and November–December | Khamdan 1998 | |
Tunisia | 17–32 | June, September and November | June | Lassoued et al. 2018 | |
Kenya | 26–32 | July, September–February, April–May | July (site2) and October (site1) | Kimani et al. 2006 | |
Australia | 15–25 | October–April and May–August and April–July (two years) | December–January and March–May | O’Connor and Lowler 2004 | |
Turkey | 14.2–27 | April–January | June–September | this study |
In the study on the growth and gonad development of the pearl oyster (
It was found that the number of females in pearl oysters increases with their length and age, as this is linked to protandric hermaphroditism and the availability of suitable food in the environment (Aideed et al. 2014; Kimani et al. 2006; Peharda et al. 2006; Acarli et al. 2018). Similarly, in this study, 33.33% of the individuals in the 40 to 50 mm length range were females, while 61.53% of the individuals in the length range between 91 and 100 mm were identified as females, and the number of female individuals clearly increased with increasing length of individuals, because
The GI is used to determine the reproductive status of individuals (Karami et al. 2014; Raleigh & Keegan 2006; Le Moullac et al. 2009). The highest GI values were recorded in the summer months when spawning peaked – 2.8 in July and September and 2.9 in August. The GI value (2.5) recorded in June was also very close to the highest value. The GI was 1 in March when there was no reproductive activity. In a similar study from Tunisia on the development of gonads in
Fluctuations in the CI were associated with the nutritional status and reproduction of mollusks (Searcy-Bernal 1984). Le Moullac et al. (2012) reported that the CI was an effective indicator of reproductive events in pearl oysters. The CI and MY in Bivalvia show seasonal variations, which was strongly related to water temperature, food availability and reproductive cycle (Fernandez-Reiriz et al. 1996). Okumus & Stirling (1998) found that the CI and MY in bivalves are affected by various external and internal factors such as water temperature and salinity, food availability and the gametogenic cycle of the animals. The main purpose of determining the CI and MY in this study was to compare seasonal differences in reproductive activity in relation to different gonad stages identified in histological examinations. The maximum CI (12.31) recorded in May started to decrease in July, with the spawning peak in August and September, which was determined as 8.23 ± 1.85 in September. Similarly, MY started to decrease with spawning. A decrease in CI and MY values during the peak of the spawning season is expected due to the release of gametes. The CI values were low due to partial fertilization in the period from October to February. In the study conducted in Tunisia, the lowest CI values for
It was the first study to determine the reproduction characteristics of the rayed pearl oyster
Figure 1

Figure 2

Figure 3

Figure 4

Figure 5

Figure 6

Mean length and total fresh weight of pearl oyster samples used in the study
Months | Pearl oyster samples | Mean length | Mean weight |
---|---|---|---|
Feb. | 30 | 73.99 ± 10.67 | 52.72 ± 23.08 |
Mar. | 75.42 ± 8.99 | 60.02 ± 19.30 | |
Apr. | 75.22 ± 9.54 | 61.25 ± 22.23 | |
May | 72.03 ± 9.28 | 51.85 ± 23.03 | |
June | 73.42 ± 11.26 | 57.03 ± 29.62 | |
July | 71.10 ± 9.60 | 54.40 ± 25.43 | |
Aug. | 72.87 ± 9.71 | 56.33 ± 24.46 | |
Sept. | 74.57 ± 11.19 | 60.45 ± 29.50 | |
Oct. | 73.87 ± 6.54 | 53.41 ± 13.59 | |
Nov. | 75.22 ± 9.54 | 55.60 ± 21.98 | |
Dec. | 72.52 ± 5.91 | 49.39 ± 13.58 | |
Jan. | 68.25 ± 6.36 | 41.38 ± 12.37 |
Observations of the reproductive status and temperature range in pearl oysters in different areas
Study area | Species | Temperature (min.–max °C) | Spawning periods | Spawning peak periods | Authors |
---|---|---|---|---|---|
South Korea | 13.5–28.3 | April–August | June–July | ||
Tunisia | 12–30 | May–December | July–November | ||
Iran | – | February–April | summer | ||
Tunisia | 12–27 | – | June | ||
Columbia | 24.7–27.5 | December–June and October | January–March and October | ||
Bahrain | 15–30 | May–December | August–September and November–December | ||
Tunisia | 17–32 | June, September and November | June | ||
Kenya | 26–32 | July, September–February, April–May | July (site2) and October (site1) | ||
Australia | 15–25 | October–April and May–August and April–July (two years) | December–January and March–May | ||
Turkey | 14.2–27 | April–January | June–September | this study |