Reproductive biology of the rayed pearl oyster (Pinctada imbricata radiata, Leach 1814) in Izmir Bay

The subtropical rayed pearl oyster P. imbricata radiata (Leach 1814) is native to the Indo-Pacific region and has been recorded in the eastern Mediterranean Sea since 1892 (Dautzenberg 1895). The pearl oyster P. imbricata radiata is a bivalve species belonging to the Pteriidae family. It is a Lessepsian species (Dogan & Nerlovic 2008; Deidun et al. 2014), occurring along the Mediterranean and Aegean coasts, with a significant presence in Tunisia, Sicily (Italy), Malta, Croatia, Portugal, Montenegro, Greece and Turkey (Streftaris et al. 2005; Tlig-Zouari et al. 2010; Antit et al. 2011; Derbali et al. 2011; Lodola et al. 2013; Dogan & Nerlovic 2008; Katsanevakis et al. 2008; Gavrilovic et al. 2017; Petovic & Macic 2017; Theodorou et al. 2019).

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 a.

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 Pinctada fucata martensii (= P. radiata) occurred in summer and fertilization continued until September (25°C; July maximum temperature of 28.3°C). The spawning of P. mazatlantica in Mexico was associated with high water temperature (27°C to 30°C; Saucedo & Monteforte 1997). Behzadi et al. (1997) reported that the beginning of P. fucata breeding in the Persian Gulf was observed when the temperature started to rise in spring and summer, i.e. at 27.6°C in April and 31.7°C in June. On the other hand, the breeding period continued for a considerable part of autumn at temperatures ranging from 32°C in October to 24°C in December. In a similar study on P. radiata conducted in Tunisia, it was found that the development started in March when the water temperature reached 17°C. The first spawning period occurred when the seawater temperature rose from 27°C in May to 32°C in August. The second spawning period occurred when the water temperature dropped from 30°C in September to 20°C in November (Lassoued et al. 2018). It was concluded that high temperatures affect the release of gametes and a decrease in temperature enabled the gonads to mature quickly in a short time (Lassoued et al. 2018). In our study, the reproduction activity of pearl oysters decreased with decreasing water temperature. Suarez et al. (2005) stated that high and low temperatures had different effects on oogenesis and spermatogenesis in their studies. Derbali et al. (2009) reported that the first increase in breeding activity in Tunisia was associated with the seawater temperature rising from 26.7°C in May to 29.7°C in June, while the second spawning occurred when the temperature dropped from 25.5°C in September to 20.6°C in October. Another study on P. radiata in Tunisia reported that a breeding peak occurred at about 25°C (Zouari & Zaouali 1994). Khamdan (1998) reported two peak periods for P. radiata in Bahrain (August–September and November–December) between 20°C and 30°C. A study from Kenya reported that P. radiata at two different locations matured at a temperature of 26°C to 32°C throughout the year, with a breeding peak at a temperature of 26°C to 29°C (Kimani et al. 2006).

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 P. radiata was probably associated with changes in water temperature accompanied by fluctuations in salinity, and salinity was a factor to be considered. In addition to the effect of environmental parameters on reproduction, the availability and abundance of food in the natural environment play an important role in the reproductive cycle (Delgado & Camacho 2007; Gervis & Sims 1992). Urban (2000) reported that the spawning of P. imbricata in the Caribbean occurred during the upwelling season, when food availability was higher. The phytoplankton concentration was generally higher in spring and early autumn compared to summer and winter (Gómez & Gorsky 2003; Valiela & Cebrián 1999). In this study, chlorophyll a reached the highest level with a value of 4.645 μg l⁻¹ in May. It appears that the peak of nutrient abundance in water triggered pearl oysters to start spawning. Chlorophyll a values were determined as 3.633 μg l⁻¹ and 3.293 μg l⁻¹ between July and August (spawning peak months), respectively, and decreased to 1.192 μg l⁻¹ in September.

In this study, spawning of P. imbricata radiata was observed in all months from April to February except for March. The spawning peak was observed in July and August, but June and September should be mentioned too as the GI was above 2.5. In the studies on spat collection conducted in the same region, it was found that P. radiata spats were mostly collected in July, August and September (Yigitkurt et al. 2017; Yigitkurt et al. 2020). However, in a similar study conducted on P. radiata in Tunisia, the reproduction period continued between May and December, and two different breeding peaks were observed in July and November (Table 2; Derbali et al. 2009). It was also reported that the spawning peak of P. radiata in Tunisia was in June (Zouari & Zaouali 1994). Another study conducted in Tunisia reported that P. radiata reproduced in June, September and November, and the spawning peak occurred in June (Lassoued et al. 2018). The study on the reproduction of P. radiata conducted in Iran reported that the mature stage was observed between February and April, and the spawning peak was in summer (Karami et al. 2014). In Bahrain, reproduction of P. radiata was observed between May and November, and the spawning peak was observed from January to March, with another breeding peak occurring in October (Khamdan 1998). In a similar study conducted in Kenya, it was determined that the gonadal activity of P. radiata was relatively continuous and its reproduction peak was in July and October (Kimani et al. 2006). Reproduction of P. fucata martensii in South Korea was observed from April to August, and the spawning peak in June and July (Choi & Chang 2003). In the study conducted on P. imbricata in Colombia, reproduction was reported from December to June and October, with the spawning peak in March and October (Urban 2000). A similar study conducted in Australia reported that the reproduction period of P. imbricata varied from year to year, so in the first year of the study it was observed from October to April, and in subsequent years from May to August and from April to July, while the spawning peaks were observed from December to January and from March to May (O’Connor & Lowler 2004).

In the study on the growth and gonad development of the pearl oyster (P. margaritifera) in the Gulf of Aden, the female to male ratio was determined as 1:1.2 (Aideed et al. 2014). In the study carried out in Gazi Bay, the female to male ratio for pearl oysters P. imbricata was 0.76:1 (Kimani et al. 2006). In this study, 44.44% of the individuals were determined as females and 33.59% as males, while 21.69% of the individuals could not be identified due to inactive gonads and 0.27% of individuals were hermaphroditic (Fig. 6). The female to male ratio was 1.32:1 and, in contrast to the above-mentioned studies, females dominated in the population. A positive correlation was found between the female to male ratio and temperature (p < 0.05). Only one individual in the studied population was hermaphroditic, which indicates that hermaphroditism is a very rare condition for this species.

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 P. radiata is a protandric successive hermaphrodite species.

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 P. radiata, the GI was referred to as “Mature Index”, with the highest value in June (4.2) and the lowest in March (1.3; Lassoued et al. 2018). These reported values were almost consistent with our study. The GI results reflect the identified gonad development stages. The increasing index indicates that the gonads are developing, while the decreasing index indicates the continuation of ovulation (Raleigh & Keegan 2006). A very strong correlation between the GI and the water temperature was found in this study (p < 0.05).

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 P. radiata were recorded in August–September and December (Lassoued et al. 2018). Le Moullac et al. (2012) associated changes in the CI with weight loss caused by gamete oscillations, demonstrating a certain degree of consistency in histological analysis of the population.

It was the first study to determine the reproduction characteristics of the rayed pearl oyster P. imbricata radiata in Izmir Bay, Turkey. As a result of histological examinations, it was concluded that July, August and September were the months when reproduction was most intense and a single peak period was determined in the study area. The reproductive activity was observed throughout the year except for March and April. It was revealed that the condition index and meat yield values decreased in the months when the reproductive activity increased. The reproduction and condition index were correlated with water temperature, salinity and chlorophyll a values. These results were the first for the region and will serve as a reference for further studies.