© 2001 by The Society for Integrative and Comparative Biology
Development of Cardiac Function in Crustaceans: Patterns and Processes1
1 Plymouth Environment Research Centre, Department of Biological Sciences, University of Plymouth, Drakes Circus, Plymouth PL4 8AA, UK
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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.
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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.
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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, Artemia, 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.
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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. 1A, B). McMahon et al. (1997b) found that heart rate increased from the onset of beating until hatching, then decreased with development (Fig. 1B). Reiber (1997), however, noted a dramatic decrease in heart rate preceding hatching in the same species (Fig. 1A). Only after hatching did heart rate start to increase with developmental stage. The reasons for the discrepancies are not yet clear.
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Exactly why the relationship between heart rate and body size is positive during early cardiac development but then becomes negative for the rest of the individual's life is unknown. In brine shrimp Artemia, at the end of the naupliar period thoracic segments are added in serial succession as are new heart sections, each bearing a pair of ostia. The initial increase in heart rate with body size coincides with differentiation of new cardiac tissue (Spicer, 1994, 1995
). Once the heart is "complete," it grows by elongation (rather than differentiation), in step with overall growth of the individual. Only then the inverse relationship between heart rate and body size appears and, for the first time, a relationship between weight-specific heart rate and body size is detectable as in other crustaceans (Schwartzkopff, 1955; Maynard, 1960a; Spicer and Morritt, 1986). The initial pattern of increase in heart rate with early development may characterize a differentiating heart. Reiber (1997) and McMahon et al. (1997b), however, rightly point out that it is difficult to extend this reasoning directly to crustaceans with globular hearts, where incremental increase in heart length does not occur. They suggest that, in decapods at least, initial increases may result from changes in the neuronal and neurohormonal control systems (see below). Clearly careful studies of the functional development of a wider range of tubular and globular crustacean hearts are required to elucidate the mechanisms underlying this pattern.
Stroke volume and cardiac output
Few data describe how cardiac output changes during development. Bourne and McMahon (unpublished data cited in McMahon et al., 1997b) report that in Artemia, stroke volume and cardiac output both increased with increasing body size. As discussed above, heart rate (post-differentiation) decreases steadily with time in Artemia, meaning that increased cardiac output must be largely the result of increasing stroke volume. This is similar to the pattern in the crayfish Procambarus clarkii (Wojciechowski and McMahon, in preparation, cited in McMahon et al., 1997b); data from this study, derived from a figure presented in the review, are presented in Figure 5 (C and D). While stroke volume and cardiac output both increased dramatically early in cardiac development, thereafter they changed little until hatching. At hatching even though heart rate decreases with increasing body size (Fig. 1B), a large increase in stroke volume indicates that cardiac output increases with increasing body size. Data for the same species at slightly higher incubation temperature, interpolated from graphs in Harper and Reiber (2001), are similar (Fig. 5A, B). They also show how stroke volume and cardiac output alter during development. Based on these limited data it appears that cardiac output tends to increase with increasing development and much of the increase is attributable to increases in stroke volume.
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Conclusion
Irrespective of phylogeny, heart design, and ecology, the onset of heart beat is suggested to be inextricably linked to the ontogeny of the thoracic segments. Initially the beat is erratic but soon becomes regular, and the rate increases with development. However, the relationship between heart rate and body size shifts very early from positive to negative, and this pattern is retained throughout the rest of the individual's life. Nevertheless, increasing stroke volume tends to increase cardiac output with development.
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DEVELOPMENT OF CONTROL SYSTEMS OF CARDIAC ACTIVITY |
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The development of the system controlling heart rate in crustaceans has been the subject of recent study. Adult crustacean hearts are generally considered neurogenic (Maynard, 1960b
; Wilkens, 1999a) although early pharmacological work suggested that some (e.g., Daphnia spp.) may be myogenic (Wilkens, 1999a). More recent electrophysiological studies have confirmed myogenicity in the heart of the adult branchiopod Triops longicaudatus (Yamagishi et al., 1997). Furthermore the embryonic heart of some species are myogenic, even if they are neurogenic as adults, e.g., the isopod Ligia exotica (see below). The key question then is, for species where adult hearts are neurogenic but embryonic hearts are myogenic, when does ‘control’ shift to the heart pacemaker, the cardiac ganglion, during development?
