Zoological Journal of the Linnean Society,63: 145-169. With 13 figures
MayIJune 1978
Locomotory mechanisms in
Antarctic pycnogonids
FREDERICK R. SCHRAM
Department of Zoology, Eastern Illinois University, Charleston, Illinois, U.S.A.
AND
JOEL W. HEDGPETH
5660 Montecito Avenue, Santa Rosa, California 95404, U.S.A.
Patterns of walking, modes of joint movement, and individual limb diversity were analysed with
the aid of cini film of several living Antarctic pycnogonids, including the 8-legged Colossendeis
australis, C. angusta, Pallenopsis patagonica, and Nymphon sp., the 10-legged Decolopoda
australis, and the 12-legged Dodecolopoda mawsoni. Appendage musculature of several of
these species and also of the 10-legged Pentapycnon charcoti and Pentanymphon antarcticurn
was dissected. At least two distinct morphotypes were identified: a short-legged, crawling
variety (P.charcoti); and the more typical long-legged, large bodied, walking forms. No gross
differences in musculature of joints were noted in the species examined. All joints are, at least
superficially, hinge joints. The coxa-body joint is largely immobile, the coxa 1-coxa 2 joint
alone exhibits promotion-remotion and all other joints are flexion-extension joints. The
8-legged forms move in an imprecise manner, there being irregularity of leg raising and
lowering and where legs touch down in relation to the body and to other legs. The 10- and
12-legged forms exhibit more precise patterns of metachronal leg movements. Although legs
move in a basic promotion-remotion, extension-flexion mode, there is a certain degree of
twisting of a leg as it is picked up, brought forward, and set down; models indicating how such
joint movement occurs were constructed. The possibility that hydrostatic pressure is employed
in extension is considered and is found to be remote. Lateral placement of legs, orientated in
almost all directions in the horizontal plane of the trunk, achieves a versatility of movement
similar to that in crabs. Comments on pycnogonid taxonomic affinities are offered.
KEY WORDS: Pycnogonida- Antarctic-octopodous-decapodous-dodecapodous-jointsmuscles-walking-rhythm-irregularity-taxonomic
affinities.
CONTENTS
Introduction
Musculature
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. . . . . . . . . . . . . . . . . . . . . . .
146
147
145
0024-4082/78/0063-0145/302.00/0
0 1978 The Linnean Society of London
F. R. SCHRAM AND J. W. HEDGPETH
146
Joint movements
Walking patterns.
Discussion
. .
Acknowledgments
References . .
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152
157
162
167
167
INTRODUCTION
The study of functional morphology of arthropod locomotion has been one
of the major developments in zoology in recent years thanks to the impressive
researches of Manton (1950-1973). As a result, three distinct phyla of living
arthropods have been suggested : the Uniramia (containing the onychophorans,
myriapods, and hexapods), the Crustacea, and a third group which includes
the chelicerates. This arrangement has received independent confirmation
in the comparative embryological studies of Anderson (1973). The Pycnogonida, however, were largely unstudied by Manton until recently (this
Volume, p. 1) and, indeed, very few pycnogonid locomotion studies have
appeared over the years.
Cole (1901) made locomotory observations along with comments on the
biology of Tanystylum orbiculare, Pallene (= Callipallene) brevirostris, and
AnopZodactylus lentus. Most of his locomotory studies were confined to
A . lentus. He noted that only the coxa 1-coxa 2 joint experienced promotion-remotion and all joints distal to that were extension-flexion in action.
Cole largely confined himself to studying the general features of appendage
motion during swimming, but he observed that walking movements were the
same, the two locomotory phases differing only in their rapidity. He also
recorded the ability of T. orbiculare to bring all legs dorsally together over
the body to form a sort of “basket” while plummetting through the water
to the bottom.
Prell (1911) studied locomotion in four species of Nymphon (N.mixtum, N.
leptocheles, N. stromi. and N. longitarse). He noted differences between
swimming and walking in the strength of the backstroke and speed of the
beat. Prell also observed that walking tends to be more “arhythmic”. His
conclusions were much the same as Cole’s, but he also noted the general
paucity of movement among the distal three segments of a walking leg, and
pointed out the importance of frictional resistance generated by setae on the
distal leg segments during swimming. He also observed the “basket configuration” of plummetting animals.
Arita (1937) studied Nymphonella tapetis and noted its ability to dig as well
as swim and walk. However, he viewed walking and swimming as basically
rhythmic. Walking in N . tapetis was achieved with legs 2 to 4 only, while
swimming occurred with all four pair of legs. He presented a graph of the
power and recovery strokes of swimming which displayed very rhythmic
metachronal waves, but it is not clear whether this chart is a composite
impression or the result of actual timing. The digging movements reported by
Arita are the only instance reported in the literature where the ovigers are
employed to assist the walking legs in locomotion.
Morgan (1971, 1972 and this Volume, p. 171) has analysed swimming in
Nymphon gracile. His study is the most rigorous to date. I t gives consideration
to angles generated by moving joints, lift forces, and Reynolds’ numbers. His
PYCNOGONID LOCOMOTORY MECHANISMS
147
observations on leg movements are much in accord with those of Cole and
Prell, but he has reported that power and recovery strokes are equal in
duration. Morgan has also observed the “basket configuration” of plummetting.
Our own efforts in this paper are confined largely to the analysis of walking
in several Antarctic species of pycnogonids, including 8-, lo-, and 12-legged
forms. We have employed analysis of cint film as well as dissection of
specimens and have attempted to model our work on that of Manton so that
comparisons with her conclusions can he made. Our leg movement graphs are
actual timed segments from the films. Because of the general irregularity of
activity and the relatively few leg pairs we had to deal with, all leg movements
are represented graphically. In the literature cited above, there is some
vagueness about what constitutes “rhythmic” or “arhythmic” movements. We
define a rhythmic or regular series of movements as metachronal, i.e., of nearly
equal duration for all legs and proceeding in regular waves along the body.
