Lee: Independent catch tentacle
TRACT
The inflated catch tentacle of Metridium senile
behaves independent of the oral disk. Close obser-
vation during aggression toward Anthopleura elegantissima
reveals clues to its hydrostatic and neural separation
from the rest of the animal. In the development of
the catch tentacle from regular tentacle, changes in
cnidom, musculature, and nerve net are necessary to
make it a functional unit.
Lee: Independent catch tentacle
INTRODUCTION
The movements of specialized, highly inflatable
tentacles in sea anemones were first described by
Gosse (1860). Hand (1955) described catch tentacles
as occurring in one percent of Metridium senile
in Central California. Catch tentacles have been
identified in six families of the acontiate anemones:
Diadumenidae, Sagartiidae, Metridiidae, Isopheliidae,
Sagartiomorphidae, and Haliplanellidae (Williams, 1975).
In Metridium catch tentacles are used in both intra-
specific and interspecific aggression (Purcell, 1977).
Purcell asserted that aggressive Metridium on the
edges of adjacent clones maintained anemone-free zones.
More recently these zones have disappeared and clones
are no longer segregated (Purcell, 1982). A similar
aggressive behavior was also observed in Anthopleura
elegantissima (Francis, 1973). Catch tentacles can
be induced after prolonged tentacle contact with
non-clonemates. After three weeks catch tentacles
were inflatable, and after nine weeks they were fully
differentiated (Purcell, 1977).
This study aimsto analyze the behavior pattern of
an inflatable catch tentacle, and the control of its
response and movement. Catch tentacles represent an
inducible developmental system which exhibits a
Lee: Independent catch tentacle
complex and prolonged endogenous behavior pattern

released by an appropriate stimulus.
MATERIALS AND METHODS
Several clones of Metridium senile were collected
from the pilings at Wharf No. 2 in Monterey Bay.
Size Tranged from 5 to 7 cm in column height and
4 to 6 cm across the oral disk. Anthopleura elegantissima
were collected from the intertidal at Hopkins Marine
Station in Pacific Grove. They were approximately
4 om across the oral disk. Separate tanks with
running sea water at 14 C held the two anemones.
They were settled on movable rocks. Every 5 days they
were fed Tegriopus. To induce catch tentacle inflation
Metridium was placed in tentacle tip contact with
Anthopleura. This constituted the start of stimulus,
and responses were timed from this point with a
watch. The catch tentacle need not be fully inflated
to count as a response, but it must be markedly
distended. Catch tentacles around the oral disk
were divided into six 60ssectors. Each time the
point of stimulus became the center of sector one.
For microscopy a whole Metridium was relaxed in
7% MgCl, sea water 1:1 for over 14 hours. Tentacles
were transected at the base and cut open to expose
Lee: Independent catch tentacle
the endoderm. Videotape was utilized to analyze
aspects of Metridium catch tentacle behavior.
RESULTS AND DISCUSSION
The typical action pattern of a catch tentacle
is described and illustrated in Figure 1.
(1) Before stimulation a catch tentacle is
still and unexpanded. It is more opaque than the
feeding tentacles.
(2) At initial contact with Anthopleura nearby
tentacles contract, and if the stimulus was large
the oral dise will retract.
(3) After a variable lag period catch tentacle
begins to elongate. This is caused by increase in
hydrostatic pressure, and maybe contraction of
muscle in the tentacle.
(4) Inflation starts at the base and moves up
to the tip. It is not a continuous process because
the catch tentacle repeatedly contracts and expands.
It can inflate to a maximum size of 0.5cm x 12 cm.
(5) The movements of the tentacle originate
at the base and transmit along the whole length.
It is analogous to the motion of a whip. Muscular
action move the inflated tentacle all around the oral
disc.
Lee: Independent catch tentacle
(6) The tentacle tip attaches anywhere on
Anthopleura. Nematocysts anchor it and then theet
Metridium contract and break the tip.
The aggressive behavior of Metridium was fairly
consistent. The response of catch tentacles followed
tentacle contact with Anthopleura. Catch tentacles
were inflated in 37/52 trials, or 71%. The response
times of this group varied greatly (Figure 2).
In this data the duration of stimulation (the time
the anemones were left together) varied from ten
seconds to the length of the trial. If the time
parameter was held constant at ten minutes, the lag
period maintained its high variability (Table 1).
The catch tentacle to inflate first was usually the
one closest to the site of stimulus (Figure 3).
Of the 37 anemones that responded, 21 or 51% inflated
more than one catch tentacle. This would occur
within a period of five minutes.
An inflated catch tentacle seems to be hydro¬
statically isolated from the rest of the coelenteron.
When red food color was injected into the column of
an anemone with inflated catch tentacles, no color
appeared in the coelenteron of the catch tentacles.
The color diffused to all other parts of the animal.
Dye injected to an unstimulated Metridium was dis-
Lee: Independent catch tentacle
charged before catch tentacles could be induced to

