AMER. ZOOLOGIST, 5:491-497 (1965).
NOTES ON THE BEHAVIOR OF THE HYDROID,
CORYMORPHA PALM A
ROBERT WYMAN
Dept. of Zoology, University of California, Berkeley
SYNOPSIS. Corymorpha, like Porpita, exhibits a synchronous oral flexion, or "concert," of its proximal tentacles. As this is unlike the contractile writhings of siphonophoran zooids, the concert may be a significant character in linking the behavior of
Porpita more closely to hydroids than to siphonophores. Except for this response the
behavior of Corymorpha and Porpita are different. In Porpita a through-conducting
system forms the only link between tentacles, whereas in Corymorpha both local and
through-conducting systems connect tentacles. Corymorpha engages in rhythmic
bottom-feeding using distal tentacles which have no homologue in Porpita. The
mechanical properties of the musculo-skeletal system are different in the two, giving
tentacle motions in Corymorpha a continuous appearance, and in Porpita a spasmodic
appearance.
Reduced glutathione, glycine, DL-serine, L-cysteine and L-glutamic acid can elicit
a feeding response in Corymorpha. Sodium thioglycollate and sucrose elicit no response. Glycine is the most effective stimulant, ca. 5 X 10"7 M solution being effective.
L-glutamic acid gives the weakest response. The presence of chemicals alone can be
sufficient to elicit the feeding reaction in starved animals. In moderately well-fed
animals, touch may be required. In fully fed animals both touch and chemicals may
be insufficient.
Parker reports that when Corymorpha is shocked electrically on its stalk it will bend
the stalk so as to apply the hydranth accurately to the stimulated spot. The response
I found was a curling of the stalk toward the side stimulated, but not to a specific
spot on the stalk. Chemical or tactile stimuli may be necessary for final location of
the stimulated site. Parker reported that the response remained accurate even after
several cuts had been made in the stalk. I could find no evidence for this.
ON BEHAVIORAL HOMOLOGIES WITH
Porpita
The behavior of Corymorpha was described early in this century by Torrey
(1904, 1905) and Parker (1917, 1919). Since
then the genus has been neglected by those
interested in behavioral mechanisms. The
morphological affinities of the Chondrophora to Corymorpha (Garstang, 1946) has
furnished strong evidence for the recently
accepted separation of the orders Chondrophora and Siphonophora (Totton, 1954).
Mackie (1959) has put forward behavioral
homologies in support of the new classification. Although Mackie was able to examine several dozen Porpita (Chondrophora),
he did not have access to Corymorpha and
had to rely on Parker's account, which is
not explicit on many of the points which
would link the behavior of Porpita with
that of Corymorpha. Consequently I have
re-examined those aspects of Corymorpha's
behavior which might ally it to chondrophorans such as Porpita.
Corymorpha palma is also noteworthy
for its si/e: the largest specimen utilized
in the work reported here had a stalk length
of 10 cm, stalk diameter of 0.5 cm, and a
tentacle sj>read of 2.5 cm. Figures 2, 4 and
5 therefore show the polyp slightly greater
than life-size.
Feeding reactions. Parker describes two
distinct modes of feeding behavior in Corymorpha. In flowing water the proximal
tentacles are spread out against the current
and individual tentacles contract around
particles of food which touch them. In
quiet water the polyp "bows" down to the
substrate and distal tentacles gather in
detritus. Occasionally, when the animals
are sitting quietly in a tank, and especially
after some brine shrimp nauplii have been
introduced, one can see feeding reactions
begin. Several of the large tentacles will
curl in upon the distal tentacles in one or
two smooth contractions. The activity will
then either die out or more tentacles will
start closing in. It is common to see tentacles in all stages of contraction and relaxation on the same animal at the same
time. Occasionally the activity will cul-
(491)
492
ROBERT WYMAN
minate in one contraction of all the tentacles together, each starting from whatever
position it happened to hold. This flexion
of all the proximal tentacles at once has
been called a "concert." T h e flexion of the
proximal tentacles at the beginning of the
"bowing" type of feeding behavior is ol
this latter type; a few tentacles begin, but
within a second most or all have contracted
to different degrees. While the contraction
of the proximal tentacles precedes the
bowing-feeding reaction, once the bowing
has begun these tentacles play no role in
the food gathering. As Parker says (1917,
p. 326), " T h e proximal tentacles seem to
play a very minor part in this type of food
gathering."
