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REVIEW/SYNTHÈSE
Neuronal control of swimming in jellyfish: a
comparative story1
Richard A. Satterlie
Abstract: The swim-control systems of hydrozoan and scyphozoan medusae show distinct differences despite similarity
in the mechanics of swimming in the two groups. This dichotomy was first demonstrated by G.J. Romanes at the end
of the 19th century, yet his results still accurately highlight differences in the neuronal control systems in the two
groups. A review of current information on swim-control systems reveals an elaboration of Romanes’ dichotomy, but
no significant changes to it. The dichotomy is used to suggest that cubomedusae are more closely aligned with the
scyphomedusae, and to highlight areas of future research that could be used to look for common, possibly primitive,
features of medusan conduction systems.
Résumé : Les systèmes natatoires des méduses hydrozoaires et scyphozoaires comportent des différences importantes
en dépit de la similitude des mécanismes de nage chez les deux groupes. Cette dichotomie a été observée pour la première fois à la fin du 19e siècle par G.J. Romanes dont les résultats sont toujours utilisés pour mettre en lumière les
différences de contrôle neurologique chez les deux groupes. Une revue de la littérature récente sur les systèmes de contrôle de la nage indique que la dichotomie de Romanes a été précisée, mais que rien de substantiel n’y a été ajouté.
Cette dichotomie laisse croire que les cuboméduses sont alignées plus étroitement avec les scyphoméduses et met en
lumière de nouvelles avenues de recherche qui pourraient éventuellement révéler l’existence de caractères communs,
possiblement primitifs, dans les systèmes de conduction des méduses.
[Traduit par la Rédaction]
Satterlie
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Introduction
Jellyfish swim by contracting circular (and sometimes
radial) musculature that lines the subumbrellar surface of the
swimming bell. This serves to decrease the volume of the
subumbrellar cavity, and the resultant expulsion of water
provides the motive force for aboral acceleration of the medusa.
This is perhaps the only statement on jellyfish swimming
that can be applied across the entire phylum, at least at the
systems level of organization. Even this statement loses its
utility if one delves into the biomechanical specifics of
subumbrellar contraction in the various medusoid representatives (Gladfelter 1973). If we want to find commonalities
in jellyfish swim control we have, at the least, to step down
to the class level of organization. Even then, there is tremendous variation in the specifics of neuronal organization that
is undoubtedly related to individual ecological and physiological peculiarities.
It is when we look at class-specific similarities in swimcontrol systems that a wonderful dichotomy captures our attention. However, before we feel too proud of ourselves, we
need to look back to the 1800s, and the work of G.J. Romanes
(1885), to see that this is not current news. Romanes managed to elegantly uncover this dichotomy and to document it
thoroughly using only the simplest of physiological experimentation, frequently relying on behavioral observations made
during cleverly designed cutting experiments. This early work
might have escaped our attention had Passano (1965, 1973)
not picked up and elaborated upon the dichotomy, using behavioral and electrophysiological techniques. So, while this
review has as its primary focus the work of Romanes, it is
also a testament to Passano’s keen comparative eye. Passano’s
motion (Passano 1965, 1973) that Romanes’ results are timeless
is seconded here; we have added to the results, but to this
day we have not significantly amended them.
In his investigations, Romanes (1885) referred to the
medusoid members of the class Scyphozoa and the class
Hydrozoa as “covered-eyed medusae” and “naked-eyed
medusae”, respectively. Despite the similarities in the
biomechanical aspects of swimming mentioned above, the
neuronal control systems in the two groups are nearly as different as night and day. Romanes says it best: “There is so
Received 7 November 2001. Accepted 16 May 2002. Published on the NRC Research Press Web site at http://cjz.nrc.ca on
15 November 2002.
R.A. Satterlie. Department of Biology, Arizona State University, Tempe, AZ 85287-1501, U.S.A. (e-mail: [email protected]).
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This review is one of a series dealing with aspects of the biology of the phylum Cnidaria. This series is one of several virtual
symposia on the biology of neglected groups that will be published in the Journal from time to time.
Can. J. Zool. 80: 1654–1669 (2002)
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DOI: 10.1139/Z02-132
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Satterlie
great a difference between the nervous system of the nakedeyed and covered-eyed Medusae, that simultaneous description of the nervous systems in both groups is not…practical”. This statement was made during his discussion of the
histological results obtained by Hertwig and Hertwig (1878);
however, Romanes’ experiments backed up the concept with
physiological evidence that fully supported the dichotomy.
We now have the advantage of well over a century of research on cnidarian nervous systems, and in this time,
numerous technical advances have allowed a more
reductionist testing of Romanes’ dichotomy. The advance of
science is somewhat saltatory, the jumps typically following
new technological developments. In between occur periods
of often intense and necessary, but slower, progress. These
intervening periods were best characterized by one of my
mentors, who said, “the nuggets have been mined, now we
are left to pan for the dust”. I add to this statement, “…until
the next vein is discovered”. Such a vein is now upon us,
with the widespread use and utility of modern molecular
techniques. For that reason this review of our knowledge of
swim control in jellyfish is very timely. Hopefully it will
serve to stimulate the next wave of advances in answering
what is a long-standing but difficult question for this “primitive” phylum: in view of the drastically different mechanisms of swim control in scyphozoan and hydrozoan medusae, which best reflects the primitive characteristics of the
common ancestor? This is a critical question for this phylum, since it is the lowest on the phylogenetic tree to have a
distinct, multicellular nervous system. With current molecular
techniques we have never been closer to a means for generating new nuggets of speculation on this question. Furthermore, one aspect of the scyphozoan/hydrozoan swim-control
dichotomy is a critical element of this speculation, and represents a classical example of how these new techniques
hold the potential for advancing our ability to answer such
“which came first?” types of questions. What that aspect of
the dichotomy is will be kept under my hat until later in the
review. Thus, while the primary aim of the review is to summarize past work on jellyfish swimming, it is also intended
to draw, drag, or otherwise coerce a new generation of researchers to pick up the challenge unwittingly started by
Romanes: how far do we have to go to defeat his dichotomy? In other words, what ground is common and what is
not, and which ground is more “primitive” as opposed to being secondarily gained or lost? There are likely to be large
nuggets waiting to be unearthed in this arena.
The following is not only a testament to the work of G.J.
Romanes, but also a challenge to his ideas. Throughout the
review, selected quotations from Romanes (1885) will be
provided to illustrate his remarkable insights into swim control in medusae. In agreement with Romanes’ view on the
nervous organization of scyphozoans and hydrozoans, the
two groups will be treated separately. There is an additional
surprise, however. Arguments for a new cnidarian class, the
Cubozoa, have been forwarded and generally accepted (Werner
1973), although two separate camps still argue about whether
the cubozoans have closer affinities to the Hydrozoa or the
Scyphozoa. Since the Cubozoa includes medusoid forms, the
cubomedusae, I will consider them after the other two groups
so that I can speculate on their affinities. Again without revealing my hand, I will say that the cubomedusae were pre-
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viously included with the Scyphozoa. We will see what the
swim system says.
