Zoological Journal of the Linnean Society, 63: 1-21.With 11 figures
MayIJune 1978
Habits, functional morphology and the
evolution of pycnogonids
S. M. MANTON, F.R.S.
Zoology Department, British Museum (Natural History), London
Recent work on functional morphology has revealed not only how a wide range of animals
work, but shows the significance of their shapes in great detail. Also, sound evidence of evolution is provided. A new approach towards the understanding of Pycnogonida comes from an
appreciation of the significance of their general habits and shapes and from the structure
and mode of action of their legs. Recent fossil evidence shows that the arachnids had at least
two terrestrial landings, occurring millions of years apart in time. At least two, but probably
more, separate arachnid lines lived in the sea. It is concluded that pycnogonids evolved from
one such aquatic group which never became terrestrial.
KEY WORDS:-Pycnogonida-habits-form-feeding-camouflage-palaeontologylocomotion-evolution-arachnids.
CONTENTS
Introduction. . . . . .
Animal shapes . . . . .
Arachnid evolution . . . .
The Pycnogonida . . . .
Arachnid and pycnogonid legs.
Conclusions . . . . . .
References . . . . . .
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INTRODUCTION
We want to know what the pycnogonids are; where they came from; what
their relationships may be; and the fossil record does not even tell us clearly
which is the head and which the tail end of a reasonably well preserved
PaZaeoisopus! Is the popular designation “sea spiders” a fairy tale or not?
Some really compelling information is available on these questions. The
significance of body shape in pycnogonids has not been appreciated; and
1
0024-4082/?8/0063-0001
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01978 The Linnean Society of London
2
S . M. MANTON
neither has the importance of the leg mechanism been understood. But in order
to realise the value of these topics in arriving at a sound interpretation of
this enigmatical group, it is necessary to consider these two fields in other
arthropods and then we can return to the pycnogonids with enlightenment.
proboscis
b
Figure 1. Pycnogonida. a. Nymphon rubrum Hodge ( 2 mm), male with eggs carried by the
ovigee (cf. Fig. 4e with hatched young); abdomen reduced; legs not in their natural positions,
see Fig. 4a, e. From Sam (1891). b. Ascorhynchus custelli Dohrn, diagrammatic longitudinal
half. From Dohrn (1881).
PYCNOGONID FORM, FUNCTION AND EVOLUTION
3
ANIMAL SHAPES
The study of functional morphology started a long time ago in a small
way, with no conception of how important this approach to structure was to
become. At one time the various forms of bivalved and gastropod molluscan
shells cast up on our beaches meant little to us, nor, for example, did the
variety of body shape in myriapods.
The different kinds of insect mouth parts took people’s fancy and the
functions performed by the various sorts of mandibles, maxillae and labia were
worked out. An order at once appeared, indicating the more generalized and
the more specialized types. The animals could then be arranged in meaningful
array. A bit more of the body was taken in by the work of Borradaile on the
feeding and respiratory organs of the crab. This did not lead directly to anything in particular, although it was a nice piece of work, recorded in the
Linnean Society’s Journal of Zoology. Cannon’s studies (see Manton (1977)
for literature) on the feeding mechanisms of the Branchiopoda, Ostracoda,
Copepoda, Cirripedia and Leptostraca proved to be much more fundamental
and also showed more of the significance of body shape. Fryer has carried this
line of work to undreamed-of extremes in detail, showing how chydorid and
macrothricid Cladocera are modified in the minutiae of every seta and in body
shape, not only in correlation with the working of the whole complex body,
where every leg is different, but also clearly demonstrating the lines of evolution which have resulted in structure suiting a large number of freshwater
micro-environments. Fryer has compared these cladocerans with the different
types of birds, which are suited to their very varied habits of life and places in
which they live.
The lifetime’s work by Sir Maurice Yonge has put function into our collections of shells and given us an understanding of how these animals work
and why they live where they do. This understanding not only brings the
shells to life but also shows with great clarity how the several evolutionary
lines among the molluscs have progressed and what the relationships of these
animals are. This new appreciation of the meaning of the shapes of the hard
and soft parts of many molluscs is based upon detailed knowledge of physiology, functional needs and habits, so that now we have indisputable evidence
of the paths of evolution within the Mollusca.
There is not space here in which to consider all the most productive lines
of work on functional morphology. It is useful now to consider in very little
detail the significance of some shapes of terrestrial arthropods and the inevitable deduction from them concerning evolution.
