The Reproductive Cycle of Potomida littoralis (Cuvier, 1798) (Bivalvia: Unionidae) in Lake Golbasi, Turkey.
In this work, reproductive cycle of Potomida littoralis, including histological description and indices of gonad maruration were investigated. There is no data previously available on the species. A total of 300 individuals were monthly collected from September 2009 to August 2010 in Golbasi Lake, Turkey. P. littoralis is dioecious and although males tended to predominate, the sex ratio was not significantly different from the expected 1:1 ratio (p Greater than 0.05). Calculation of the condition index (CI), gonadosomatic index (GSI) and histological examination of the gonads showed that gametogenesis began in January. Spawning occurred in June. Annual maximum GSI value peaked in May. A decrease of CI was observed during gametogenesis. When mussels had the highest GSI value, CI was the lowest value.
This results suggest that gametogenesis and reproductive cycle are the key factor in mussels physiology and important for captive breeding/artificial mussels production and conservation status (e.g. When to obtain gravid females, when to relocate, when to restock, when to introduce fish host, when not to allow harvesting).
Key Words: Reproductive cycle, gonadostomatic index, condition index, freshwater mussel, sex ratio.
Freshwater mussels (Unionoidea) are among the most endangered invertebrates in the world (Machordom et al. 2003; Nagel, 2004; Strayer et al., 2004; Lydeard et al., 2004; Gomez and Araujo, 2008). Their decline is the result of increasing human alterations regarding freshwater habitats, such as water transfer, water abstraction, river channelization, dredging, impoundment, collecting of mussel, pollution, lack of host fish etc (Vaughn and Taylor, 1999). A total of 200 unionoid species are on the Red List of the IUCN (The International Union for Conservation of Nature) (IUCN, 2012). Although Potomida littoralis is not yet protected under European legislation and it has also not been listed in the Red List of the Invertebrates of Turkey. But it has been recently listed in the Red List of the Invertebrates of Spain (Araujo, 2006).
Given the limited resources for species-by species approaches to conservation, it has been suggested that conservation biologists examine and identify reproductive biology. Reproduction biology and ecology of juvenile and mature mussels are key factors that determine the survival abilities of freshwater mussel populations.
Turkish P. littoralis belongs to the family Unionidae, order Unionoida. There are three subspecies of Potomida native to the Golbasi Lake; Potomida littoralis delesserti, Potomida littoralis semirugata and Potomida littoralis homsensis (Schutt, 1982). The generic name of this species Psilunio, Potomida and Unio, is still under discussion (Araujo, 2008). This author suggested using Potomida littoralis as a valid name for the West European populations.
There have been several studies on unionoids in Turkey. Cek and Sereflisan (2006) studied on Unio terminalis delicatus. They concluded that this species has great potential for aquaculture use. The glochidium of P. littoralis as a hookless larvae has been first described by both Guisti (1973) and Araujo et al. (2009). Later Sereflisan et al. (2009a) studied on three species of freshwater mussels including Potomida littoralis. According to that study, the glochidia of P. littoralis which were parasitic on the gills of freshwater fish, have no hooks. Following these studies, Sereflisan et al. (2009b) examined gametogenesis hermaphroditism and gametogenic cycle of Anodonta gabilotia pseudodopsis. Nagel (2004) studied first the reproductive biology of P. littoralis. He stated that this species was most likely a tachytictic consecutive brooder. But, Nagel (2004) used only macroscopic features in P. littoralis from different European countries.
However, without examining testes and ovaries under light microscopy above conclusion remain doubtful. Since research by Cek and Sereflisan (2011) on a unionoid is comprehensive. They demonstrated that CI and macroscopic observation of the gonads are inadequate measure of reproductive activity. Their study also provides the first quantified histological analysis of temporal changes in spermatogenesis and egg production in an Unionid.
This paper describes in detail the gametogenic cycle of P. littoralis in Golbasi Lake, South Eastern Turkey. The gametogenic cycle, oocyte growth and sex ratio are described using histological analysis. These data will be essential to improve understanding of unionid biology (i.e. reproductive season and population sex ratio) and hence to make this information relevant for promoting a future extensive culture for this species, and to design action plans aimed at conserving the population.
MATERIALS AND METHODS
Specimens of P. littoralis were collected by scuba diving (1-6 m depth), in one area of the Golbasi Lake, a major water storage located c. 50 km east of Antakya. The site was deep lake (Fig.1); this site was classified as first-degree clean water by Sereflisan et al. (2009a). Total area of Golbasi Lake is 1200 ha which consists of 400 ha with marshy area. The lake is fed by underground water and used for agricultural irrigation and recreational facilities.
