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AMER. ZOOL., 39:199-214 (1999)
Evolution of the Cardiovascular System in Crustacea1
JERREL L. WILKENS
2
Department of Biological Sciences, University of Calgary, Calgary, Alberta T2N 1N4, Canada
SYNOPSIS. An attempt is made to explain the evolution of different cardiovascular
morphologies of crustaceans on the basis of (1) changes in the development of the
body plan of different species, (2) the advent in the malacostracans of segmental
arteries that provided the circulatory potential for growth in body size and speciation, (3) the need for more powerful hearts to propel blood through larger
bodies, and (4) the embryological substrate that would allow for the development
of regional specialization. Electrophysiological evidence supports the hypothesis
that the archetypal crustacean heart was myogenic, but in more advanced forms
this pacemaking mechanism has become subservient to the neural drive from the
cardiac ganglion. This transition may have been the result of the selective advantages to possessing a discrete cardiac ganglion, which itself was easily controlled
by nervous inputs from the CNS and by circulating hormones.
INTRODUCTION
This essay on the evolution of the cardiovascular system (CVS) in the Crustacea
is constructed on the recognition that evolutionary change in form must be functional. Functional requirements of the CVS
of a crustacean are the adequate supply to
all tissues of oxygen and nutrients and the
removal of waste products, coordination
(hormone distribution), and temperature
regulation (insects and possibly in other
thermoregulators such as terrestrial crabs).
These requirements have resulted in some
type of circulatory system in all metazoans
above the flatworms. When animals are
small enough or sedentary they may not
need anything more than the ability to
move coelomic fluid, but larger animals require a dedicated pump and a distribution
system.
It is assumed that a tubular heart without
arteries is a plesiomorphic feature of the
crustacean blood-vascular system. The early forms must have possessed a more-orless uniform segmentation and an extended
tubular heart running from the head to the
tail. The different CVSs that are found in
many extant groups are viewed as apomorphic derivatives of the archetype. This
discussion will be guided by three princi' Invited essay on circulation to commemorate the
life and career of Charlotte Mangum.
2
E-mail: [email protected]
pies: (1) "the interpretation of form must
always be tempered with an understanding
of function" (Schram, 1982); (2) generalized structures that appear to be primitive
may in fact represent a secondary simplification and may not represent temporal priority (Gould, 1977); and (3) new structures
and functions are more likely to have been
layered on preexisting ones rather than to
have arisen as de novo inventions.
RELATIONSHIP BETWEEN PHYLOGENY AND
CVS ANATOMY
It is useful, as a first approach to understanding the evolution of the CVSs in the
crustaceans, to consider the evolution of
the major groups of the subphylum. Unfortunately, the fossil record for the Crustacea is uneven (Schram, 1982) and many
of the supposedly primitive forms appear
later than more advanced forms. For example, the earliest decapods are identified
in the Permian (286-245 Ma), while the
supposedly more primitive Cladocera and
Copepoda first appear in the Cretaceous
(144-65 Ma) and Tertiary (65-1.8 Ma), respectively (Benton, 1993). The late appearance in the fossil record of the supposedly more primitive representatives
may be explained because they are small,
delicate and might not have been preserved easily. On the other hand, the cladistic synthesis of the evolution of the
Crustacea by Schram (1986) places the
199
200
JERREL L. WILKENS
FIG. 1. Cladogram depicting the relationships of the selected classes to orders of Crustacea based on Schram
(1986). The four classes are named along their respective lower branches of the tree. Orders are at the top of
the cladogram except for the isopoda and amphiopoda which are suborders of the order Edriophthalma. The
cardiovascular characters mapped onto the cladogram are: tubular heart extending the length of the body (1);
reduced heart restricted to thorax (2); reduced heart restricted to abdomen (3); loss of heart (4); myogenic
pacemaker (5); neurogenic pacemaker (6); segmental paired lateral arteries (7).
decapods on an earlier branch than the
Phyllopoda and Maxillopoda, and each of
latter two groups contains supposedly
primitive species. Further research may
clarify these phyletic relationships. Since
the fossil record is incomplete, I am working from the assumption that the major
groups are related as illustrated in cladograms and taxonomic listing presented by
Schram (1986) and illustrated in Fig. 1.
