Wu: Pedal Locomotion
ABSTRACT
Videotapes, both in real time and time lapse, were
made of moving anemones stimulated by Aeolidia papillosa.
Close analysis of the videotapes provided a detailed descrip¬
tion of the development and progression of locomotory pedal
waves in Anthopleura elegantissima. The mean velocity of
all anemones studied was 13.6 mm/hr. A correlation between
the movements on the column with that of the pedal disc during
locomotion provides a basis for the explanation of muscular
systems involved.
Wu: Pedal Locomotion
I. Introduction
Although anemones have been known to locomote for well
over, a hundred years (Gosse 1860), no detailed analysis of
pedal locomotion exists. Furthermore, the majority of the
works relating to locomotion have been conducted with the anemone
Metridium senile. Almost no work has concentrated on Anthopleura
elegantissima except for a brief mention in Edmunds et al
(1976).
Some of the earlier accounts of pedal locomotion can
be found in Parker (1917) for Metridium marginatum, Sagartia luciae,
Condylactis passiflora and Actinia bermudensis. Additional
accounts using Metridium senile are from Batham and Pantin (1951),
Pantin (1952) and Robson (1976).
In this study, the pedal locomotion of Anthopleura
elegantissima was studied to provide a detailed description
of the development and progression of the locomotory waves.
Aeolidia papillosa was used as stimulus for the anemones.
Videotaping, in both real time and time lapse, was employed as
well as simple observation.
Questions examined during this study included a detailed
description of the mechanics of the pedal waves, the temporal
characteristics of the waves and the correlation of movements
on the column with that of the pedal disc, to arrive at an
explanation of the muscles involved in locomotion.
Wu: Pedal Locomotion
II. Materials and Methods
The experiments were conducted at the Hopkins Marine
Station, Pacific Grove and the Monterey Bay Aquarium, Monterey.
Both Anthopleura elegantissima and Aeolidia papillosa used were
collected from wharf +2 in Monterey. Anemones and nudibranchs
were held for approximately seven weeks in 13°c runningsea water.
Aeolidia were kept submerged in three feet ofses water to cure
and prevent bubble disease. Feeding was intermittent. Only
animals that had been without food for at least 24 hrs. were
used in experiments. Twenty-four hours without food normally
elicits predatory behavior in Aeoldia (cited in Edmunds et al,
1976). Sizes of anemones ranged form 1-3cmacross the
oral disc.
A. Observation
Simple observation of anemones attached to the wall of
a glass tank was employed initially. An eolid was introduced
until contact was initiated and feeding began. Only eolids
of comparable size to anemones were used. Anemone locomotion
or detachment would follow.
B. Time Lapse
Time lapse was conducted at the Monterey Bay Aquarium
with a Betacam recorder video camera. Footage was analyzed
on a Panasonic Omnivision II VHS videotape system which
allowed stop frame, slow speed and normal speed (30 frames/sec)
Wu: Pedal Locomotion
viewing. One frame was taken every 1.89sec. Filming duration
ranged from 1-2hrs. Anemones were attached to the tank wall
or a glass plate and then positioned vertically for filming.
Filming took place in sea water at room temperature (20°:c)
and 14-15°C. Fiber optic lights were employed to reduce
heat transfer. All anemones were stimulate by Aeolidia as
explained earlier.
C. Real Time
A Panasonic VHS video recorder was used for filming in real
time. Anemones were attached to the vertical walls of small plex¬
iglass tanks. Temperature of the sea water during recording
was approximately 17°C. Anemones were stimulated by Aeolidia.
D. Locomotion of Anemones Without Oral Disc
The oral disc of the anemone was cut off using a pair
of surgical scissors. A. elegantissima were allowed to recuperate
for approximately 24hrs. Filming conditions were similiar
to real time recording. stimulus provided by Aeolidia.
E. Quantitative Data
Data were gathered from approimately 30 anemones.
Not all data were collected from each anemone, that is,
only anemone velogity was collected from some anemones while
others provide a complete data set. Anemone velocity was measured
from the leading edge of the anemone in its original position
Wu: Pedal Locomotion
to the leading edge of its final position. Wave velocity was
measured as the wave travelled across the latter half of the disc
where it was easier to follow. Only the number of complete
waves crossing thepedal disc were tabulated. Some waves
would travel across the disc then die out upon nearing the
leading edge.
III. Results
A. Pedal Wave
Pedal locomotion of Anthopleura elegantissima involves
monotaxic, direct waves. Waves originate at the point of
stimulus and travel across the disc to the leading edge.
The posterior portion of the pedal disc is sectioned into
lobes by radial furrows running along mesenteric lines.
These furrows are areas of contraction and detachment from the