Deviations from this are viewed by us as irregular or arythmic, i.e., no similarity
of duration of strokes or a lack of waves of movement along the leg series.
Two general body types were noted. The most common among the Antarctic
species is the long-legged variety (Fig. la-d; Fig-lO), exemplified by the
8-legged Colossendeis australis or 12-legged Dodecolopoda mawsoni. In these
forms the legs are essentially stilts and suspend the body some distance from
the substratum. The other type is short-legged (Fig. l e g ) of which
Pentapycnon charcoti is the only example in our study. In these latter forms
the legs and the constituent segments are short and somewhat prehensile and
apparently adapted to an epizoic life-style. Some differences exist in the
musculature of these two types. Unfortunately, we had cint film of species of
the long-legged variety only and so could not establish whether the modes of
locomotion of the two types were different.
MUSCULATURE
To establish a basis for the terminology used in this paper, the pycnogonid
walking leg is considered to have the following structure (Fig. 2a). The walking
legs articulate with a lateral cylindrical extension of the body. Typically the
three most proximal segments are short (coxa 1, coxa 2, coxa 3). These coxae
are followed distally by three long segments (femur, being most proximal;
patella; and tibia). The three most distal segments (tarsus 1, tarsus 2, and the
terminal pretarsus) can vary considerably in size from species to species. In this
paper a joint is referred to by a hyphenation of the adjacent segments, e.g., the
first joint is body-coxa 1, the second is coxa l-coxa 2, and so on.
To facilitate the joint and muscle descriptions, those of Colossendeis
australis are presented (Fig. 2) as typical. Any variations noted in other species
are indicated. The body-coxa 1 in C. australis is apparently barely moveable;
there are no definite pivot points and the arthrodial membrane is very much
reduced. However, in spite of this apparent immobility, there is a set of dorsal
and ventral muscle bands which originate on the lip of the opening of the
cylindrical body extension with the trunk cavity and insert on the dorsal and
ventral rims of coxa 1.
Coxa 1-coxa 2 hi the only promotion-remotion pivot joint of the leg, having
prominent points of articulation middorsally and mid-ventrally with extensive
F. R. SCHRAM AND J. W. HEDGPETH
148
b
d
e
f
Y
Figure 1. a, b. Colossendeis australis: a, oblique view of the whole animal; b, dorsal view of
the trunk with distal portions of the walking legs removed. c , d. Dodecolopoda mawsoni:
c, oblique view of the whole animal; d, dorsal view of the trunk with the distal portions of
the walking legs removed. eg. Penrapycnon charcoti: e, dorsal oblique view of the whole
animal; f , dorsal view of the trunk with the distal portions of the walking legs removed; g,
lateral oblique view of the whole animal. Note the squat profile as opposed to that of the
long-legged forms in a and c.
PYCNOGONID LOCOMOTORY MECHANISMS
149
a
d
et
et
Figure 2. a-f. Colossendefs austr~li.~:
a, anterior view of a walking leg; b, anterior view of most
proximal segments displaying the cl-c2 promotor muscles (remotors identical) ; c, ventral
view of the distal coxal segments with the flexor muscles of c2-c3 and c3-femur; d, dorsal
view of distal coxal segments. Note the chevron extensor muscles of c2-c3; e, dorsal view of
femur-patella joint with short extensors; f, ventral view of femur-patella joint with long flexor;
g, Decolopoda australis, dorsal view of distal coxal segments with chevron extensors at c2-c3
and c3-femur. B, body extension; C, coxa; F, femur; P, patella; T, tibia; Ts,tarsus;Pt, pretarsus; pr, promotor; rm, remotor; et, extensor; fl, flexor.
150
F. R. SCIIRAM AND J. W. HEDGPETH
arthrodial membranes to facilitate movement. The promotor and remotor
muscles are equal in size (Fig. 2b). These muscles each have three heads: a
medial head taking origin on respectively the anterior or posterior surface of
the cylindrical extension of the body, and dorsal and lateral heads taking origin
on the dorso-lateral and ventro-lateral surfaces of coxa 1; all three heads of
each muscle have a common insertion on either the anterior or posterior rims
of coxa 2. All the other joints of the leg are extension-flexion in action, i.e.,
dorso-ventral or latero-medial in movement depending on orientation of the
joint at any particular time.
The flexor and extensor muscles of coxa 2-coxa 3 are different from each
other, The dorsal extensor (Fig. 2d) is actually two muscle bands together
forming a chevron; the origins are in the antero-dorsolateral and posterodorsolateral fields of coxa 2. Their insertions are adjacent to each other, but
separate along the dorsal, proximal rim of coxa 3. The coxa 2-coxa 3 flexor
(Fig. 2c) is Y shaped. The muscle fibres originate on the antero-ventrolateral
and postero-ventrolateral fields of coxa 2 and insert on a tendon which in
turn crosses the joint and inserts on the ventral proximal rim of coxa 3.
The coxa 3-femur muscles are similar to each other. The extensor is a
shallow Y shape and similar to the coxa 2-coxa 3 flexor (Fig. 2d). The two
separate muscle masses insert along a tendon which in turn inserts on the
dorsal, proximal rim of the femur. The coxa 3-femur flexor is longer than
the extensor but still basically Y-shaped with a very short tendon of insertion
on the ventral proximal rim of the femur.
The femur-patella and patella-tibia muscles are similar to each other in
arrangement. The extensors (Fig. 2e) are relatively short with a series of
fibres originating on the distal half of the dorsal surface of the femur and
patella, inserting on a tendon extending the length of the distal half of these
segments. The tendons in turn insert on the proximal rims of the patella and
tibia respectively. The flexors exhibit the same general form as the extensors
but their fibres take origin along almost the entire length of the femur and
patella.