Neural control of swimming in
scyphomedusae (covered-eyed medusae)
Location of pacemakers
Romanes (1885) examined the location of swim pacemakers in Aurelia sp., in what he referred to as the “fundamental
experiment”, where he used tissue ablation as a method of
localizing the sites of pacemaking activity. Aurelia sp. and
other scyphomedusae have marginal sensory structures called
rhopalia (lithocysts to Romanes), which include a statolith,
sensory epithelia, and an ocellus. The number of rhopalia is
variable and species-specific, most frequently 8 or 16, although some species have more, typically in multiples of 4.
Romanes (1885) found that removal of all rhopalia left the
medusa unable to produce spontaneous swimming contractions. His account of pacemaker localization includes the
following statement (Romanes 1885): “…all the remarkable
paralyzing effects which…are obtained by excising the entire
margin…are obtained in exactly the same degree by excising
the eight lithocysts alone…”. Similar results have been obtained from several other scyphomedusae (Passano 1965,
1973; personal observations).
Stimulation of the subumbrella in an animal with all
rhopalia removed produces a conducted contraction which
appears very like that in the intact animal (Romanes 1885).
Thus, while the rhopalial pacemakers are responsible for initiating contractions, their removal does not alter the conduction of excitation through the subumbrellar muscle sheet.
Coordination of pacemakers
Each rhopalial pacemaker is capable of initiating a contraction of the subumbrellar swim musculature. The current
view on pacemaker interaction is that activity from an active
pacemaker “resets” all others, so the pacemaker with the
fastest rhythm controls the swim system (Pantin and Vianna
Dias 1952; Horridge 1959). Since there are eight or more
rhopalia in scyphomedusae, there is a constant shifting of
control within the set of pacemakers. The rate of firing of individual rhopalial pacemakers is variable and can be directly
influenced by sensory inputs, which presumably modify a
baseline discharge rate of the pacemaker. When a frequency
histogram of pacemaker output from a piece of medusa containing a single rhopalium is plotted, the distribution shows
a single broad peak with a long tail, suggesting that even under controlled experimental conditions, the output of a single
swim pacemaker is quite variable (Horridge 1959; Lerner et
al. 1971). The effects of linking several of these variable
pacemakers together have been tested theoretically, first by
Horridge (1959) and then by Lerner et al. (1971) and Murray (1977). In all three studies, output data from a piece of
medusa containing a single rhopalium was used to simulate
the linkage of different numbers of statistically identical pacemakers into a single network to determine the overall output
in terms of swim frequency. In all three studies, pacemaker
interactions were assumed to be of the resetting type. Three
advantages emerged from the linking of multiple pacemakers (Horridge 1959; Lerner et al. 1971; Murray 1977). First,
the overall output of the network was much more regular
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than that of individual pacemakers: as the number of pacemakers was increased, there was a decrease in the variation
of interpulse intervals, producing a “tighter” frequency histogram. Second, the overall mean swim frequency increased
as pacemakers were added to the network. Finally, Murray
(1977) was able to show that the network was more sensitive
to “sensory” perturbations, provided such inputs were common
to all pacemakers. Since scyphozoans have a large number
of swim pacemakers, the question about pacemaker redundancy is answered by the resultant increase in both swim
frequency and swim regularity, with the possibility of greater
sensitivity to some types of sensory input. Furthermore, their
arrangement around the margin of the swimming bell places
sensory structures in a distributed array that best serves the
needs of these radially symmetrical animals.
Conduction of an action potential between pacemakers is
accomplished by the same conduction system that distributes
excitation to the swim musculature throughout the subumbrella.
In other words, there are no direct “commissures” connecting
the rhopalial pacemakers (Romanes 1885; Horridge 1954,
1956b; Passano 1965, 1973). The main consequence of this
organization is the possibility of more than one pacemaker
discharging during a single time interval. When this happens, two separate waves of contraction are initiated, and
these cancel at the point of collision, owing to a state of
mutual refractoriness in the area surrounding the meeting. In
these cases, the swim musculature in any one part of the animal sees only a single input, so the resultant contraction is
not that different, mechanically, from one which is initiated
by a single pacemaker.
Organization of the conduction system that initiates
swim contractions
As mentioned above, the conduction system that links the
rhopalial pacemakers is the one which is responsible for
spread of excitation throughout the subumbrellar muscle
sheet. This nerve net was originally called the giant fiber
nerve net (Passano 1973), but was later renamed the motor
nerve net (MNN; Anderson and Schwab 1981, 1983;
Figs. 1A, 1B). Three observations are critical in understanding MNN function. First, it is “through-conducting.” An impulse generated in one part of the conduction system is transmitted through the entire system without failure (Romanes
1885; Horridge 1956a, 1956b). Second, since the swim musculature is found throughout most of the subumbrella, as is
the MNN, spread of excitation is referred to as “diffuse conduction”. Third, transmission of excitation is nonpolarized
(Anderson 1985; Romanes 1885); it can occur in any direction through the conduction system, although the normal initiation of activity from rhopalial pacemakers imposes some
limits on conduction direction.
In early histological work, such as that of the Hertwigs
(Hertwig and Hertwig 1878) and Schafer (1878), the organization of nervous tissue was described as a loose network of
mostly randomly oriented neurons (see Figs. 1A, 1B).
Armed with this background histology, Romanes (1885) observed the ability of the swim system to conduct activity
around a series of complex incisions, testing both the diffuse
and the nonpolarized nature of the nerve net. His take on the
situation is best summed up in his words: “The extent to
which the neuro-muscular tissues of the Medusa may be
Can. J. Zool. Vol. 80, 2002
mutilated without undergoing destruction of their physiological continuity is in the highest degree astounding”. Romanes
coupled his physiological knowledge with the histological
information on nerve-net structure to put forward this analogy of the motor nerve net: “…if the reader will imagine a
disc of muslin, the fibres and mesh of which are finer than
those of the finest and closest cobwebs, and imagine the
mesh of these fibres to start from the marginal ganglia, he
will gain a tolerably correct idea of the lowest nervous system in the animal kingdom”.
We now know that the neurons which make up the MNN
in scyphomedusae are bi- or multi-polar, and are unpolarized
in terms of the direction of action-potential propagation
through their neurites (Anderson and Schwab 1981, 1983).
Furthermore, the nerve net is synaptic (Anderson and
Schwab 1981, 1983; Anderson 1985; Anderson and Grunert
1988; Westfall 1996). Where the neurites of two neurons cross,
or come in close contact, chemical synapses are found.
These synapses are unique in that they are bidirectional;
each terminal of the synapse can serve as the pre- or postsynaptic element (Anderson and Schwab 1981; Anderson
1985; Anderson and Grunert 1988). It is this feature of
bidirectionality that allows the nerve net to be unpolarized in
terms of the direction of propagation of activity.
Romanes (1885) was aware that the nerve net is made up
of individual, discrete neurons, and that these neurons share
some type of physiological connectivity throughout the
nerve net. From his writing, it is evident that similar physiological connectivity had been “discovered” within the spinal
cord of vertebrates, even though the concept of the chemical
synapse was not yet formulated. In Romanes’ words,
“…there can scarcely be any doubt that some influence is
communicated from a stimulated fibre a to the adjacent fibre
b at the point where these fibres come in close apposition”.
