Journal of Experimental Marine Biology and Ecology,
228 (1998) 273–290
L
Jointed setae – their role in locomotion and gait transitions
in polychaete worms
Rachel Ann Merz*, Deirdre Renee Edwards
Department of Biology, Swarthmore College, Swarthmore, PA 19081, USA
Received 15 August 1997; received in revised form 3 February 1998; accepted 7 February 1998
Abstract
Many families of polychaete worms have jointed setae in which the joint is external to the body
and is not directly controlled by muscles or nerves. We assessed the role of these specialized
structures in the hesionid polychaete, Ophiodromus pugettensis, by examining speed, step length,
stride distance, stride frequency and gait transitions in worms with and without setal joints.
Individual worms were videotaped while they moved over sandy surfaces at a range of speeds.
The worms were then anaesthetized and all their compound setae were trimmed either distally or
proximally to the setal joints. After two days of recovery the worms were videotaped a second
time while they again moved over sandy surfaces at a range of speeds. From the video tapes we
analyzed their locomotory performance before and after setal ablation. Animals in which the setae
were shortened but in which the joint was left intact showed no consistent change in speed, step
length, stride distance, stride frequency or gait transitions. Animals in which the joint had been
removed both changed gaits at slower speeds (walking to undulatory walking and undulatory
walking to swimming) and showed a significant decrease in maximum swimming speeds and
stride distance. A subset of data containing only cases where the worms were moving at the same
speed in the same gait before and after setal ablation was analyzed. In these instances, after the
removal of the joint, the worms had significantly smaller stride distances and compensated for this
by increasing stride frequency. In O. pugettensis, the undulatory walking gait is analogous to the
trot–gallop transition in quadrupedal mammals because the animal switches from moving the
appendages on a relatively rigid body to using a combination of body flexion and appendage
movement to achieve propulsion, however, unlike quadrupedal mammals this transition takes
place over a wide range of speeds and at different sites on the body as speed increases. These
experiments indicate that jointed setae may be important both in allowing a worm to better control
setal contact and traction with the substrate as well as in altering the effectiveness of its swimming
stroke.  1998 Elsevier Science B.V. All rights reserved.
Keywords: Annelids; Polychaete worms; Ophiodromus pugettensis; Setae; Locomotion; Gaits
*Corresponding author. Tel.: 1 1 610 3288051; fax: 1 1 610 3288663; e-mail: [email protected]
0022-0981 / 98 / $ – see front matter  1998 Elsevier Science B.V. All rights reserved.
PII: S0022-0981( 98 )00034-3
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1. Introduction
Polychaete annelids typically have dorsal and ventral arrays of chitinous setae
associated with the parapodia of most segments (Fig. 1). Although these familiar
structures are used extensively for identification by taxonomists, there is relatively little
known about the way they function on living worms (although, see Mettam, 1971, 1984;
Roy, 1974; Knight-Jones and Fordy, 1979; Knight-Jones, 1981; Woodin and Merz,
1987). One major variety of these structures, known as jointed or compound setae, are
found in 28 polychaete families (Fauchald, 1977; Fauchald and Rouse, 1997). Compound setae are associated with mobile or discreetly mobile worms but never with
sedentary polychaetes (as defined by Fauchald and Jumars, 1979).
Each compound seta is the product of a single cheatoblast and associated follicular
cells and extends out of the body from the setal sac within a parapodium (Bobin, 1947;
Bauchot-Boutin and Bobin, 1954; Schroeder, 1967, 1984; O’Clair and Cloney, 1974;
(Fig. 1)). In compound setae, the joint has a socket in which the distal blade of the seta
is typically anchored by both a ligament and a hinge (Gustus and Cloney, 1973) (Fig. 2).
A functioning joint, therefore, is external to the body and is neither directly controlled
Fig. 1. SEM of a midbody parapodium of O. pugettensis, viewed from a ventral anterior position. The
notopodium is relatively reduced. Compound setae can be identified throughout the neuropodium, scale bar is
200 mm.