The tibia-tarsus joint has no extensor, but only a flexor, which is similar to
that of the femur and patella and which originate along virtually the entire
length of the ventral surface of the tibia. The tarsus 1-tarsus 2 joint has no
muscles, while the tarsus 2-pretarsus joint has equally well developed extensor
and flexor muscles with fibres taking origin along the whole length of the
dorsal and ventral surfaces of tarsus 2. These insert on a tendon, which in turn
inserts on the rim of the pretarsus.
The Antarctic pycnogonids studied all appear to have a basically similar
musculature to that presented above for C.australis. Even a relatively distinct
form such as Pentapycnon charcoti does not differ substantially in the basic
pattern. Although no cine film of P. charcoti was available to analyse walking,
all the long-legged forms from which film was available displayed no differences
in the method of leg and joint movement-a functional similarity thus reflecting the anatomical similarity.
Pallenopsis patagonica possesses some segment and joint variations in the
coxal region (Fig. 3a). Of all the species examined, P. patagonica is the only
one that has a moveable body-coxa 1joint. The articulation points and arthrodial membranes are moderately well developed and capable of some movement.
PYCNOGONI D LOCOMOTORY MECH AN1 SMS
151
a
b
T
F
d
I
1
h
Figure 3. a-e. PaIlenopsis patagonica: a, proximal segments of the leg showing the differing
sizes of the coxae; b, distal segments of the leg with a small ring-like tarsus 1;c, anterior view of
proximal coxal segments with a Yshaped promotor (remotor identical); d, dorsal view of
femur-patella joint with short extensor; e, ventral view of femur-patella joint with short flexor.
f-h. Pentapycnon charcoti: f, anterior view of walking leg, note generally short, stout segments;
g, anterior view of proximal coxal segments with fan-shaped promotor on cl-c2 (remotor
identical); h, dorsal view of proximal segments of leg displaying the generally short chevron
or quasi-chevron extensors of the joints. Conventions as in Fig. 2.
152
1;.
R . SCHKAM A N D J . W. HEDGPETH
Probably as a result, the coxa 1-coxa 2 promotor and remotor muscles lack
the medial heads that take origin on the cylindrical body extensions (Fig. 3c).
P. patagonica also possesses a long coxa 2, but this length has not been matched
with an increase in coxa 2-coxa 3 muscle development. In addition, tarsus 1 is
reduced to a short ring between the tibia and tarsus 2. The flexors (Fig. 3e) of
the femur, patella, and tibia of P. patagonica are less well developed than those
of C. australis, occupying approximately the distal half of the segments only
and thus being only slightly more developed than the extensors (Fig. 3d) of
the femur and patella.
Decolopoda aitstralis presents few differences from the muscle arrangements of C. australis except that the tibia-tarsus 1joint does have an extensor,
the fibres of which originate along the distal half of the tibia and insert on a
tendon which itself inserts on the proximal rim of tarsus 1. In addition, both
the coxa 2-coxa 3 and coxa 3-femur extensors exhibit the chevron arrangement seen in the coxa 2-coxa 3 extensors of C. australis, i.e., two muscle
bands with adjacent but different insertions (Fig. 2g). Dodecolopoda mawsoni
is identical to Decolopoda australis in its leg musculature.
Pentapj*nzon (Fig. 3f-h) has shorter, stouter leg segments and also shorter,
stouter muscles different from those of C. australis. The coxa 1-coxa 2 promotor and remotor muscles (Fig. 3g) are single broad bands taking origin on
the anterior and posterior inner surfaces respectively of coxa 1. All the
extensor muscles of the leg are wide and have adjacent but separate insertions
with the chevron arrangement seen only in the most proximal joints of the
long-legged species (Fig. 3h).
Pen tapiwzon is probably a sedentary benthic organism, like the octopodous
species of Pycnogonum. They feed as ectoparasites of sea anemones, tunicates
and other soft-bodied invertebrates, and apparently use their legs as grasping
appendages, sinking their tarsal claws into the host organism while piercing
the integument with their proboscis. Living specimens of Pycnogonum move
seldom and very slowly in aquaria, even when separated from their food
source.
JOINT MOVEMENTS
Analysis of the cine film of long-legged forms revealed that the joints themselves moved in an identical manner whether in 8-, 10, or 12-legged
forms. The body-coxa joint is virtually immobile (except in Pallenopsis
patagonica, where some dorso-ventral movement occurs). The coxa 1-coxa 2
joint is the only promotion-remotion joint in the leg and is equipped with the
largest musculature of any of the joints. Though this is the only joint to move
the legs anteriorly and posteriorly it illustrates a general mechanical principle
of pycnogonid legs: although any joint may have a relatively small degree of
movement in and of itself, any motion is magnified by the great elongation of
the entire leg, largely achieved by the long femur, patella, and tibia. For
example, one of the C. australis specimens had a trunk length of 2 cm and a leg
length of 9.6 cm. In a sequence of modest coxa 1-coxa 2 actions the distal end
of coxal 2 might move 0.2 cm in an anterior to posterior distance and this
0.2 cm movement was translated into a movement of 4 cm at the distal tip of
the pretarsus.