Schram (1986) recognizes four classes of
crustaceans as opposed to the six listed by
most earlier authors (Bowman and Abele,
1982; Brusca and Brusca, 1990; Barnes
and Harrison, 1992). The CVS characterSubphylum Crustacea
Class Remipedia
Class Malacostraca
Subclass Hoplocarida
Order Stomatopoda, Squilla oratorio
Subclass Eumalacostraca
Order Syncarida
Suborder Anaspidacea
istics discussed in this paper are mapped
onto the cladogram. Even though it is proposed that a myogenic pacemaker (character5) is plesiomorphic, this characteristic
does not map at the root of the cladogram
because the only form where the origin of
the heart beat is known to be myogenic is
Triops longicaudatus (Phyllopoda, Notostraca). The species on which there are
physiological observations are included in
the taxonomic listing that follows. In this
list the major groups from which it is desirable to obtain more data are readily apparent, namely the Remipedia, Phyllocarida and Maxillopoda.
CRUSTACEAN CARDIOVASCULAR EVOLUTION
201
Order Euphausiacea
Order Amphionidacea
Order Decapoda
Suborder Dendrobranchiata
Superfamily Penaeoidea, Metapanaeus ensis
Suborder Reptantia
Infraorder Astacidae, Procambarus clarkii, Homarus americanus
Infraorder Palinura, Palinurus japonicus, Palinurus interuptus
Order Mysida
Order Edriophthalma
Suborder Amphipoda
Suborder Isopoda, Bathynomus giganteus, Ligia exotica
Class Phyllopoda
Subclass Phyllocarida
Order Leptostraca
Subclass Cephalocarida
Subclass Sarsostraca
Order Anostraca, Artemia sp.
Subclass Calmanostraca
Order Notostraca, Triops longicaudatus
Order Cladocera, Daphnia sp.
Class Maxillopoda
Subclass Ostracoda
Subclass Copepoda
Subclass Thecostraca
Order Cirripedia
I will begin by reviewing the morphology of the CVSs of adult stages based on the
descriptions presented by McLaughlin
(1980, 1983) (Figs. 2 and 3). This is followed by functional considerations. The
systems described demonstrate a clear progression from simple to complex morphologies. Even though this discussion presents
the CVSs in a generalized manner, it is recognized that there is further variation possible in each group.
The heart
The CVS in the Remipedia (order Nectiopodia) consists of an elongate middorsal
vessel running the length of the body
(Schram, 1986). The CVS of the "primitive" Phyllopoda (orders Brachypoda, Anostraca and Notostraca) is also viewed as
being antecedent to more derived systems.
In these forms it consists of a middorsal
heart tube that extends the length of the
body (Fig. 2A). As there are no arteries,
blood exits from the heart into the hemocoel through an anterior cardiac opening.
Blood is probably channeled through the
body in specific pathways before it reenters
the heart through 14 to 18 pairs of segmental ostia. This simple contractile tube without arteries may represent the simplest plan.
In the Malacostraca the heart remains an
elongated tube in the mantis shrimps (order
Stomatopods) (Fig. 3A), but there appears
to have been a change from a tubular to a
shorter heart in the eumalacostracans (Fig.
3B—D). Most authors group the Leptostraca
(Phyllocarida) at the root of the Malacostraca, and these forms also have an elongated tubular heart. In the Eumalacostraca
the heart is a shorter tube in the Syncarida
and Edriophtalma amphipods, and a shorter
organ in the Mysidacea, Decapoda and Edriophthalma isopods. There is a further
trend toward shorter pumping organs within
each of these two broad group of Eumalacostraca. Different portions of the heart
tube have been retained because the heart
is located in the thoracic region of mysids,
euphausids, and decapods (Fig. 3B, D), but
in the abdomen in most isopods (Fig. 3C).
202
JERREL L. WILKENS
ostia
heart
B
ostium
ostium
heart
D
anterior
artery
heart
ostium
FIG. 2. Drawings of the body plan showing the heart and, if present, the anterior aorta of representatives of
the (A) Class Phyllopoda, Order Notostraca, (B) Phyllopoda, Order Cladocera, (C) Maxiilopoda, Ostracoda, (D)
Class Maxiilopoda, Order Copepoda, and (E) Class Phyllopoda, Order Leptostraca (drawings modified from
McLaughlin, 1980; classification from Schram, 1986).
The heart of decapods is thought to represent the condensation of the first three segments of the ancestral heart (Wilkens et ai,
\991b). The reduction in heart length seems
to have been an irreversible occurrence
even in very small species (see below for
functional considerations).
The class Phyllopoda contains orders that
have primitive tubular hearts (Anostraca,
Notostraca, Leptostraca, Brachypoda) (Fig.
1A, E) as well as the Cladocera (Fig. IB)
where a globular heart is associated with
reduction in number of body segments.
