203 
THE REPRODUCTION AND EARLY LIFE HISTORY OP THE GASTROPOD 
BEMBICIUM NANUM (LAMARCK, 1822) (FAM. LITTORINIDAE). 
By D. T. Anderson, University of Sydney. 
(Plate viii; five Text-figures.) 
[Read 26th July, 1961.] 
Synopsis. 
Spawning in B. nanum talies place during- the spring- and summer. Eggs are laid in 
gelatinous egg masses attached to the rock surface and hatch after about 12 days as pelagic 
planktotrophic veligers. The relationship between habitat and breeding in New South Wales 
littorinids is similar to that of littorinid species in other parts of the world. 
Introduction. 
It is well known (Anderson, 1960) that the littorinids present an intriguing 
problem of development, some species of the mid- and upper reaches of the shore 
lacking a free-swimming stage (e.g., Littorina obtusata, L. saxatilis, Pelseneer, 1911; 
Delsman, 1914; Linke, 1934; Thorson, 1946), others of similar habitat retaining plankto- 
trophic veligers (e.g., L. neritoides, Lebour, 1935; L. angulifera, Lebour, 1945). The 
marked zonation of the New South Wales rock-platform littorinids Bembicium nanum 
(Lamarck), Melaraphe unifasciata (Gray) and Nodilittorina pyramidalis (Quoy and 
Gaimard) raises the question, whether corresponding anomalies exist among these 
species. A partial answer can now be given on the basis of the present study of the 
reproduction and life history of B. nanum. 
Spawning. 
Observations during 1960 and 1961 on- the breeding season and spawning of s 
population of B. nanum inhabiting the rock platform at Harbord, north of Sydney, 
showed that both males and females contained ripening gametes by the beginning of 
September, but the first egg masses were not found in this locality until the end of 
October. Thereafter, however, they were commonly found until the end of April. No 
female of B. nanum was observed in the act of spawning, but the egg masses of the 
species were identifiable on the more indirect criteria of correlation between the onset 
of seasonal sexual ripening and the occurrence of egg masses in the habitat, and of 
exact correspondence of dimensions and colour of ovarian eggs transferred to sea- 
water and eggs in the egg masses. The occasionally observed close association of 
females with newly deposited egg masses also supported the identification. 
Egg masses of various ages were maintained in dishes of aerated seawater and 
observed at frequent intervals and drawings of living embryos made using a camera 
lucida. 
The photographs of Plate viii were taken by the Department of Medical Artistry, 
University of Sydney. 
Development. 
The spawn (PI. viii) consists of an irregularly distributed, closely packed series of 
oval transparent jelly masses each containing about 100-200 creamy-white eggs lOOfi in 
diameter, surrounded by ovoid transparent envelopes 200-220/^ in length and 190-210//. in 
width. The group of jelly masses is firmly attached to the rock surface, generally in a 
sheltered position either in a fissure or under weed, in the habitat occupied by the 
adults. 
The eggs develop rapidly, passing in about two days through a simple yolKy 
trochophore stage (Text-fig. 1), then gaining in the succeeding two days the apical 
Proceedings of the Linnean Society- op New South Wales, 1961, Vol. Ixxxvi, Part 2. 
,2.04 
KEPKODUCTION AND EARLY LIFE HISTORY OF BEMBICIUM NANUM, 
tuft, blunt transverse foot and lateral velar lobes of the young veliger (Text-fig. 2). 
Rotation within the envelope begins at about this time. 
During the next five days, the veliger enlarges and becomes more elaborate, with a 
well-developed bilobed velum and a pair of black eyespots, a ciliated foot with paired 
otocysts and thin operculum and a visceral hump covered by a shell in which the 
IOO|A 
Text-figs 1-5. — B. nanum. 1. Trochophore, 2 days. 2. Early velig-er, 4 days, dorsal view. 
3. Velig-er, 7 days, ventral view. 4. Veliger, 12 days, lateral view. 5. Veliger, newly hatched. 
beginnings of coiling are visible (Text-fig. 3). Growth and development, however, 
continue for a further five days before hatching, the shell becoming brown-pigmented 
and distinctly coiled, with a widely flared aperture, the larval heart conspicuous and 
active and the yolk reserves of the embryo almost completely resorbed (Text-fig. 4). 
Withdrawal into the shell also becomes possible during this time. 
On hatching from its envelope, the veliger makes its way to the surface of the 
jelly and escapes into the surrounding water. The velar lobes, each of which has a 
black-pigmented dorso-lateral margin, spread out, the velar cilia begin to beat rapidly 
and the veliger swims immediately to the water surface (Text-fig. 5). Pelagic plankto- 
BY D. T. ANDEIBSON. 205 
trophic life is maintained for at least four days. Attempts to keep the veligers alive 
beyond this time and follow their metamorphosis have so far proved unsuccessful, but 
it seems likely that pelagic life is of several weeks' duration. 
The rate of development outlined above is typical of eggs at the periphery of the 
jelly mass. Eggs in the interior of the mass develop more slowly, so that veligers 
continue to escape from the jelly for several days. 
Discussion. 
B. nanuni thus follows early development within the protection of a gelatinous, 
spawn by escape as a pelagic planktotrophic veliger. In this it resembles the Atlantic 
species of similar habitat, Lacuna clivaricata (Hertling and Ankel, 1927; Hertling, 
1928; Lebour, 1937; Thorson, 1946) and Littorina littorea (Hayes, 1929; Linke, 1934; 
Labour, 1937; Moore, 1937; Thorson, 1946), save that the latter lays its eggs in floating 
capsules. 