All the other joints on the leg have extensor-flexor movement. Yet move-
PYCNOGONID LOCOMOTORY MECHANISMS
153
ments of the joints are not equal. The three most distal segments of the leg,
tarsus 1 + 2 and the pretarsus, typically move as a unit with little joint
bending, while the tibia-tarsus 1 joint usually bends less than any of the
more proximal joints. However, extension and flexion do occur at all joints to
some extent, although the tarsus 1-tarsus 2 joint has no musculature and the
tibia-tarsus 1 may have a flexor only. Extension was observed at these joints
while the leg was rising. This phenomenon of extension in arthropod joints
lacking extensor muscles has been attributed to hydrostatic pressure in arachnids (Ellis, 1944), but the structure of the pycnogonid leg and the circulatory
system available do not indicate that there are mechanisms available for leg
extension by hydrostatic pressure, although it could be possible. The greater
drag of a structure in sea-water would require more force than for a similar
structure in a terrestrial animal. Probably, in such delicate distal segments as
the tibiae and tarsi of pycnogonids, extension is achieved by the elastic action
of the cuticle at the joint, as suggested by Wainwright et al. (1967) for arthropod joints under conditions of light loading.
The pycnogonid walking legs do not move entirely in a strict promotionremotion, extension-flexion mode. There is a slight twisting of the leg. In this
motion the dorsal surfaces of the distal segments come to face slightly anteriorly on the power backstroke and come to face slightly posteriorly on recovery
as the distal tip is raised and brought forward. The method of achieving this
might seem difficult to explain with an arrangement and function of joints
described above. Close study of the cint film revealed that the area of origin of
this peculiar motion was localized in the coxal joints. The arthrodial membranes are very greatly developed on these joints to the degree that, although
the articulations are hinge joints, the spacing of the pivot points is such that the
membranes allow a measure of twisting of one segment on the other. The
development of the extensor muscles at these joints does in fact allow for a
natural twisting to take place. It will be recalled that the extensors in this area
are developed as two adjacent muscles in a chevron form whose insertions
flank the middorsal line. Models were constructed of paper tubing segments,
tape arthrodial membranes, and string muscles (Fig. 4). Placement of the
insertion of the twine extensor and flexor at the mid-dorsal and mid-ventral
points respectively resulted in a simple “up-down” or extension-flexion movement (Fig. 4a-b). Such an arrangement replicates the condition in the more
distal joints of the pycnogonid leg. When the twine extensor was arranged as a
chevron pair with adjacent insertions, various movements were possible. If both
parts of the chevron were “contracted” simultaneously a simple upward or
extensor movement resulted. If the posterior member of the pair was
“contracted” (Fig. 4d), the segment of insertion moved upward and posteriorly
with a slight counterclockwise twist as viewed from the body to the distal tip
of the leg. If the anterior member was “contracted” (Fig. 4e), the segment of
insertion moved upwards and anteriorly with a slight clockwise twist as viewed
from the body looking towards the leg tip. Thus, the differential contraction of
the extensor chevron pairs, combined with a generally “twistable” joint can
achieve the twisting motion of the leg. Although such twisting is slight at the
site of the joint, it also may be magnified along the leg depending on the leg
posture. The net result of this twisting is to increase somewhat further the
promotion-remotion movement at the distal end of the leg.
F. R. SCHRAM AND J. W. HEDGPETH
154
a
Figure 4. a, b. Movement of joints with muscles with a single tendinous insertion: a, resting
state; b, contraction of muscle to move joint equally at lateral hinge points. c, d. Movement
of joints with chevron-like extensors with adjacent but separate insertions; c, resting state;
d, contraction of the right muscle with slippage at hinge joint, distortion of the arthrodial
membrane, and a slight rotational movement dorsally and to the right; e, contraction of the left
muscle with slippage at the hinge joint, distortion of the arthrodial membrane, and a slight
rotational movement dorsally and to the left.
The mechanical possibilities of joint movements have been recently examined by Wainwright et al. (1976), who described the various movements or
actions of joints in terms of “degrees of freedom”. There are six ways in which
joints may move: three of displacement, parallel to the coordinate axes, and
three of rotation (Fig. 5 ) . Another alternative exists in that the joint may not
move at all, that is, remain rigid. Most biological systems involve a choice of
three types of-joint movement: rigid, one degree of freedom, or six, but in the
latter type of joint the movements are usually restricted in one way or another
so that there may not effectively be more than three degrees of freedom.
According to this mechanical description, the twisting or rocking movement of
coxal joints is simply an accommodation of another degree of freedom within
the articulation. Since additional movements require additional or more highly
developed musculature, we should expect to find such joints to be capable of
housing the muscles, as in coxal joints of insects and arachnids, and, obviously
in those of pycnogonids.
The joints coxa 2-coxa 3 and coxa 3-femur exhibit an unusual degree of
flexibility. The typical maximum degree of extension of the more distal
joints is a straight configuration and at most only a slight flexion is main-
PYCNOGONID LOCOMOTORY MECHANISMS
155
RxU
Figure 5. Degrees of freedom of a joint. There are six possible degrees of freedom: three of
rotation (R,,,, R,,, R y z ) and three of displacement (D,, D,,, Dz).From Wainwright et al.
(1976).
tained (Fig. 6a). However, the two joints flanking coxa 3 can “extend” in
such a manner as to bring the distal ends of paired femora together above the
animal (Fig. 6d). The extreme contraction of these extensors will bring the
femur and coxa 2 almost, but not quite, to a parallel arrangement.
The functional significance of this extreme extension is related to two
factors. Pycnogonids can move forward, backward, or sideways without reorientating the trunk. In the lateral movements the legs on opposing sides
of the body function in a push-pull manner. In pushing to move laterally the
femur is brought to a vertical or dorsally procumbent position in order to
place the end of the pretarsus as close under the body as possible. In pulling,
the leg on the other side of the body extends the segments out as far laterally
as possible before setting the pretarsus down. Thereafter, flexion of the distal
joints pulls the body laterad, the pretarsus remaining down until the body is
positioned almost over it, requiring the extensors of coxa 2 joints to bring
the femur to a vertical (or even procumbent) position. This extreme extension
thus allows the lateral movement to be achieved by a few giant strides rather
than several shorter ones.
