The molluscan cardiovascular system typically incorporates a transient extracardiac structure, the larval heart, early in development, but the functional importance of this structure is unclear. We documented the ontogeny and regulatory ability of the larval heart in relation to two other circulatory structures, the true heart and the velum, in the intertidal gastropod Littorina obtusata. There was a mismatch between the appearance of the larval heart and the velum. Velar lobes appeared early in development (day 4), but the larval heart did not begin beating until day 13. The beating of the larval heart reached a maximum on day 17 and then decreased until the structure itself disappeared (day 24). The true heart began to beat on day 17. Its rate of beating increased as that of the larval heart decreased, possibly suggesting a gradual shift from a larval heart-driven to a true heart-driven circulation. The true heart was not sensitive to acutely declining P(O(2)) shortly after it began to beat, but increased in activity in response to acutely declining P(O(2)) by day 21. Larval heart responses were similar to those of the true heart, with early insensitivity to declining P(O(2)) (day 13) followed by a response by day 15. Increased velum-driven rotational activity under acutely declining P(O(2)) was greatest in early developmental stages. Together, these findings point to cardiovascular function in L. obtusata larvae being the result of a complex interaction between velum, larval and true heart activities, with the functions of the three structures coinciding but their relative importance changing throughout larval development.