Then, “…much more remarkable does this fact become
when we find that no two of these constituent nerve fibres
are histologically continuous with one another”. Romanes
recognized that “no…anatomical continuity exists, but…
physiological continuity is maintained by some process of
physiological induction…”, although he revealed that it was
“premature to speculate” on the mechanism of physiological
induction. Once again, Romanes’ cutting experiments demonstrated the nonpolarized, diffuse nature of conduction
through the subumbrellar nerve net (Romanes 1885).
Based on several pieces of evidence, it is believed that
neurons of the MNN do not interact via electrical connections. First, electrophysiological recording from both preand post-synaptic neurons does not reveal direct current flow
between the two (Anderson 1985; Anderson and Spencer
1989). Second, synaptic delays were consistent with those of
chemical synapses in other animals (Anderson and Spencer
1989). Third, neurons injected with Lucifer Yellow did not
show dye-coupling with other neurons in the network (Anderson and Schwab 1981, 1983).
Action potentials in MNN neurons are conventional compared with those of “higher” animals (Anderson and Schwab
1983). In particular, voltage-clamp experiments have shown
that the various ion currents involved in action-potential generation are very similar to those found in other animals (Anderson 1989).
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Anatomical and physiological evidence suggests that
transmission of excitation from the MNN to the associated
swim musculature is also synaptic, although direct recordings from individual muscle cells are lacking (Anderson and
Schwab 1981). Romanes (1885) found that neuromuscular
transmission exhibits frequency-dependent facilitation, a fact
that was elaborated by Bullock (1943), Pantin and Vianna
Dias (1952), and Horridge (1956a).
Romanes (1885) also discovered a second nerve net,
called the diffuse nerve net (DNN; Horridge 1956a), that interacted with the MNN, primarily at the rhopalia. Romanes’
demonstration of the two nets, using elaborate experiments
that involved cutting through the swimming bell, is illustrated in Fig. 2. Activity in the lower threshold DNN produced a wave of tentacle contraction, without contraction of
the swim musculature, that survived the series of cuts shown
in Fig. 2, which were specifically designed to test the diffuse
nature of the conduction system. Once the conducted DNN
impulse reached the rhopalium, and following a slight delay,
a wave of MNN-induced subumbrellar contraction was
transmitted back through the subumbrella in a direction opposite to that of DNN activity. Like DNN activity, MNN activity survived all of the interdigitating cuts. The concept of
two diffuse subumbrellar nerve nets was confirmed and advanced by Horridge (1956a, 1956b) and Passano (1965, 1973),
who found that the DNN conducted impulses at around half
the conduction velocity of the MNN, and that DNN impulses
interacted with MNN impulses primarily at the rhopalia,
where DNN activity usually caused an acceleration of MNN
output. All three investigators, including Romanes, found an
additional peculiarity of the DNN. Even though it was incapable of directly producing a swimlike contraction of the
subumbrellar musculature, its activity was capable of enhancing MNN-induced contractions (Romanes 1885; Horridge
1956a, 1956b; Passano 1965, 1973). Thus, this “dual
innervation” of the swim musculature includes direct synaptic control via the MNN and modulatory control by the
DNN. With the combination of frequency-dependent facilitation within the MNN neuromuscular connections and the
modulatory influence of the DNN, the swim musculature is
capable of a wide range of contractility patterns.
Immunohistochemical and physiological evidence suggests that taurine may be a neurotransmitter used by the
MNN neurons of scyphomedusae (Carlsberg et al. 1995). In
addition, two families of neuropeptides, RFamides and
RWamides, have been identified in all four cnidarian classes
(Grimmelikhuijzen et al. 1989). More recently, specific
RFamides similar to those that have been identified in members of the class Anthozoa (anthoRFamides; Anderson et al.
1992; Moosler et al. 1997) have been identified in scyphomedusae. In scyphomedusae, the distribution of neurons
expressing immunoreactivity to RFamide antibodies includes
networks in the tentacles, subumbrella, exumbrella, oral lobes,
and gastric cavities (Anderson et al. 1992), and Carlsberg et
al. (1995) present convincing evidence that at least some
networks of these neurons represent the DNN. In our hands,
a commercial FMRFamide antibody gave similar staining in
four scyphomedusan species, confirming these results and
suggesting a distribution that was similar to the anatomical
descriptions of the DNN (Fig. 1C; R.A. Satterlie, in preparation). In particular, intense nerve-net staining was found in
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the marginal regions of the bell, which showed an increase
in neuron density near and around the rhopalia. Furthermore, putative sensory cells were stained within the rhopalial
epithelium and in the epithelium lining the rhopalial niche
(Fig. 1C). Less intense staining, with a lower density of neurons, was found throughout the subumbrella. Staining was
again intense in the oral arms and other regions of the digestive system. An immunoreactive exumbrellar nerve net, like
that found by Anderson et al. (1992), was found in some
species.
It was determined that the FMRFamide immunoreactive
nerve nets are separate from the neurons of the MNN,
which stained brightly with antibodies against α- and βtubulin. The latter MNN neurons were larger in diameter
than the FMRFamide-immunoreactive fibers, and were much
more numerous in the regions of the subumbrellar in which
the swim musculature was found. Furthermore, the tubulinimmunoreactive nerve net clearly originated in the rhopalia
and fanned out across the subumbrella, excluding the extreme margin, where FMRFamide staining was most intense
(R.A. Satterlie, in preparation). FMRFamide-immunoreactive
neurons were occasionally stained with the tubulin antibodies, as determined by double labeling, but the staining was
extremely weak and clearly distinct from that of the MNN
network. Our anti-tubulin staining in the circular-muscle
regions of the subumbrella is virtually identical with that obtained by Carlsberg et al. (1995) using an anti-taurine antibody.
Neural control of swimming in
hydromedusae (naked-eyed medusae)
Location of pacemakers
Romanes (1885) conducted his “fundamental experiment”
on a member of the genus Sarsia and came up with quite
different results to those obtained from scyphomedusae. In
the hydromedusae, excision of the entire margin was necessary to paralyze the swimming bell. In Romanes’ words,
“Excision of the extreme margin of a nectocalyx causes immediate, total and permanent paralysis of the entire organ”,
while the “…severed margin continues rhythmical contractions”. Only a small portion of the margin needs to remain
attached to the bell for it to continue to produce swim contractions in Sarsia. As Romanes noted, “…it has been a matter of the greatest surprise to me how very minute a portion
of the intertentacular marginal tissue is sufficient, in the case
of this genus (Sarsia), to animate the entire swimming-bell”.