The second factor is that of “leg resting”. When standing still, or even during
movement, legs are sometimes brought to a vertical position and held there.
As will be discussed below, pycnogonids can walk quite effectively while
employing fewer than their full complement of legs. In addition, when plummetting or drifting through water, Colossendeis will bring all its legs into a
position above the body, forming a sort of “basket”, until the bottom is
reached. This basket plummetting has been noted by several other workers.
This posture was illustrated by Bouvier (1917: pl. 2, fig. l), although the
drawing may have been made from a preserved specimen. In Pallenopsis
patagonica the legs are pulled together even move compactly above the trunk,
a reflection perhaps of the dorso-ventral movement possible between the bodycoxa joint mentioned above. The adaptive value of this action is obvious, as it
enables the animal to sink rapidly to the bottom. Living Pallenopsis, when
156
F. R. SCHRAM AND J. W. HEDGPETH
Figure 6. Movements of proximal leg joints in Colossendeis australis; a, with leg extending
laterally as far as possible for maximum stride, femur angle with body plane 20”;b, typical
position of leg for minimum stride or in position of recovery stroke; c , maximum contraction
of the proximal extensor muscles, femur 40° from the vertical plane, to bring legs into d, the
“basket position” above the body. Other conventions as in Fig. 2.
dropped into the aquarium, immediately assume this basket posture until they
reach the bottom of the tank whereupon the legs are extended and the animals
begin to walk on the bottom (pers. obs. JWH). Colossendeis was much slower
to assume this dorsal basket posture and in some cases did not do so at all in
the time it took the animal to sink about two feet. Another reaction, of the
opposite kind, was noted in aquarium specimens of Colossendeis in which the
legs were bowed ventrally, to form an open sort of basket; specimens assuming
this posture rolled about the bottom of the tank when the water was stirred or
a slight current was entrained by the incoming water or air.
PYCNOGONID LOCOMOTORY MECHANISMS
157
WALKING PATTERNS
In analysis of the cink film it became evident that the 8-legged forms
differed behaviourally from the 10- and 12-legged varieties. Only longlegged, large-bodied forms could be studied. The difference is that octopodous
forms have, generally, more varied gaits, as opposed to the more regular and
precise gaits of the polypodous species. This is undoubtedly related to the
need for closer coordination of ten or twelve legs. The relative length of the
body in polypodous forms is no different from that of octopodous forms.
Thus, in effect, polypodous forms crowd more legs into the same relative peribody field than do the octopods. Thus, the necessity for more precisely controlled gaits is crucial. It must be pointed out, however, that all the pycnogonids photographed were on a somewhat unnatural substratum, either smooth
glass or fine gravel, in contrast to the soft mud of the localities in which these
animals live. However, they do encounter stony bottoms in other parts of their
range, e.g. McMurdo Sound, and so it is most probable that the motions
observed were not very different from those occurring under natural
conditions.
Octopodous species can be described as casual in their mode of walking.
Legs are lifted up for several leg cycles, or put down and left down to drag
along while other legs operate. It is not uncommon for legs of octopods to
overlap and tangle with each other. Nor is there any regularity as to how long a
leg may stay down on a power stroke and how long a recovery stroke may take.
A power stroke may last 20 seconds or 0.5 seconds and the same is true of a
rising recovery stroke. The maximum arc any leg can subtend is approximately
90”. A power or recovery stroke may cover the maximum arc, or something
near it, or it may subtend only a few degrees. Lateral legs may operate in a
fully extended position while moving forward or backward and a recovery
stroke may then, by contraction of the coxa 3 and femur extensors, bring
the leg into a more flexed orientation without a break in stride.
Many of these features can be seen in the graphs of the walking of Colossendeis australis and Pallenopsis patagonica in Figs 7 and 8. The six sequences
illustrated were selected from a series of graphs of cinC film, being chosen as
representative sequences of patterns generally evident in walking octopodous
py cnogonids.
Some walking sequences of Colossendeis australis are shown in Fig. 7.
Irregularity in the patterns of power and recovery strokes in straightforward
walking are evident in Figs 7a and 7b. There are no persisting metachronal
waves, some legs having two power strokes for every one of an adjacent leg;
nor are opposite sides alike. Figure 7a displays left legs 3 and 4 operating in a
rhythm different from that of all the others and not contributing significantly
to locomotion in their drag phases. A “five point walk” with left legs 3 and 4
held in a raised position, while right leg 4 is dragging, is indicated in Fig. 7c.
The other appendages in this case display metachrony, although, again, irregularities are evident in the length of the power strokes.
Pallenopsis patagonica walking sequences are illustrated in Fig. 8. The
specimens generally moved at a slower speed than did C. australis. The longer
power strokes display more persistent metachrony, but again irregularities are
introduced by extra short or extra long power strokes. These irregularities are
F. R. SCHRAM AND J. W. HEDGPETH
r
--I
2\--
’
’
”
’
,
+-----
- 2
Figure 7. Graphical representation of the typical walking gaits of Colossendeis australis. See
text for discussion. (Horizontal axes show time in seconds.)
evident in C.australis and other forms, but are magnified by the slower gait of
P. patagonica. Figure 8b again reveals the pycnogonids’ ability to walk without
using all legs; in this case a “four point walk” is executed with left legs 3 and 4
permanently raised and right legs 3 and 4 dragging. The use or non-use of a leg
does not seem to affect in any way the ability of a particular pycnogonid to
move in either forward, backward or lateral directions, or its ability to shift
direction freely without breaking stride. This is shown in Fig. 8a, where a backward and circling move to the right flows easily into a forward walk (there was
a short break in the film that interrupted exact timing from beginning t o end
of the sequence).