Porpita's tentacles are presumably homologous to the proximal tentacles of
Corymorpha. Porpita has no structure homologous to distal tentacles, and no bottom
feeding behavior. (Porpita floats on the
water surface.) Porpita has only one mode
of tentacular motion which might be used
in feeding; namely, adoral flexion of the
tentacles either spontaneously or in response to stimulation. Mackie (1959) describes rhythmic tentacular movements in
Porpita. This behavior occurs spontaneously at approximately i/£ min intervals, a
whole bout lasting perhaps 5 min. Activity
within each half minute period lasts about
10 sec, followed by about 20 sec of rest.
In quiet water, Corymorpha initiates a
feeding cycle by contraction of the proximal
tentacles, then bows down and feeds for
approximately 1 min, straightens up, rests
about 2 min, and repeats the cycle.
Evidence for through-conducting
and
local nerve nets. "In Porpita if two or
more tentacles are stimulated and respond,
their flexions are synchronized whether they
are near together or not. . . . Xo exceptions
to this rule of synchrony were observed."
(Mackie, 1959). In Corymorpha it is common, as mentioned above, to see tentacles
in all states of contraction and relaxation,
with contractions of each tentacle staitin^
independently. In Porpita "the synchronization ol tcnUuukn ucti\it\ indicate1* that
each motor nenous discharge is throughconducted lo all utiions. \ o evidence Im
decremental spread of impulses was found."
(Mackie, 1959). This description of Porpita
does not fit Corymorpha, in which local
responses predominate and through-conducted responses appear only occasionally.
With increasing intensity of stimulation to
a Corymorpha proximal tentacle, the responding area is at first limited to the tentacle itself, but then spreads to other proximal tentacles, the proboscis, distal tentacles
and finally the stalk.
Mechanism of tentacle contractions. A
similarity between Porpita and Corymorpha is that they both show synchronous
orally-directed flexions of their tentacles,
the "concert" movements. This response
does seem to ally Porpita more closely to
hydroids than to siphonophores (Mackie,
1959). The concerted flexion of all the
tentacles is unlike the uncoordinated writhings characteristic of siphonophoran zooids.
(But according to Mackie (1959) in another
chondrophoran, Vellela, the tentacles are
in continual movement, writhing and
changing in length.) However, the character of the flexions in Porpita and Corymorpha are quite different. The tentacles
of Porpita are filled with "enormous vacuolated cells closely packed together. These
cells . . . are known to be skeletal in character, providing a certain stiffness and resistance" (Mackie, 1959). Against this stiffness work longitudinal muscle fibers which
are capable of imparting to the tentacles
"spasmodic, sharp, flicking flexions." "The
tentacles do not shorten appreciably when
the muscles contract, but bend at their
bases." The muscles are apparently not
capable of slow or sustained contraction,
and all motion is done with jerks. The
tentacles may be held nearly still by jerking
very rapidly (200/min) with \er\ low amplitude. The tentacle is never held motionless away from its rest position, and
between jerks it starts springing back to the
rest position. About seven jerks are required to bring the tentacle to its innermost position.
The proximal tentacular motion in Coiymvrphn is not a -itiff flicking from the hail.
but a curling in upon the distal tentacles
in a coiling tashion through one ot tun
BEHAVIOR OF
distal tentacles
inactive
proximal tentacles
FIG. 1. A Corymorpha tentacle uncurling.
turns, during which the tentacle shortens
down to % of its rest length. One smooth
contraction suffices to obtain full incurling,
although just as frequently two or three
distinct contractions may be involved.
When an individual tentacle is drawn in,
the two or three contractions may take as
long as 6 sec. A tentacle may be held in
nearly the same contracted position for up
to 3 sec without renewed contraction. This
suggests that the musculo-skeletal system
has quite different properties from that of
Porpita, which needs 200 twitches per minute in order to maintain a maximally flexed
position.