In the Maxillipoda the living representa-
tives of the ostracods and copepods possess
simple CVSs that may represent apomorphic reductions from the plesiomorphic plan,
again associated with a reduction in the
number of body segments (Fig. 1C, D). All
representatives are small, have a reduced
number of somites, and the heart is a short
organ that receives blood through one or
two pair of ostia (Fig. 2B-D). The cirripeds
and some small ostracods lack a true heart
but possess a secondarily derived membranous blood pump that moves blood by cycles of compression and relaxation of the
pumping structure by contractions of vis-
203
CRUSTACEAN CARDIOVASCULAR EVOLUTION
B
ant.
artery
ostium
lat.
artery
heart
abd.
heart adorsal
.
lat. ant. med. ant.
rter
y
artery artery ostium /
lat. artery
i
sternal artery
hepatic
artery
FIG. 3. Drawings of selected representatives of the Class Malacostraca with the components of the cardiovascular system labeled. (A) Order Stomatopoda; (B) Subclass Eumalacostraca, Order Amphipoda; (D) Subclass
Eumalacostraca, suborder Isopoda; (E) Subclass Eumalacostraca, Infraorder Astacidae (drawings modified from
McLaughlin, 1980; classification from Schram, 1986).
ceral or somatic muscles. It is assumed that
portions of the heart, derived from segmental blocks of mesoderm, were deleted as the
number of somites was reduced. A single
anterior artery leaves the heart in some ostracods, but in only some species of the cladocerans and copepods. If the reductions in
size of the heart occurred in ancestors of
these present day small species, the limitations in blood distribution may have been
an important factor that has prevented representatives of the sub-malacostracan classes from attaining large body size, except
in some sedentary cirripeds.
204
JERREL L. WILKENS
phyllopodian Leptostraca possess a very rudimentary arterial system that consists of at
most a single anterior artery leaving the
heart, although this artery may branch.
Malacostracans and Leptostraca differ dramatically in having a more or less elaborate
segmental arterial system along the entire
length of the body. The classification
schemes that group the Leptostraca with the
Malacostraca makes sense if we assume
that the appearance of segmental arteries
was a singular event that made possible the
unique radiation displayed by the Malacostraca. On the other hand, segmental lateral
arteries may have arisen independently
more than once. In these two groups, anterior, posterior, and segmental arteries arise
from the heart regardless of whether it is
tubular or shortened. The advent of a segmental arterial supply to the limbs and other
tissues remote from the heart may have
been the evolutionary innovation that allowed some of the more advanced members
of this class to become large. The simple
squeeze and slosh circulatory dynamics of
animals with a heart tube and no arteries
would not have been able to move blood
through the 2 meter long legs of spider
crabs or to all parts of large animals such
as American lobsters of 25 kg body weight.
Once segmental arteries were developed,
the advantage to the direct supply of blood
to remote tissues would continue even if the
heart tube were shortened. When we examine malacostracans with shortened or
globular hearts we observe that several arteries leave the heart. This would occur if
the remnant of the original heart tube had
pulled along the segmental arteries from the
somites from which it withdrew (Fig. 4).
Following this argument, the anterior arteries (median anterior, lateral anterior, and hepatic arteries) of decapods are thought to be
the original segmental lateral arteries to cephalic and anterior thoracic somites as are
Vasculature
found in the more primitive forms such as
All representatives of the phylum Ar- the phyllocaridian Leptostraca and hoplothropoda possess an open circulatory sys- caridian Stomatopoda (mantis shrimps).
tem where at least the "venous" return
A second line of evidence supporting the
pathways are through hemocoelomic tissue proposition that shortened hearts were despaces and sinuses, not in actual vessels. rived from tubular ancestors is found in the
Arteries are present in some forms. All innervation of the heart in decapods and
crustaceans except the Malacostraca and the isopods. The points of origin in the ventral
Ostia
Blood returns to the heart through valved
ostia. In the most primitive condition a pair
of ostia may occur in the heart tube in each
body segment (see below for embryonic origin of ostia), but they may have been secondarily lost from variable numbers of segments of the tube (Anostraca, Notostraca,
Stomatopoda, Decapoda). As the heart tube
became shorter, possibly in parallel with reduction of number of body segments, many
of the segmental ostia were lost. Any ostia
present in an animal are probably derived
from the ancestral segmental ones rather
than de novo structures, given their embryonic origin. Thus, the number of pairs of
ostia, unless they were secondarily lost,
could indicate the number of segments of
the ancestral heart tube that have been retained. By this argument, the heart of the
cladocerans, ostracods and copepods should
represent only one or two segments of the
primitive heart tube. The heart of decapods
must represent the fusion, and enlargement,
of at least three segments of the heart tube
because there are three pairs of ostia (Fig.