Decolopoda australis shows an example of a polypodous gait. The metachronal pattern is obvious in Fig. 9 . Compared to octopods, there is less variation in the duration of power and recovery strokes and less variation in the
subtended arc of these strokes. The pretarsi are lifted and set down at times
PYCNOGONID LOCOMOTORY MECHANISMS
Backward motion
& circle to right
159
Slow straight forward walk
0
3
Left
4
A
0
Left
20
3
~
7
--4-
4
I-----
4
?
----
Figure 8. Graphical representation of the typical walking gaits of Pallenopsis patagonica.
(a contains a break in the sequence of undetermined length, which precludes exact determination of the sequence times.)
0
40
Figure 9 . Graphical representation of the typical walking gaits of Decolopoda mawsoni.
and in positions when and where there will be little interference with the
operation of other legs. All legs participate in walking, i.e., legs are not held up
off the substratum or dragged along while other legs continue to operate
(Fig. 9 ) . The particular animal photographed had all five legs on the left side
intact. The legs on the left displayed metachronal rhythm with waves of power
strokes passing down the sequence of legs and overlapping nicely with adjacent
160
F. R. SCHRAM AND J. W. HEDGPETH
Figure 10. Decolopoda australis. Sketch of living animal by J.W.H., from notes and photographs
taken at Palmer Station, Antarctica.
legs. The right side had leg 4 missing and it is interesting to note that, although
there was some irregularity, the wave of power strokes generally passed over the
missing fourth leg and was transmitted to the fifth.
The same general pattern was evident in film of Dodecolopoda mawsoni;
the legs moved in a clearly metachronal pattern. The nature of the tanks the
animals were in and the placement of the camera precluded gathering exact
timing data on this species, but the general features noted above for Decolopoda were observed in Dodecolopoda. One interesting feature especially well
displayed by Dodecolopoda mawsoni occurs when the animal is tightly confined or stands in one place. The body is never quiet but executes a four to six
point “standing walk”, with six to eight legs held in the basket position above
the body. Other species, whether with 8 or 10 legs, engaged in the “standing
walk” while remaining in position, some legs treading up and down but at least
a few remaining raised above the body.
The method of leg movements employed in swimming appears to be a little
different from that used in walking.
The characteristic lateral displacement of pycnogonid legs on the body is
important for movement. In this regard the lateral orientation is reminiscent
of what has happened in many other arthropod groups (Fig. 11). Primitive
crustaceans (Fig. 1l a , b) have legs originating directly ventrally along the
midline, while forms with an ability to execute a variety of gaits, such as
palinuran lobsters, brachyuran crabs (Fig. 1lc), or pygocephalomorph mysidaceans have a lateral displacement of their legs (Schram, 1974). In uniramians
a more generalized arrangement occurs in diplopods (Fig. 1le) with legs arising
midventrally while more versatile forms such as chilopods (Fig. l l f ) displace
PYCNOGONID LOCOMOTORY MECHANISMS
161
C
syncarid
Hutchinsoniella
true crab
f
e
diplopod
trilobite
chilopod
h
eurypterid
Limulus
i
arachnid
pycnogonid
Figure 11. Body cross sections of various arthropods demonstrating the tendency in many
groups to move the legs from a ventral position, which does not allow much versatility in leg
movement, to a position lateral to the body mass and allowing more versatility in movement.
a-c, Crustaceans; d, trilobitomorph; e and f, uniramians;g-i, chelicerates; j, pycnogonid.
the legs laterally (Manton, 1965). Trilobites (Fig. l l d ) have legs directed
essentially ventro-laterally. Other chelicerates, to which the pycnogonids are
related, such as xiphosurans (Fig. log), eurypterids (Fig. l l h ) , and arachnids
(Fig. 1li) all have legs arising from the ventral midline.
The lateral orientation of pycnogonid legs achieves what is seen in these
other arthropod groups, viz., a great versatility in movement. It was common
for the pycnogonids in our study to change directions of travel abruptly and
easily without reorientating the body or breaking stride. Legs are orientated in
all directions on the trunk. In forward movement in octopodous forms, such
as Ammothea, Colossendeis, or Pallenopsis, the first and fourth pairs of legs
operate almost exclusively with extensors and flexors to “push-pull” parallel
to the main axis of the body, while the second and third pairs of legs are
directed laterally and, operating perpendicular to the body long axis, employ
the promotion and remotion muscles and the twisting action to propel the
animal. Confrontation with another pycnogonid, a barrier or obstru.ction, or
even apparently random chance shifts will cause a change, such that pairs 1 and
4 predominate i n promotion-remotion while 2 and 3 take on a push-pull
extension-flexion action.
Another peculiar phenomenon was witnessed in Decolopoda australis.
162
F. R. SCHRAM A N D J. W. HEDGPETH
When the animal walked some distance in a straight line, the body axis changed
its orientation, i.e., although the direction of travel remained the same, the long
axis of the trunk came to lie 15’-20” off the direction of travel. The animal appeared and behaved normally in all other respects.
DISCUSSION
This study is a response to the questions raised by large octopodous and
polymerous Antarctic pycnogonids: how do they move, and is there any
difference between coordination and movement in the 10- and 12-legged
forms as compared with those having eight legs? These questions arise from
observations of small intertidal species, usually encountered as small individuals tangled among hydroids and bits of seaweed in the miscellany brought
back in a collecting bucket from a field trip. When shaken or teased out of their
refuge in a sorting dish the animals appear to stumble aimlessly along the
bottom until they find something to cling to. If they happen upon another
pycnogonid they tangle together in an almost inextricable mass. Others, of the
squat, lethargic genus Pycnogonum, appear to do almost nothing, remaining
immobile. Everyone who has observed the motions of crabs, insects, and
spiders is struck by the obvious coordination of movements of these animals.
