The reproductive biology of the tropical rocky oyster Ostrea iridescens (Bivalvia: Ostreidae) on the Pacific coast of Costa Rica

Aquaculture, 101 (1992) 371-378 Elsevier Science Publishers B.V., Amr+erdam

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The reproductive biology oft oyster Osfrea irkdescens ( the Pacific coast of Co Maria-Luisa Fournier ECOTEC Consuhoria Ecolbgica y TPcnica de Costa Rica S.A., Apartado postal 10028. San Josh, Costa Rica (Accepted 23 April 199 I )

ABSTRACT Fournier, M.-L., 1992. The reproductive btology of the tropical rocky oyster Osrrea iridescens (Bivalvia: Ostreidae) on the Pacificcoast ofCosta Rica. Aquaculture, 101: 371-378. A histological survey of the gametogenic cycle of the oyster Ostrea iridescens was conducted in Costa Rica, Central America, during 1986 and 1987. Reproductive activity occurred continuously throia&out the year, ripeness was detected ZPthe rqd of the dry season; and spawnirzg started at the beginning of the rainy season when salinity decreased from 32 to 29O#1o. The reproductive activity was highly correlated with dry weight/wet weight tissue ratios. The ratios val ied widely in the range 0.290.14, with augmented values representing the ripe condition and depressed values the spawning period. Gonadal development was asynchronous and parallel in both sexes, and there were proportionally more females in the larger size classes. Mature individuals of both sexes were detected at a minimum length of I5 mm. The sex ratio was approximately 3: 1 (312 males, 101 females and 57 indeterminates), and sexes were generally separate, though around ~O%I hermaphrodites were encountered. The monthly proportions of females and males suggested sex reversal. Brooding females were not seen, and egg diameter was small (42.5 F 6.7 pm ), suggesting that this species is a broadcast spawner with eggs that develop into plnnktotrophic larvae. The effect of salinity on gonad activity is discussed.

lNTRODUCTION

Qstrxx iridesceros,a synonym of Striostrea prismatica (Bernard, 1983), is a large oyster ( 100-l 30 mm) that attaches to intertidal and shallow subtidal rocks on high energy shores in the tropical eastern Pacific. Recently, almost all of the Costa Rican oyster beds have been overfished for local consumption. The commercial value of 0. irideswns has stimulated the study of its general biology and potential for aquaculture. Limited information is available for Qstrea iridescens. Cuevas and Martinez ( 1979 ) surveyed a neotropical population and found a distinct annual reproduction pattern: a gonad resting phase of 7 months with a brief spawn0044-8486/92/$05.00

0 I992 Elsevier Science Publishers B.V. All rights reserved.

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ing period during August and September coincident with a temperature increase above 27.5 ‘C, and constant salinity. In the present study, two natural unexploited oyster beds of 0. iridescens were identified and studied in Cur& Gulf of Nicoya, Costa Rica. The population of both beds was estimated to be about 144 500 individuals, with an average density of 176 oysters/m2, anid a mean length of 75 mm (Campos and Fournier, 1989). The present pa.per describes the annual gametogenic cycle and the relationship between gonadal condition and environmental parameters. MATERIAL AND METHODS

Between 33 and 43 Ostrea iridescens ( 15-150 mm shell length) were collected at monthly intervals from the intertidal northern rocky coast at Curti, Gulf of Nicoya, Costa Rica (Fig. 1 ), between April 1986 and June 1987. Each oyster was measured for length along its largest axis, opened, examined for larvae and its meat removed. Upon microscopic and macroscopic examination of the gonad, the sex of the individual was determined and the reproductive condition was classified into one of the following five stages (modified from VClezand Epifanio ( 1981) ) . Indeterminate. Follicles are present in the gonadal area, but without evidence of gametes. The external appearance of the whole gonad is watery. The complete stomach is visible. Early development. Slight development of the gonad with few small follicles; spermatogonia, spermatocytes or oogonia present, but no free oocytes or spermatozoa. More than 50% of the stomach is evident. Late development. Many follicles with more than 30% of the gametes free in the lumen. Abundant interfollicular connective tissue. Less than 50% of the stomach is apparent. Mature. Increase in ‘total area of gonads, complcgely occupied by follicles with more than 50% of the gametes free in the lumen. Externally, the gonad has a dense and creamy appearance and most of the stomach is imperceptible. Spawned. Partially spawned follicles still contain gametes but these are less numerous than in the ripe stage, and almost empty follicles with few residual oocytes and spermatozoa. The gonad is soft and filled with channels. One half of each monthly sample was used for histological analysis and the other half (about 65-85 mm size) for the determination of tissue dry/wet weight ratios. For histological analysis, two transverse sections 5-6 mm thick were made from each gonad and fixed in saline (30%0) Bouin’s solution for a 24-h period. The flesh was then dehydrated in alcohol, cleared in xylene, embedded in wax, sectioned at 5-6 pm, mounted, and stained with haematoxylin and eosin (Howard and Smith, 1983 ).