Work in this field originally started with an analysis of locomotory mechanisms, but it soon became apparent that other habits were just as important in
correlation with the determination of body shape. We now have an understanding of the functional significance of the main features of shape in all the
principle taxonomic groups of the Uniramia (Onychophora, Myriapoda, Hexapoda) and many of their subdivisions. Hitherto, we have had no idea what functions are served by the slow movements, unstriated muscles and shape changes
in the Onychophora; of what service is the fusion of most trunk segments in
pairs to form the diplosegments of the Diplopoda; what is the use of a cylindrical shape in most diplopods, a half cylindrical shape in others; a flat back in
4
S. M. MANTON
those diplopods provided with keels; and by long or by short bodies. Within the
centipedes, pauropods and symphylans we now know the usefulness of extra
tergites, alternate sized tergites, long tergites over legs 7 and 8 . We know why
it became advantageous to possess just three pairs of legs and not larger numbers. Moreover, an understanding of how legs work in the various groups
demonstrates incompatibility between the solutions of common problems,
thus indicating parallel evolution of the associated features. The animals
possessing mutually exclusive characters cannot have evolved one from another,
but only as divergent parallel lines. Existing land arthropods do not show
arrested stages in the evolution of so-called higher types. None of the four
myriapod classes could have given rise to any other myriapod group or been
derived from the Onychophora as we know them today, if functional continuity has existed, as indeed it must. One cannot imagine any evolving line of
arthropods losing its efficiency in any important matter and still succeeding
in meeting the struggle to exist, without going under in competition with those
animals maintaining or advancing their particular efficiencies. Hessler &
Newman (1975) imply that I have claimed that Onychorphora gave rise to the
Myriapoda and that the Hexapoda came from the myriapods. The exact opposite happens to be the case. I have shown, on plenty of structural and functional evidence, that the evolving separate lines of arthropods culminating in
present day Onychophora, four myriapod and five hexapod classes could only
have been derived in parallel from some basic uniramian stock first inhabiting
the land. Moreover, these taxa could not have evolved in any other way
(Manton, 1972, with summary in fig. 4-0;1973a, b; 1977). The evolution of
mandibles, other mouth parts, the leg and the locomotory mechanisms of the
uniramian taxa supports these conclusions.
I t is unlikely that the invasion of the land by ancestral uniramians took place
just once. I t is more likely that the invasion was accomplished by many individuals and perhaps at different times (cf. Arachnida below). However, in either
case, an initial divergence towards four habits took place:
(i) Gently seeking a way into shelter or under cover without pushing,
culminating in the Onychophora.
(ii) Head-on shoving into the substratum, like a bulldozer, using the
motive force of the legs, culminating in the Diplopoda.
(iii) Selecting a route through small existing crevices by the twisting and
turning abilities of small animals, not by pushing or by body deformation, culminating in the Symphyla.
(iv) Speedy running after prey or escape from predators, which would
inevitably lead to the morphology of the several orders of centipedes; the earthworm-like burrowing perfected by the geophilomorph centipedes in its initial stages must have characterized all
Chilopoda.
Hexapod divergent evolution along five separate lines depended on uniquely
contrived jumping mechanisms in Collembola and jumping gaits in Thysanura
and the mutually exclusive provisions for leg movement on the body in the
other classes (Manton, 1972). The evolution of the uniramian groups can be
summarized as on the right hand side of Fig. 2. The diverging lines indicate taxa
progressively changing their morphology as they perfected particular habits of
life of basic importance to each group. The diverging lines are not united at the
PYCNOGONID FORM, FUNCTION AND EVOLUTION
Merostornata
Tril
ta
CrL
cea
Eurypterida Xiphosura
5
Uniramia
He:
Arachnids
PHYLUM
CHELICERATA
TR-JBITA
k.*fLUM
PHYLUM
UNIRAMIA
Figure 2. The grouping of arthropodan taxa on the basis of present knowledge. The three
phyla Chelicerata, Crustacea and Uniramia appear to be quite distinct from each other. The
Trilobita are distinct from the Crustacea and show no certain relationship with the Merostomata. The Pycnogonida appear to have diverged from an ancestral aquatic arachnid group
and the Tardigrada probably have a distant affinity with the Onychophora, but there is no
direct evidence.
base because we have no evidence that there was much, if any, arborization,
but the myriapod and hexapod single lines represent the four and five classes
respectively in each group.