Sampling was carried out between September 2009 and August 2010. The condition index (CI) and gonodosomatic index (GSI) were estimated from 25 specimens, measuring between 4.70+-0.52 and 12.45+-01.18 cm in shell length, sampled every 30 days. The bivalves were washed in the lake water, were transported over ice in a cooler box and were processed within 24 hours. In the laboratory, shell length (SL), height (SH), and width (SW) were recorded to the nearest 0.01mm. The shell was opened and the soft body removed and weighed for the total weight of wet tissue (TWW) to the nearest littoralis incubates the embryos in the four gills. In the middle portion of the inner demibranchs of the females the interlamellar septa were distinctly thickened to provide structural support for the developing young (Jupiter and Byrne, 1997). This was a permanent feature and in non-brooding specimens facilitated identification of females.
Determination of sex was also made macroscopically. Since the visceral mass of the P. littoralis was thick and gametes were often evident. To test whether the sex ratios observed were significantly different from the expected sex ratios of the mussels-based on secondary sex characteristics and on gonad histology the Chi- Square (kh2) test was used (Zar, 1996).
Ovaries and testes samples from specimens for each month were directly fixed in 10 % neutral buffered formalin. After being, preserved in formalin for about one week, transverse sections of the central portion of the gonad samples were dehydrated in graded ethanol, embedded in paraffin, sectioned at 5mm and stained with haematoxylin and eosin (Merck) for histological examination (Cek and Sereflisan, 2006). After histological work, all slides were examined under a light microscope (CH-2 Olympus-Japan). Developmental stages of female and male gamete cells were identified according to descriptions given by Cek and Sereflisan (2006) and Sereflisan et al. (2009a). The stages of oocytes and spermatozoa development were classified on the basis of observations of changes in the nucleus, nucleoli and cytoplasm.
The gonads surrounded the glandular digestive tissue and the gut. They were diffused organs consisting of highly branched follicles surrounded by connective tissue and haemocoel spaces. In P. littoralis male and female gametes were separately organized in follicles (Figs. 2C, D; 3C, D). The oogenesis of the P. littoralis was divided into five stages: oogonia, early vitellogenic oocytes, vitellogenic oocytes, late vitellogenic oocytes and mature oocytes (Fig. 2A, B, C).
Spermatogenesis was also divided into five stages: spermatogonia, primary spermatocyte, secondary spermatocyte, spermatids and spermatozoa. Oogenesis was intense in January, February and March. In March, the ovarian follicles were well-ordered, situated radially around distal genital ducts. Oogonia cells were present in the follicle of the P. littoralis throughout the reproductive cycle (Fig. 2D). This stage was mostly detectable in August and September.
At the beginning of cytoplasmic growth, each oocyte had an egg stalk and was attached to the follicle walls of the oogenic follicle (Fig. 2B). Most of these oocytes retained their attachment to the germinal epithelium, by this basal stalk until an advanced stage of development when they moved to the lumen in preparation for spawning (Fig.2A, D).
Previtellogenic and early vitellogenic oocytes were present for most of the year and these were scattered along the follicular wall. Throughout the year some females contained a large store of unspawned eggs while others had fewer loosely arrayed oocytes. In February, March and April, many small early vitellogenic oocytes were attached to the thickened follicle walls (Fig. 2D). In July the follicle wall became thinner relative to the early developmental stages (Fig. 2A). The ovaries reached their maximum gravid stage in May. At this time they were filled with fully-grown eggs and the inter- follicle space was minimal. After the onset of spawning June/September the eggs were loosely arrayed and the follicles were less crowded (Fig. 2C). This condition was maintained through the spawning season, during the autumn month. In the spawning season some post-ovulatory follicles had an opening to the ciliated gonoduct through which mature oocytes had been released (Fig. 2E).
At the end of the breeding season in November all the mussels had spent gonads containing few or no oocytes and gonads were almost completely replaced by connective tissue (Fig. 2E, F). Ripe mussels of both sexes were dominant in May. P. littoralis with no gametogenic activity predominated in November and December. These gonad sections contained no follicles at all or only a very few contracted follicles between connective tissue, and showed resorbtion of the undischarged eggs in follicle of the females (Fig. 2F). In some females, very thin follicle cells occasionally still surrounded the oocytes. In November follicles were occasionally disturbed. Such follicles suggested degenerating ovarian follicles with granular follicle cells (Fig. 2F). Degenerating female follicle and Atretic oocytes were clearly detected in post-spawned P. littoralis in December (Fig. 2D, F).