Electrophysiological evidence
The ontogenic shift from myogenicity to neurogenicity in the isopod Ligia italica has received relatively detailed attention from Yamagishi and co-workers (Yamagishi, 1990, 1996; Yamagishi and Hirose, 1992, 1997; Sakurai et al., 1999; Sakurai and Yamagishi, 2000). Late embryos (1 and 2 days before hatching) and early juveniles (newly-hatched and 1 and 2 days after hatching) displayed periodic burst discharges within the heart muscle in the absence of cardiac ganglion activity (Fig. 6, arrow a). The heart was myogenic. However, in newly hatched juveniles experimental stimulation of the cardiac ganglion produced excitatory junctional potentials within the heart muscle. These excitatory junctional potentials could reset and entrain myogenic heart rate. Also two excitatory cardioacceleratory neurons were identified in early juveniles. Stimulation of these changed heart rate by directly affecting cardiac muscle. Seven days after hatching, spontaneous activity was recorded in the cardiac ganglion although coordinated activity in the constituent cells was not yet established (Fig. 6, Arrow b). After 10 days the cardiac ganglion showed spontaneous coordinated bursting (Fig. 6, Arrow c) and was now the dominant pacemaker. From now on the heart possessed two pacemaker sites, the cardiac ganglion and the heart itself (i.e., it was both myogenic and neurogenic), but with the cardiac ganglion being the primary pacemaker, entraining heart muscle activity to a higher frequency via excitatory junctional potentials. Whether or not the shift from myogenicity to neurogenicity took place around the time that the relationship between heart rate and development changed from a positive to a negative one is still an open question. The data presented in, and derived from, Yamagishi and Hirose's (1997) study does not rule anything out (Fig. 6).
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Unfortunately Yamagishi and coworkers' investigations of Ligia are the only detailed studies of the shift from myogenic to neurogenic control in crustacean hearts. Furthermore they considered the type of neurogenic heart in Ligia, (neurogenic entrainment of myogenic beat) to differ considerably from those of some other (i.e., solely neurogenic) adult crustaceans studied. Consequently there is urgent need for comparable electrophysiological studies of the myogenic-neurogenic transition where the adult heart is only neurogenic The extent to which ion kinetics, upon which all pacemakers depend whether myogenic or neurogenic, alter during development, is an area central to developing controls of cardiac activity. Nothing is known here. The most important currents for investigation are likely (a) the depolarizing pacemaker potential (Na+ and/or Ca2+) and (b) the magnitude of the repolarizing currents (voltage-dependent and Ca2+-dependent K+ currents) (J. L. Wilkens, personal communication).
Pharmacological evidence
Another approach taken to examine the development of cardiac regulation and control is to inject cardioactive drugs intravenously and record the effect elicited on heart rate, stroke volume and cardiac output. The difficulty with this approach is that any observed effect can be taken as an indication either that the heart is innervated or that only the receptors for the drugs of choice are present and functional. Although it is difficult to disentangle the two, such studies still have merit.
McMahon (personal communication) found that injecting serotonin (5-HT) into the hemocoel of the shrimp Metapenaeus ensis resulted in bradycardia in larvae but tachycardia in older juveniles. Furthermore application of tetrodotoxin, which blocks impulse generation in the cardiac ganglion, had no effect on the larval heart but stopped the heart of older juveniles from beating. This could be interpreted as meaning that the cardiac ganglion takes over heart rate control, just as Yamagishi and co-workers studies on Ligia have shown.
Intravenous injection of four cardioactive drugs (
-aminobutyric acid, octopamine, proctolin and 5-HT) into four different developmental stages of crayfish Procambarus clarkii have yielded interesting, if confusing, data (Harper and Reiber, 1999b, 2001). All test drugs except -aminobutyric acid elicited significant changes in stroke volume in late, but not early, developmental stages. There also seemed to be some transition in cardiac regulatory pattern between stages XIII and XV (days 13–17 of embryonic development) but the exact timing and nature of the transition is still unclear. Evidently, as noted by Harper and Reiber (2001) the embryonic crayfish heart is not regulated in an analogous manner to the larval or adult crayfish heart.
