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Home , Austrocochlea, Austrocochlea constricta, Cantharidus, Diloma, Gibbula, Gibbula tumida

/. Moll. Stud. (1987), 53, 24-32. © The Malacological Society of London 1987

THE REPRODUCTIVE CYCLES OF THREE TROCHID GASTROPODS FROM THE TRANSKEI COAST, SOUTHERN

THERESA LASIAK Department of Zoology, University of Transkei, Private Bag X5092, Umtata, Transkei, Southern Africa (Received 20 January 1986)

ABSTRACT described by Mcquaid (1982,1983). The breed- ing cycle of this population was established by Changes in gonadal histology were used to determine Joska & Branch (1983) from changes in the ratio the reproductive cycles of three trochid gastropods of gonadal/somatic dry weight. The repro- commonly found along the Transkei coast. They were ductive modes of other South African trochids dioecious, the sexes being evenly distributed both in terms of numbers and size. Despite some asynchrony, have not been studied previously. Observations australis had a distinct reproductive cycle on the breeding cycle of trochids elsewhere have with a short inactive period during the winter, gonadal been made by Williams (1965), Desai (1966), development coincided with increasing sea tem- Duch (1969). Underwood (1972a, 1974) and peratures and spawning took place from late summer Grange (1976). to autumn. Both tabularis and O. variegata exhibited asynchronous intermittent spawning throughout the study period. However, intensified METHODS spawning activity by O. tabularis was noted between April and September. The reproductive cycles and At monthly intervals, between August 1982 and mechanisms of these trochids are compared with those September 1983, specimens of M. australis, O. tabu- elsewhere. laris and O. variegata were collected from the shore at Hluleka (31 49'S, 29 19'E). All collections were made at spring low tides. Samples of 20 to 30 large INTRODUCTION specimens of each were taken. It was not always possible to find this many O. variegata. Each Trochid gastropods are amongst the most con- individual was measured, either along the columellar spicuous intertidal grazers in many parts of the axis in the case of M. australis, or across the maximum world. Three species: shell width in the case of the Oxystele. Lamarck, 1822, (Anton, Portions of the gonad and surrounding digestive 1839) and Oxystele tabularis (Krauss, 1848) are gland were removed, fixed in either Bouin's or 10% commonly found along the Transkei coast. The formol-saline prior to routine preparation for his- latter species is abundant throughout the inter- tological examination. The embedded material was tidal zone, whereas M. australis and O. varie- sectioned at 7 fan then stained with Delafield's haema- gata are restricted in distribution to the upper toxylin and eosin. The sectioned material was sub- jectively allocated a maturity index based on the dif- littoral. Modern classifications of the family Tro- fering proportions of the various gametogenic cells chidae treat Oxystele as a subgenus of present (Table 1). These maturity indices are based Philippi, 1845, however, the name is so firmly on those described by Orton, Southward & Dodd entrenched in the South African literature that (1956) for the limpet Patella vulgata. Stage PS rep- a change has been deemed injudicious (Kilburn resents a gonad in which there was evidence of partial & Rippey, 1982). This paper describes the loss of gametes from the follicles. It could not be reproductive cycles of the afore-mentioned tro- ascertained whether such follicles would continue to chids on the basis of changes in gonadal discharge until they emptied or whether they would histology. produce more gametes and revert back to stage d3 in preparation for further spawning. Quantitative Little is known of the biology of trochid gas- analyses of some ovarian sections were also made by tropods in southern Africa. The zonation, popu- counting the numbers of pre- and post-vitellogenic lation dynamics and growth of O. variegata at oocytes in 5 to 10 microscopic fields at 400x Dalebrook on the Cape Peninsula have been magnification. REPRODUCTIVE CYCLES OF TROCHID GASTROPODS 25 Table 1. Stages in the reproductive cycle of trochid gastropods. Contents of follicles

Stage Male Female Developing Some spermatogonia, mainly Small immature oocytes spermatocytes interspersed with groups of undifferentiated germ cells attached to trabeculae Number of spermatocytes Most oocytes now medium to approximately equal to that large with vitellogenesis well of spermatids and advanced. Some small oocytes spermatozoa remain attached to trabeculae Some spermatocytes, but Majority of oocytes large and of spermatids and spermatozoa uniform size, surrounded by a now predominant basophilic jelly layer. Few small oocytes remain attached Ripe Follicle full of spermatozoa Uniform mass of large eggs with and spermatids. Few only traces of original trabeculae spermatocytes present present Spawned ps Follicles show partial loss of Less uniform in appearance. spermatozoa Mature oocytes still abundant but several gaps evident indicating partial spawning sp Most follicles empty a few Pronounced gaps with a few with residual spermatozoa residual mature oocytes. Small and spermatids oocytes present on trabeculae