Thus, the first question is: are pycnogonids as aimless and uncoordinated as
they seem to be on the first impression gained from the intertidal forms seen in
a sorting dish? The second question, posed by the large Antarctic forms, is:
does the pattern of movement of the polymerous species shed light on the
basic movement of the small intertidal species?
Previous studies of leg movement in pycnogonids have been concerned for
the most part with the actions of swimming. Among large pycnogonids, such as
Colossendcis, the animals may be moved easily by currents near the bottom, as
was observed by Monod (1954) in one of the early bathyscaphe dives. Quite
possibly the large deep sea pycnogonids may not move about very much under
their own power, or they may proceed very slowly. Several deep sea
photographs of large pycnogonids show them in apparently stationary posture
with all tarsi standing literally “tip-toes” on the bottom (see Heezen &
Hollister, 1971: figs 2.75 and 2.76).
Our studies, although based for the most part on cinC film of large
pycnogonids in aquaria on uncharacteristic substrata, indicate that the
fundamental metachronal pattern inevitable in metarneric animals, as
demonstrated by studies of motion in annelids and arthropods in general,
clearly persists in the polymerous pycnogonids, but is obscure in the
octopodous species. There are five or six well defined decapodous species and
two dodecapodous species of some 600 species of pycnogonids known and it is
evident from the data presented that these large polymerous forms exhibit a
higher degree of coordination in their leg movements than the often very
similar octopodous forms. Unfortunately, we know nothing of the natural
history, reproduction, or early developmental stages of these large
pycnogonids.
We may then summarize our observations on locomotion in pycnogonids as
follows :
PYCNOGONID LOCOMOTORY MECHANISMS
163
1. Pycnogonids typically execute somewhat inaccurate and variable stepping
movements. While the decapodous forms move in a somewhat more coordinated fashion than octopodous forms, this may be either aberrant or specialized
if, as seems possible, the octopodous condition is primitive.
2. The promotor-remotor action is limited to one joint. The r81e of this
action can be very minor because the radial arrangement of legs on a pycnogonid trunk can allow the animal to move without any promotion-remotion
activity depending on the direction of travel and use and non-use of individual
legs.
3 . The twisting action in a single leg movement-comparable with but slightly
different from the “rocking” described by Manton, is important in supplementing the promotion-remotion movement.
4. The mechanisms of extension in those joints lacking extensor muscles are
not clearly understood yet, and could not be demonstrated in our material. It
may possibly involve hydrostatic pressure, as has been suggested for some
terrestrial arachnids.
All of these features have been discussed by Manton (1973) and Ellis (1944)
as important features of locomotion in various chelicerates, but the degree of
relationship between arachnids (chelicerates in the broad sense) and pycnogonids is difficult to arrive at on the basis of functional morphology of locomotion alone (Hedgpeth, 1954).
When the polymerous condition in pycnogonids first came to general notice
at the turn of the century, long after the discovery of Decolopoda australis by
Eights (1835), it was suggested by Cole (1905) that Decolopoda represented
the most primitive state of pycnogonids, and a possible ancestral type. I t does
seem possible that the decapodous condition may be very old, as suggested by
the Jurassic fossil discussed by Hedgpeth elsewhere in this volume. However,
this possibility still does not resolve the problem discussed by Hedgpeth & Fry
(1964) of the nature of polymery in these animals, i.e., whether polymery is a
repeated “sport” resulting from metameric instability, or is a phenomenon of
polyploidy. The solution of these questions still waits on adequate living specimens and on the application of refined techniques of observation and preparation of material. It is obvious, however, that the addition of ganglia (Fig. 12b,
c and f) accompanies the addition of metameres or somites, so that the components of the nervous system needed for locomotory coordination are available in the polymerous forms, whether they be primitive survivals or recent
aberrations. In any event, this polymerous condition is unique among arthropods in the broader sense, however we may choose to recognize higher categories of classification.
It seems most probable that the need for synchronization of appendages in
locomotion has been diminished by the quasi-sedentary, ectoparasitic habit of
most adult pycnogonids. In a sense this was suggested by Lankester (1910) in
his essay on the classification of the Arachnida: “The reduction of the organism to seven leg-bearing somites, of which the first pair, as in so many euArachnida, are chelate, is a form of degeneration connected with a peculiar
quasi-parasitic habit . . .” (p. 301). In this famous article on the Arachnida,
Lankester recognized under the Class Arachnida, the Grades Anomomeristica
and Nomomeristica. The first grade included the trilobites, the second was
divided into the subclasses Pantopoda and Euarachnida. Thus, he did concede
F. R. SCHRAM AND J. W. HEDGPETH
164
that the pycnogonids stood aside from all the other arachnids, or “EUarachnida”. Zoological opinion has removed the trilobites from this array,
and for the most part agrees that the pycnogonids stand quite apart from the
arachnids sensu stricto.
Cole (1905), while commenting on the possible primitive nature of the
decapodous condition in the pycnogonids, criticized the classification proposed by Lankester in 1902 (see Lankester, 1910) in his article for the Encyclopedia Britannica, but concluded nevertheless: “It is thus obvious that
naturalists are no nearer to agreeing today upon the systematic position of
the Pycnogonida than they have been at any time in the past” (p. 414). An
interesting additional commentary is provided by Savory (1964) in his general
work on arachnids: “. . . the association of the Pycnogonida [to the Arachnida]
is close enough to justify a short consideration of these animals. The similarity
is from the first suggested by the fact that nearly all Pycnogonida possess
four pair of legs; if the five pairs which are found in Pentanyrnphon and
Pentapycrzon, or the six pairs in Dodecolopoda, were common among other
families the distinctive nature of the sea spiders would no doubt have been
more readily admitted.” (p. 216). After suggesting that perhaps the Pycnogonida “like Arachnida and Merostomata . . . have selected and preserved a
different set of alternative characteristics”, Savory concluded : “If this be
true, the misleading resemblance to Crustacea becomes intelligible, and a
slightly closer relationship to Arachnida can be admitted without the need
to assume that all points of similarity are due to convergence. And finally
the Pycnogonida can justifiably be placed in a subphylum by themselves
without the feeling that by doing so the problem of their affinities is merely
being evaded.” (p. 218).