A strong blow to a tentacle with a glass
rod will usually produce an immediate reaction. A soft blow may produce an immediate reaction, one delayed by a second or
so, or none at all. I have not been able
to determine under what conditions an
immediate or delayed response is obtained.
When a tentacle is uncurling after a contraction it requires a much greater amount
of mechanical stimulation to cause a new
contraction to occur.
When the tentacle is not in its rest position it is rarely held motionless. When a
proximal tentacle uncurls, usually the basal
part straightens first while the tip is held in
a tight but static coil for 2 or 3 sec (Fig. 1).
The uncurling is sometimes extremely slow.
Under light anesthetization (isotonic
MgSO4 approx. 1:6 with sea water) the
tentacles of Corymorpha become very stiff
and when displaced spring back very
quickly. The much slower speed of returning from an autogenic displacement when
Co)\morplm
•193
unanesthetized seems to indicate that tension is maintained in the muscle fibers for
quite a while during relaxation. However,
it is also possible that changes in turgor
due to the changed ionic composition during anesthetization is responsible for this
effect.
Although the visually observable behavior of single tentacles of Corymorpha
and Porpita are quite different, the neurophysiological events may be similar. Tubularia (from the same family as Corymorpha)
performs concerted tentacle elevations, as
in Corymorpha, that are usually a single
smooth movement, but sometimes appear
as one or more brief twitches. Josephson
(1962) has shown that the underlying electrical pattern is composed of a burst of 3-12
discrete pulses. In Corymorpha also the
concert movements are accompanied by
similar electrical pulses (Josephson, personal communication). It seems probable
that patterns of spontaneous electrical activity similar to those in Tubularia and
Corymorplia would also be recorded from
Porpita (Josephson, 1962). In that case
the sharp, flicking flexions of Porpita would
be responses to individual pulses. Thus
the difference in the appearance of tentacle
motion during a concert is probably not
due to different neurophysiological mechanism, but to different mechanical properties of the respective musculo-skeletal systems. In that case the neurophysiological
mechanism may have been less modified in
evolution than the visually observable
behavior.
ON THE GI.UTA1HIONE FEEDING REACTION
Loomis' contention (1955) that the leeding response in Hydra depends exclusively
on reduced glutathione has now been called
into question by Forrest (1962; but see
Lenhoff, 1965). Lenhoff and Schneiderman
(1959) have claimed that Physalia physalis
gastrozooids "exhibit a feeding response
when exposed to low concentrations of reduced glutathione (10—-"'-] 0—° M)" while
"cysteine failed to induce a feeding response
at concentrations at which GSH was active." These authors also mention without
494
RORF.RT WYMAN
reference "recent observations that Cam- •with Wagner's (1905) findings that the
pan ularia flexuosa . . . gives a feeding re- mechanical factor in stimulation declines
in importance with increasing need for
sponse to GSH."
Squirting sea water with a capillary pi- food in Hydra.
pette onto the distal tentacles of Corymorpha usually elicits no reaction. The
ON A STIMULUS LOCALIZING REACTION
animal remains quiescent even after several
Parker (1917, p. 316) reports a remarktaps on the small tentacles with the pipette.
3
able
reaction of Corymorpha. "If a faradic
10"" M reduced glutathione in sea water,
stimulus
is applied to one side of the stalk
when sprayed on the tentacles, also pro.
.
.
the
stalk
bends to that side and usually
duces no response. However, an accompresses
the
hydranth
with great accuracy
panying or immediately following touch
causes the bending-in of all the large ten- against the stimulated spot." In the stalk,
tacles either together or in small groups. the longitudinal transmission tracts preThis is the same behavior as seen when dominate over diffuse conduction paths
small food particles are carried by a current (Parker, 1919). Thus the stimulus could
onto the expanded proximal tentacles. excite these longitudinal paths which could
Glycine, DL-serine, and L-cysteine (all 10~3 then cause the musculature along the stimuM in sea water) give results very much the lated side to contract. This would result in
same as that from glutathione. L-Glutamic a bending in the proper radial direction,
acid (10~3 M in sea water) sometimes gave but does not explain the localization as to
a weaker response or none at all, and at level of the stimulated point, which Parker
other times normal reactions. I obtained no (1919) says is usually accurate. Further
reaction with sodium thioglycollate (10~3 complex information processing properties
M in sea water) or a much stronger sucrose are indicated by the following (Parker,
1917, p. 316-317):
solution.