substrate (Fig. 1a). As one wave would near completion (Fig. ib).
another wave would begin by detaching the back edge and drawing
its pedal disc away from the eolid feeding site. Furrows
associated with mesentaries begin to deepen and enlarge. As
the wave continues to progress, these furrows travel around
the edge of the pedal disc becoming a moving wave, and extending
toward the center of the disc (Fig. 1c. d).
At approximately halfway across the disc (in the direction
of locomotion), the furrows become a complete, propagating,
direct, monotaxic wave (Fig. le). The wave maintains its
Wu: Pedal Locomotion
definition as it travels across the remainder of the disc,
usually with a slight convexity viewed from the anterior
(Fig. 1f,g). Just before the leading edge, the anterior
edge of the wave stops and the posterior catches up and forms
a crease (Fig. 1h). The column around the leading edge is
folded Junder slightly in front of this crease. This folded
under portion is flipped out in the final pedal wave sequence.
B. Quantitative Data
All quantitative data are summarized in Table 1.
A similiar "range of variability in each set of data was
found for each anemone as well as for the entire experimental
group; no conclusive correlation existed between size and velocity,
movement forward/wave, etc.
C. Movement of the Column during Locomotion
Upon initial contact with Aeolidia, Anthopleura
would lean towards the eolid with tentacles expanded. But
as Aeolidia began feeding, the tentacles were withdrawn
slightly and the oral disc contracted down. The anemone
soon assumed its original position. The posterior edge
inflated and the column moved away from the eolid (Fig. 2a).
During the course of a pedal wave the column experiences
several peristaltic-like waves passing up and down the column;
no conclusive correlations could be made to events in the
pedal disc.
Wu: Pedal Locomotion
Initiation of the wave began as the back edge was simul¬
taneously detached from the substrate and pulled forward
toward the leading edge (Fig. 2b). Reattachment occured
as the back edge gradually came back into contact with the
substrate (Fig. 2c). The wave continues around the posterior
pedal disc perimeter as a small fold. Accompanying the appearance
of this fold is a lowering of the oral disc located above the
wave (Fig. 2d). As the wave becomes a well defined band across
the pedal disc, the oral disc above the back edge was raised
and a crease was evident in the oral disc (Fig. 2e). Con¬
tinuation of the pedal wave involves a constriction of the
lower half of the column, especially near the leading edge
(Fig 2f). The anemone begins to lean forward; the column
bulges out above the leading edge and gradually makes contact
with the substrate (Fig. 2g), folding under in the process.
A slight downward contraction of the entire oral disc coincides
with this folded pertion being flipped, out as a circumfer¬
ential wave (Fig.2h).
IV. Discussion
Thus far, the anemone has been Viewed as jeparate elements¬
the pedal disc and column. By correlating the movements of
the column to the pedal disc, an attempt at an analysis of the
musculature involved is possible. The muscle systems will
be generalized from the literature but the studies were
largely done one Metridium (Batham and Pantin, 1951).
Wu: Pedal Locomotion
A. Muscle Systems
The two major muscle systems involved in locomotion are
the parieto-basilar and endocoelic parietals (Batham and Pantin,
1951). The parieto-basilars provide horizontal to diagonal lines
of stress along a mesentery. This muscle system runs from the :
pedal disc to the lower half of the body walland are found exocoel¬
ically in perfect and imperfect mesenteries. The parietals
provide vertical stress lines within a mesentery. Kunning
from the pedal disc to the body wall, parietals exist in the
endocoel of microcnemes (Fig.3).
Other possible minor contributers are the retractors and
the longitudinal muscles of mesenteries (Fig. 4).
B. Musculature During Locomotion
From my observations,I believe almost all muscle
related activity occurs in the mesenteries other than some
contraction of the circular muscles of the column.
Initiation of a wave is accomplished by the parieto¬
basilars drawing in the back edge while the parietals simul-
taneously lift the back portion of the pedal disc off the substrate
(Fig. c). The furrows of detachment and contraction that develop
are due mainly to the parietals contracting and the parieto¬
basilars contributing (Fig 5d).
These furrows are able to propagate around the edge
of the disc by progressing from one mesentery to another.
Analysis of the Videotapes supports this theory as the furrows
move through the visible attachment lines of successive mesenteries
Wu: Pedal Locomotion
In addition, the creases or lowered oral disc above the wave
(Fig2d-f) indicate involvement of the mesenteric longitu -
dinal muscles. During a wave, a narrow band of contraction
running vertically up the side of the column from the fold at
the disc perimeter probably results from both the parietals