Gametogenesis in male P. littoralis had the similar continuous pattern seen for the females (Fig.3A-F). The male follicle also contained sperm at various stages of development with clusters of spermatocytes and spermatids along the male follicular wall. The testicular follicles were neat and regularly arranged in spring months (Fig. 3A). Spermatogonia cells were also present in the male follicle of the P. littoralis throughout the reproductive cycle. Spermatids were polyhedral and the nucleus was completely homogeneous. The spermatids developed into spermatozoa (Fig. 3B). Their diameter was recorded, as 3.4um. Spermatozoa were smaller than the spermatids and were strongly basophilic. Its diameter was 2 um. Yellow-brown granules were a common feature of the follicles in September and December. Minute Yellow-brown granules were also often seen in the epithelia of the genital ducts (Fig. 3F).
In June the follicles contained a quantity of sperm, which in many males was flooding into the genital ducts (Fig.3D). It was clear that mature spermatozoa exited a male follicle through a ciliated gonoduct (Fig. 3E). Sperm morulae were detected in May, June and July and in most study specimens. Sperm morulae, multi-nucleated aggregations of sperm cells were also common (Fig. 3A, B). Males partly spawned in April. In June, July and August male gonad was almost identical to that observed in April (Fig. 3). In October, the follicle contained mature spermatozoa, many of which were degenerating. Male follicle was also degenerating. (Fig. 3E, F). By December, the male follicle was almost empty and spermatogonia were at the male follicle periphery (Fig. 3E). The entire male gamete cell line from the spermatogonia to the spermatozoa was present in spring and summer months.
In two of the tree hundred specimens, the demarcation of the two advanced oocytes were easily discernible microscopically in the male gonads. But no female follicle was detected. Male follicles were arranged in brown clusters, while mature oocytes were located in the male gonoduct (Fig. 4A-C). and therefore their sex was readily identified. Of the 300 Golbasi P. littoralis examined, 161 (53.66%) were males, 137 (45.66%) were females. The male: female sex ratio (1.17M: 1F, n=300) did not differ significantly (p Greater than 0.05) from the expected ratio of 1M: 1F. Two micro hermaphrodite P. littoralis was observed at the lake (Table I).
Table I.- Ratios of absolute and relative (%) frequencies of male (M) and female (F) Potomida littoralis from Lake Golbasi between September 2009 and November 2010 with results of the Chi- Square (kh2) test for a significant difference from 1:1 in the sex ratio.
Year###Sex distribution###Sex ratio (%)
###(Female: Male)###F : M
###F : M###
2009-2010 137:161###45.97:54.03###1.93, d.f.= 1,n.s.
Results of the condition index calculations for P. littoralis, from September 2009 to August 2010 are represented in Figure 5. In the 2009-2010 breeding season, a gradual increase of CI from May (9.75+-0.35) to August (13.99+-0.92 g) did coincide with spawning. Condition index dropped dramatically from September (13.25+-0.49) to November (11.56+-0.94) when most of P. littoralis released their gonadal mass through spawning (Fig.5). During the 2009 to 2010 season, the mean CI ranged from 9.75+-0.35 to 13.99+-0.92 g. The peak CI was recorded in August (13.99+-0.92 g). CI varied seasonally which was expected since reproductive development typically drives a seasonal physiological cycle.
Results of the gonadosomatic index calculations for females and males, from September 2009 to August 2010 are represented in Figure 6. In the 2009-2010 breeding season, there was one major period of spawning. In October gonads of males and females were almost empty (Fig. 6). During the 2009 to 2010 season, the index ranged from 15.95+-1.13 to 28.37+-0.93g. The peak GSI was recorded in May (28.37+-0.93g for females, 22.51+-0.79 for males). The index then dropped dramatically to 23.27+-1.19g in June and 21.21+-0.8g in July for females. Similar observations recorded for males. The lowest value of GSI was recorded for females (17.97+-1.02) and males (15.95+-1.13) in September. In this month gonads of males and females were almost empty.
DISCUSSION AND CONCLUSION
The present study briefly described histological characteristics of developing oocytes that were assigned to 5 stages. In P. littoralis, as in other unionids, oogonia turned into early vitellogenic oocytes, which subsequently grew within follicles, formed vitellogenic oocytes, entered late vitellogenesis, underwent maturation, and finally were ovulated into marsupia. During these phases the changes were similar to those previously reported for other unionids (Grande et al., 2001; Park and Chung, 2004; Cek and Sereflisan, 2006; Sereflisan et al., 2009a). A number of studies exist on various aspects of spermatogenesis in unionids (Park and Chung, 2004; Cek and Sereflisan, 2006, 2011; Sereflisan et al., 2009a). As in oogenesis, spermatogonia undergo proliferation, growth and maturation and division. However, unlike oogenesis, the growth stages were not clearly defined. In spermatogenesis there was a transformation stage at the end.