4C). In isopods the shortened heart retains
one or two pairs of ostia and it appears that
portions of the heart lack ostia. It has been
argued that ostia may have been lost from
segments of a heart that do not receive oxygenated blood (Burnett, 1984). Stomatopods have abdominal gills and the the abdominal portions of the heart tube have ostia. The caudal heart of isopods, and therefore the location of the ostia, is correlated
with the respiratory function of the pleopods (Barnes and Harrison, 1992). In decapods the dorsal abdominal artery is thought
to represent a remenant of the primitive
heart tube (see below), but there are no abdominal gills and the dorsal abdominal artery does not possess ostia.
CRUSTACEAN CARDIOVASCULAR EVOLUTION
205
AMA
HA
DAA
FIG. 4. Schematic drawings of the cardiovascular systems of a primitive malacostracan, (A) based on stomatopods, (B) a hypothetical intermediate or transitional state, and (C) a decapod. Anterior to left,; anterior median
artery (AMA), anterior lateral artery (ALA), hepatic artery (HA), sternal artery (SA), dorsal abdominal artery
(DAA), non-muscular flap valve (flap). (From Wilkens et al., 1997b).
nerve cord of the cardioregulatory nerves
are similar if not homologous. One pair of
inhibitory and two pairs of acceleratory
neurons occur in each group. In isopods the
cell bodies of the cardioinhibitory neurons
are located in the first thoracic ganglion
(Tanaka and Kuwasawa, 19916), and one
pair of cardioacceleratory neurons occurs in
both the second and third thoracic ganglia
(Tanaka and Kuwasawa, 1991a; Sakurai
and Yamagishi, 1998). In the decapod spiny
lobster, Panulirus argus, where the thoracic
and abdominal ganglia are concentrated
into a single thoracic ganglion, the cardioinhibitor nerves arise from the anterior region
of this ganglion and the two pairs of cardioaccelerators arise immediately posterior
(Maynard, 1953). Although the cell bodies
of these neurons have not been traced by
dye injection, their points of origin appear
to be homologous to those of the isopods.
The heart itself sends an artery directly
to each of the thoracic and abdominal appendages in the phyllocaridan leptostracans
and some hoplocarids. This pattern is modified somewhat in the ediophtalmian iso-
pods in that the anterior lateral artery
branches to supply the first four thoracopods. The dorsal abdominal artery (modified ancestral heart tube) in the anaspids,
mysids, euphausids and decapods supplies
arteries directly to the pereopods, but in the
thorax a single artery (descending or sternal
artery) divides to send an artery into each
pleopod and to the ventral nerve cord. In
decapods, and perhaps in the other orders
where it occurs, the sternal artery seemingly arose from one of the segmental lateral
arteries (Fig. 5). The tendency for a single
artery to branch to supply blood to several
appendages may have occurred as the heart
tube became shortened in length. Although
it does not in itself suggest an evolutionary
process, the present plan is much simpler
than would have resulted if all of the ancestral segmental arteries had been retained.
The dorsal abdominal artery
It is proposed that the dorsal abdominal
artery of prawns, spiny lobsters and chelate
lobsters may represent the modified posterior remnant of the original heart tube (Bur-
206
JERREL L. WILKENS
DAA
Gut
SegLA
Flex
VNC
FIG. 5. Drawing of a stylized transverse section of the 2nd abdominal segment of a lobster, Homarus americanus, showing the dorsal abdominal artery (DAA), the pair of segmental lateral arteries (Seg. LA) and the
asymmetric large medial branch on one side. It is proposed that the sternal or descending artery is derived from
one of the segmental lateral arteries. Ext, abdominal extensor muscles; Flex, abdominal flexor muscles; VNC,
ventral nerve cord. (From Wilkens et al., 1997b).
