The reproductive cycle of Littorina kraussi was determined on the basis of changes in gonadal histology over a 14-month period. This animal is dioecious, the sexes being evenly distributed both in terms of numbers and size. Despite some asynchrony within the population, L. kraussi showed a well defined reproductive cycle. Gonadal proliferation took place from August to January with peak spawning taking place from December to March.S. Afr. J. Zool. 1987, 22(2

Lasiak, T

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170 Short Communications Reproductive cycle of the supralittoral gastropod Littorinll kraussi (Rosewater, 1970) Theresa Lasiak Department of Zoology, University of Transkei, Private Bag X1OO1, Umtata, Transkei Received 23 April /986; accepted 16 September 1986 The reproductive cycle of Littorina kraussi was determined on the basis of changes in gonadal histology over a 14-month period. This animal is dioecious, the sexes being evenly distri· buted both in terms of numbers and size. Despite some asyn· chrony within the population, L. kraussi showed a well defined reproductive cycle. Gonadal proliferation took place from August to January with peak spawning taking place from December to March. Die reproduktiewe siklus van Littorina kraussi is bepaal op die basis van vercwldering in gonadiese histologie oor 'n tydperk van 14 maande. Die dier is eenslagtig en die geslagte is eweredig versprei, beide in terme van getalle en grootte. Ten spyte van asinkronie binne die bevolking, het L. kraussi nogtans 'n goed gedeflnieerde reproduktiewe siklus. Gonadiese proliferasie het plaasgevind tussen Augustus en Januarie, met die piek kuit· skietperiode vanaf Desember tot Maart. Several criteria have been used to define the reproductive cycles of littorinid gastropods. Temporal changes in the incidence of copulation and spawning have frequently been described (Linke 1933; Lenderking 1954; Fretter & Graham 1962; Struhsaker 1966; Borkowski 1971; Pilkington 1971; Berry & Chew 1973; Gallagher & Reid 1974). Seasonal changes in the morphology and histology of the reproductive tract have also been outlined (Williams 1964; Palant & Fishelson 1968; Bergerard 1971; Fish 1972; Underwood 1974; Jordan & Ramorino 1975; Goodwin 1978). Spawning periods have also been inferred from data on the recruitment of juveniles (Underwood 1974; Potter 1984). This paper describes the reproductive cycle of the common supralittoral gastropod Lillorina kraussi solely on the basis of changes in gonadal histology observed during a 14-month study. Specimens of L. kraussi were collected monthly, between August 1982 and September 1983, from rocky shores within Hluleka Nature Reserve, Transkei (31 ° 49'S/29° 19'E). All samples, varying in size from 10 to 25 animals, were taken at spring low tide. The shell height of each individual was recorded prior to dissection. Portions of the gonad and interdigitating digestive gland were removed, fIXed in either Bouin's fluid or 10OJo formal-saline, embedded in paraffm wax and sectioned at 7 11m. The sections were stained with Dela-field's haematoxylin and counterstained with eosin. Sections were allocated a maturity index based on the criteria given in Table 1. Although some cognizance of follicle contents is used, the arbitrary stages are also based on the relative size and apposition of gonadal follicles within the connective tissue surrounding the digestive gland. A total of 255 sexually mature individuals, ranging in size from 7 to 24 mm shell height, were examined. The sex ratios found in the mt>nthly collections were compared using the S.-Afr. Tydskr. Dierk. 1987,22(2) -c test, and only three samples (August, September and November 1982) showed significant departures from a 1: 1 ratio (p < 0,005). There were no differences in the size distri-bution of male and female L. kraussi. Detailed descriptions of the morphology and histology of the genital systems of littorinids are given in Linke (1933), Fretter & Graham (1962) and Bedford (1965). The gonad is situated in the visceral apex overlying the digestive gland. The gonoducts are found along the columellar surface of the visceral coil. In males the duct dilates to form the seminal vesicle whilst in females it becomes convoluted before linking up with the receptaculum seminis. Examination of sectioned material revealed six distinct developmental stages in the gonads of L. kraussi: inactive (in), early (d l ), mid (d2), and late developing (d3), ripe (r) and partially spent (PS) (fable 1). All the ovarian sections inspected contained both immature and mature oocytes. These were easily distinguished on the basis of size and staining properties, as described by Under-wood (1974). Cytolysis of unshed mature oocytes was evident in partially spent animals. There was considerable variation in the extent of cytolysis, in some instances it appeared to be restricted to a few follicles, whereas in others extensive cytolysis was evident throughout the gonad. There was no relationship between the extent of cytolysis and size of individual. Within the gonadal follicles of all male L. kraussi the various stages of spermatogenesis were observed simulta-neously. In addition to the gametogenic cells several larger bodies, characterized by a fmely vacuolated cytoplasm, were found lying alongside spermatozoa in the lumen of the follicles. The term nurse-cells has been given to these bodies, as they are thought to aid in the transfer of sperm to females (Fretter & Graham 1962). Spermatozoa, apparently attached to these nurse-cells, were frequently observed in an unorien-tated mass within the seminal vesicle. Phagocytosis of ripe spermatozoa and nurse-cells, by amoebocytes, was evident within gonadal follicles and ducts. Degeneration of ripe eggs and phagocytosis of male sexual products have been noted in other littorinids (Linke 1933; Palant & Fishelson 1968; Underwood 1974). No attempts have been made to assess the energetic cost of these processes. The subjective staging of gonadal development indicated little gametogenic synchrony Within the population (Figure 1), individuals in several developmental stages being present in each of the samples. From August to January L. kraussi showed a progressive increase in gonadal development. Ripe, pre-spawning animals were found from December to March. In female L. kraussi development appeared to be a continual process, there being no well-defmed period of inactivity. Partially spent individuals, in which cytolysis of unspawned mature oocytes was evident, also showed signs of continued gametic proliferation. These animals may be capable of spawning again later in the reproductive cycle. Totally spent individuals were not observed in female L. kraussi making it difficult therefore to separate late spent from early deve-loping littorinids. Inactive males, with rudimentary follicles devoid of gametic activity, were prevalent from June to September. Little is known of the reproductive biology of South African littorinids. Histological studies indicate that L. kraussi spawns during summer (December to March) on both the Transkei (this study) and Natal coasts (potter 1984). From monthly counts of juveniles and copulating pairs at Chaka's Rock, Natal, Potter (1984) has established that Nodolillorina natalensis spawns in summer, whereas L. tifricana tifricana, I Reproduced by Sabinet Gateway under licence granted by the Publisher (dated 2010). I S. Afr. J. Zool. 1987, 22(2) Table 1 Arbitrary stages in the reproductive development of Littorina kraussi Stage Inactive Developing d. Ripe r Relative size of follicles Rudimentary follicles visible within the connective tissue matrix surrounding the digestive gland. Follicles still small. Follicles enlarged, occupying more space within the connective tissue matrix. Follicles large, occupying most space within the connective tissue matrix. Follicles closely apposed to each other and the digestive gland. Post-spawning ps Follicles reduced in size, connective tissue evident in the interstices. 100 10 10 70 I 10 10 40 M 20 10 0 A S 0 N D , .. A .. J J Male follicle contents Lumina packed with undifferentiated tissue, no spennatogenic cells seen. All stages of spennatogenesis now apparent, also a few nurse-cel.ls evident. Large quantities of undiffe-rentiated tissue still present. Quantity of undifferentiated tissue clearly reduced, contents otherwise as in d •. No undifferentiated tissue. Follicles packed with all stages of spennato-genesis plus the occasional amoebocyte. Vesicula seminalis densely packed with spennatozoa and nurse-cells. Contents as above, some evidence of dispersion of spermatozoa and nurse-cells. Vesicula seminalis densely packed as above. All stages of spennatogenesis still evident, but clearly reduced in numbers. Numerous amoebocytes evident within follicles. Vesicula seminalis invaded by numerous amoebocytes, dispersal of contents also seen. 100 10 10 