External application of 5-HT, or its injection (10–12–10–6 M, 20°C in both cases) into the hemolymph of the cladoceran Daphnia magna had no effect on heart rate in any of the different developmental stages investigated (onset of cardiac activity to sexually mature adult). At high (lethal) concentrations (10–3 M), however, there was a marked depression of heart rate (K. Drabwell, unpublished observations, JIS, unpublished). This supports the view that Daphnia species, like other branchiopod species examined, have a myogenic heart. That Daphnia may have a myogenic heart throws some doubt on the hypothesis, advanced above, that the shift from a positive relationship between heart rate and body size to a negative one early in development (which Daphnia exhibits), is in some way linked to, or associated with, the shift from myogenicity to neurogenicity.
Conclusion
Some crustaceans, notably in more ‘primitive’ groups, develop and retain a myogenic heart beat. Others, whether or not they have a globular (e.g., crayfish) or tubular (e.g., isopods) heart, shift from myogenicity to neurogenicity some time during early development. This shift appears to take place at, or after, the point at which the relationship between heart rate and body size which is initially positive, becomes negative.
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EFFECT OF EXTRINSIC FACTORS ON HEART RATE OF DIFFERENT DEVELOPMENTAL STAGES |
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Only three important environmental factors have been examined with respect to their influence on the function of the developing heart, but none of them in any detail. These are temperature, hypoxia and pollutants (specifically trace metals).
Temperature
Spicer (1994) found that at the onset of cardiac activity in brine shrimp Artemia franciscana it was not possible to discern an effect of temperature on heart rate (over the temperature range 24–31°C). Once the newly formed heart had differentiated but was still growing by elongation, heart rate had become slightly more temperature-sensitive (Q10 = 1.25). Bourne and McMahon (unpublished, cited in McMahon et al., 1997b) also found that heart rate for Artemia was sensitive to temperature throughout an extended developmental range (though they did not specify what stages were examined) although Q10 was low and in the same range as that calculated by Spicer (1994), i.e., Q10 = 1.3–1.4 (T°C = 10–30). Bourne and McMahon also examined the effect of temperature on stroke volume. Q10 varied from 2 (T°C = 20–30) to 5 (T°C = 10–20).
Oxygen
Reiber (1997) examined the effect of exposure to acute hypoxia on heart rate of crayfish Procambarus clarkii at a number of different developmental stages. He found that while early embryonic heart rate decreased when PO2 < 4.33 kPa, this was not the case for embryos just before hatching (Fig. 7). He correlated this ability to maintain heart rate with a dramatic decrease in normoxic heart rate in this late embryonic stage (see Fig. 1A). Newly hatched individuals also had hypoxia-insensitive hearts even although mean normoxic heart rate increased markedly with development. However by the third instar individuals displayed a strong hypoxia-induced bradycardia which was also a characteristic of adult crayfish (Fig. 8). Exactly why heart rate became insensitive to PO2 midway through embryonic development only to become even more sensitive by the third instar, and well after hatching, is not clear.
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SENS = increase in sensitivity of heart function to environmental factors, F = fertilization, S = segmentation, M = sexual maturity, H = hatching (*indirect development, **direct development), MT = metamorphosis, 
or dashed line = not always presentHypoxia insensitivity of early developmental stages was also a feature of the grass shrimp Palaemonetes pugio (Reiber et al., 2000
). Neither heart rate nor stroke volume was significantly affected by stepwise exposure (approx. 3.3 kPa O2 steps) to hypoxia until < PO2 = 10 kPa. Below this O2 tension, however, pronounced bradycardia occurred, although stroke volume was unchanged. The overall result was a decrease in cardiac output < PO2 = 10 kPa. Juveniles, as did adults, exhibited an increase in heart rate although a decreased stroke volume when exposed to hypoxia. This meant that overall there was no change in cardiac output down to PO2 = 10 kPa, below which tension cardiac output declined significantly. By contrast McMahon et al. (1995) found that when larval Metapenaeus ensis were exposed to moderate hypoxia, heart rate increased. This response persisted into the early juvenile stages, but later juveniles exhibited the bradycardic response typical of adults. Finally, the effect of culturing Triops under hypoxic conditions has been shown to bring the development of a functional heart forward in the overall developmental itinerary (Harper and Reiber, personal communication). The ecological and physiological implications of such an ‘early appearance’ of the heart are unexplored.