Neural organization of the bell margin
The traditional diffuse nerve nets of most cnidarians are
not well represented in the swim-control system of hydromedusae. Instead, the important neural elements for swim control are found in one of two marginal nerve rings: the inner
nerve ring (Fig. 3). To some, including Romanes (1885), this
represents a step up in organizational terms: “My experiments have shown that the nervous system in the naked-eyed
Medusae is more highly organized, or integrated, than in the
covered-eyed Medusae” through a “gathering together of nervefibres into definite bundles or trunks”. The hydrozoan innovation
can be viewed as a compression of the nerve-net architecture
into two marginal nerve rings: the subumbrellar inner nerve
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Can. J. Zool. Vol. 80, 2002
Fig. 1. Structure of the nerve net in scyphomedusae. (A) Beta-tubulin immunoreactivity of the motor nerve net (MNN) of
Phacellophora sp. near a rhopalium (the brightly stained structure at the top of the figure). Note that stained neurons radiate in two
tracts which leave the rhopalium and then form a more random network orientation. (B) Beta-tubulin staining of the subumbrellar muscle sheet of Phacellophora sp., showing the random orientation of stained MNN neurons. (C) FMRFamide immunoreactivity in the
margin of Cassiopeia sp., including a rhopalium and part of the rhopalial niche. Note that intense staining is limited to the marginal
region (the subumbrellar muscle sheet starts in the dark area at the top of the figure). Also, the staining lining the rhopalial niche and
in the rhopalial epithelium is most intense. In both of these places, stained cells with surface projections are numerous. The stained
network continues throughout the subumbrellar muscle sheet, but the staining is not nearly as bright and the density of neurons is
greatly reduced. The rhopalium in A is 500 µm in width; B is at the same magnification as A; the rhopalium in C is 300 µm in width.
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Fig. 2. Margin of the scyphomedusa Aurelia sp., showing one
type of cutting experiment used by Romanes (1885). The strip of
tissue is from the margin and shows the series of interdigitating
cuts used to demonstrate diffuse, nonpolarized conduction. The
initial stimulus was delivered at “A” and was subthreshold for
subumbrellar muscle contraction. However, it activated the DNN;
conduction is shown as a wave of margin tentacle contraction. A
single rhopalium is shown at “B”. When the DNN impulse
reached the rhopalium, a wave of subumbrellar muscle contraction, controlled by the MNN, ran in the opposite direction to the
arrow, back toward the original stimulation site. Both DNN and
MNN activity survived the tortuous conduction pathway imposed
by the cuts (modified from Romanes 1885).
ring and the exumbrellar outer nerve ring. Both nerve rings
are found at the junction of the swimming bell and the velum, a narrow flap of muscular tissue that extends inward
from the margin and serves to narrow the bell opening during a swim contraction (Fig. 3).
When viewed with oblique substage illumination, a network of large neurons is visible in the inner nerve ring of
many hydrozoans, extending a short distance down onto the
velum (Fig. 3C). When one of these neurons is penetrated
with microelectrodes, overshooting action potentials are recorded that precede swim contractions (Anderson and
Mackie 1977; Anderson 1979; Spencer 1981; Satterlie and
Spencer 1983; Satterlie 1985a). Perhaps the most unique
feature of this network, in a comparative sense, is the widespread electrical and dye coupling of component neurons
(Fig. 3D; Spencer and Satterlie 1980; Satterlie 1985a). Presumably each of these neurons in the network is capable of
acting as a pacemaker for the swim-control system, and with
the electrical coupling, not only can a different neuron act as
initiator, but also the contractile output of the swim system
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is the same irrespective of which neuron is the initiator. In
the anthomedusa Polyorchis penicillatus, this network has
recently been found to include strands of neurons which
connect those of two adjacent radii at the top of the
subumbrellar muscle sheet, so that the network of swim
motoneurons totally surrounds the muscle sheet of each
quadrant (Lin et al. 2001). Using a monoclonal antibody that
stained all neurons in P. penicillatus, Lin et al. (2001) also
provided the most complete anatomical picture of the nervous system of any cnidarian medusa.
In Polyorchis sp. (Spencer 1978, 1979) and several other
hydromedusae (Satterlie and Spencer 1983; Satterlie 1985b),
neurons of the “identified” inner nerve ring network form
chemical synapses with overlying epithelial cells. The epithelial cells are electrically coupled to one another and to the
adjacent circular myoepithelium of the subumbrella and velum via gap junctions (Fig. 4). For convenience I will refer
to this network as the swim motor network (SMN). Because
of the widespread electrical coupling in the muscle sheet of
each quadrant, SMN neurons act as motoneurons for the
swim system (Anderson and Mackie 1977; Anderson 1979;
Spencer 1981). Thus, spread of activity in the swim system,
in a circular direction, is achieved by the electrical coupling
within the SMN of the inner nerve ring. In P. penicillatus,
electrically coupled swim motoneurons also extend up either
side of each of the four radial canals and connect at the apex
of each quadrant (Lin et al. 2001). Excitation in a radial direction throughout the muscle sheets of the four quadrants is
spread via electrical coupling between epithelial and
myoepithelial cells (Fig. 4), aided by synaptic input from the
swim motoneurons of the radii. Muscle cells produce longduration, overshooting action potentials, aiding this spread
of activity through the subumbrella (Spencer 1978; Satterlie
and Spencer 1983; Satterlie 1985b) This basic overall organization of the swim system, with or without the radial elements of the SMN, is found in a variety of hydromedusae
(Satterlie and Spencer 1983).
An interesting feature of the anthomedusa Polyorchis sp.
is the change in both the breadth of the SMN action potential and its relationship to synaptic delay as the action potential is conducted around the margin of the bell (Spencer
1981, 1982). The action potential is broad, with a distinct
shoulder near the site of initiation, but as it is conducted
around the margin, the spike narrows. Near the initiation
site, the synaptic delay between SMN neurons and the
overlying epithelial cells is longest, and it decreases as the
action potential is conducted around the bell (Spencer 1982).
The combination of conduction delay but lesser synaptic delay
in regions farthest from the spike-initiation site results in a
nearly synchronous contraction of the subumbrellar swim
musculature in all parts of the bell. It is interesting that
Romanes (1885) commented on the similar near-synchronous
contraction of the swimming bell in another anthomedusa,
Sarsia sp. Perhaps similar neuromuscular mechanisms are
common in all bell-shaped anthomedusae. The leptomedusae,
which typically have more disk-shaped swimming bells, do
not display the same degree of synchrony, presumably because of the longer conducting distances between the two
opposite sides of the bell.
Romanes observed that only a small piece of marginal tissue is necessary to produce a coordinated contraction, and
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Fig. 3. (A) Schematic diagram of a generalized hydromedusa, showing the organization of the bell margin. INR, inner nerve ring;
NME, nonmuscular epithelium; M, mesoglea; ONR, outer nerve ring; RC, ring canal; SCM, subumbrellar circular musculature; Tri,
tripart branch of the mesoglea near the nerve rings; VCM, circular musculature of the velum. (B) The same type of marginal section,
showing the organization of the swim motor nerve net of Polyorchis sp. The vertical extensions of the nerve network run on either side
of a radial canal. (C) Photograph of the inner nerve ring region of a live Polyorchis sp., viewed with oblique substage illumination.
The banana-shaped cells are neurons of the swim motor nerve net. (D) The same neurons as in C following injection of a single neuron with Lucifer Yellow. The largest neurons in this network are 30 µm in diameter.
this is due to the widespread electrical coupling which is a
hallmark of the subumbrellar circular muscular sheets of
hydromedusae. Although some hydromedusae have diffuse
nerve nets associated with the subumbrellar muscle, these
species typically have a layer of radial muscle in addition to
the circular swim muscle in the subumbrella. Mackie et al.
(1985) suggest that the subumbrellar nerve nets are associated with the radial, not the circular, musculature.