nett, 1984; Martin et al., 1989; Wilkens et assist or assume the primary role of pumpal, 1997b). The lateral walls of the dorsal ing blood as mentioned above for barnacles
abdominal artery contain bands of muscle and small copepods and ostracods. The cor
whereas all other arteries lack muscle. The frontale of the median anterior artery of
contractions of these muscles in Homarus decapods (Steinacher, 1979) is an example
are modified by the neurohormone procto- of an auxiliary pump where the small dilin in similar manner to cardiac muscle ameter and length of an artery would result
(Wilkens et al., 19976). No function has yet in high resistance to flow. The guiding prinbeen identified for this muscle. If the dorsal ciple here is that the muscular development
abdominal artery is derived from the orig- of the heart, in particular its ability to geninal heart tube, the absence of segmental erate force, must be correlated with the reostia may have occurred in parallel with the sistance and afterload to blood outflow that
loss of abdominal gills (see below). Further, arises from the cumulative length of the arthe bicuspid valves at the origin of each of terial system and its branches and the mean
the segmental lateral arteries leaving the blood pressure. When the circulatory pathdorsal abdominal artery and of the arteries way is short, as in quite small organisms,
leaving the heart appear to be homologous the seemingly low pressure and low veloc(Alexandrowicz, 1932).
ity pumping action of a pulsatile tube is adequate. Contraction of the tubular heart in
FUNCTIONAL MORPHOLOGY: RELATIONSHIP
branchiopods occurs as a peristaltic wave in
BETWEEN BODY SIZE, LIFE SYLE AND THE
T. longicaudatus (Yamigishi et al., 1997)
COMPLEXITY OF THE CVS
and Artemia sp. (Doyle and McMahon, unHeart
published observations). The hydrodynamThe heart is generally the pump for the ics of tubular hearts await study, but the
circulatory system, but other pumping pressures developed by peristaltic waves of
mechanisms such as accessory pumps may contraction may be lower than those of a
CRUSTACEAN CARDIOVASCULAR EVOLUTION
heart that contracts as a single unit. Those
forms lacking a heart are able to move
blood (coelomic fluid) through the hemocoel by movements of the body and gut
(McLaughlin, 1980).
From a functional perspective, one can
ask why the primitive heart tube that runs
from the head to tail regions has been shortened in some forms. The heart tube may
have been shortened in the Cladocera, Ostracoda and Copepoda as body segments
were fused and eliminated. A second possible reason for condensation may have
been the need for a more powerful pump to
propel blood though longer and more highly branched arteries. Moving from the more
primitive and smaller phyllocaridans to the
most advanced and often large malacostracan decapods, the heart has changed from
a thin walled tube no more than one muscle
cell layer thick to a thick walled highly
muscular ventricle. The proposed folding
and the incorporation of at least three body
segmental components of the original heart
tube to form the decapod heart (Wilkens et
al., 1991 b) may have allowed for the development of a thicker walled heart, one
composed of multiple layers of muscle vs.
the single layer of muscle found in tubular
hearts. This would have allowed the heart
to generate greater force which in turn
would have allowed the heart to pump
blood into longer and more extensive vascular spaces. A powerful heart is clearly a
necessity to move blood throughout larger
crustaceans such as crabs and lobsters. The
lobster heart generates systolic pressure of
1.6 kPa as it overcomes a total peripheral
resistance of 1.93 kPa s ml"1 (Wilkens et
al., 1997a).
Ostia
Whereas the number of pairs of ostia
may indicate the number of segments of the
primitive heart tube that are retained, it is
recognized that ostia may be lost from portions of the heart. Ostia are present in those
abdominal regions of the stomatopod heart
tube that receive oxygenated blood from
gills or related gas exchange structures
(Burnett and Hessler (1973), but they are
absent in these regions in decapods that
lack abdominal gills. It appears that the loss
207
of gas exchange structures in a group of
animals has been accompanied by the loss
of ostia from the corresponding regions of
the heart tube. It is adaptive for the heart to
only pump oxygenated blood.
Peripheral circulation
Video recordings show the movement of
hemolymph in radiating and anastomosing
tissue spaces in the integument immediately
below the carapace in myodocopid and podocopid ostracodes (Abe and Vannier,
1995). The short diffusion distance across
the thin cuticle indicates that the integumentary circulation plays a respiratory
function. These elaborate channel patterns
occur on the shells of fossil ostracodes dating from the middle Cambrian (Vannier et
al., 1997). These findings point to the elaboration of a circulatory system early in the
evolution of the Crustacea. The circulatory
paths in the animals in the classes other
than the Malacostraca are relatively short,
and even the anostracans and notostracans
that attain lengths of 10 cm are small in
cross section. The smallest of these animals
often lack blood vessels. The only vessel
leaving the heart in any of these animals is
a single anterior artery supplying the head
region. Either segmental lateral arteries
were never present or, less likely, they were
secondarily lost. The absence of extensive
arterialization may account for the small
size of animals in these five classes of crustaceans.