R. A. Merz, D.R. Edwards / J. Exp. Mar. Biol. Ecol. 228 (1998) 273 – 290
275
Fig. 2. SEM of morphological details of the compound setae of O. pugettensis. (a): Tip of the distal blade,
scale bar 5 1 mm. (b): Ventral view of two unbent setal joints, scale bar 5 10 mm. (c): Lateral view of two setal
joints with their distal blades displaced slightly to the side, scale bar 5 2 mm. (d): View of the socket of the
setal shaft, the base of the distal blade and the ligamentous attachment, scale bar 5 2 mm.
by muscles nor innervated by nerves (Gustus and Cloney, 1973). The way in which
compound setae bend at the joint is controlled by the shape of the cup and the
attachment of the ligament (Gustus and Cloney, 1973; Schroeder, 1984; Merz and
Woodin, 1987) (Fig. 2). We are aware of no report in the literature of the direct
observation or test of the function of these setae (Schroeder, 1984). Gustus and Cloney
(1973) suggest that based on morphology they expect the blade to move relative to the
shaft, although it has no intrinsic power. When the seta is thrust against a substrate the
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joint would allow flexibility, albeit confined to some degree by the hinge and ligament.
This flexibility would presumably confer increased friction and reduce slippage.
To understand if and how these structures function in polychaete locomotion, we
compared the locomotory performance of worms with unaltered setae to the same
animals’ performances after the compound setae had been trimmed either distally or
proximally to the joint (the distal treatment is essentially a control for the process of
trimming and the effect of shortening setae; the proximal treatment examines the role of
the joint per se). If the joint is crucial in locomotion, then we expected a diminution in
performance when it is removed. Merely shortening the setae could also have a negative
effect on locomotion; if that is true, then animals with setae that are ablated distal to the
joint should have a diminished performance.
For our test animal we chose the hesionid polychaete, Ophiodromus pugettensis
( 5 Podarke pugettensis) which lives from British Columbia to the Gulf of California. It
is an active, mobile worm that is found in a variety of habitats including muddy bays,
rocky shores, among fouling organisms on floats and pilings and in the subtidal to the
continental shelf (Morris et al., 1980; Kozloff, 1983). It can be free living with a diet of
small invertebrates (Shaffer, 1979; also see Oug, 1980) or can live as a facultative
commensal with a number of different partners (e.g., within the ambulacral grooves of
starfish (mainly Pateria) (Hickok and Davenport, 1957; Lande and Reish, 1968), on the
holothurian Protankyra bidentata (Okuda, 1936), with the terebellid polychaete
Eupolymnia heterobranchia (Shaffer, 1979), or on hermit crabs together with a nereid
polychaete (Berkeley and Berkeley, 1948)).
O. pugettensis was selected for this project because (1) it readily displays a variety of
locomotory gaits, (2) it naturally lives and moves on a variety of substrates, (3) it has a
morphology and size that make it amenable to experimental alteration and (4) it readily
adapts to life in the laboratory (often occurring as an accidental resident in sea-water
tables).
2. Materials and methods
2.1. Collection and housing of animals
Worms were collected by hand during low tide from the mud flats of Garrison Bay,
San Juan Island, Washington. They were found crawling on a variety of substrates
including the surface of the mud, under and on cockle and clam shells, in mats of algae,
and on an old sock. After collection the worms were transferred to sea-water tables at
the Friday Harbor Laboratories where they were housed with Enteromorpha and Ulva
collected at the same site and presumably inhabited by the copepods and other small
invertebrates that are reported to make up the diet of O. pugettensis (Shaffer, 1979).
Even though O. pugettensis is often found in the sea-water tables at the laboratories and
appears to live well under those circumstances, for these experiments we used only
animals that we had collected from the field within the previous ten day period.
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277
2.2. Videotaping techniques
We used only active worms whose setae, parapodia and body wall appeared to be
undamaged. The worms were relatively similar in size (mean length 21.0 mm, S.D.61.6
mm, n 5 15). Each worm was filmed both before and after setal trimming (see below) in
a 7.2 3 7.2 cm plastic container in which there was a layer of fine grain white sand
covered with about 1 cm of sea-water. We used a Sony DXC-107 CCD color video
camera attached to a Pentax macrolens mounted above the field of view which was
illuminated with a GenRad GR 1546 stroboscope held 7.5 cm above the substrate,
flashing at 60 flashes / second. The images were taped at 30 frames / second (this rate was
confirmed during data collection). Each taping sequence began by video recording a
millimeter scale placed on the sand surface. At a minimum, each worm was recorded
until it completed at least four episodes of walking, undulatory walking and swimming.
If necessary, worms were gently nudged with a blunt probe to encourage them to move
through the field of view.
2.3. Video analysis
We used only episodes in which a worm moved at a continuous speed and was in
focus throughout the measurement period. For each test episode, the frame by frame
video image of the progress of a worm was traced onto acetate sheets. Worm speed was
measured by counting the number of frames it took a worm to move along a measured
distance. We attempted to analyze each worm throughout its entire speed range.