Like scyphomedusae, hydromedusae have multiple, parallel
conducting systems, most of which are compressed networks
within the marginal nerve rings, just like the SMN (Passano
1973; Ohtsu and Yoshida 1973; Spencer 1975; Mackie 1975).
Passano (1973) estimates that there may be as many as six
parallel networks in the marginal nerve rings of some medusae
(however, see the section on Aglantha sp. below). Two of
these conducting systems, the B (for “bursting”) system and
the O (for “oscillation”) system (Spencer and Arkett 1984;
Arkett and Spencer 1986a, 1986b), in the outer nerve ring of
Polyorchis sp. have been electrophysiologically studied in
some detail. The B system consists of an electrically coupled
network of outer nerve ring neurons which receive information
from the system of marginal ocelli and convey that informa-
tion to the SMN of the inner nerve ring (Spencer and Arkett
1984). A shadow falling on the medusa results in a burst of
spikes in the B system and a synaptic depolarization of the
SMN. Facilitating excitatory postsynaptic potentials (EPSPs)
have been recorded in SMN neurons following B-system
spikes (Spencer and Arkett 1984).
The B system also has a direct motor output, as its firing
frequency directly determines the contractility of the marginal tentacles. B-system firing is correlated with the length
of the tentacles, so that during high-frequency activity, the
tentacles are fully contracted. Since a swimming bout is preceded by contraction of the tentacles, presumably to decrease
drag, the B system plays a dual role in preparation for
swimming: shortening the tentacles and stimulating the SMN
(Spencer and Arkett 1984). Marginal conducting systems
that appear to be homologous to the B system have been recorded in a number of hydromedusae by means of extracellular electrodes (Passano et al. 1967; Ohtsu and Yoshida
1973; Spencer 1975; Mackie 1975).
Another outer nerve ring network has been identified and
characterized in Polyorchis sp. (Spencer and Arkett 1984).
Like the B system, the O system is made up of a compressed
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Fig. 4. Subumbrellar swim musculature of the hydromedusa
Polyorchis sp. (A) Low-power micrograph showing that the striated muscle is formed from the basal processes of
epitheliomuscular cells. (B) Where the basal processes of two
such cells come in contact, two types of intercellular junctions
are common: desmosome-like contacts and gap junctions. A gap
junction between two desmosome-like contacts is shown.
network of electrically coupled neurons. Elements of the O
system are found in the ocelli, suggesting that either primary
photoreceptors or their following neurons are included in the
network. The O system does not produce spikes; rather it
produces regular membrane-potential oscillations that can be
up to 20 mV in amplitude. In response to a shadow, the system hyperpolarizes and stops oscillating with a latency of
around 150 ms. An increase in light produces a depolarization of the network and increases the amplitude and frequency of network oscillations (Spencer and Arkett 1984).
As in scyphomedusae, a subset of hydromedusan neurons
contain and produce RFamide and related peptides (Grimmelikhuijzen 1983; Grimmelikhuijzen and Spencer 1984; Grimmelikhuijzen et al. 1988, 1989, 1992, 1996). Networks of RFamideor FMRFamide-immunoreactive neurons have been visualized
in various hydromedusae, including compressed networks in
the nerve rings of nearly all species examined. In addition,
uncompressed nerve nets are found associated with the radial canals of most hydromedusae (Fig. 5A), and are also
found in the subumbrellar muscle sheets in some, most notably the leptomedusae (Fig. 5B). RFamides may be involved
in swimming only indirectly, however, since double-labeling
experiments in Polyorchis sp. confirm that the SMN and the
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B and O systems are not RFamide-immunoreactive (Satterlie
and Spencer 1987). Furthermore, in those hydromedusae that
contain subumbrellar networks of RFamide-immunoreactive
neurons, the stained neurons appear to be associated with the
radial subumbrellar musculature that is used for feeding and
protective responses rather than the circular musculature used
in swimming (Mackie et al. 1985).
A common feature of hydrozoans is epithelial conduction,
most often found in the exumbrella of hydromedusae (Mackie
and Passano 1968; Mackie 1970, 1976; Josephson and Schwab
1979; Anderson 1980). Epithelial conduction systems represent independent signaling pathways, since their activation
can trigger, or alter, a number of behavioral systems, including swimming (reviewed in Anderson 1980).
A special case: escape swimming in the hydromedusa
Aglantha digitale
The trachymedusa Aglantha digitale produces two types of
swimming: slow spontaneous swimming, which is believed
to be similar to that in other hydromedusae, and a ballistic
escape swimming response evoked by stimulation, which
involves superimposed, parallel conducting systems within
the nerve rings (Roberts and Mackie 1980; Mills et al. 1985).
The same subumbrellar circular musculature and the same
motor innervation are used for both; however, there are differences in how the musculature is activated in the two forms
of swimming: escape swimming involves specializations for
rapid propagation and faster activation of the musculature
(Roberts and Mackie 1980; Mills et al. 1985; Mackie 1989).
For normal swimming, an inner nerve ring network of
neurons acts as the swim pacemaker network (“pacemaker
network”), and directly synapses onto eight radially oriented
motor giant neurons (Fig. 6). The motor giant neurons, in
turn, directly activate the swim musculature and also activate
lateral motor neurons, which then activate the musculature
(Donaldson et al. 1980; Kerfoot et al. 1985). Thus, for slow
swimming, circular conduction of excitation involves the
pacemaker network as well as the lateral motoneurons.
Radial conduction is via the motor giant neurons. Although
the circular muscle cells are electrically coupled, they do not
appear to conduct action potentials for any distance without
nervous intervention, and depending on the nervous input,
they can contract strongly or weakly (Kerfoot et al. 1985).
Control of swimming is not that simple. First, the motor
giant neurons are also active during escape swimming, but in
this case they produce a contraction which is much stronger
than that seen during normal swimming. Mackie and Meech
(1985) found that the motor giant neurons are able to produce two different types of spikes: a low-amplitude calcium
spike and an overshooting sodium spike. The former produces the weak contractions characteristic of normal swimming and the latter the strong contractions that produce the
ballistic escape response. The ionic bases of these two types
of spikes have been uncovered (Meech and Mackie 1993a,
1993b), and the differences in the inputs that are responsible
for their generation have been described (Meech and Mackie
1995). Basically, the type of spike that will be triggered
is determined by the size and rate of depolarization inputs,
and these are at least partly determined by the activation/
inactivation properties of potassium currents in these neurons (Meech and Mackie 1993a, 1993b, 1995).
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Fig. 5. FMRFamide staining in hydromedusae. (A) In Proboscidactyla sp., a network of immunoreactive neurons runs from the marginal nerve rings along each of the branches of the radial canals. (B) In those hydromedusae that have subumbrellar radial muscle, a
immunoreactive network is found throughout the subumbrella. The network shown, from Aequorea sp., runs predominantly in a radial
direction (top to bottom). In A and B the neuronal cell bodies are 5 µm in diameter; in A the tentacle bulbs are 150 µm in diameter.
Fig. 6. Schematic diagram of the marginal conducting systems related to swimming (normal and escape) in Aglantha sp. C, carrier
system; EP, epithelial conducting system; MG, motor giants; NO, nitric oxide system (not discussed here); R, relay system; RG, ring
giant; RI, rootlet interneuron; TG, tentacle giant pathway; TS, tentacle slow system. (From Mackie and Meech 2000, reproduced with
the permission of J. Exp. Biol., Vol. 203, © 2000 The Company of Biologists.)