inflate. Methylene blue, carmine, and graphite
particles gave similar results.
Examination of the oral disc revealed that
catch tentacles occurred only between pairs of perfect
mesenteries (Table 2). Under the base of an inflated
tentacle one could see a mesentery pair coming
together, creating a small compartment. If the
mesenteric stoma closes and the circular and radial
muscles of that endocoel contract, that would isolate
the endocoel from the rest of the coelenteron
(Figure 4). Movements of the catch tentacle did
not affect the appearance or activity of feeding
tentacles. A Metridium often inflated 2 to 6 tentacles
without effect on the oral disc. Touching an inflated
tentacle caused it to retract, but with no reaction
around the oral disc. All the observations together
suggest a separate hydrostatic and neural control
of the catch tentacle from the oral disc and regular
tentacles.
Catch tentacles and regular tentacles were
anaesthetized, slit longitudinally, and prepared as
whole mounts for viewing. Figure 5 shows the
longitudinal muscle fibers of a regular tentacle,
The neuromuscular structure of Metridium tentacles
Lee: Independent catch tentacle
have been described by van Marle (1976), and only
longitudinal fibers were mentioned. Batham and
Pantin (1951) described, in addition, circular
endodermal muscles, which were not observed in this
study. The catch tentacles have cross fibers oriented
at 90° (Figure 6). Higher magnification (1000 x)
revealed spindle-shaped cells. The thicker, longitudinal
fibers were closer to the epithelium and the cross
fibers were just above them. In swimming sea anemone
Gonactinia prolifera, tentacles were used for walkingi
and swimming. The tentacles had ectododermal longi-
tudinal fibers and endodermal circular fibers
(Robson, 1971). Although the activity of catch
tentacle is not as strenuous as walking and swimming,
the tissue undergoes frequent expansion and retrac¬
tion. The crossing muscular system also provides a
full range of motion in its aggressive behavior.
GENERAL DISCUSSION
The catch tentacle of the clonally reproducing
Metridium senile represents a behavioral system with
some interesting properties. A simple structure with
complex behavior can be developmentally induced from
a regular tentacle, and it can regress to its
original structure (Purcell, 1977, Hand, 1955).
Lee: Independent catch tentacle
The nerve nets of coelenterates have received con¬
siderable attention, and a picture of separate
conducting systems controlling a variety of behaviors
with varying degrees of linkage between these systems
is emerging. The nerve net of Metridium has been
characterized for the mesentery and column
(Batham, et al, 1960, Robson and Josephson, 1969).
The neural control of the catch tentacle adds another
layer to this with a system having interesting and
tractable properties. Spread of excitation from the
stimulus site, tip of a regular tentacle, down to the
oral disc and to the catch tentacles takes much longer
than expected for conduction in a nerve net. The
wide range of response times of Metridium to ag-
gressive stimulus make speculation on the speed of
this conduction difficult. Probably there is some
utilization time to release the endogenous mechanism.
In any case the nervous control of the catch tentacle
appears to be independent of the general nerve net.
The feeding tentacles resume normal activities after
initial contact with Anthopleura, and lack remark-
able movement during catch tentacle aggression.
A large, noxious stimulus such as a hypodermic
injection causes overall contraction and retraction
of inflated catch tentacle. Five or six inflated
Lee: Independent catch tentacle
tentacles of a stimulated anemone gradually move
toward the site of stimulus. However there is lack
of coordinated movement among these tentacles.
Thus each tentacle can exhibit spatial orientation
toward the site of stimulation, though it is removed
from that sector.
Catch tentacles can be induced from feeding
tentacles in Metridium by prolonged contact with
non-clonemates (Purcell, 1977). She recorded changes
in size, opacity, and cnidom. Microbasic b-mastigophores
and atrichs are arranged from the most mature at the
tip to the least at the base (Watson and Mariscal, 1983).
The cells migrate to the tip after autonomy so that
the catch tentacle becomes effective again.
In addition to the observed increase in size and
nematocyst content a number of other changes must
occur to yield a fully functional catch tentacle.
The crossing muscle fibers of Metridium catch tentacle
lie very close to the epithelium. The mesoglea is
not distinct under the polarizing microscope. It is
likely that the connective tissue reduced during
development to allow the tentacle great extension
and ease of inflation. The tissue was fragile and
difficult to manipulate for biomechanical tests.
Since the normal tentacles are not affected by
Lee: Independent catch tentacle
10
inflation of å catch tentacle, two possible explana¬
tions arise: (1) the increase in pressure to the
catch tentacle is very slight, (2) the structure of
the feeding tentacle is more rigid such that it
requires more pressure than a catch tentacle to extend.
Coelenteron pressure has a small pressure range,
averaging from 2.6mm to 6.5mm of water (Batham and
Pantin, 1950). A better explanation would be that
the catch tentacle lost structural support so that
small pressure changes can easily affect its size.
A catch tentacle can become six times longer in one
minute or less.
To summarize, a feeding tentacle near the pharynx
that is between a pair of perfect mesenteries can
be induced to develop into catch tentacle. During
this development structural changes in the muscle,
the mesoglea, and the nematocysts occur along with
the differentiation of a conduction system specific
to a catch tentacle. Together a whole complex
behavior system emerges that displays action patterns
and independent control.
Neural recording from the oral disc and tentacles
might reveal the properties of the conduction system.
Lubbock and Shelton (1981) recorded a triphasic
spike in Anthopleura after contact with allogeneic
Lee: Independent catch tentacle
11
tissue. Clonemates and objects fail to evoke elec-
trical activity. It would be exciting to find the
electrical stimulus that will release the agonistic
action pattern, beginning with an increase in hydro-
static pressure. A closer examination of the histo¬
logical changes in the mesoglea, the musculature, and
the nerve net before and after induction will
provide insight to the control of catch tentacle
activity.
I thank Chuck Baxter for his advice on this
work and many stimulating discussions, and also for
critically reading the manuscript; Freya Sommer for
collecting animals; and the people at Hopkins Marine
Station for their enthusiasm.
Lee: Independent catch tentacle
12
REFERENCES
Batham, E.J. and C.F.A. Pantin, 1950. Muscular and
hydrostatic action in the sea-anemone Metridium
senile (L.). J. exp. Biol. 27:264-289.
Batham, E.J. and C.F.A. Pantin, 1951. The organization
of the muscular system of Metridium senile.
Quart. J. Micro. Sci. 92:27-56.
Batham, E.J., et al, 1960. The nerve-net of the
sea-anemone Metridium senile: the mesenteries
and the column. Quart. J. Micro. Sci. 101:487-510