Along with the speed, the gait used in each episode was identified. Preliminary
observations revealed that O. pugettensis has two distinct gaits (walking and swimming),
with a transitional gait between them (undulatory walking) (Fig. 3). We considered an
animal to be walking if its body was held in a relatively rigid linear position and its
parapodia moved independently of the motion of the body, regularly contacting the
sediment during the step cycle. A swimming worm was propelled by whole-body
undulating waves that originated in the tail and were coordinated with parapodial
movement. During swimming there was no contact between the solid substrate and the
body. Any gait that contained elements of both walking and swimming was considered
an undulatory walk In this gait the posterior portion of body undulated while anterior
section remained relatively rigid. As speed increased, the amount of body undergoing
flexion increased (Fig. 3).
To examine the position and timing of parapodial movements at different speeds,
selected parapodia and their associated scale bar were traced onto acetate sheets from the
video images. Typical parapodia on the right and left side of the body were selected for
analysis, based on their midbody position and their clear visibility as the animal moved
through the field of view. We measured the maximum distance that occurred between
these selected parapodia and their adjacent neighbors ( 5 step length) for as many
locomotory cycles as were visible in a given run (where a locomotory cycle is measured
as one complete sequence of limb movements from initiation of the power stroke
extension through the recovery stroke back to where the selected limb resumes its initial
position relative to the body). These values were then averaged for each run to give an
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Fig. 3. Tracings of sets of six consecutive video frames of the same unmodified worm, displaying three
different gaits. In each case the worm is moving from left to right, the vertical line was added to the image to
provide a reference point to evaluate the progress of the animal, the shaded boxes highlight the movement
away from that line, the time elapsed is 0.2 s. The walking speed was 3.75 mm s 21 , the undulatory walking
speed was 10.71 mm s 21 and the swimming speed was 19.57 mm s 21 .
estimate of step length at a given speed. We measured stride distance (distance traveled
in one complete locomotory cycle) by monitoring how far these target parapodia traveled
parallel to the axis of movement during a single locomotory cycle for as many cycles as
were visible in a given run; these values were averaged to estimate stride distance at a
given speed for an individual worm. The number of frames between repeated stages of
the locomotory cycle were counted, averaged for a single worm moving at a given speed
and used to calculate stride frequency.
2.4. Ablation techniques
To trim setae, individual worms were anaesthetized by isolating them in a petri dish
with a small amount of sea-water. Isotonic MgCl was slowly dropped into the water
until the worms were quiescent (usually a matter of a few minutes). While viewing the
animals under a dissection microscope, the setae were trimmed with iridectomy scissors.
All the compound setae on an individual worm were trimmed either immediately distal
or proximal to the joints (depending on the assigned treatment regime) (Fig. 4). The
distal and proximal cuts removed approximately 9 and 12%, respectively, of the total
setal length. These distances were measured on 20 setae selected at random from five
mid-body parapodia of a preserved animal (21 mm in length). The mean total setal
length for these setae was 1.066.13 mm; mean distance to the point of distal cut was
0.106.03 mm, and the mean distance to the point of a proximal cut was 0.136.03 mm).
The ablation procedure took about 10 to 20 min. The fluid around the worm was then
exchanged with fresh sea-water. When the worm began to move it was returned to the
R. A. Merz, D.R. Edwards / J. Exp. Mar. Biol. Ecol. 228 (1998) 273 – 290
279
Fig. 4. Schematic illustration of the experimental modifications of the jointed setae of O. pugettensis (worm
illustrations modified from Uschakov, 1955; Banse and Hobson, 1974; Shaffer, 1979). The worm is illustrated
from the dorsal view. The parapodia are drawn from the anterior view.
sea table and transferred to a small floating plastic container made of fine mesh
screening that allowed fresh sea-water to move constantly through the container. Within
a few minutes worms typically regained their normal posture and behavior. Only those
worms that appeared to have no behavioral changes or physical damage from this
treatment were subsequently used for comparison. The worms were allowed to recover
for two days before being videotaped for a second time, after which they were held for a
period of 1 to 2 weeks to confirm that they continued to show no side effects of the
ablation procedure. The worms were then preserved in a 10% buffered formalin solution.
2.5. Scanning electron microscopy
To examine setal morphology, unaltered formalin fixed specimens were dehydrated in
an ethanol series and held in 100% ethanol for a minimum of 24 h. Dehydrated
specimens were then placed in a small amount of hexamethyldisilazane which was
allowed to evaporate under a fume hood at room temperature overnight (Dykstra, 1993).
