EARLY LIFE-HISTORY OF MELAMPUS AND THE SIGNIFICANCE OF SEMILUNAR SYNCHRONY

1. The salt-marsh pulmonate snail, Melampus bidentatus, is placed in the Ellobiidae which family encompasses the most primitive of living Pulmonata and is regarded as not far removed from the ancestral stem-group of both modern land snails and freshwater pulmonates. Inhabiting the higher levels of salt marshes. Melampus is "amphibious": although an air-breather with a gill-less vascularized mantle-cavity functioning as a lung, if retains an archetypic pattern of reproduction with small eggs and a free-swimming veliger larva. 2. Field and laboratory studies over several years (based on natural populations at Little Sippewisset, Cape Cod, Massachusetts) have shown that egg-laying, hatching, and larval settlement are each confined to cycles of about four days in phase with the spring high tides. Adaptively such semilunar synchronies ensure that these processes occur only during the 2.3% to 4% of each month when the Melampus habitat in the upper 12% of the intertidal zone is bathed by seawater. 3. The annual reproductive period extends from late May or early June through early July. with either three or four cycles of egg-laying occurring at two-week intervals in phase with the tides of new and of full moon. Synchrony of egg-laying (and of the patterned aggregation and copulation which precede it) is obligate. Stocks of Melampus brought into the laboratory in spring will maintain the same semilunar rhythm of reproductive behavior during the summer period. 4. Eggs are small (about 109 ng organic carbon) and are laid in gelatinous egg-masses averaging 850 eggs. Mean numerical fecundity is 33,150 eggs per snail per year. For most freshwater pulmonates fecundity would lie in the range 8-800 eggs per snail per year. At 18° C, development to a well-differentiated and active veliger within the egg-shell takes 11 days. 5. Hatching shows semilunar synchrony in the field: enormous numbers of newly hatched veligers can be collected on the flood of appropriate spring tides. A series of experiments with laboratory-laid egg-masses showed that eclosion normally occurs in response to a sequence of about 4 tidal floodings in under 50 hours. Hatching can occur from egg-masses from 10 to 24 days after laying. Being facultative, the process allows better survival and overlap of cohorts but also reestablishes the synchronization with spring tides. 6. Veligers feed actively and grow from shell length 127 µ to 280 µ during their time in the plankton, deduced to be 14 ±2 days. The bulk of the settlement is into the exact vertical zone occupied by adult Melampus. 7. A period as a crawling, radula-feeding postlarva (after loss of velar lobes and operculum) is followed by an abrupt metamorphosis of the mantle and shell. Postmetamorphic spat grow rapidly. In terms of organic carbon or ash-free dry weight, growth extends through two orders of magnitude during veliger and early spat life, through more than three during the first eleven weeks, and six in the entire 3-4year life-span. In contrast, similar biomass growth measures in freshwater pulmonates involve only two to three orders in their life-span. 8. In Melampus, the shells of late veligers and of post-larvae show sinistral coiling, and those of metamorphosed spat and of adults dextral coiling. There is a metamorphosis of mantle and shell alone; throughout development, larval and spat stages, the internal organs are in their adult dextral arrangement. Such a metamorphosis from a hyperstrophic shell condition to an orthostrophic one is known to occur in the ectocommensal opisthobranch family Pyramidellidae and in certain other snails with planktonic larvae. The present study provides the first description of the succession of shell stages and metamorphosis for any pulmonate. 9. In conclusion, the small eggs, the mantle-shell metamorphosis, and the semilunar synchrony are discussed in their evolutionary setting. "Primitive" reproduction with small eggs, as retained in Melampus, confers advantages in dispersal and genetic potential. Evolution of larger eggs, as in the freshwater pulmonates, may have involved selection pressures to reduce the temporal extent of immature growth in seasonally variable environments. Mantle-shell changes in Melampus, including the metamorphosis, can be interpreted simply in terms of the changing needs for protective containment at different stages in the life-cycle. Semilunar synchrony of reproductive and of larval stages has evolved in response to the concursion of specialized aerial respiration and the primitive pattern of spawning large numbers of small eggs. The combination of both obligate and facultative processes in producing these synchronies is thought to be significant in relation to the long evolutionary history which can be hypothesized for these semilunar rhythms.