RESULTS 1983 and in August 1983. There was no evidence of cytolysis or resorption of unshed mature Monodonta australis oocytes in spent females. Ripe males comprised a major proportion of the population in May and A total of 406 individuals were dissected, 205 of June 1983, but were also recorded in November these were males and 201 females. There were 1982, February and August 1983. Relatively few no significant deviations from the expected 1:1 M. australis were found in a spent or in an early sex ratio nor could any difference in the size phase of development which suggests that the frequency distribution between sexes be resting stage between reproductive cycles is of detected. Specimens examined ranged in size short duration. from 13 to 30 mm. The ovary of M. australis The percentage of mature oocytes increased retained a dark green pigmentation throughout gradually from August reaching a peak in the reproductive cycle. The testis underwent a January-February (Fig. 2a). Spawning took colour change from grey-green (August 1982) place between February and June, as indicated through fawn (October 1982) to cream (January by the declining percentage of mature oocytes to March 1983) and then back to grey-green present in the ovaries. From August onwards (June to September 1983). the proportion of mature oocytes began to rise The subjective staging of gonad development again. (Fig. 1) indicated little gametogenic synchrony, individuals in several developmental stages being present in most samples. From August Oxystele tabularis 1982 to February 1983 the population showed a A total of 398 specimens were examined, 186 of progressive increase in gonadal development. these were female and 212 male. There were no Ripe, pre-spawning female M. australis were significant departures from the expected 1:1 sex evident between December 1982 and February ratio nor any differences in the size frequency PERCENTAGE PERCENTAGE i • - hi w - 2*1 o- O -Y////////////////////77//

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M MONTHS Fig. 2. Reproductive cycles of three trochid gastropods as indicated by the percentage of mature oocytes present in sectioned material (a) Monodonta australis (b) Oxystele tabularis and (c) Oxystele variegata. Vertical bars indicate standard deviations and numbers above the bar show the sample size. distribution between sexes. dissected in February and May. The percentage of ripe ranged in width from 7 to 16 mm. As repro- oocytes present in O. tabularis ovaries fluctuated ductive development progressed the testes between 34 and 69%, with no trends apparent changed colour from brown through green to (Fig. 2b). orange or pink. The ovary retained a dark green pigmentation throughout the reproductive cycle. Oxystele variegata The occurrence of individuals at various A total of 222 individuals were sectioned, rang- developmental stages in the monthly samples ing in width from 10 to 26 mm. There were no indicated that gametogenesis at the population significant differences from the expected 1:1 sex level was asynchronous. From September 1982 ratio. No differences were found in the size to March 1983 O. tabularis underwent a gradual frequency distributions of male and female progression in gonadal development (Fig. 3). specimens. Changes in the pigmentation of the Ripe, pre-spawing females were found through- gonads during the reproductive cycle were simi- out the study period but were particularly com- lar to those described in O. tabularis. mon in August 1982 and from February to Gametogenesis was asynchronous, as indi- March 1983. Between April and September 1983 cated by the occurrence of individuals at various partially spawned females predominated. Spent developmental stages in the monthly samples. females were observed between May and July. No distinct trends in the reproductive cycle were Progression of gonadal development took place detected (Fig. 4) possibly as a result of small at a slower rate in male O. tabularis with the sample size. Ripe females were found through- majority of individuals being at stage d2 between out the study period with some indication of an August and November 1982, and at stage d3 intensification of spawning activity in September from December 1982 to May 1983. Ripe males 1983. This basically concurs with the findings of comprised a major proportion of the population Joska & Branch (1983) on the reproduction of in July to August 1983, but were also found O. variegata in the Cape. They concluded that - VI - VI 0. VI a o D. 0. u « s C/l "8 Q O ft. O f a < - <