An arterial system may be a requirement
to allow growth in body size beyond some
minimal limit, or, stated another way, increased body size may require more extensive arterial arborization for adequate perfusion of tissues remote to the blood pumping organ. Highly aerobic tissues such as
the central nervous system require a dedicated blood supply particularly if they are
large or are down stream of other metabolically active tissues. This seems to apply to
the vascularization of the decapod central
nervous system (Sandeman, 1967; Shivers,
1970; Abbott, 1971), particularly if that tissue is behind a well developed blood-brain
barrier (Abbott, 1970; Brown and Sherwood, 1981). Circulatory development
therefore is clearly related to the require-
208
JERREL L. WILKENS
ments for minimal diffusion distances. On
the other hand, arterial development may
not be correlated closely with activity levels
if the animal is small, sedentary, or when
there is an alternate route to supply oxygen
and remove CO2
There is relatively great flexibility in the
degree of development of the peripheral
vascular system. For example, the polychaete and oligochaete Annelida possess an
extensive closed vascular system made up
of mesodermally derived arterial and venous vessels, but in the Hirudinea hearts are
secondarily derived (McMahon et al.,
1997). Flexibility in vascular system development is also seen in mammals where
blood vessels readily extend into expanding
tissues such as into adipose tissue of obese
individuals, into neoplastic tumors, and
even into transplanted tissues. The growth
in body size and appendage length in the
large Malacostraca may have stimulated
elongation of the arteries to supply the
"new" tissues.
PHYSIOLOGICAL EVOLUTION
Origin of heart beat
Evolution has been conservative when it
comes to functionally important molecules
and processes; notable examples that extend
across the animal kingdom include photoreception (Randall et al., 1997) and voltage
gated ion channels (Hille, 1992). The conservative nature of successful evolutionary
processes predicts that, because of its vital
importance, the control of the heart contractile rhythm throughout the Crustacea
will also be conserved. Until the last few
years crustaceans were thought to possess
neurogenic hearts in which the pacemaker
was a small ganglion of neurons, the cardiac ganglion, located on or in the heart itself, even though pharmacological experiments indicated that anostracan and cladoceran hearts might be myogenic (Maynard,
1960). The acceptance of the universality of
a neurogenic mechanism in the Crustacea
should have been questioned given that the
hearts of annelids and molluscs are all myogenic (McMahon et al., 1997). On the assumption that myogenic mechanisms are
the more primitive, is it possible to identify
at what point the switch from myogenic to
neurogenic pacemaking occurred in this
sub-phylum?
The heart beat pacemaker of the notostracan T. longicaudatus is myogenic throughout the entire life cycle (Yamagishi et al.,
1997). The simple tubular heart does not
contain nerve cells, and tetrodotoxin
(TTX), the highly specific blocker of neuronal activity, does not affect the beat
rhythm. The myocytes are electrically coupled so that the heart is a functional syncytium. The myogenic pacemaker rhythm
consists of 20-30 mV slow waves of depolarization without spikes that sweep via
gap junctions along the length of the heart.
The wave of depolarization will cause a
peristaltic wave of contraction. For a heart
beat arising from spontaneous myogenic
pacemakers to work, the myocytes need to
be linked by gap junctions that will allow
the wave of depolarization to sweep across
the entire muscle sheet. Myocytes in T. longicaudatus are coupled electrically and they
function as a single muscle oscillator (Yamagishi et al., 1997). Because the Notostraca are considered to have been among the
earliest groups of crustaceans to appear, the
peristaltic contraction of a myogenic heart
is probably the most primitive. Gap junctions are retained in mantis shrimp (Irisawa
and Hama, 1965) and lobster (Van der
Kloot, 1970) hearts.
Moving to the Malacostraca we find that
the heart of the adult isopod Ligia (Megaligia) exotica displays both myogenic and
neurogenic activity (Fig. 6A, Ai, 1966).
The posterior portion of the heart, behind
the level of the 6 neuron cardiac ganglion,
displays spike potentials riding on slow
waves of depolarization when innervated
by the cardiac ganglion, but only slow
waves after it is sectioned from the rest of
the heart (Fig. 6B). These latter slow wave
potentials are typical of a pacemaker potential. Slow pacemaker potentials are not recorded from the anterior innervated regions
of the heart, but rather action potentials
arise abruptly from a stable baseline as
would be expected if myogenic pacemaking
were subordinated to neural drive (Fig. 6C).