The slow-swimming system also involves activation of
other nerve ring conduction systems (Fig. 6). The pacemaker
system directly activates a “relay system”, which then activates a slow conducting pathway in the tentacles that produces a slow contraction of the tentacles to accompany
normal swimming (Mackie and Meech 1995a). The pacemaker system also provides excitatory inputs to another parallel system in the margin, the “carrier system”, which is
closely associated with the ring giant, a greatly oversized
neuron of the outer nerve ring that plays a central role in
rapid conduction around the margin and in excitation of the
motor giant neurons during an escape swim (Mackie and
Meech 1995b). Since the carrier system is closely associated
with the ring giant, the two conduct impulses together, but
it is the carrier system that links ring-giant activity to the
giant-fiber systems of the tentacles to trigger an extremely
rapid tentacular contraction during the escape response
(Mackie and Meech 1995b). The ring giant receives a threepart excitatory EPSP during normal swimming from (i) direct inputs from the pacemaker system, (ii) direct inputs
from the relay system (which is activated by the pacemaker
system), and (iii) direct inputs from the carrier system (also
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activated by the pacemaker system and the relay system). Input from these sources can cause spiking in the ring giant,
which may allow the animal to occasionally contract the
tentacles rapidly even during slow swimming. Thus,
components of the escape circuitry can be used in non-escape
swimming.
During an escape swim, the characteristic fast contraction
of the tentacles is coordinated with the strong contraction of
the subumbrellar circular muscle in the following ways. Initiation of an escape swim is normally triggered by mechanical input from highly sensitive hair cells that are arranged in
tactile combs, and these activate spikes in the ring giant
(Arkett et al. 1988). As mentioned above, activity in the ring
giant produces similar activity in the carrier system, which
in turn activates the fast-contraction system of the tentacles
(Mackie and Meech 1995b). The ring giants also provide
disynaptic activation of the motor giant neurons that is fast
and large enough to exceed the threshold for fast sodium
spikes (Meech and Mackie 1995). Following stimulation of
the subumbrella that leads directly to production of sodium
spikes in the motor giant neurons, fast excitation is again
distributed circularly, between the motor giant neurons, this
time by a system of rootlet neurons (in the inner nerve ring)
that are dye-coupled and presumably electrically coupled to
motor giant neurons (Mackie and Meech 2000). Between
each pair of motor giant neurons, the rootlet neurons interact
via chemical synapses. The rootlets thus provide a circular
pathway for activation of the motor giant neurons all around
the bell without direct involvement of the ring giant, allowing coordinated escape swimming to be evoked by stimulation on the subumbrellar side (Fig. 6). However, the ring
giant can be fired indirectly during this process because excitation of motor giant neurons causes spiking in the pacemaker system, and this leads to excitation of the relay and
carrier systems as described above. When, as a result, the
ring giant fires, the tentacles will perform fast-twitch contractions, as in the case of the escape response evoked by
exumbrellar stimulation. Whether fired by input from the ring
giant (in the case of exumbrellar stimulation) or via the rootlets (in the case of subumbrellar stimulation), the motor giant
neurons respond with a rapidly conducted sodium spike, which
activates a strong contraction in the subumbrellar circular
muscle.
One additional input to the swim system deserves mention. Like that of other hydromedusae, the exumbrellar epithelium of A. digitale is electrically excitable. Mechanical
stimulation of the exumbrella produces conducted spikes that
have been shown to inhibit the pacemaker system (Mackie
and Singla 1997).
Mackie and Meech (2000) indicate that the total number
of distinct conduction systems in A. digitale is now up to 14,
only a few of which have been described here (Fig. 6).
While this inventory may be larger than that found in
hydromedusae which lack an escape response, the number
and diversity of separate conduction systems give us a window on the types of neuronal complexity that underlie the
behavioral richness of the hydromedusae. Any reticence in
acknowledging the complexity of the central nervous system
of these animals, and of their integrative abilities, should be
abandoned. An appreciation of cnidarian neurobiology does
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require a cultural shift, however, owing to the lack of
cephalization imposed by radial symmetry. This should not
detract from the utility of these preparations in contributing
to our knowledge of nervous-system function.
Neural control of swimming in
cubomedusae
Cubomedusae are extremely efficient, agile swimmers.
Most can change direction in just a few swim contractions,
and have been shown to do so in response to a variety of
photic or visual stimuli. Their swimming bell is about as tall
as it is wide, which contributes to their swimming efficiency
and places them in a league with many of the bell-shaped
hydromedusae. In terms of swimming efficiency, it also
places them ahead of the scyphomedusae and those hydromedusae that have disk-shaped bodies. In the hydromedusae,
both bell- and disk-shaped, swimming efficiency is increased
through use of a velum. The cubomedusae have a shelf of
tissue, called the velarium, that is similar to the velum of
hydromedusae and has a similar function. Considering that
the cubomedusae were traditionally placed within the class
Scyphozoa, do the bell shape and the presence of the velarium
represent a wonderful case of convergence, or are there clear
affinities with the hydromedusae? While this question will
not be addressed in detail, a basic description of the swimcontrol system of cubomedusae should provide some insights that are of comparative value in our speculation, particularly in light of the distinct dichotomy in the methods of
swim control in the hydromedusae and scyphomedusae.
Location of pacemakers
The cubomedusae possess four rhopalia, which are found
in indented exumbrellar niches partially covered by an overlying flap of tissue. This was probably an anatomical clue
that contributed to the placement of the cubomedusae with
the covered-eyed medusae. The rhopalia of cubomedusae
contain a statolith, sensory epithelia, two complex lensed
eyes, and up to four pigment-cup ocelli (Fig. 7A). Thus, the
cubomedusan rhopalia are similar to, but much more complex than, the rhopalia of scyphomedusae. Removal of the
four rhopalia leaves cubomedusae unable to produce spontaneous swim contractions. Furthermore, when the entire margin is removed except for a single rhopalium, swimming
activity continues until the final rhopalium is removed. Cutting experiments on individual rhopalia indicate that the
pacemaker region is in the upper region, near the emergence
of the rhopalial stalk (Satterlie 1979)
Coordination of pacemakers
With four spatially separated pacemaking centers (rhopalia),
the challenge for swim coordination is very similar to the
one faced by scyphomedusae. As expected, pacemaker coordination in cubomedusae is based on the same mechanism as
in scyphomedusae: the rhopalium that shows the fastest
pacemaking rhythm drives swimming, at least for part of the
time. Two aspects of pacemaker coordination are unique to
the cubomedusae (in comparison with scyphomedusae). First,
a nerve ring is found connecting the rhopalia to one another
and to the four tentacle bases (Fig. 8A). Since the rhopalia
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are placed a short distance up from the margin, the nerve
ring loops up to connect with a rhopalium, then down to the
adjacent tentacle base, then up to the next rhopalium, and so
on around the bell. Although its function has not been studied
in detail, the nerve ring appears to provide a rapid conduction route between rhopalia to aid in pacemaker coordination. The nerve ring conducts rhopalial impulses directly to
the other rhopalia at the same time as the impulses are conducted throughout a subumbrellar motor nerve net that is
very similar to the MNN of scyphomedusae.