70 I .0 10 40 M 20 10 0 A • A S 0 N D ISSI dl IZ:ZI d2 .. ~s dS I::!Q!I r III!BI!II ,. IZZl In ISSI dl I'l2Zd 171 Female follicle contents Much intrafollicular material. Some immature oocytes at the edge of the follicles and a few mature oocytes in the lumina. Numerous immature oocytes at the edge of the follicles, similar number of mature oocytes lying free in the lumina. Little intrafol1icuIar material present. Densely packed with mature oocytes, some immature oocytes also present. Follicles partially empty, numerous mature oocytes and a few immature oocytes still evident. Some mature and immature oocytes present. Degeneration of mature eggs evident, their contents having been released into the lumina. , .. A .. A S d2 ~SdS I::!Q!I r III!BI!II ,. Figure 1 The reproductive cycle of (a) female and (b) male Littorina kraussi based on the proponion of the population at various maturity stages (in, inactive; d!, d2, d3 developing; r, ripe; ps panially spawned). Numbers represent sample size. despite evidence of a summer peak in spawning activity, breeds throughout the year. In the Western Cape, McQuaid (1981) found L. ajricana knyS1Ull!nsis to recruit throughout the year with peak settlements in winter (May to June) and summer (December to January). These differences in spawning periodi-city may reflect variations in geographical distribution of the species. The temperature regime may be suitable for conti-nuous reproduction in the warm temperate L. ajricana, whereas spawning in the two tropical species L. kraussi and N. natalensis may be restricted to the warmer months towards their southern limit of distribution (potter 1984). Detailed comparison of the present study with that of Potter (1984) revealed considerable differences in the reproductive cycles of animals at Hluleka and Chaka's Rock. At the latter site, Potter (1984) found that males maintained a high level of gametogenic activity throughout the year whereas females were virtually inactive between April and November. The present study, however, indicated a definite period of inactivity in male L. kraussi (June to September) and although cytolysis was evident in females, gametic production appeared to be continuous. Reasons for these differences remain obscure. Many supralittorallittorinids, including L. kraussi (Lasiak & Dye, pers. obs.) exhibit pelagic development involving the release of planktonic egg capsules and planktotrophic larvae (see Mileikovsky 1975, for review). These animals are depen-dent on some means of facilitating the delivery of egg capsules Reproduced by Sabinet Gateway under licence granted by the Publisher (dated 2010). 172 to water. This problem has been overcome by downshore migrations during the breeding season (Lysaght 1941; Lebour 1945; Kojima 1959; Pilkington 1971) and by rhytlunic spawn-ing activity concomitant with spring tides (Lysaght 1941; Lenderking 1954; Struhsaker 1966; Borkowski 1971; Berry & Chew 1973; Gallagher & Reid 1974; Grahame 1975). In other gastropods it has been shown that spawning activity is stimulated by rough seas (Rao 1973; Grange 1976). A further possibility is the release of eggs into littoral fringe tide pools. Downshore migration of mature female L. kraussi prior to spawning has been observed on the Natal coast (potter 1984). Whether this species has other adaptations promoting the successful delivery of eggs has yet to be established. Histological studies on the reproductive systems of lit-torinids have met with varying success. Goodwin (1978) found that the gonads of L. obtusata maintained a high level of development throughout the year. He found no significant variations in the relative proportions of different spermato-genic stages, nor did his visual examination of ovarian sections produce any clear trends. Similarly, Jordan & Ramorino (1975) observed that most of the L. peruviana they examined had ripe gonads throughout the year. However, clear annual rhytluns of development and degeneration have been demon-strated in the gonads of L. kraussi (this study), L. punctata and L. neritoides (palant & Fishelson 1968) and L. unijasciata, N. pyramidalis and Bembicium nanum (Underwood 1974). To provide a complete picture of reproductive periodicity histological studies should be combined with field observations on the incidence of copulation and the settlement of juveniles. Acknowledgements The University of Transkei provided [mancial assistance and the Department of Nature Conservation, Umtata