Development of cardiovascular function in the marine gastropodLittorina obtusata(Linnaeus)

Abstract

SUMMARYThe 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 O2 shortly after it began to beat, but increased in activity in response to acutely declining P O2 by day21. Larval heart responses were similar to those of the true heart, with early insensitivity to declining P O2 (day13) followed by a response by day15. Increased velum-driven rotational activity under acutely declining P O2 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.

Differences in the timing of cardio-respiratory development determine whether marine gastropod embryos survive or die in hypoxia

“…Chronic hypoxia stimulated larval heart activity, and larval beat frequencies in hypoxia exceeded those of the control. This study lends further credence to an earlier hypothesis that the production of the beat in the two hearts is regulated in similar ways (Bitterli et al, 2012). Unfortunately, we know little of the ontogeny of adult heart regulation in molluscs (McMahon et al, 1997), let alone that of the larval heart, or the effect of environmental perturbation on both.…”

“…The velar ridge (shown in Fig. 1) is well supplied with haemolymph, which is circulated from the velum to the inner body of the animal by the larval heart (Werner, 1955;Kriegstein, 1977;Bitterli et al, 2012). Hence, it is perhaps not surprising that this gas exchange organ was enlarged in L. obtusata cultured under hypoxia, which could enable an increase in gas exchange through an increase in the area available for O 2 uptake and CO 2 elimination under hypoxic conditions.…”

“…1), larval heart and larval kidney that carry out important functions before, or at the same time as, adult structures such as the shell and adult heart develop (Page, 2009). While the development of molluscan larval structures is reasonably well documented in terms of when they appear and develop under standardised conditions, the development of their physiological function is not (although see Bitterli et al, 2012). Similarly, while there is considerable information on the effect of changing environmental factors (e.g.…”

“…This oxygen tension was considered moderate as eggs of this species can encounter considerably lower P O2 in intertidal pools where the species is found (Morris and Taylor, 1983), and is not as severe as the level that some ecologists would designate as a threshold for hypoxia (Vaquer-Sunyer and Duarte, 2008). In a recent paper, we described the structures associated with cardio-respiratory physiology in L. obtusata embryos (Bitterli et al, 2012), namely: the bi-lobed, ciliated velum, which is used early in development in locomotion, feeding and gas exchange (Chaparro et al, 2002;Strathmann and Leise, 1979;Fretter, 1967;Fioroni, 1966); the larval heart, a thin-walled, ectodermal vesicle connected to the foot and velum (Werner, 1955); and the adult heart. These structures are part of four phases in development of cardio-respiratory function: (i) velar-associated, cilial rotation, which we proposed enhanced gas exchange; (ii) circulation by the larval heart; (iii) circulation by both the larval and adult hearts; and (iv) a final phase when circulation is carried out only by the adult heart (Bitterli et al, 2012).…”

“…In a recent paper, we described the structures associated with cardio-respiratory physiology in L. obtusata embryos (Bitterli et al, 2012), namely: the bi-lobed, ciliated velum, which is used early in development in locomotion, feeding and gas exchange (Chaparro et al, 2002;Strathmann and Leise, 1979;Fretter, 1967;Fioroni, 1966); the larval heart, a thin-walled, ectodermal vesicle connected to the foot and velum (Werner, 1955); and the adult heart. These structures are part of four phases in development of cardio-respiratory function: (i) velar-associated, cilial rotation, which we proposed enhanced gas exchange; (ii) circulation by the larval heart; (iii) circulation by both the larval and adult hearts; and (iv) a final phase when circulation is carried out only by the adult heart (Bitterli et al, 2012). Here, we were particularly interested in investigating whether this species exhibited plasticity in either the timing or activity (or both) of these phases and their associated organs; we also wanted to investigate whether certain developmental itineraries were more likely to lead to individuals surviving hypoxic conditions.…”