After the samples were completely dry, they were mounted on aluminum stubs, and
coated with gold–palladium in a Technics Hummer V Sputter Coater. Specimens were
examined in a JEOL JSM 35 C scanning electron microscope.
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2.6. Statistical analysis
To insure that there were no initial performance differences between the treatment
groups, the initial top speeds reached at each gait were compared using unpaired,
two-tailed t-tests. The top speeds reached at a given gait before and after setal
manipulation were compared within each treatment group using paired, two-tailed
t-tests. To examine what elements of the locomotory cycle might be affected by setal
manipulation, we compared step length, stride distance and stride frequency at the top
speed reached at a given gait before and after setal manipulation. Within each treatment
group we used paired, two-tailed t-tests. The only consistently significant effects were
associated with worms with setae trimmed proximally to the joint. Within that group we
extracted all the records (n 5 29) for instances in which an individual worm had been
recorded moving at the same speed (defined as two locomotory bouts with a measured
speed within 1 mm s 21 of each other) in the same gait (walking, undulatory walking or
swimming) before and after the joints were removed. For these samples we compared
whether step length, stride duration or stride frequency had increased or decreased
compared to the original performance of the unmodified worm. The frequencies of the
response of each of these variables were compared with a G-test using William’s
correction for the two-cell case and assuming a null hypothesis of 0.50 frequency of
occurrence in each instance (Sokal and Rolf, 1995).
3. Results
3.1. Characterization of locomotory cycle
O. pugettensis increase their speed of locomotion by altering different elements of the
locomotory cycle. One element of this increase in speed comes from changes in the
maximum distance between any two adjacent parapodia ( 5 step length) during the
locomotory cycle. (This change in distance between parapodia is due to changes in the
relative positions of the parapodia but not changes in whole segment length, which when
measured at the middorsum of an individual remains constant over the range of speeds
exhibited in any particular gait.) At very slow speeds the maximum distance between
adjacent parapodia is small, and as speed increases so does this distance. For all fifteen
pre-operative worms this inter-parapodial step length reaches a maximum after which it
no longer increases with speed (an example for a single individual is given in Fig. 5(a)).
Another mode by which speed is increased is for the animals to increase stride distance
– the distance traveled by the body from one foot fall to the next. This increase in
distance is accomplished both by the size of the ‘‘step’’ (as described above), and, also
by the amount the body is pushed forward by the action of other segments when a given
parapodium is in its recovery phase. In about half of the unmodified worms we
observed, this trait increased throughout the observed range of speeds (Fig. 5(b)). In the
other half, this quantity leveled off to a fairly constant maximum value at the highest
speeds. Worms can also increase their rate of locomotion by increasing stride frequency
(the number of strides per second). Again, about half of the unmodified worms we
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281
Fig. 5. The relationship between step length, stride distance and stride frequency with speed for a
representative unmodified worm (number 13, Fig. 7). Circles indicate walking, squares indicate undulatory
walking, and triangles indicate swimming.
observed increased stride frequency throughout the range of speed, whereas the others
reached a plateau above which stride frequency did not increase (Fig. 5).
Worm gaits, as defined by our other criteria (see Methods and Materials), were not
definitively associated with specific changes in these elements of the locomotory cycle
(Fig. 5). In most cases, however, the maximum inter-parapodial step length was
achieved in either faster walking speeds or in the slower speeds of the undulatory-
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walking gait. Likewise, if stride distance and stride frequency leveled off, it was always
within the swimming gait.