The anterior regions still can display myo-
CRUSTACEAN CARDIOVASCULAR EVOLUTION
B
A
arteries
CG
209
\
/
<
s
—.
a
ostia ,.-—
——
7
8
9
10
III
11
\
/
12
13
h
FIG. 6. (A) Schematic drawing of Ligia exotica heart (dorsal view), (B) two examples of potentials recorded
from segment 12. In the intact heart a spike arises from a slow a slow diastolic depolarization (i), but this is
lost when input from the cardiac ganglion is removed when the heart is sectioned at segment 9 (ii), (C) electromyograms from the anterior half of the heart (i) from the dorsal surface of the anterior half of the heart and (ii)
from a region hear the ganglionic trunk (From Ai, 1996).
genie rhythmicity when functionally denervated (see below).
The heart beat of the embryo and early
juvenile L. exotica is strictly myogenic (Yamagishi, 1996; Yamagishi and Hirose,
1997). In early juveniles less than 5 days
old the rate of slow wave muscle potentials
is unaffected by TTX, although sodium-de-
pendent spike potentials arising from them
are eliminated (Fig. 7A). The cardiac ganglion of these early juveniles innervates the
myocytes, but does not yet produce bursts
of action potentials. Stimulation of the ganglion at this stage produces excitatory synaptic junctional potentials (EJP) in the muscle that are able to reset and entrain the
210
JERREL L. WILKENS
A
50 mV
01s
50 mV
a> 3 I
"-
05s
0.5 min
0 5s
B
100 mg
cr
FIG. 7. Effects of tetrodotoxin (TTX) on the cardiac ganghonic and muscle activities in (A) early juvenile two
days after hatching and (B) adult Ligia exotica (Isopoda) hearts. (Al) Simultaneous intracellular microelectrode
recordings from the heart muscle (upper trace) and extracellular recordings from cardiac ganglion (lower trace).
(A2) Effects of TTX on heart muscle activity recorded intracellularly (upper trace) and frequency of muscle
burst discharge (Hz, lower trace). The arrowhead shows the time when the perfusion saline was changed to
TTX-containing saline (10 6 M). (B) The impulse activity recorded from the cardiac ganglion (top trace), the
mechanical contractions of the heart (middle trace) and the frequency of the heartbeat (bottom trace). TTX (10 6
M) was applied during the period indicated by the black bar. (From Yamagishi and Hirosi, 1997).
myogenic rhythm. The onset of spontaneous, but irregular, EJP-like small depolarizing potentials from the cardiac ganglion
occurs between days 5 to 12. These EJPs
are blocked by TTX. When the cardiac ganglion begins producing regular bursts of action potentials in the motoneurons that innervate the myocardium the heart becomes
neurogenic. However, even adult hearts display slower oscillatory (myogenic) potentials after the neural activity is blocked by
TTX (Fig. 7B). Thus, the myogenic rhythm
has become subordinated to, but not eliminated by, neurogenic drive. The ionic conductances responsible for the myogenic
rhythm persist in adults.
The anatomy of the CVS of the Stomatopoda is considered to reflect a primitive
condition (McLaughlin, 1980); however the
heart of Squilla oratorio is electrically silent when isolated from the cardiac ganglion neurons (Shibuya, 1961). By the hypothesis proposed here, the loss of myogenicity represents a derived condition involving the loss of expression of the ionic
channels that produce pacemaker potentials
by the myocytes.
Heart beat in adult decapods appears to
be purely neurogenic; however, embryonic
hearts may be myogenic. In H. americanus
the heart arises from segmentally derived
lateral blocks of mesoderm, and myoblasts
CRUSTACEAN CARDIOVASCULAR EVOLUTION
and neuroblasts are both present in embryonic hearts at the onset of contractions
(Burrage, 1978; Burrage and Sherman,
1978). These authors concluded that the initial twitches of the heart result from cardiac
ganglion input because the sides of the, as
yet incompletely formed, heart twitched
synchronously. There is no evidence to indicate whether at this stage of development
the two blocks of muscle are in direct communication with one another. The increase
in heart rate and regularity in beating on the
second day after the initial beats may represent the proliferation of neuromuscular
synapses and the continued development in
the neuropil of the cardiac ganglion. Embryonic hearts that have just begun to beat
(1 to 2 contractions during a 5 minute interval) contain a 9 neuronal cardiac ganglion. At this stage the embryonic heart has
fully developed contractile units and innervation with distinct synaptic junctions;
however, these morphological observations
do not allow us to evaluate whether the
heart beats are myogenic or neurogenic. In
the decapod shrimp Metapenaeus ensis,
TTX does not prevent heart beat in early
juveniles of less than 5 mg body weight,
but it does arrest heart beat in larger ones
(Doyle and McMahon, 1998). In larger juveniles, whose heart beat has been arrested
by TTX, electrical stimulation still causes
heart contractions. Because these observations were made on intact animals by video
techniques, it is not known whether the early juvenile hearts exhibit any membrane potential oscillations or whether the beat
rhythm can be reset as would be expected
if the rhythm was myogenic. Histological
evidence of the presence of cardiac neurons
in these seemingly myogenic stages is
wanting at this point.