Second, pacemaker interactions have been studied using
sequential rhopalial removal and modeling of pacemaker interactions based on real data from single-rhopalium animals
(Satterlie and Nolen 2001). Model networks were constructed to simulate pacemaker interactions that were of the
resetting type (resetting network), similar to those suspected
to exist in scyphomedusae, and to simulate pacemakers that
were totally independent of one another (independent network). Frequency histograms produced by one-, two-, three-,
and four-rhopalium animals were compared with similar histograms produced by the two models. Interestingly, the real
data were midway between those from the resetting and independent models, suggesting that pacemaker interactions in
cubomedusae are semi-independent rather than of the strictly
resetting type. The combination of semi-independence of
pacemakers and the small number of pacemakers in cubomedusae allows two-way modulation, and thus is essential to
the production of asymmetrical contractions in these efficient swimmers (Satterlie and Nolen 2001). A reexamination
of pacemaker interactions in scyphomedusae is now warranted, coupled with similar modeling, to see if they exhibit
similar semi-independent coupling.
Organization of the conduction system that initiates
swim contractions
The circular musculature of the subumbrella and velarium
of Carybdea sp. and Tripedalia sp. is innervated by a diffuse
network of large neurons which is structurally similar to that
found in scyphomedusae (Fig. 8). The motor nerve nets of
Carybdea sp. and Tripedalia sp. stain with antibodies to αor β-tubulin, and interestingly, the density of the networks
is greater in the velarium than in the subumbrella (Fig. 8B).
This may speak to a significant role of the velarial circular
musculature in steering, since Gladfelter (1973) showed that
an enhanced contraction in one area of the velarium produced a directional funnel for water ejection which caused a
turn of the swimming bell.
Neurons of the motor nerve net have been recorded with
intracellular electrodes (Satterlie 1979; Satterlie and Spencer
1979), and they show conventional action potentials that
look very much like the ones obtained from the MNN neurons of scyphomedusae (Anderson and Schwab 1983; Anderson 1989). Action-potential doublets were occasionally
recorded that were limited to the quadrant of initiation,
which produced extra-large subumbrellar contractions, suggesting that asymmetrical muscle activity also occurs within
the subumbrellar swim musculature (Satterlie and Spencer
1979; Satterlie and Nolen 2001).
Neuromuscular transmission appears to be synaptic, and it
exhibits frequency-dependent facilitation (Satterlie and Spencer
Can. J. Zool. Vol. 80, 2002
1979). Intracellular recordings have been made from a few
muscle cells, and they produce graded, summing junctional
potentials with each swim (Satterlie and Spencer 1979).
There is no evidence for electrical conduction within the
muscle sheet, and gap junctions have not been found in any
cubomedusan tissue to date.
Evidence for multiple nerve nets has been found in Carybdea sp. and Tripedalia sp., as FMRFamide-immunoreactive
fibers have been found in the rhopalia and nerve ring, and in
a loose network that runs in the subumbrella and velarium
(M.M. Coates and R.A. Satterlie, in preparation). In the rhopalia,
FMRFamide-immunoreactive neurons form a horseshoe-shaped
compressed network surrounding the emergence of the rhopalial
stalk (Fig. 7B). The swim pacemaker cells are also found in
this region (Satterlie 1979). Double-labeling experiments
indicate that the FMRFamide- and tubulin-immunoreactive
nerve nets are distinct in size, density, and location. In addition,
there is physiological evidence that impulses of rhopalial origin, triggered by light-off stimulation of a single rhopalium,
which inhibits pacemaker output from that rhopalium, can
be conducted in the nerve ring to other rhopalia, where they
can inhibit these distant pacemakers as well (R.A. Satterlie,
unpublished observations). Severing the nerve ring prevents
conduction of these impulses. Also, tentacle withdrawal can
be restricted to a single tentacle, or with stronger stimuli can
involve all four tentacles. Again, severing the nerve ring prevents the nonstimulated tentacles from responding (R.A.
Satterlie, unpublished observations). Thus, it appears that the
cubomedusan nerve ring contains multiple conducting systems which presumably represent compressed nerve networks, similar to the situation found in hydromedusae.
Currently, there is no evidence for conducting epithelia in
cubomedusae. Furthermore, a survey of intercellular junctions in epithelia, subumbrellar muscle, and nervous tissue
has not uncovered the presence of gap junctions, although
the survey is hardly exhaustive (R.A. Satterlie, unpublished
observations).
Cubomedusan affinities
On balance, the organization of the swim-control system
of cubomedusae lines up most closely with that of the
scyphomedusae. The restriction of swim pacemakers to discrete sensory organs (rhopalia) and the distribution of excitation throughout the subumbrellar muscle sheet by a diffuse
synaptic nerve net are both decidedly scyphozoan. Also,
neuromuscular facilitation as a means of producing contractile variability is important in both scyphomedusae and
cubomedusae. Finally, negative evidence is provided by the
fact that hydromedusae make extensive use of gap junctions
within the conducting systems of the swim-control system,
within the myoepithlium of the subumbrella, and in the
excitable epithelium of the exumbrella. Evidence for such
electrical transmission, and its morphological correlate, gap
junctions, is lacking in both scyphomedusae and cubomedusae
(Mackie et al. 1984).
Cubomedusan structures that have apparent hydrozoan
counterparts include the velarium (which is similar to the
hydrozoan velum) and the nerve ring. The velarium of
cubomedusae contains circular musculature that contracts
with the subumbrellar muscle, as in hydromedusae, but some
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Fig. 7. Structure of the rhopalia in the cubomedusa Carybdea sp. (A) Transverse section of the lower compound eye showing (from
top to bottom) the cellular lens and photoreceptor, pigment, and neural layers. The separation between the lens and photoreceptor processes is an artifact of fixation. (B) Sagittal section of a rhopalium showing the upper and lower complex eyes (with lenses) and two
of the four pigment-cup ocelli (with pigmented receptors). (C) One of the pigment-cup ocelli has lens-like cells between the pigment
cells. (D) FMRFamide immmunoreactivity of a rhopalium; a horseshoe-shaped network of stained neurons surrounds the emerging
rhopalial stalk. The stained neurons are found in the same area as the swim pacemaker cells (believed to be larger, nonstained cells in
the same area). Some nonspecific autofluorescence is seen in the lens cells of the pigment-cup ocelli. The rhopalium is 750 µm in diameter, and this is also the diameter of the lower complex eye.
Fig. 8. Subumbrellar motor nerve net of cubomedusae stained with an antibody to α-tubulin. (A) The nerve ring is brightly stained in
Tripedalia sp. and gives rise to the subumbrellar (left) and velarial (right) nerve nets. Note that the velarial network is much denser
than the one running into the subumbrella. (B) Subumbrellar nerve net of Carybdea sp., showing the random orientation of the stained
neurons. The nerve ring in A is 40 µm in width; A and B are at the same magnification.
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of the hydromedusae also have radial muscle which is used
to asymmetrically adjust the shape of the velum so that a directed jet of water can produce turning during bell contractions. In the cubomedusae, radial muscle is lacking, so
asymmetrical velarial contractions are accomplished through
enhanced contractions of the circular muscle.