Of the species which replaces B. nanum in the upper littoral, Melaraphe unifasciata, 
we have at present no direct knowledge of the life history. The corresponding Atlantic 
species, Littorina obtusa, which has a gelatinous spawn, and L. saxatilis, which is 
oviviviparous, hatch at the crawling stage (Pelseneer, 1911; Delsman, 1914; Linke, 
1934; Thorson, 1946). Intensive searching of the habitat of the Harbord population of 
M. unifasciata at a time (November- January) when the females contain ripe yellow 
ova has failed to yield corresponding egg masses, and no animals have yet been found 
to contain developing embryos. It seems probable that M. unifasciata resembles the 
supra-littoral Atlantic species Littorina neritoides (Lebour, 1935), laying its eggs in 
floating capsules and hatching as a planktotrophic veliger, especially as recent work by 
Habe (1956) and Kojima (1958) has revealed an identical mode of spawning for 
Nodilittorina pyramidalis, whose supra-littoral distribution overlaps that of M. 
unifasciata. The curious anomaly of adaptation to extreme exposure and retention of 
planktotrophic early development thus appears to be especially marked in New South 
Wales rock-platform littorinids. 
The present study of B. nanum also supplements the work of H. Anderson (1958) 
on spawning and development in B. melanostoma and B. auratum. The former, in 
contrast to B. nanum, shows adaptation to prolonged exposure by spawning fewer and 
larger eggs in jelly masses from which the young hatch at the crawling stage (compare 
Littorina oMusata). In B. auratum, however, although the habitat extends to the 
supra-littoral of mangrove swamps, the egg masses resemble those of B. nanum and 
the embryos probably hatch as planktotrophic veligers. This further example of 
retention of planktotrophic development in a supra-littoral species finds a parallel in 
the oviviviparous supra-littoral mangrove species of Bermuda and Florida, Littorina 
angulifera, in which the young are released either as free eggs or as planktotrophic 
veligers (Lebour, 1945; Lenderking, 1954). 
Acknowledgements. 
I should like to thank Miss I. Bennett for discussion of this paper and for allowing 
me to use as illustrations the photographs of Plate viii, and Dr. G. Thorson for bringing 
to my notice certain papers on littorinid reproduction. 
References. 
Anderson, D. T., 1960. — The life histories of marine prosobranch molluscs. Journ. malaiol. 
Soc. Aust., 4: 16-29. 
ANDERSON;, H., 1958. — The gastropod genus Bembicium Phillipi. Aust. J. Mar. Fresliw. Res., 
9: 546-568. 
Delsman^ H. C, 1914. — Bntwicklungsgeschichte von Littorina obtusata. Tijdschr. ned. dierk. 
Ver., 13: 170-340. 
Habe, T., 1956. — The floating egg ca,psules of the Japanese periwinkles (Littorinidae). Ventis. 
19: 117-121. 
Hates, P. R., 1929. — Contribution to the study of marine gastropods. III. Development, growth 
and behaviour of Littorina. Contr. Canad. Biol., Toronto, N.S., 4 : 413-430. 
Hertling, H., 1928. — Beobachtung und Versuche an den Eiern von Littorina und Lacuna. 
Bedeutung d'er Eihiillen. Wiss. Meeresuntersuch. Abt. Helgol., 17 : 49 pp. 
206 REPRODUCTION AND EARLY LIFE HISTORY OF BEMBICIUM NANUM. 
Hesrtling, H., and Ankel, W. E., 1927. — Bemerkungen uber Laiche und Jungendformen von 
Littorina und Lacuna. Ihid., 16 : 13 pp. 
KojiMA, Y., 1958. — On the floating egg capsule of the periwinkles, Littorina squalida Broderip 
et Sowerby and Nodilittorina pyramidalls (Quoy et Gaimard). Venus, 19: 233-237. 
L.EBOUR, M. v., 1935. — The breeding of Littorina neritoides. J. mar. Mol. Ass. U.K., 20: 373-378. 
, 1937. — The eggs and larvae of British prosobranchs, with special reference to those 
living in the plankton. Ibid., 22 : 105-166. 
, 1945. — The eggs and larvae of some prosobranchs from Bermuda. Proc. zool. 3oc. 
Lond., 114: 462-489. 
LiENDERKiNG, R. E., 1954. — Soms recent observations on the biology of Littorina angulifera 
Lam. of Biscayne and "Virginia Keyes, Florida. Bull. mar. Sci. Gulf and Caribbean, 
3: 273-296. 
LiNKE, O., 1934. — Beitrage zur Sexual biologie der Littorinen. Z. Morph. Ohol. Tiere, 28: 170- 
177. 
Moore, H. B., 1937. — The biology of Littorina littorea. Part I. Growth of the shell and tissues, 
spawning, length of life, mortality. J. mar. biol. Ass. U.K., 21 : 721-742. 
Pelseneer, p., 1911. — Recherches sur I'embryologie des Gastropodes. Bull. Sci. Fr. Belg., 
44: 1-167. 
Thorson, G., 1946. — Reproduction and larval development of Danish marine bottom 
invertebrates. Medd. Komm.. Danmarks Fish., ser Plankton, 4 : 1-523. 
EXPLANATION OF PLATE VIII. 
1. B. nanum, : Female and spawn, x 3. 
2. B. nanum, : Jelly masses containing eggs at a late cleavage stage, x 40.