REPRODUCTIVE BIOLOGY OF OSTREA IRIDESCENSON

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Fig. 1. Gulf of Nicoya, Pacific coast of Costa Rica. Location c;f the Curir site on the lower gulf.

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Other species bivalves change the volume of flesh after spawning (Broom, 1983; Peredo et al., 1987); therefore the ratio of dry to wet weight of flesh was used as an estimate of condition. For each animal, excess fluid was allowed to drain away and the meat was weighed, dried at 80°C for 48 h and reweighed. Water temperature and salinity data were measured at the study site during sampling. RESULTS AND DISCUSSION

Data concerning the gametogenic cycle of the oysters are indicated in 2. Reproductive activity occurred continuously throughout the year, an

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Fig. 2. Gametogenic cycle of Ostreu iridescensat Cuni, Gulf of Nicoya, Costa Rica. Percentages of indeterminate, spawned, mature, early/late development and proportions of females and ma!cs.

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evidence of a resting period was found. During 9 of the 14 months surveyed, about 50-90% of the population was spawning. Spawning was initiated at the beginning of the rainy season, coincident with a salinity decrease from 32 to 29%0 (Fig. 3 ). Significant negative correlations were found between spawning and salinity, and between spawning and dry weight/wet weight tissue ratio (r= - 0.65 and r= - 0.63, respectively, P< 0.0 1 in both cases). Temperature showed a low variation ( Fig. 3 ) , and it is unclear if a seasonal , pattern existed. Hcwever, a synergistic effect with salinity changes may affect reproduction. Studies on tropical mussels have reported greatest spawning activity during the lowest temperature of the cycle and inhibition of gametogenesis by high temperature; however, the contrary appears in other tropical bivalves (VClez and Epifanio, 198 1) and so behaviour cannot be generalized. Differences in the gametogenic cycle of Crassostrea cucuflata from East Africa were reported dependent upon geographic distribution of the popula-

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Fig. 3. Annual variation of temperature, salinity and t.he ratio dry weight/wet weight of tissue of Oscmz iridescensin Cur& Gulf of Nicoya, Costa Rica. Means and one standard deviation ;are presented. Period of spawning is indicated for reference.

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tions; in temperate waters reproduction was related to seasonal temperature variations, but this environmental parameter did not regulate gametogenesis in tropical populations (Lasiak, 1986). Similar geographic variation may also be the case with 0 iridescens,whose reproductive behaviour in the northern population studied in Mexico is clearly related to temperature (Cuevas and Martinez, 1979). Nigh percentages of fully mature oysters were present at the end of the dry period. There was a strong positive correlation between maturity and dry weight/wet weight tissue ratio (~0.86, P< 0.005). The ratio varied widely in the range 0.29-0.14, with augmented values representing the ripe condition and depressed values the spawning period (Fig. 3 ) The presence of oysters at several developmental stages in the monthly samples indicated asynchronous development within the population. Gametogenesis of the males seemed to parallel that of females; however, there was a higher percentage of females undergoing maturation than males during 1987 (Fig. 2 ). A §tudent’s t-test showed differences in the mean size of the two sexes (males: f 78.93 225.58 mm, n= 336; females: X 89.97 + 26.25 mm, n=83; t= - 3.50; PC 0.05); and there was a higher proportion of females in the larger size classes. The smallest size at which mature individuals of both sexes were detected was 15 mm. The proportions of males of the Japanese oyster Crassostreagigas decreased with increasing shell length (Buroker, 1983). The overall sex ratio was determined to be approximately 3 : 1. Of the 470 oysters sectioned, 66.4% were males, 2 1.6% females and 12.0% indeterminate sex. Sexes were separate, and around 2% hermaphrodites were encountered. Forty percent of the sampled oysters were staged as indeterminate in the middle of the spawning season (Fig. 2 ), suggesting that individuals can spawn more than once during the period. A x2 test showed highly significant differences (PC 0.001) between the monthly proportions of females and males, there were also signs of sex reversal (Fig. 2). Alternative sexuality is characteristic of oysters in which adults are separate sexes and may or may not reverse by the next reproductive season (Mackie, 1984). No previous reco exist on the reproductive habits of the genus Striostrea (Harry, 1985). In oding species about lo-20% of individuals incubate through the spawning phase (O’Sullivan, 1980; Wilson and Simons, 1985 j and species with direct development have large iSalvo et al., 1983 j. In the case of 0. iridescens,brooding females were not seen, Furthermore, eggs size was small (42.5 16.7 pm in diameter), a characteristic of oysters that hadcast their eggs anf,“.develop into planktotrophic larvae (Macki,e, 1984). The effect ofsalinity on gonadal maturation is unclear. Where a correlation has been demonstrated in nature, it may reflect changes in nulri;tion, rather l