The nerve ring of cubomedusae serves many of the same
functions as the nerve ring of hydromedusae, notably fast
conduction between tentacles and sensory structures and a
condensation of multiple conducting systems into the radially
symmetrical animals’ version of centralization. The nerve
ring of cubomedusae is not placed on the margin as it is in
hydromedusae, and does not include both inner and outer
nerve ring components. Since the two similarities between
cubomedusae and hydromedusae are only superficial, the
balance of evidence is that the cubomedusan swim-control
system is built on the scyphomedusan plan, and that the two
hydrozoan-like specializations may well be examples of convergence of traits that are essential to highly efficient, directed locomotion.
Common and unique features of jellyfish
swim-control systems
With an eye toward the lofty question of the evolution of
behavioral control systems within the Cnidaria, we can list
common features of jellyfish swim-control systems on the
assumption that common features may reflect a common origin. While this is an extremely risky enterprise, it is a starting point for discussion and thus serves a useful purpose,
even if the assumptions are later shown to be ridiculously
wrong. As we have seen in cubomedusae, apparently common
features may be superficial, and in some cases explained
through convergence, where a common physiological or ecological need has imposed similar constraints on functional
morphology, producing similar end-points from very different starting points. Similarly, we are assuming that features
found in only one group are not ancestral merely because
they are absent in other groups. This would ignore the possibility of a secondary loss of features in a subset of the
groups. All of this being said, the following is intended to be
not only speculative, but also provocative. It is a call to the
molecular systematists, the evolutionary biologists, the molecular physiologists, and most of all the comparative biologists to mine the nuggets that lie just beneath the surface of
this question. If the following serves as such a stimulus, then
whatever is put down here may be incorrect, but it is not
wrong.
So what common features can be found in all three jellyfish groups, scyphomedusae, hydromedusae, and cubomedusae?
First on my list is the use of circular, striated muscle for
rapid constriction of the swimming bell during a contraction.
In some cases the cells are musculoepithelial cells, in others
they do not have a surface epithelial component. However,
there is no doubt that the orderly arrangement of myofibrils
into sarcomeres is a cnidarian mainstay. Second is the use of
organized systems of neurons for conducting electrical activity, either to other systems of neurons or to effectors. In
some cnidarians the neurons are arranged in diffuse nerve
nets, in others compressed networks take the form of distinct
connectives within nerve rings. Even then, however, the nerve-
Can. J. Zool. Vol. 80, 2002
ring networks that have been identified morphologically via
dye injections still resemble networks of relatively small
neurons. Whether neurons are part of a diffuse or a compressed network, they appear to maintain their identity as
part of a distinct conducting system. In this phylum, in which
many tissues contain multifunctional cell types (e.g., epitheliomuscular cells), this multifunctionality does not seem to extend to the neurons that make up these conduction systems.
Exceptions exist, such as in the rootlet, motor giant neuron,
and ring-giant systems of A. digitale, but these represent
highly specialized adaptations in a startle system that is superimposed on an existing swim-control system very much
like that in other hydromedusae.
Third, the use of multiple, parallel conducting systems
seems to be a common theme in the three jellyfish groups.
Even in the scyphomedusae, the two identified nerve nets,
the MNN and the DNN, run throughout most of the
subumbrella and overlap in most areas. It is possible that additional unidentified networks are present in scyphomedusan
swim-control systems. The presence of nerve rings, regardless of their origin, seems to have allowed the development
of greater numbers of parallel conducting systems, and one
is tempted to relate the presence of nerve rings in medusae
to more elaborate (or better coordinated) behavioral repertoires. The collection of multiple conducting systems into a
nerve ring, or rings, along with the accumulation of neurons
and sensory cells in ganglia (rhopalia), could be considered
the equivalent of centralization in radially symmetrical animals. In this regard, then, both the hydromedusae and the
cubomedusae would be considered “more advanced” than
the scyphomedusae, supporting Romanes’ view, quoted earlier (Romanes 1885).
Fourth, the use of chemical synapses is common to all
cnidarian groups. In some cases the synapses are symmetrical; however, this occurs in forms either with or without
nerve rings, so the “centralization” represented by the condensation of conducting systems into nerve rings apparently
does not eliminate the usefulness of two-way, symmetrical
synapses. This suggests that symmetrical synapses are common to, and even necessary for, proper coordination within
the radially symmetrical cnidarian body plan.
Fifth, in the context of chemical communication, peptide
transmitters, particularly with respect to a family of RFamides
and the similar RWamides, seem to be ubiquitous within the
phylum. Outside of these peptides, convincing identification
of transmitters in jellyfish conducting systems has been sparse,
and represents an area of need for speculating about group
affinities.
Since Anctil and colleagues have found that the endocrine
systems of anthozoans are complex (Mechawar and Anctil
1997; Anctil 2000; Gillis and Anctil 2001), this represents
another area of needed research on the scyphozoans and hydrozoans. At the very least, the combination of endocrine
messengers and chemical synapses suggests that chemical
signaling is a common theme in the phylum.
Returning to our discussion of Romanes’ dichotomy, we
immediately see one glaring difference between hydromedusae and scyphomedusae/cubomedusae: the use of gap
junctions to conduct meaningful electrical information
within conducting epithelia, muscle sheets, or neural networks. This is a profound advance, since it decreases the
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Satterlie
need for diffuse neuronal conduction through the muscle
sheet, thus allowing more neural “centralization”, and decreases the need for symmetrical chemical synapses for twoway conduction, since gap junctions are frequently bidirectional
(although they may rectify).
The use of gap junctions for epithelial conduction has
been thoroughly investigated in cnidarians (Horridge 1968;
Mackie and Passano 1968; Mackie 1970, 1976; Spencer 1974;
Josephson and Schwab 1979; Anderson 1980), and has even
been proposed to represent a primitive condition (Horridge
1968; Mackie 1970). However, one could argue that it is unlikely that such an important advance would be totally lost,
secondarily, in three of the four cnidarian classes; convincing examples of gap junctions have not yet been found in anthozoans, cubozoans, or scyphozoans (Mackie et al. 1984).
Despite this, there is recent evidence that connexin-like proteins
are present in the anthozoan Renilla koellikeri (Germain and
Anctil 1996). This finding elevates the significance of the
question about gap-junction distribution in the Cnidaria. While
it is possible that gap-junctional communication has escaped
our description in three of the four classes, it is also possible
that gap-junction proteins are present in all forms, but either
the full complement of subunits or the mechanisms for their
assembly into functional gap junctions are lacking in these
groups. Since connexin proteins (frequently called innexins
in invertebrates; Phelan and Starich 2001) have four transmembrane domains, it is possible that individual connexin-like
proteins serve (or served) a function other than as low-resistance
intercellular passageways in some cnidarians. In this regard,
connexins could be common to all cnidarians, but complete
gap junctions, capable of allowing current spread between
cells, are not. This is a prime example of the potential use of
modern molecular techniques to answer important questions
regarding the evolution of conducting systems in the
Cnidaria. Other examples come to mind, but they will be left
to the reader’s imagination: simply envision what Romanes
would do if he had had the tools of the twenty-first century
at his fingertips.
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