3.2. Comparison of locomotion in worms with and without joints
There was no significant difference in the locomotory performance (as measured by
the maximum speed at each gait) between the treatment groups before the setae were
trimmed (walking, df 5 13, t 5 0.574, P 5 0.5756; undulatory walking, df 5 13, t 5
0.422, P 5 0.6800; swimming, df 5 13, t 5 1.322, P 5 0.2089). When setae were
Table 1
The results of paired two-tail t-tests comparing the locomotory performance for O. pugettensis, before and
after their compound setae have been trimmed either distal or proximal to the joints
Mean (S.D.) of
maximum values
for untrimmed
worms
Mean
difference
after
trimming
df
t-value
P-value
Distal treatment (n 5 7)
Walking
speed (mm s 21 )
step length (mm)
stride distance (mm)
stride frequency (strides s 21 )
8.78
0.92
3.15
2.38
(6.39)
(0.16)
(0.91)
(0.82)
2 2.93
0.01
2 0.88
0.50
6
6
6
6
2 1.463
0.104
2 2.740
3.066
0.1938
0.9204
0.0338
0.0220
Undulatory walk
speed (mm s 21 )
step length (mm)
stride distance (mm)
stride frequency (strides s 21 )
21.47
1.04
5.21
4.09
(4.77)
(0.15)
(0.82)
(0.63)
2 2.54
0.07
2 0.57
2 0.19
6
6
6
6
2 1.054
1.211
2 1.023
2 0.191
0.3324
0.2715
0.3456
0.5126
Swimming
speed (mm s 21 )
step length (mm)
stride distance (mm)
stride frequency (strides s 21 )
43.75
1.17
8.33
5.56
(7.37)
(0.22)
(1.80)
(0.88)
0.67
2 0.07
0.12
0.02
6
6
6
6
0.240
2 1.406
0.166
0.031
0.8181
0.2093
0.8737
0.9765
Proximal treatment (n 5 8)
Walking
speed (mm s 21 )
step length (mm)
stride distance (mm)
stride frequency (strides s 21 )
10.47
1.04
3.15
2.89
(5.04)
(0.17)
(1.15)
(0.61)
2 4.20
2 0.01
2 0.86
2 0.28
7
7
7
7
2 2.518
2 0.307
2 2.466
2 0.833
0.0399
0.7676
0.0431
0.4324
22.79
1.09
5.75
3.98
(6.95)
(0.17)
(2.13)
(0.56)
2 7.99
0.00
2 1.84
2 0.05
7
7
7
7
2 3.844
0.023
2 3.109
2 0.169
0.0063
0.9822
.0171
0.8706
50.16
1.12
9.24
5.70
(10.79)
(0.14)
(2.25)
(0.94)
2 11.66
2 0.05
2 2.26
2 0.31
7
7
7
7
2 5.892
2 1.048
2 2.825
2 0.798
0.0006
0.3294
0.0256
0.4510
Undulatory walk
speed (mm s 21 )
step length (mm)
stride distance (mm)
stride frequency (strides s 21 )
Swimming
speed (mm s 21 )
step length (mm)
stride distance (mm)
stride frequency (strides s 21 )
In each case the values described and compared are those at the top speed of a given gait.
R. A. Merz, D.R. Edwards / J. Exp. Mar. Biol. Ecol. 228 (1998) 273 – 290
283
shortened, but the joints were left intact, locomotory performance as measured by top
speed at each gait was unchanged (Table 1). In contrast, when the joints were removed
from the setae, worms did not move as fast at a particular gait and thus switched to the
next gait at lower speeds (Table 1, Fig. 6).
Examples of the performance of two typical individuals are illustrated in Fig. 6. In the
case of the animal with the distal ablation, there is a similar range of speeds exhibited
within each gait, and the maximum speed at a particular gait is quite similar before and
after the removal of the setal tip (Fig. 6a). In contrast, when a worm has had its joint
removed, it has a slower maximum speed at each gait and subsequently switches to the
next faster gait at a lower speed (Fig. 6b).
A comparison of the change in the top locomotory speed for each animal at each gait
before and after setal ablation reveals that the animals that lost only the setal blade distal
to the joint had no particular pattern of change (striped bars, Fig. 7). About half of these
Fig. 6. Examples of changes in locomotory performance after ablation of setae either distal or proximal to the
joint for two worms. (a): The setae of this worm (number 10, Fig. 7) were trimmed distally, leaving the joint
intact. Its initial performance is indicated by the gray triangles and its posttrimming performance by the black
triangles. There is little difference in performance in top speed at a given gait or in the speeds at which the
worm changes gaits. (b): The setae of this worm (number 9, Fig. 7) were trimmed just proximal to the joint. Its
initial performance is indicated by gray circles and its posttrimming performance by black circles. Without the
joint, the worm’s top speed at a given gait is diminished and it switches to the next gait at a slower speed.
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Table 2
The results of a G-test comparison of the difference in step length, stride distance and stride frequency for 29
instances when the same speed and gait (walking, undulatory walking or swimming) were recorded in a worm
before and after the setal joints had been removed
Step length
Stride distance
Stride frequency
Number of
positive
responses
Number of
negative
responses
Number of
positive or
negative
responses
predicted
by the null
hypothesis
G value
P value
15
8
21
14
21
8
14.5
14.5
14.5
0.0344
2 8.0338
8.0338
. 0.750
, 0.005
, 0.005
worms showed a faster performance at a given gait before the ablation and about half the
worms actually had faster performances after the ablation. The pattern for those animals
that had the joint removed is distinctly different – in almost all cases top speed for a
particular gait was lower after ablation than before (black bars, Fig. 7).