permitted access and collections from Hluleka. References BEDFORD, L. 1965. The histology and anatomy of the reproductive system of the littoral gastropod Bembicium nanum (Lamarck) (Fam. Littorinidae). Proc. Linn. Soc. N.S. W. 90: 95-105. BERGERARD, J. 1971. Facteurs ecologiques et cycle sexuel de Littorino saxoti/is (Olivi) (Mollusques, Gasteropodes). Cah. Bioi. Mar. 12: 187 - 193. BERRY, A.J: & CHEW, E. 1973. Reproductive systems and cyclic release of eggs in Littorina melanostoma from Malayan mangrove swamps (Mollusca: Gastropoda). J. Zool., Lond. 171: 333-334. BORKOWSKI, T.V. 1971. Reproduction and reproductive periodicities of Southern Floridian Littorinidae (Gastropoda: Prosobranchia). Bull. Mar. Sci. 21: 826 - 840. FISH, J.D. 1972. The breeding cycle and growth of open coast and estuarine populations of Littorina littorea. J. Mar. Bioi. Ass. U.K. 52: 1011-1019. FRE1TER, V. & GRAHAM, A. 1962. British prosobranch molluscs. Ray Society, London. GALLAGHER, S.B. & REID, G.K. 1974. Reproductive behaviour and early development in Littorina scabra anguli/era and Littorina irrorata (Gastropoda: Prosobranchia) in the Tampa Bay region of Florida. Malacol. Rev. 7: 105 -125. GOODWIN, B.J. 1978. The growth and breeding cycle of Littorina obtusata (Gastropoda: Prosobranchiata) from Cardigan Bay. J. Moll. Stud. 44: 231 - 242. GRAHAME, J. 1975. Spawning in Littorina littorea (L.) (Gastropoda: Prosobranchiata). J. Exp. Mar. Bioi. &01. 18: 185 -196. GRANGE, K.R. 1976. Rough water as a spawning stimulus in some trochid and turbinid gastropods. N. Z. J. Mar. Freshwater Res. 10: 203 - 216. S.-Afr. Tydskr. Dierk. 1987,22(2) JORDAN, J. & RAMORlNO, L. 1975. Reproduccion de Littorina (Austrolittorina) peruviana (Lamarck, 1822) y Littorina (Austrolittorina) araucana Orbigny, 1840. Rev. Bioi. Mar. Valparaiso 15: 227 - 261. KOJIMA, Y. 1959. The relation between seasonal migration and spawning of the periwinkle, Littorina brevicula (Philippi). Bull. Bioi. Sin. Asamushi 9: 183 -186. LEBOUR, M.V. 1945. The eggs and larvae of some prosobranchs from Bermuda. Proc. Zool. Soc. Lond. 115: 462-489. LENDERKING, R.E. 1954. Some recent observations on the biology of Littorina angulifera Lam. of Biscayne and Virginia Keys, Florida. Bull. Mar. Sci. Gulf Caribb. 3: 273 - 296. LINKE, O. 1933. Morphologie und Physiologie des Genital-apparates der Nordseelittorinen. WISS. Meeres. 19: 1 - 60. LYSAGHT, A.M. 1941. The biology and trematode parasites of the gastropod Littorina neritoides of the Plymouth Breakwater. J. Mar. Bioi. ASS". U.K. 25: 41-67. MCQUAID, C.D. 1981. Population dynamics of Littorina q/ricana knysnaensis (Philippi) on an exposed rocky shore. J. Exp. Mar. Bioi. £Col. 54: 65 -76. MILEIKOVSKY, S.A. 1975. Types of larval development in Littorinidae (Gastropoda: Prosobranchia) of the world ocean, and ecological patterns of their distribution. Mar. Bioi. 30: 129-135. PALANT, B. & FISHELSON, L. 1968. Littorina punctata and Littorino neritoides (Mollusca: Gastropoda) from Israel: ecology and annual cycle of genital system. Isr. J. Zool. 17: 145 - 160. PILKINGTON, M.C. 1971. Eggs, larvae and spawning in Melarapha cincta (Quoy & Gaimard) and M. oliveri Finlay (Littorinidae: Gastropoda). Aust. J. Mar. Freshwater Res. 22: 79-90. POTIER, C.M. 1984. Aspects of the biology of the Natal Littorinidae. M.Sc. thesis, University of Natal, Pietermaritzburg. RAO, M.B. 1973. Sex phenomenon and reproductive cycle in the limpet Cellano radiata (Born) (Gastropoda: Prosobranchia). J. Exp. Mar. Bioi. £COl. 12: 263 - 278. STRUHSAKER, J.W. 1966. Breeding, spawning, spawning periodicity and early development in the Hawaiian Littorino: L. pintado (Wood), L. picta Philippi, L. scabra (Linne). Proc. malac. Soc. Lond. 37: 137 -166. UNDERWOOD, A.J. 1974. The reproductive cycles and geographical distribution of some common Eastern Australian prosobranchs (Mollusca: Gastropoda). Aust. J. Mar. Freshwater Res. 25: 63 - 88. WILLIAMS, E.E. 1964. The growth and distribution of Littorina littorea (L.) on a rocky shore in Wales. J. Anim. &01. 33: 413-432. I Reproduced by Sabinet Gateway under licence granted by the Publisher (dated 2010). 

Short CommunicationsReproductive cycle of the supralittoral gastropod Littorina kraussi (Rosewater, 1970)

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Short CommunicationsReproductive cycle of the supralittoral gastropod Littorina kraussi (Rosewater, 1970)

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