Development of cardiac function in crustaceans: Patterns and processes

Development of Cardiac Function in Crustaceans: Patterns and Processes1

SYNOPSIS. Patterns and mechanisms involved in the onset and development of cardiac function in a number of crustacean groups are critically reviewed. Irrespective of phylogeny, heart design and ecology, the onset of heart beat seems inextricably linked to the ontogeny of the thoracic segments where the heart is located. Initially the beat is erratic but soon becomes regular and the rate increases as development proceeds. However, still early in development the relationship between heart rate and body size shifts from a positive to a negative one. Nevertheless cardiac output continues to increase with increasing development, via increasing stroke volume. Some species in more 'primitive' groups develop and retain a myogenic heart beat. Others, with globular and tubular hearts, exhibit a shift from myogenicity to neurogenicity around the time the body size vs. heart rate relationship becomes negative. Very early cardiac function seems generally insensitive to external factors, such as temperature, oxygen and pollutants. Sensitivity to environmental factors increases with development, perhaps over the same timescale as the cardiac regulatory mechanisms appear.

INTRODUCTION

Our understanding of cardiac function in adult crustaceans has increased dramatically in the last decade or so (McMahon and Burnett, 1990; McMahon, 1999a, b, 2001; McMahon et al., 1997a; Wilkens, 1999a, b; see also De Pirro et al., 1999; Harper and Reiber, 1999a; Kuramoto, 1999; Yazawa et al., 1999; McGaw and Reiber, 2000; Sakurai and Yamagishi, 2000; Yamagishi et al., 2000). Crustaceans possessing many primitive features tend to have myogenic hearts, although neurogenicity is dominant in the more advanced malacostracan groups (Wilkens, 1999a; Yamagishi et al., 2000) and possibly members of the Ostracoda. Exactly how the heart is regulated, via neuronal and neuro-hormonal controllers, has recently been investigated and there is a long history of examining the effect of environmental factors (e.g., hypoxia, salinity) on aspects of cardiac function (McMahon, 1999a, 2001; De Pirro et al., 1999). In particular the advent of non-invasive techniques to measure heart rate has opened up possibilities for more realistic measurements both in the laboratory and the field (e.g., Paul et al., 1997; Lundebye and Depledge, 1998; Bloxham et al., 1999).

While much remains to be done, our understanding of how cardiac function comes into being during ontogeny is still, quite literally, embryonic. There are relatively few published studies. Many of the data that exist are unpublished, or are found only in abstract form. Given the resurgence of interest in the development of physiological systems in the last few years, investigations into the onset and development of cardiac activity in crustaceans are timely both for our understanding of that particular group and also for testing ideas concerning the ontogeny of physiological systems generally (Spicer and Gaston, 1999). Critically reviewed here is our knowledge of the development of cardiac function in crustaceans using these disparate data. Two questions are addressed centering on the development of cardiac activity in crustaceans; these concern patterns and mechanisms. First, when during development does the heart appear and begin to function? And how does this function change during development? Second, what are the major factors modifying or controlling cardiac activity at different stages during early development. The article ends with perspectives and suggestions for a research agenda for those investigating the development of cardiac function in crustaceans specifically but also those interested in the ontogeny of physiological systems generally.

BASIC PATTERNS

Rate of beating

How heart rate changes during early in development is known, in detail, for only eight crustaceans (Figs. 1-3, see also data for Ligia, below). The overall pattern is strikingly similar across the limited range of species investigated, despite the fact that crustacean species with hearts possess one of two very different cardiac designs (McMahon et al., 1997): either a "globular heart," as in Daphnia, Nephrops, Meganyctiphanes, Metapenaeus and Procambarus (Figs. 1 and 2) or a "tubular" heart as in, Anemia, Gammarus (Fig. 3) and Ligia. A large number of different developmental trajectories are also represented ranging from species that hatch as nauplii (with number of naupliar stages varying between species), e.g., Artemia and Metapenaeus, to others where embryonic development is abbreviated and largely takes place within the egg. The latter hatch either as larvae that subsequently undergo a major metamorphosis, e.g., Nephrops, or as "miniature adults," e.g., Procambarus. Furthermore the species here span a number of major habitats from marine to brackish water to fresh water.

The appearance of cardiac activity is associated with the ontogeny of thoracic segmentation. The heart cannot be constructed until there is somewhere for it to be expressed, i.e., the thoracic segments. In some genera this event is prehatch (Procambarus, Gammarus) while in others it is post-hatch (Artemia, Daphnia, Metapenaeus, Meganyctiphanes). Initially heart rate is slow and irregular. However, over a relatively short period, in some cases hours (Fig. 4), heart rate becomes regular. Thereafter, at least initially, heart rate increases with both morphological development (involving the differentiation of new tissues and organs) and somatic growth. In practice, however, it is difficult to differentiate between these two often covarying processes. Although the exact timing varies from species to species, heart rate reaches a maximum value and thereafter declines slowly with further development. Now heart rate could be predicted using allometry, although the slope of the line regression between body size and heart rate differed slightly between species with tubular compared with globular hearts (Spicer and Morritt, 1996). Also data for crayfish Procambarus clarkii conflict (Fig. IA, B). McMahon et al. (1997b) found that heart rate increased from the onset of beating until hatching, then decreased with development (Fig. IB). Reiber (1997), however, noted a dramatic decrease in heart rate preceding hatching in the same species (Fig. IA). Only after hatching did heart rate start to increase with developmental stage. The reasons for the discrepancies are not yet clear.