When we compared differences in step length, stride distance and stride frequency at
the top speed for each animal at each gait we found that the two treatment groups had
different patterns. The animals that retained their setal joints did not show any consistent
significant change in these variables after distal trimming (Table 1). In the walking gait,
although neither speed nor step length was significantly different after trimming the
setae, there was a significant decrease in stride distance and an increase in stride
frequency (Table 1). For the undulatory-walking and swimming gaits there were no
significant differences in any of the locomotory characteristics that were measured. In
contrast, the animals in which the joints had been removed had a stride distance that was
consistently significantly smaller after joint ablation in each gait (Table 1). There were
no significant differences in either step length or stride frequency at the gait transitions
for these jointless-worms (Table 1).
Because we know that the top speed at a particular gait is diminished for worms
without their joints, we also compared step length, stride distance and stride frequency
for 29 cases where a proximally trimmed worm had been recorded moving at the same
speed (within 1 mm s 21 ) within a gait (any gait) before and after treatment. We found
that these animals have no difference in step length before and after ablation, but do
have a significantly diminished stride distance and a significantly faster stride frequency
(Table 2). Thus, these joint-less worms have diminished forward progress with each
stride cycle after their setae are trimmed. Therefore, to attain the same speed at the same
gait they increase the rate of the stride cycle
4. Discussion
The value of the conclusions that can be drawn from this experiment hinge on
whether or not the effects seen by ablation of the setae proximal to the joint are a
product of the lack of the joint or a result of the setae being shorter. Two things argue
that the effect is due primarily to the loss of the joint. The first is that these results are
R. A. Merz, D.R. Edwards / J. Exp. Mar. Biol. Ecol. 228 (1998) 273 – 290
285
Fig. 7. Comparison of the change in the top locomotory speed for each gait before and after setal ablation for
all worms. In the animals with distal ablations but intact joints there was no consistent pattern of change
(diagonal striped lines). In the animals with proximal ablations there was a general diminution of performance
after the joint was removed as measured by the maximum speed at a given gait (solid black bars).
compared with those from animals whose setae were shortened without loosing the joint.
These animals lost about 9% of their total setal length and showed no consistent
significant change in any of the locomotory parameters that were measured and had no
significant diminution in speed. The second argument addresses the concern that the
worms with jointless setae did still have slightly shorter setae than did the worms with
proximally trimmed setae. The jointless worms’ setae were shortened by approximately
12% of their total length. We suggest that it is unlikely that this estimated 3% difference
in setal length (between the treatment groups) is responsible for the difference in
performance between worms with and without joints because the setal bundle is a
dynamic structure that can be extended or withdrawn depending on the muscular action
within the parapodium.
In particular, the setae within polychaete parapodia are bundled together and held
within setal sacs. There can be several setal sacs within a single parapodium. Each setal
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sac has an attachment to intrinsic parapodial protractor muscles that run between the
setal sac and the parapodial wall (Mettam, 1967, 1971; Lawry, 1971). Setal sacs also
have a connective tissue attachment to an aciculum, a robust internal seta that is attached
to intrinsic parapodial retractor and protractor muscles. Contraction of the chaetal
retractor muscles pulls the aciculum deeper into the parapodium and subsequently causes
the setal sac and its associated setae to withdraw. Contraction of the protractor
musculature pulls the setal sac towards the parapodial surface, causing the setae to be
extended and the aciculum to move into its more distal position (Mettam, 1967, 1971;
Lawry, 1971). Thus, the movement of the setae is accomplished indirectly by muscular
attachment to the setal sac and aciculum rather than attachment of muscles to individual
setae and, to a large degree, the extent of the external extension of setae is under the
control of the worm. When we observed O. pugettensis under a dissection microscope
moving at a range of speeds over natural substrates we could see the movement of the
setal bundles. It was rare that the setae ever appeared to be fully extended; these details,
however, were more difficult or impossible to see at the fastest speeds. Thus, we expect
that for most of its speed range, O. pugettensis can easily compensate for a 3%
difference in setal length and therefore the difference in performance of the two
treatment groups is associated with the presence or absence of the joint rather than the
difference in setal length.