In another words, the proliferation of spermatogonia was a gradual but short process in P. littoralis. The proliferation of sperm cells occurred suddenly in contrast to the slower maturation of oocytes.
In P. littoralis gonadal tissue intermingles with the digestive cells as in other unionoids in which gonadal tissue occurs among gut loops and even enveloping the digestive gland (Cek and Sereflisan, 2006, 2011; Sereflisan et al., 2009a). The footed stalks and microtubules of the oocytes of the Turkish P. littoralis were similar to those described in a Finland freshwater mussel species, Margaritifera margaritifera (Hansten et al., 1997). The genital canals of P. littoralis had ciliated cells and mucous cells. The mucous cells were mostly basophilic as they were in M. margaritifera (Hansten et al., 1997; Byrne, 1998), Unio terminalus delicatus (Cek and Sereflisan, 2006), Anodonta gabillotia pseudodopsis (Sereflisan et al., 2009a) and Leguminaia whaetleyi (Cek and Sereflisan 2011). Because the oocytes apices were free even in the ovary studied in October, the flat cells maybe abnormal vestiges of follicle cells.
Because all the oocytes were nearly of similar size, the ovaries thus are assumed to be nearly mature. In the present study, sperm morulae were found in dioecious and microhermaphrodite specimens this finding is contradictory to those of Grande et al. (2001). They concluded that sperm morulae are a sing of microhermaproditism in M. margaritifera. Coe and Turner (1938) explained cytolysis of sperm morulae in Mya arenaria as a possible way of supplying nutrients and according to Kotrla (1989) these structures are evidence of abnormal spermatogenesis in certain bivalves. Heard (1975) suggested that some sperm morulae become mature sperm although their viability is unknown. Heard (1975) found sperm morulae in June in Anodonta grandis, but by July all sperm morulae had disappeared and the follicle were full of mature sperm.
Our study suggests that sperm morulae are simply clusters of spermatids and become mature sperm when environmental conditions are suitable. Our data concurs with data for Anadonta grandis (Heard 1975), Unio terminalis delicatus (Cek and Sereflisan, 2006), Anodonta gabillotia pseudodopsis (Sereflisan et al., 2009a) and Leguminaia whaetleyi (Cek and Sereflisan, 2011). Similar to those of Heard (1975) we found sperm morulae in May, June and July in most of the studied specimens of P. littoralis but by October all sperm morulae had disappeared and the follicle were full of mature sperm.
In the population studied, P. littoralis appeared to be a dioecious species. Nagel (2004) studied on P. littoralis and showed that sexes were typically separate. Studies of other freshwater mussels show that sexes are typically separate (Pekkarinen and Valovirta, 1997; Cek and Sereflisan, 2006). However some species may become hermaphrodites capable of self-fertilization when population density is low (Ghiselin, 1969; Grade et al., 2000). Moreover some species of bivalvia are recorded as micro hermaphrodite and some true hermaphrodite (Byrne, 1998; Grande et al., 2001). Byrne (1998) found that females predominated in samples of Australian freshwater mussel. Recently Anodonta gabillotia pseudodopsis (Sereflisan et al., 2009a), Leguminaia whaetleyi (Cek and Sereflisan, 2011) were found to be hermaphrodite with self-fertilization capacity.
Seasonal variation in the condition index indicates that the P. littoralis has one large spawning event with various minor spawnings. Seasonal variation in CI is also associated with seasonal fluctuations in food availability (Lee et al., 1999). In our study CI was largely influenced by the gametogenetic cycle. A decrease of CI during gametogenetic period could be explained by the important energetic cost to form reproductive cells. The gametogenetic cycle leads to important variations of body weight due to storage and further use of metabolic reserves and by the production and release of gametes. Kautsky and Wallentinus (1980) showed that over the 90% of the energy goes into gamete production. Thus a positive effect of food supply on mussel growth was covered up by gametogenesis. Lemaire et al. (2006) demonstrated a great influence of gametogenesis on the mussel growth and energy reserves. Their study supported our findings. It seemed that when GSI value was higher, the CI value was lower.
The GSI is widely used as an index of gonadal activity and development and has been particularly useful in the study of the molluscs (Lubet, 1983; Wolff, 1988). An increase in the average value of this index is interpreted as the beginning of sexual maturation, while a sudden drop in this index is indicative of a spawning event. Changes in GSI in females and males followed a similar pattern during gametogenesis in winter months. This finding is similar to that reported for other freshwater mussel species (Alfaro et al., 2003). On the basis of the results obtained from the GSI, it is suggested that P. littoralis posses a single large spawning event in June.
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|Author:||Sereflisan, Hulya; Cek, Sehriban; Sereflisan, Menderes|
|Publication:||Pakistan Journal of Zoology|
|Date:||Oct 31, 2013|
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