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70 - 60 - i 50 I 40 I 30 - Si 20 - i 1 i s M M MONTHS i IVTA D1 D2 D3 SP Fig. 4. The reproductive cycle of (a) female and (b) male Oxystele variegata based on the proportion of the population at various maturity stages. (Abbreviations as in Fig. 1). REPRODUCTIVE CYCLES OF TROCHID GASTROPODS 31 this trochid was probably capable of spawning wood, 1972a; and Garwood & Kendall, 1985). throughout the year, with increased activity in Grange (1976), however, has shown that the February and between September and October. trochid Zediloma atrovirens On the Transkei coast males at an advanced ripens as the sea temperature declines during stage of development were prevalent. Insuf- autumn-early winter. ficient specimens were obtained to draw any In broadcast spawners synchronization of conclusions from the analysis of percentage gametogenesis within the population and the mature oocytes present in the ovaries (Fig. 2c). simultaneous release of gametes by males and The occurrence of partially spawned females females clearly enhances the likelihood of suc- suggests that O. variegata may spawn piecemeal, cessful fertilization. Many broadcast spawners as would also appear to be the case in O. maximize their chance of reproductive success tabularis. by having restricted, synchronized breeding periods (Giese, 1959). Synchronization of spawning activity is also thought to be important DISCUSSION in continuous reproducers reliant on external fertilization (Creese & Ballantine, 1983). The Histological sections revealed that the mature three gastropods studied did not show the oocytes of M. australis, O. tabularis and O. degree of synchrony expected of broadcast variegata were enclosed in a gelatinous coat. spawners. They all exhibited asychronous game- Simpson (1977) considered such a covering to togenic development and spawning. Such repro- be indicative of broadcast spawning and external ductive cycles have been noted previously in fertilization. Several trochids have been ident- broadcast spawning trochids (Williams, 1965; ified as broadcast spawners, releasing their Desai, 1966; Simpson, 1977; Joska & Branch, gametes freely into sea water, these include 1983). The two continuous breeders, O. tabu- constricta (Underwood, 1974); laris and O. variegata, appeared to spawn piece- coruscans (Simpson, 1977); Gib- meal. Such partial spawning activity, in which bula cineraria, magus and Gibbula only a few ripe gametes are liberated at a time umbilicalis (Robert, 1902); Monodonta lineata has been observed in trochids by Williams (1965) (Desai, 1966) and niloticus (Moor- and Underwood (1972a). house, 1932). However, the mode of gamete Various other mechanisms have been pro- release is not consistent amongst the . posed to enhance and maximize the chances of Some species deposit their eggs in a jelly mass or successful fertilization by broadcast spawners. ribbon: Calliostomapapillosum and Calliostoma Pair formation and/or aggregation in groups has zizyphinum (Lebour, 1936; and Crofts, 1955); been reported in several trochids (Desai, 1966; Cantharidus exasperatus and Cantharidus striata Duch, 1969; Simpson 1977). Both O. tabularis (Robert, 1902); Euchelus gemmatus (Duch, and O. variegata occur in clusters which ensures 1969); (Gersch, 1936) and Mar- the close proximity of the sexes during spawn- garites helcinus (Thorson, 1935). No brooding ing. Although development and spawning or laying of egg cases were observed in the appeared to be asychronous within the popu- Transkeian trochids. lation the possibility of group synchronism can- There are no phylogenetic or geographic not be discounted. Several exogenous factors relationships amongst the Trochidae with have been implicated in the co-ordination of respect to the pattern and timing of reproductive spawning activity in trochid gastropods. Grange cycles. Both O. tabularis and O. variegata (1976) has shown that vigorous water movement appear to breed continuously throughout the during rough seas induced Melagraphia aethiops year, as do (Under- and Z. atrovirens to release gametes. This is wood, 1974), Cantharidus coruscans (Simpson, unlikely to induce spawning in trochids on the 1977) and Gibbula cineraria (Underwood, Transkei coast since they are subjected to con- 1972a). Other species have well-defined repro- tinuous heavy surf. Increasing temperature has ductive cycles with distinct periods of inactivity, been found to enhance spawning in some species gametogenesis and spawning. Gametogenic (Gersch, 1936; Ducros, 1957; and Underwood, development in M. australis coincided with 1972b). Stimulatory substances released by the increasing sea temperature (18° to 23°C) and gonad have also been found to induce spawning spawning took place in late summer. Similar by individuals of the opposite sex (Robert, cycles have been reported in two British 1902). trochids, Gibbula umbilicalis and Monodonta The reproductive strategies exhibited by the lineata (Williams, 1965; Desai, 1966; Under- three species examined may constitute adaptive 32 T. LASIAK responses to the unpredictable temperature JOSKA, M.A.P. & BRANCH, G.M. 1983. The repro- regime off the Transkei coast. The sea tem- ductive cycle of the trochid gastropod Oxystele perature ranges seasonally between 18° and variegata (Anton, 18S9). Veliger, 26, 47-51. 