So, in what way do passive joints at the ends of setae function? Our suggestion is that
when the parapodia are in cyclic contact with the surface, these joints allow the setal tips
to bend in such a way as to increase the setal contact with the substrate during the power
stroke. This allows a parapodium to have more effective ground contact with an
unpredictably irregular surface. During the recovery stroke when the setae are lifted off
the substrate, the joints passively resume their normal position to be reconfigured during
the next contact with the surface. We have observed this phenomenon many times. That
it is likely to contribute to the effective locomotion of the worm is demonstrated by the
fact that worms that lack these joints have diminished stride distances (distance the body
is moved forward with each locomotory cycle) even though step lengths (the maximum
distance between adjacent parapodia during the locomotory cycle) are not significantly
different (Tables 1 and 2). Because of reduced traction, each cycle of the limbs with
jointless setae produces less forward movement of the worm than when the joints are
intact (Tables 1 and 2). For an aquatic pedestrian that must contend with drag and
buoyancy in addition to gravity, the ability to maintain contact with the substratum is
particularly important (Martinez, 1996), and jointed setae may greatly increase the
effectiveness of contact of each parapodial step.
An additional issue is the role of sculpture or teeth on the distal blades of setae. Their
shape suggests that they might have a role in increasing the friction between setae and
the substratum. The fact, however, that the distally trimmed worms which lacked the
portion of the blades with serrations did not suffer a significant diminution in
locomotory performance suggests that these features did not contribute significantly to
performance in this instance. But, since these experiments only measured performance
on sand, it may be that the serrations are more important in providing traction on
different surfaces.
Because we have not been able to observe closely the action of these jointed setae
during swimming, we have less understanding of how the joints function in this gait.
R. A. Merz, D.R. Edwards / J. Exp. Mar. Biol. Ecol. 228 (1998) 273 – 290
287
Rough-bodied polychaetes, like O. pugettensis swim by means of drag-based thrust
production (Clark and Tritton, 1970; Clark, 1976; Vogel, 1994). Given this mode, one
could hypothesize that the setal joints make the power and recovery strokes more
effective. In the power stroke the setae could be fully extended increasing the amount of
water pushed by the moving parapodium. In the recovery stroke the joints would allow
the setae be folded back against the body, diminishing the drag on the parapodium as it
moves forward. A similar mechanism has been demonstrated for the passively controlled
setal blades of the aquatic mite Limnochares americana (Barr and Smith, 1979). There
are a couple of problems, however, with this interpretation for swimming O. pugettensis.
The first is that the worms with trimmed setae, but intact joints, do not have a significant
decrease in swimming performance (Fig. 7, Table 1). In that case, the setal blades aren’t
available to assist the rest of the parapodium to push the water during the power stroke,
and so we would expect those animals with shortened setae to be slower at this gait if
this were the mechanism by which jointed setae function in swimming. Second, an
examination of pelagic worms reveals that although many are reported to have jointed
setae (e.g., Alciopidea, Lopadorhynchidae, Pontodoridae; Fauchald, 1977) the joints of
the compound setae of at least one alciopid, Rhynchonerella, are reinforced in such a
way that they are not particularly flexible in any way at the joint (pers. obs). In species
that go through a metamorphosis from a benthic form to a reproductive swimming
epitoke, the new swimming setae are dramatically modified. The blades are flattened and
enlarged into an oar-shaped structure, the joint socket is much deeper and narrower
(Schroeder, 1967). This change in morphology substantially stiffens the joint and
restricts flexure of the setae at the joint (pers. obs.). Thus, at least some polychaetes that
do a substantial amount of swimming (as opposed to the presumably rare escape-type
swimming exhibited by O. pugettensis) have setae that lack or have lost the ability to
bend at a predetermined joint.
This still leaves us with the problem of why a worm with setae with intact joints but
lacking blades doesn’t show a diminution in swimming performance, whereas, the loss
of joint and setal blade results in a significant loss in ability (Fig. 7, Table 1). It would
be interesting to experimentally ‘‘lock’’ the joint so that flexure at it is not possible,
however, the small size of the structures and the necessity of animals remaining in
sea-water has thwarted our attempts to glue or stiffen the setae at the joints. It may be
that high-speed close-up video will reveal what the normal motion of the intact
parapodia and setae are during swimming strokes and will thus give a clue to function of
the joint under these circumstances.