In conclusion, there does not seem to be any one pattern of cardiac response to hypoxia, with each of the three examples described above being quite different from one another. Clearly work is still required to clarify this situation, and in particular to begin to explore the ecological and evolutionary implications of such patterns.
If there are few data concerning hypoxic exposure, there are even less for hyperoxia. Interestingly Reiber and Harper (personal communication) found that exposing embryos of crayfish Procambarus clarkii to hyperoxia (>26.7 kPa) resulted in an increase in heart rate. This suggests that embryonic crayfish under conditions that we would refer to as normoxic are O2-limited. It is difficult to see exactly how this fits in with the observation that these same embryos are able to maintain heart rate during acutely declining PO2s, but certainly the phenomena warrants urgent attention.
Trace metals
Exposure to waterborne copper (3.46–14.94 µmol·l–1) delays the onset of cardiac function in Artemia franciscana. A functional heart always appeared in the same developmental stages (3 or 4) but copper exposure slowed overall development, thus delaying the onset of segmentation and associated differentiation of cardiac tissue (Spicer, 1995). For individuals exposed to lethal copper concentrations (9.13–14.93 µmol·l–1) most mortality occurred just before or as the heart and gills began to appear. Once heart function began, the metal no longer affected the relationship between heart rate and time.
Conclusion
There is some evidence that very early cardiac function is insensitive to external factors, such as temperature, oxygen and pollutants, although generalizing this statement would require much more work. Sensitivity to environmental factors appears and increases with development, perhaps over the same timescale as the cardiac regulatory mechanisms develop.
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PERSPECTIVES |
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Our understanding of the patterns of, and mechanisms underlying, cardiac development in crustaceans is fragmentary at best. However, summarizing the current state of our knowledge can inform and facilitate testing by subsequent workers. This is a difficult task given problems with comparability of crustacean taxa and developmental stages. Some problems are inherent, e.g., are the terms larva and juvenile comparable among taxa, and if not what criteria can we employ to generate comparability? Others are introduced by investigators, e.g., use of different staging schemes, even for the same species. Figure 8 frames the main tentative conclusions of each of the sections above. What results should, however, be treated more as a source of hypotheses to be tested, rather than an attempt to generalize on the basis of extant data.
Finally, for those interested in questions concerning the development of physiological function per se, the crustacean heart is an excellent model system. At what stages of development do physiological regulations go into action, and do the components of that regulation appear serially, or all at once? (Adolph, 1968). To what extent is it possible to manipulate the physiological trajectory of an individual or of one physiological system, and are there any common underlying mechanisms? (Adolph, 1968; Spicer and Gaston, 1999). To what extent can environmental factors influence a physiological trajectory? And which factors are most important in this regard? (Spicer and Gaston, 1999). All of these questions can be addressed through using the development of cardiac function in crustaceans, particularly if species are chosen such that heart development is pre-hatch and individuals are transparent so that the cardiovascular system is easily visualized using specially-constructed optical methods (e.g., Paul et al., 1997).
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ACKNOWLEDGMENTS |
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I thank Stacy Chapman, Brian McMahon and Carl Reiber for allowing me to cite some of their, as yet, unpublished work. I also thank Roddy Williamson and Jerrel Wilkens for reading and commenting on early drafts of the manuscript, Alan Kohn for his unstinting editorial assistance, and an anonymous reviewer whose comments helped to improve the manuscript. This paper is dedicated to Brian McMahon for the inspiration he has been to me and countless others working on various aspects of crustacean physiology.
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FOOTNOTES |
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1 From the Symposium Ontogenetic Strategies of Invertebrates in Aquatic Environments presented at the Annual Meeting of the Society for Integrative and Comparative Biology, 3–7 January 2001, at Chicago, Illinois.
2 E-mail: jispicer{at}plymouth.ac.uk
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