"The stalk of a polyp was cut transversely
Glycine was the most effective stimulant.
Fifteen seconds after pipetting 0.5 cc of halfway through at a point midway its
10~3 M glycine in sea water on one Cory- length and the polyp was then allowed to
morplia in a 7-gallon tank, a closing re- come to rest in a vertical position. On
action was seen in another standing 3 cm stimulating locally below the wound and
away; and 10 sec thereafter in two other in- on the side away from it, the hydranth, as
dividuals another 3 cm away on opposite might have been expected, was applied
sides. Assuming homogeneous distribution accurately to the stimulated spot. On apthrough a sphere of 6 cm radius, this would plying the stimulus directly below the
imply that a concentration of 5 X 10~7 was wound the hydranth was turned to that
effective. This estimate is high if diffusion side but never descended far enough to
was the main component of the spread. cover the actual region of the stimulus.
The estimate is low if the chemical was The failure here seemed to be due to the
transported by currents. Loomis (1955) has deficiency in the musculature as a result
reported that Hydra responds to from 10~° of the operation rather than a defect in
transmission." " . . . a decapitated stalk
to 10~" M glutathione.
responds
to local stimulation . . . as a norNewly collected and presumably well-fed
mal
one
does." " . . . a decapitated stalk
animals did not respond to spraying of
glutathione on the large tentacles even which has been partly cut through transwhen accompanied by touch. Groups un- versely at several different levels and from
fed for several days responded immediately several different sides, as Torrey (1904, p.
to the combination of glutathione and 407) has already described, will ne\erthetouch. In starved individuals glutathione less localize, though incompletely, a stimuapplied hn longer periods (.SO set) nm lated point."
cause the same reaction without the accomA diffusely conducting nerve net would
paming ta( tile stimulation. This cm relates allow the wounded p<>hp to react; the nerve
BEHAVIOR OF Cnrymorpha
495
FIG. 2. Corymorpha responses to stimulation, a. Twisting spirally away from stimulating electrodes, b. An unusual response involving bends in opposite directions.
impulses could get around any cut. However, such a simple hypothesis will not explain how the hydranth manages to localize the stimulus. How can the information
as to where the stimulus has been applied
be preserved in the devious conduction of
the impulses around the cuts?
This remarkable reaction is assumed to
le a protective response by which Corymorpha drives off the small nudibranchs
which feed upon it. I have several times
seen these nudibranchs curled around the
base of a Corymorpha which was making
no response to the gastropod at all. In the
laboratory the response to local stimulation
is enormously varied. Corymorpha has a
whole repertory of bendings, leanings,
twistings, and curlings, which move the
stalk away from stimuli (Fig. 2, a and b).
I can find no stimulus which will regularly
FIG. 3. Aboral flexion of distal tentacles.
call forth a bending and localizing reaction.
If one gives a series of shocks to the stalk
of a polyp, the first response is usually an
aboral flexion of all the distal tentacles in
unison (Fig. 3). Further stimulation may
cause contractions of the proximal tentacles, followed by a bending or twisting
away from the electrodes. If one follows
the stalk with the electrodes, after about
30 shocks (each 10 msec in duration and
delivered 5 sec apart) the animal will sometimes start bending to the stimulated side.
If the reaction is allowed to proceed, the
bending will be seen to continue until the
stalk is formed into a tight coil along the
stimulated side (Fig. 4a, b, c). The hydranth in fact is not affixed to the spot, as
Parker says, except incidentally and briefly
in the course of coiling. It is possible that
the coiling serves to bring the oral tentacles
close to the attacked spot, and that a chemical or tactile stimulus is required for final
location of the predator or other irritant. A
generalization which appears to be true is
that when a protective response of the bending type occurs, it is usually specific to the
particular side stimulated, but not to the
level of the stimulation.