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than sa: inity (Angel& 1986). The reduction of salinity, associated with heavy rains, is correlated with changes in levels of nutrients in the upper Gulf of Nicoya; but surface water in the lower gulf (study site location ) is poor in nutrients almost all year-round (Epifanio et al., 1983). Given the lack of productivity data at Cur& it is difficult to relate food abundance to gonadal development of this species. Furthermore, studies on the biochemical composition of oyster tissue would be needed to interpret the conversion of reserve nutrients and the nutrients derived from food source into gamete material (Stephen, 1980). In order to develop larviculture techniques for 0. iridestens, the combined effect of temperature, salinity and nutrition has to be investigated for optimum management of spawners in the laboratory. A broodstock whose gonadal development is in an optimum stage produces the maximum larval survival (Lannan et al., 1980). ACKNOWLEDGMENTS

This research was supported by grant No. 808-86-073 of the Vicerrectoria de Investigation, Universidad de Costa Rica. This is Contribution No. 152 from CIMAR, Universidad de Costa Rica. Thanks are expressed to Rita Vargas for her technical assistance and to Dr. William Szelistowski for reading the manuscript.

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Harry, H.W., 1985. Synopsis of the supraspecific classification of living oysters (Bivalvia: Gry-

phaeidae and Ostreidae). Veliger, 28: 12 I- 158. Howard, D.W. and Smith, C.S., 1983. Histological techniques for marine bivalve mollusks. US Department of Commerce, Massachusetts. NOAA Technical Memorandum NMFS-F/NEC25: 97 pp. Lannan, J.E., Robinson, A. and Breese, W.P., 1980. Broodstock management of C~~~&reu gigas. II. Broodstock conditioning to maximize larvP5survival. Aquaculture, 2 1: 337-345. Lasiak, T., 1986. The reproductive cycles of the intertidal bivalves Crassustreacucullata(Born, 1778) and Perna perna (Linnaeus, 1758) from the Transkei coast, Southern Africa. Veliger, 29: 226-230. Mackie, G.L., 1984. Bivalves. In: A.S. Tompa, N.H. Verdonk and J.A.M. Van den Biggelaar (Editors), The Mollusca, Vol. 7. Reproduction. Academic Press, Inc., New York, NY, pp. 351-418. O’Sullivan, B.W., 1980. The fertility of the Port Lincoln oyster (Ostreaangasi Sowerby) from West Lakes, South Australia. Aquaculture, 19: l-l 1. Peredo, S., Parada, E. and Valdebenito, I., 1987. Gametogenesi,; and reproductive cycle of the surf clam Mesodesmadonacium ( Lamarck, 18 18) ( Bivalvia: Mesodesmatidae) at Queule Beach, Southern Chile. Veliger, 30: 55-68. Stephen, D., 1980. The reproductive biology of the Indian oyster Crassostreamadrasiensis (Pres&on). II. Gametogenic cycle and biochemical levels. Aquaculture, 21: 147-l 53. Velez, A. and Epifanio, C.E., 1981. Effects of temperature and ration on gametogenesis and growth in the tropical mussel Perna perna ( L. ). Aquaculture, 22: 2 l-26. Wilson, J.H. and Simons, J., 1985. Gametogenesis and breedins of 0stred edtdison he west coast of Ireland. Aquaculture, 46: 307-32 1.