The ostial valve muscles of crustacean
hearts are considered to be a model system
for the study of the myocardium much as
trabeculae are used in the study of mammalian hearts (Yazawa, Wilkens, ter Keurs
and Cavey, unpublished observations). The
isolated ostia from adult H. americanus
hearts do not exhibit spontaneous changes
in membrane potential or contraction, but
they contract when electrically stimulated.
As with Squilla, adult Homarus myocardi-
211
um appears to have lost its myogenic pacemaker; however, not all attributes of a myogenic system are lost since gap junctions
are retained in both hearts (Irisawa and
Hama, 1965; Van der Kloot, 1970, respectively).
The available data suggest that the hearts
of embryonic and early juvenile decapods
have retained the 'primitive' myogenic contractile rhythmicity, but that the myogenic
potential is lost as neurogenic drive becomes established. I advance the hypothesis
that the earliest crustaceans possessed myogenically driven hearts, but in more advanced groups there is a shift toward neurogenic pacemaking arising from a group of
neurons, the cardiac ganglion, found on
(stomatopods, Alexandrowicz, 1934) or inside (decapods, Alexandrowicz, 1932) the
heart. There may be a strong evolutionary
advantage to neurogenicity since it is found
in all Malacostroca that have been examined. It is not know whether the cardiac
ganglion of stomatopods and decapods is
homologous. The evolutionary pressures
that might have driven this process are not
known, but the evolutionary opportunities
provided may be substantial. Two possible
advantages are envisioned. In Squilla the
cardiac ganglion causes simultaneous contraction of the entire elongated tubular heart
(Shibuya, 1961) which will generate more
force that would the peristaltic waves of
contraction in myogenic hearts. Such synchronous contractions are able to move
blood into all arteries including the posterior artery, something that would be more
difficult in forms where the tube contracts
peristaltically. Second, it appears more efficacious for the cardioregulatory nerves
from the central nervous system to synapse
on the cardiac ganglion than to innervate
the complete myocardium. The advantage
of rapid responses is obvious in the abrupt
cardiac arrest that is used as part of a defensive strategy by decapods to avoid detection by preditors such as sharks that locate prey by electroreception (Wilkens et
al, 1974).
EMBRYOLOGY
Even though it is highly variable across
the subphylum, the embryonic development
212
JERREL L. WILKENS
of the CVS may provide some clues to the differentiation reflects the fact that the orievolution of this system in the Crustacea. gin and early elaboration of these systems
Embryology does not tell us much about lies within the early history of the Metazoa
the origins and interrelationships of crusta- itself. The Hox genes are a highly concean classes, but there is an underlying uni- served homeobox that programs a characty in terms of fundamentally similar fate teristic sequence of morphological gene exmaps of the blastula or blastoderm and the pression (Averof and Akam, 1993; Osorio
retention of a nauplius state in development et ah, 1997). Does a cluster of homeotic
(Anderson, 1982). The development of the genes also mediate the expression of genes
postnaupliar somites is similar from bran- that specify the CV system? If or when the
chiopods to the malacostracans including genetic analysis of developing body plans
the elaboration of the segmental mesoderm is extended to intra-arthropod diversity, we
that produces the cardiac and perivisceral may learn whether Hox-type gene clusters
hemocoel. The segmentally derived meso- account for the different CV systems, or
dermal pericardial septum proliferates into whether the types of plans are developmenthe pericardial hemocoel a mass of cells tal consequences of different body plans.
that grows toward the midline and forms
ACKNOWLEDGMENTS
the wall of the heart (Kume and Dan, 1968;
Anderson, 1982). The ostia arise from inI thank Dr. B. Chatterton, Department of
tersegmental spaces between the cardiac Geology and Geophysics, University of Alcomponents of successive somites. The se- berta, for providing paleontological guidrial repetition of this pattern would produce ance, and Dr. B. R. McMahon for helpful
the heart tube with intersegmental ostia comments on the manuscript. This study
along the entire length of the embryo. If the was supported in part by the Natural Scimorphology of the adult heart reflects ence and Engineering Research Council of
changes in body plan and circulatory de- Canada.
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Corresponding Editor: Gary C. Packard