Given the current discussion of the possibility the existence of several phyla
of arthropods, we would concur with Savory.
It should be no surprise, therefore, that in the second edition of
“Arachnida Savory (1977) has resolved the matter by recognizing the Pycnogonida as a subphylum of equal rank with the Chelicerata (agreeing with
Hedgpeth, 1955) and thus distinct from the Arachnida, and removing this
aberrant group from his lifelong and loving concern with the terrestrial archnids. However, Savory does not agree with Manton, “whose opinions can never
be neglected” (1977, p. 4), that the arthropods are polyphyletic, but staunchly
begins his second edition of the book with “The Phylum Arthropoda”.
The problems of the exact affinities and phylogeny of pycnogonids still
remain; neither Manton in her series of studies on arthropod locomotion and
jaw structure (1950-1973) nor Anderson’s (1973) investigation of embryology
of annelids and arthropods were concerned with pycnogonids. Other investigators, in an attempt to seek a solution to this issue, have addressed the
problem of homologies of head segments and innervations (Manton, 1949;
Beklemishev, 1969; Bullock & Horridge, 1964), but all that can be stated without any debate is that pycnogonids have no deutocerebrum, a condition they
share with chelicerates (Fig. 12a, d and e).
The curious problem alluded t o above, of the matter of leg joints lacking
extensor muscles, might be elucidated by investigations along the lines suggested by the work of Firstman (1971). He studied the morphology of the
chelicerate circulatory system, with especial reference to the condition of the
”
PYCNOGONID LOCOMOTORY MECHANISMS
b
C
m
P
f
Figure 12. Central nervous systems of pycnogonids. a, Nymphon sp. (modified from Wirtn,
1918),brain and anterior nerves in relation to the oesophagus; b, trunk ganglia of Nymphon
pixillae (modified from Henry, 1953); c, trunk ganglia of Dodecolopoda mawsoni; d, brain and
anterior nerves in relation to the head anatomy of D. mawsoni; e, brain and anterior nerves in
relation to the head anatomy of Colossendeis australis. f, trunk ganglia of C. australis. spg,
Supraesophageal ganglion; sbg, subesophophageal ganglion; cec, circumesophageal commissure;
opn, optic nerve; chn, chelifore nerve; rn, rostral nerve; ppn. pedipalp nerve; on, oviger nerve;
e, oesophagus; chd, chelifore diverticulum; ppd, pedipalp diverticulum; ch, chelifore; pp.
pedipalp; 0,oviger; 1st wl, first walking leg; pr, proboscis; plm, proboscis levator muscle.
165
166
F . R. SCHRAM AND J. W. HEDGPETH
E
pre-chelicerat e
Figure 13. Postulated phyletic relationships of some Chelicerates (modified from Firstman,
1971), demonstrated by cross sections through the anterior trunk regions to display the relationships of Dohrn's membrane and the endostemites to the general trunk anatomy. a, Hypothetical pre-chelicerate stage suggested by certain pycnogonids; b, Colossendeis; c, EndezS;
d, Pycnogonum ; e, hypothetical ancestral merostome-arachnid; f, Limulus; g, hypothetical
ancestral arachnid; h, tick; i, typical tracheate arachnid; j, Scorpionida; k, typical pulmonate
arachnid; 1, lungless spider. a, aorta; g, gut; n, central nervous system; DM, Dohrn's membrane;
PVM, penneural vascular membrane; NIO, neural intestinal omentum; H, horizontal membrane;
E , endostemite; VS, ventral suspensor muscle; DS, dorsal suspensor muscle; TM, transverse
muscle; PIM, peri-intestinal membrane; TS, thoracic sinus.
PYCNOGONID LOCOMOTORY MECHANISMS
167
endosternite anatomy. Unfortunately, this work, based on gross dissections, has
not been verified by more critical microscopic sections, but it does suggest that
this structure, which Firstman considers to be represented in pycnogonids by
Dohrn's membrane (Dohrn, 1881; Cole, 1910), might have some function in
maintaining internal hydrostatic pressure. Firstman was unable to find a
functional heart in Pycnogonum and Pentapycnon, which suggests that there
could be some relationship between the more discrete development of leg
musculature in these genera and a modified circulatory system. On the basis
of his observations on a representative suite of chelicerates, Firstman places
the pycnogonids as an early offshoot of the primitive stock giving rise to the
chelicerates (Fig. 13). Our findings suggest to us that that hypothesis might be
investigated profitably. Obviously, here is one more possibly rewarding loose
end meriting further consideration and study.
ACKNOWLEDGMENTS
The following people and agencies greatly assisted the genesis of this study:
The specimens for dissection and the cine film were procured by W. G. Fry,
J. C. McCain, J. W. Hedgpeth, and S. V. Shabica at McMurdo Sound and
Arthur Harbor, Antarctica during the tenure of various grarits from the United
States Antarctic Research Program of the National Science Foundation to
JWH. The analysis of the film and dissections were done under the aegis of
National Science Foundation Grant GB-35484and grants from the Eastern
Illinois University Council on Faculty Research to FRS. Miss J. Stanis assisted
in data processing and R. Fleeharty and N. Bartlett assisted in the preparation
of th'e illustrations.
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