As polychaetes move from a stationary position through walking to swimming, they
display different gaits. During walking, the worm’s body is resting on the substratum
and forward progress is a result of the sequential action of individual parapodia moving
in a step cycle along the body. The intrinsic muscles of a parapodium lift it from the
substrate, move it obliquely forward where the tip of the neuropodium contacts the
substrate ( point d’ appui, Foxon, 1936) and then pushes against the surface in a power
stroke causing the associated section of the worm’s body to pivot over the point of
contact. (This process has been described by a number of authors including Gray, 1939;
Mettam, 1967, 1971, 1984; Lawry, 1971). In swimming, the worm’s body is moving
through the water (only rarely or incidentally contacting the substrate) and whole body
waves caused by the alternate contractions of the longitudinal muscles provide
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propulsion. In some cases these body waves are coordinated with power and recovery
strokes of the parapodia (Gray, 1939, 1968; Clark and Clark, 1960; Clark and Tritton,
1970; Clark, 1976). The neuropodia are no longer in contact with the ground and there is
no sense of ‘‘poling’’. At least in some worms the action of the parapodia augments the
flow of water along the length of the worm and adds to the propulsive stroke (Gray,
1968; Clark and Clark, 1960; Clark and Tritton, 1970; Clark, 1976). Between these two
extreme gaits, different species of polychaetes may exhibit an intermediate gait in which
the weight of the body is still largely on the substrate, the parapodia continue to move
through their step patterns and where the extra-parapodial contractions of the longitudinal musculature cause large whole body sinusoidal movement. In some cases authors
have named and described this intermediate gait (e.g., ‘‘rapid crawling’’, Gray, 1939) in
others its existence is only implied by the description of the worm’s locomotion
(Manton, 1973). This intermediate gait in O. pugettensis (‘‘undulatory walking’’) is
characterized by the anterior segments continue to perform walking movements with
individual parapodia while the posterior segments exhibit body waves from the
contraction of longitudinal muscles. This gait is transitional along the worm’s body – as
the worm’s speed increases the fraction of the body participating in the undulatory
movement increases, moving anteriorly until the whole body is consumed in the
contractions and the animal is swimming. Although each of these three gaits operates
over a range of speeds and is uniquely and clearly identifiable, the undulatory walking
gait is transitional between the other two.
The undulatory walking gait in Ophiodromus is analogous to the trot-gallop transition
in small quadrupedal mammals in the sense that the animal switches from locomotion
where the appendages move on a relatively rigid body to using a combination of body
flexion and appendage movement to achieve propulsion. In mammals (Heglund et al.,
1974; Heglund and Taylor, 1988) (with many fewer legs than polychaetes), or an
arthropod with a stiff body (e.g., crabs) (Blickhan et al., 1993; Full and Weinstein, 1992)
the trot-gallop transition takes place at a relatively specific speed. In polychaetes such as
Ophiodromus that have many pairs of appendages and a flexible body, this transition may
take place over a wider range of speeds and at different places on the body of the
individual as its speed increases. Other species of polychaetes, depending on their
morphology and habitat, have variations on walking and swimming gaits. In the relatively
stiff-bodied amphinomid, Chloeia, swimming is achieved by an increase in the rate of the
power-stroke of the parapodia without any undulation of the body (Mettam, 1984).
Locomotion in these aquatic pedestrians is challenged by a wider variety of physical
forces and a different scale of landscape topography than is typical of the more widely
studied terrestrial vertebrates. In addition, the polychaete body is replete with structures
whose functions are largely unknown even though they may be associated with everyday
activities. The data in this paper demonstrate that joints of compound setae have a
crucial role in effective locomotion for at least some polychaetes and that considerations
of gaits and gait transition need to include the possibilities offered by the complex
modular morphology of their flexible bodies.
Acknowledgements
We would like to thank Friday Harbor Laboratories and Dennis Willows for providing
R. A. Merz, D.R. Edwards / J. Exp. Mar. Biol. Ecol. 228 (1998) 273 – 290
289
facilities as well as the Schwartz family for allowing us to collect animals from their
dock. Brian Clark, Barbara Best and Sally Woodin provided interesting, helpful
discussions about locomotion and worms. Two anonymous reviewers provided detailed
and stimulating comments; Anne Rawson and Brian Clark gave editorial suggestions.
Jacob Weiner and Peter Stoll provided advice about statistics. Emi Horikawa and Meg
Spencer of the Swarthmore Science Library helped with obtaining a variety of references
and Tom Bradley graciously helped with Russian transliteration. This work was funded
by a Swarthmore Faculty Research Grant to R.A.M. and a Howard Hughes Medical
Institute Undergraduate Biological Science Education Program Grant (No 71194505802) to D.R.E.
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