If any wound or cut is made in the polyp,
its responses to stimulation become less predictable. Sometimes one sees a nearly normal response such as the following. If the
stalk is cut halfway through a few mm
above the theca, the stalk immediately
49fi
ROBERT WYMAN
FIG. 4. Stages o£ the "localizing reaction." a. )80°
bend in propel' radial direction, b. The hydranth
contacts the stalk and passes the stimulated point.
c. The response continues into a full coil, bringing
the hydranth away from the stimulus.
bends far over to the side away from the
cut, but within 10 min the stalk is nearly
straight again (but bending toward the
uncut side slightly) and the vacuolated
cells begin to pop out from the wound,
keeping the cut surfaces apart. Stimulating
2 to 3 mm below the cut causes the stalk
to bend toward the cut side, but very incompletely. The bending occurs mostly at
two points, just above the cut and just
below the hydranth, with the stalk remaining straight in between (Fig. 5). Parker
reported, "The failure here seemed to be
due to the deficiency in the musculature as
a result of the operation rather than a deficit in transmission." The fact that muscles
very close to the cut contract while those
farther away are the deficient ones seems
to argue against Parker's explanation.
Stimulation on the side opposite to the cut
will often cause a more normal bending
to that side.
Horridge (1955) has found a similar
situation in the hydromedusan Geryonia
proboscidalis. Here the mouth is quickly
applied to the position of a stimulus on
the underside of the bell. If a 5 mm cut
is made between the stimulus and manubrium the response can still be obtained.
Horridge comments, "As the core of the
manubrium is solid, muscles on opposite
sides are antagonistic so that a little spread
of the excitation strengthens the response
with no impairment of the accuracy of the
pointing as a whole." This surmise might
explain the occurrence of a normal response
in a Corymorpha which has been cut
through less than halfway. The nerve impulses generated by a stimulus would have
to go around the ends of the cut before they
could ascend the stalk to contract longitudinal muscles. The forces produced by
longitudinal muscles symmetrically disposed on both sides of the stimulated point
would then sum vectorially to produce a
bending toward the stimulated point. However, if the stalk were cut through more
than halfway, the sum of the forces of the
longitudinal muscles would be greater on
the side away from the stimulus. This
would cause bending to the side opposite
a stimulus located under the cut. Even
after cutting as much as 70% of the circumference I have seen Corymorpha bend
toward a -.tiiiiulus located under the cut,
but it usually does not do so. It is possible
top of
theca •
l re.
1 h e
loi J I I / H I L ;
ir.uhuii
.illii
,i i n !
BKHAVIOR OF
that the muscles under the cut contract,
and that a mechanical artifact is transmitted through the vacuolated cells and
causes the muscles above to contract. However, there is rarely any bending beneath
the cut, and any contraction of the muscles
there is too small for visual resolution. The
vacuolated cells are very turgid, and immediately eject any object pushed into the
cut for the purpose of restricting mechanical transmission.
The above type of nearly normal response may occur when a cut is made and
a stimulus placed below it. However, it
does not always, or even usually, occur.
There is a question as to whether the response occurs often enough, and with a
great enough accuracy, that it could not
be explained by random bendings which
would sometimes result in a bend toward
the stimulated spot. The span of the tentacles is several times the diameter of the
stalk, so it is not possible to state accurately
where the tentacles are applied. Stimulating below a cut may often call forth no
response, or only slight twistings or bendings, and then it cannot be determined
whether this is even an abortive localizing
reaction. If all these various instances ot
response are included in the sample, then
the percentage of accurate responses becomes very small and not significant. In
summary, the response of wounded Corymorpha is too varied to allow a determination by visual inspection of whether the
animal can retain information as to the
position of a stimulus when the nervous
impulses must make detours.
ACKNOWLKDGM ENTS
This work was done in the summer ot
1961 at the Scripps Institution of Oceanography in the laboratory of Prof. E. W.
Fager; and in the summer of 1962 at the
Kerckhoff Marine Laboratory, California
Corymurpha
197
Institute of Technology, for which accommodation I must thank Prof. Wheeler
North and Prof. Ray Owen. Prof. D. M.
Wilson suggested many improvements in
the manuscript. I was supported by a predoctoral fellowship from the National Institutes of Health.
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