23°C, however, frequent incursions of cold KlLBURN, R. & RIPPEY, E. 1982. Seashells of Southern water (10°C), resulting from upwelling, are Africa. South Africa. Macmillan. LEBOUR, M.V. 1936. Notes on the eggs and larvae of experienced (Macnae, 1962). In the event of a some Plymouth prosobranchs, Journal of the Marine sudden drop in sea temperature asychronous Biological Association of the United Kingdom, 20, intermittent spawning would ensure that only a 547-565. small proportion of potential recruits are lost at MACNAE, W. 1962. The fauna and flora of the Eastern any one time. The prolonged recruitment from coasts of Southern Africa in relation to ocean cur- continuous dribble spawning may be an rents. South African Journal of Science, 58, 208- additional advantage in unpredictable environ- 212. ments (Newell, Hilbish, Koehn & Newell, MCOUAID, CD. 1982. The influence of desiccation 1982). and predation on vertical size gradients in popu- lations of the gastropod Oxystele variegata (Anton) on an exposed rocky shore. Oecologia, 53,123-127. MCQUAID, CD. 1983. Population dynamics and ACKNOWLEDGEMENTS growth of the gastropod Oxystele variegata (Anton) on an exposed rocky shore. South African Journal This work was financed by the University of of Zoology, 18, 56-61. Transkei's Research Committee. MOORHOUSE, F.W. 1932. Notes on Trochus niloticus. Scientific Report of the Great Barrier Reef Expedition, 3, 145-155. NEWELL, R.I.E., HILBISH, T.J., KOEHN, R.K. & REFERENCES NEWELL, C.J. 1982. Temporal variation in the reproductive cycle of Mytilus edulis L. (Bivalvia, CREESE, R.G. & BALLANTINE, W.J. 1983. An assess- Mytilidae) from localities on the east coat of the ment of breeding in the intertidal limpet Cellana United States. Biological Bulletin, 162, 299-310. radians Gmelin. Journal of Experimental Marine ORTON, J.H., SOUTHWARD, A.J. &DODD, J.M. 1956. Biology and Ecology, 67, 43-59. Studies on the biology of limpets. 2. The breeding of CROFTS, D.R. 1955. Muscle morphogenesis in primi- Patella vulgata L. in Britain. Journal of the Marine tive gastropods and its relation to torsion. Pro- Biological Association of the United Kingdom, 35, ceedings of the Zoological Society of London, 125, 149-176. 711-750. ROBERT, A. 1902. R6cherches sur le developpement DESAI, B.N. 1966. The biology of Monodonta lineata des troques. Archives de Zoologie Experimental et (Da Costa). Proceedings of the Malacological Generate, 10, 269-538. Society of London, 37, 1-17. SIMPSON, R.D. 1977. The reproduction of some DUCH, T.M. 1969. Spawning and development in the littoral molluscs from Macquarie Island (Sub-Ant- trochid gastropod Euchelus gemmatus (Gould, arctic). Marine Biology, 44, 125-142. 1841) in the Hawaiian islands. Veliger, 11, 415-417. THORSON, G. 1935. Studies on the egg capsules and DUCROS, C. 1957. Induction de l'evacuation des pro- development of Arctic marine prosobranchs. Med- duits sexuel chez gibbules. Comptes Rendu Heb- delelserom Gr0nland, 100, 1-71. domadaires des Stances de VAcaitmie des Sciences UNDERWOOD, A.J. 1972a. Observations on the repro- de Paris, 151, 285. ductive cycles of Monodonta lineata, Gibbula GARWOOD, P.R. & KENDALL, M.A. 1986. The repro- umbilicalis and Gibbula cineraria. Marine Biology, ductive cycles of Monodonta lineata and Gibbula 17, 333-340. umbilicalis on the coast of Mid-Wales. Journal of UNDERWOOD, A.J. 1972b. Spawning, larval devel- the Marine Biological Association of the United opment and settlement behaviour of Gibbula Kingdom, 65, 993-1008. cineraria (: Prosobranchia) with a reap- GERSCH, M. 1936. Der genitalapparat und die sexual- praisal of torsion in gastropods. Marine Biology, biologie der Nordseetrochiden. Zeitschrift fur Mor- 17, 341-349. phologic und Okologie der Tiere, 31, 106-150. UNDERWOOD, A.J. 1974. The reproductive cycles and GIESE, A.C. 1959. Annual reproductive cycles of geographical distribution of some common Eastern marine invertebrates. Annual Review of Physi- Australian prosobranchs (: Gastropoda). ology, 21, 547-576. Australian Journal of Marine and Freshwater GRANGE, K.R. 1976. Rough water as a spawning Research, 25, 63-88. stimulus in some trochid and turbinid gastropods. WILLIAMS, E.E. 1965. The growth and distribution of New Zealand Journal of Marine and Freshwater Gibbula umbilicalis (Da Costa) on a rocky shore in Research, 10, 203-216. Wales. Journal of Ecology, 33, 433-442.