Francis, L., 1973.
Intraspecific aggression and its
effects on the distribution of Anthopleura
elegantissima and some related sea anemones.
Biol. Bull. 144:73-92.
Gosse, P.H., 1860. A History of the British Sea
Anemones and Corals. Van Voorst, London, 362pp.
Hand,
C., 1955. Sea anemones of central California
coast, part III: The Acontiarian anemones.
Wassmann J. of Biol. 13(2):189-251.
Lubbock, R. and G.A.B. Shelton, 1981. Electrical
activity following cellular recognition of self
and non-self in a sea anemone. Nature. 289:59-60.
Purcell, J.E., 1977.
Aggressive function and induced
development of catch tentacles in the sea
anemone Metridium senile. Biol. Bull. 153:355-368.
Purcell, J.E., 1982. Intraspecific aggression and
population distribution of the sea anemone
Metridium senile. Biol. Bull. 162:345-359.
Robson, E.A., 1971. The behavior and neuromuscular
system of Gonactinia prolifera, a swimming
sea anemone. J. exp. Biol. 55:611-640.
Robson, E.A. and R.K. Josephson, 1969. Neuromuscular
properties of mesenteries from the sea-anemone
Metridium senile. J. exp. Biol. 50:151-168.
C
Lee: Independent catch tentacle
13
van Marle, J., 1976. Contribution to the knowledge
of the nervous system in the tentacles of some
coelenterates. Bijdragen tot de dierkunde.
46(2):219-260.
Watson, G.M. and R.N. Mariscal, 1983. Comparative
ultrastructure of catch tentacles and feeding
tentacles in the sea anemone Haliplanella.
Tissue and Cell. 15(6):939-953.
Williams, R.B., 1975. Catch tentacles in sea anemones:
Occurrence in Haliplanella luciae (Verrill) and
a review of current knowledge. 9. Nat. Hist.
9:241-248.
Lee: Independent catch tentacle
14
FIGURE CAPTIONS
Figure 1
a-i, Behavior sequence of a catch tentacle
in aggression.
Figure 2
Appearance of catch tentacle, measured from
initial contact.
Figure 3
Schematic representation of oral disc and
distribution of initial catch tentacle
response.
Figure 1
Musculature of a perfect mesentery, taken
from Batham and Pantin, 1951.
Figure 5
Longitudinal muscle fibers of regular
tentacle. (400 x)
Figure 6 Longitudinal and crossing muscle fiber
of catch tentacle. (400 x)
Lee: Independent catch tentacle
15
TABLE CAI
TION
Table 1 Response time of Metridium catch tentacle
to 10-minute stimulus by Anthopleura.
Table 2
Tentacles found between perfect mesenteries.
Only the regular tentacles closest to the
pharynx were counted.
L

C

ad
A

Fiodre

S




1
S
—
—
8
ure 2

1

0 +
25
d

—

—





—


—


Z
1
O
—



—

-

N-40




















—

—








POINT OF STIMULUS







66.6%
3.3%
4.8%
4.8%
—





-

—

—






—




IiI


6.6%



—






—
ORAL STOMA
RETRACTOR
LONGITUDINAL
RADIAL
PARIETO-BASILAR

DISK CIRCULAR


Egre
Fgre
.L
Figon 6
—
MINUTES

10
— —
2

18
20
25
30

5
NO RESPONSE



—
o ble
NUMBER OF
ANEMONES
—
2
C

—
—

CATCH TENTACLES
REGULAR TENTACLES

NUMBER
19/19
20/42

abe
O