and parieto-basilars creating a line of tension between column
and pedal disc.
The appearance of a distinct wave approximately half¬
way across the disc could be due to two perfect mesentaries
contracting their parietal muscles; each situated opposite
the other along a radial axis (Fig. 5e).
For the wave to maintain its definition as it progresses
forward through radially arranged mesenteries, isolated con¬
tractions of the fibres in both the parietal and parieto¬
basilar muscle seem necessary (Fig. 5f). These muscle fibers
would be in the mesenteries situated at angles perpendicular
to the wave. A cinched in contortion appears and passes
down the column as the wave approaches the leading edge.
This appearance would seem to indicate a contraction of the
parieto-basilar muscles propagating the wave across the pedal
disc (Fig. 2f, Fig. 5e).
As the wave nears competion it becomes a sharp crease,
a result of two processes: 1) the excess pedal discmaterial
being pushed up against the momentarily stationery leading
edge, and 2), the leaning forward and folding under of the column.
Wu: Pedal Locomotion
10
Additional observations I made include experiments conducted
upon anemones which had their oral discs removed. These
anemones, when stimulated by Aeolidia, locomoted normally.
This observation agrees with the view that the pedal disc
and agacent parts contain all the neuromuscular mechanisms
needed for locomotion (Parker, 1917). Decapitation would
not affect the parietal and parieto-basilar muscles since
they are attached to the body wall.
I also noticed a reduction of the pedal disc area
before locomoting in anemones which had their pedal discs
spread out. Waves would be initiated and propagate as far
as the front portion of the pedal disc but then stopped.
This is probably associated with contraction of the circular
muscles of the pedal disc to reduce its area.
Further work is clearly indicated to clarify the two
previously mentioned behavioral responses. A detailed analysis
of the musculature of A. elegantissima especially during lo¬
comotion would greatly contribute to our understanding of
pedal locomotion. Questions such as, why is the manner of
propagation seemingly different in the beginning compared to
the end of a wave and, what manner of nervous activity is involved,
remain unanswered.
edal
moti
I would like to thank everyone at Hopkins Marine
Station, particularly Freya Sommers, and Chuck Baxter for
his invaluable guidance and assistance. A special thanks
to Mark Shelley and Alex Edwards of Monterey Bay Aquarium
for their time, energy and generosity in allowing me to use
the time lapse photography equipment.
Wu: Pedal Locomotion
12
REFERENCES
Batham, E.J. and Pantin, C.F.A. 1950 Muscular and Hydrostatic
Action in the Sea Anemones Metridium senile (L.)
Journ. of Ex. Biol. 27:264-289.
Batham, E.J., and Pantin, C.F.A. 1951 The Organization of
the Muscular System of Metridium senile.
Quart. Journ. Micro. Sci. 92:27-54.
Edmunds, M. et al 1976 Defensive Behavior of Sea Anemones
in Response to Predation by the Opisthobranch Mollusc
Aeolidia papillosa (L.). J. Mar. Biol. Ass. U.K.,
56:65-83.
Pantin, C.F.A. 1952 The Elementary Nervous System.
Proc. Roy. Soc. B.140:147-168.
Parker, G.H. 1917 Pedal Locomotion in Actinians.
Journ. of Exp. Zool., 22:111-124.
Robson, E.A. 1976 Locomotion in Sea Anemones: The Pedal Disk,
In Coelenterate Ecology and Behavior (ed G.O. Mackie),
Plenum Press. New York and London.
Wu: Pedal Locomotion
FIGURE CAPTIONS
Figure 1: Sequence of pedal wave outlines during locomotion.
The two major muscle systems associated with
Figure 2:
locomotion. Taken from Batham and Pantin (1951)
for Metridium senile.
Figure 3:
Musculature of a perfect mesentery. Other muscle
systems which may have minor involvement in locomotion--
longitudinal, retractors and circular. Taken from
Batham and Pantin (1951) for Metridium senile.
Figure 4:
Movement of the column during locomotion as it
relates to the pedal wave. Anemone was stimulated
by Aeolidia papillosa.
Figure 5:
Mesentery musculature during locomotion. a) Top viey
of mesenteries. b) Cross-section of a mesentery, c)
wave
beginning as shown in one mesentery. Parietals and
parieto-basilars contract. d) Deepening furrows through
contraction of parietals and parieto-basilar.
e) View of one half of pedal disc. Perfect mesentery
contracting muscies along vertical axis. f) Section
of pedal disc showing three simplified mesenteries.
g) Cross section of mesentery with edge of column
folded under. Contraction of parieto-basilars
combined with hydroståtic pressure flip folded under
portion back out.
1

3







9
9
—--




W










(
(
O
(C
ORAL STOMA
RETRACTOR
LONGITUDINAL
RADIAL
PARIETO-BASILAR
DISK CIRCULAR
4
szasse
11
—
(C
(c)
(a)
Se

k
(f)

(d)
A


(g)

(b)





(e)
———
„— —

.

PARIETAL
r PARIETO-BASILAR
RETRACTOR
-- CIRCULAR¬
C
Wu: Peda
comotion
TABLE CAPTIONS
Table 1: Anemone and wave velocities of A. elegantissima
in response to an attack by Aeolidia papillosa.
14
2

NO




—
1N
O


L
I


LL


—:—


LE

2






—



—
—

AT
E