ARACHNID EVOLUTION
The evidence, as far as it goes, suggests that the arachnids did not all take to
the land at the same time. A quite advanced terrestrial arachnid, AZkenia, lived
in the Lower Devonian at the same time as the gilled scorpion, WaeringoScorpio, lived in the water (Fig. 3) (St~rmer,1970). AZkenia presumably had
considerable terrestrial antecedents. It follows that arachnids probably did not
all become terrestrial at once, since there must have been aquatic arachnids
separate from the gill-bearing scorpions. All Silurian scorpions are thought to
have been aquatic, respiring in most cases by branchiae covered by coxal
plates, as in eurypterids.
Arachnid systematists have long doubted the validity of the concept that
scorpions could have given rise to other extant arachnid orders. Nor do they
see much, if any, basic arborization within the terrestrial arachnids.
Embryological evidence is against a scorpion-like ontogeny ever having
given rise to those of other arachnids; but all could have descended independently from an ontogeny such as is seen in LimuZus (Anderson, 1973). However, this does not imply a xiphosuran origin of arachnids and we know nothing
of the ontogeny of eurypterids.
Thus palaeontology , taxonomy and embryology suggest that modern terrestrial arachnids did not originate from one ancestral aquatic group. This
conclusion is of considerable importance for considerations of pycnogonids.
6
S. M. MANTON
Figure 3. a. Wuengoscorpio heften' Stgrmer (21 mm), Lower Devonian, an aquatic scorpion
with external gills seen on either side. From Stbrmer (1970). b. .4lkenia rnirabilfs Stormer
( 1 3 mm), Lower Devonian, the earliest known terrestrial arachnid. From Stermer (1970).
THE PYCNOGONIDA
In the face of so much functional information on the meaning of animal
shapes in, e.g., molluscs and uniramians, it is unlikely that the shape of pycnogonids is without significance. Hedgpeth (1947)has shown the variety in form
which is present among the pycnogonids. These animals show an exaggeration
of the hanging stance found among most arthropods, except those with very
short legs (Fig. 4).Arthropods do not stand up on their legs as do mammals,
they hang down from them. Pycnogonids lead an unusual life; they can walk
and swim, but the habit of greatest significance in directing their evolution
appears to be associated with feeding in an exposed manner on large prey
which does not walk about.
PYCNOGONID FORM, FUNCTION AND EVOLUTION
PERIPATUS
"bottom gear
PAUROPUS
f
BUTHUS
CRYPTOPS
'top gear"
POLYDESMUS
7
FORFICULA
SPIDER
ASTACUS
LlGlA
Figure 4. Pycnogonida and the hanging stance in arthropods. a. Ammothea euchelata
Hedgpeth ( 3 mm trunk width) in anterior view. Note the large proboscis; chelifores; palps and
walking legs 1. b. Dorsal view of same. c. Ventral view of right chelifore. d. Right palp. From
Hedgpeth (1949). e. Eoreonymphon robustum Bell, male with young. From D'Arcy Thompson
(1909). f. Diagrammatic segments in transverse section of various arthropods to show the legs
as in life, relative to the ground. Except when legs are short, the hanging stance is employed.
Scorpion and spider show walking legs 3, Astacus and earwig walking legs 2 and Ligia walking
legs 6.
8
S.
M. MANTON
J
Figure 5. The caprellid crustacean Phfisica marina (8.5 mm) drawn from a photograph of a
living animal clinging to the branches of a hydroid by legs 7 and 8. Legs 4-6 are small, legs
2-3 arise from united segments and leg 1, the maxillipede, is visible. (After a photograph by
Dr J . P. Harding.)
Mouthfuls of polyps from Hydrozoa, Bryozoa, Alcyonaria and even pieces of
sponge are taken. Pycnogonid structure enables the proboscis to move from
one polyp to another with no change in footholds or obvious body movements. The tarsal claws are long and strong; the leg jointing provides forward,
PYCNOGONID FORM, FUNCTION AND EVOLUTION
9
backward, sideways, and up and down movements of the trunk without change
of footholds, enabling the proboscis to move from one polyp to another.
The leg jointing also permits the longer-legged species to sway with the currents, still maintaining the same footholds, and by such movements to avoid
detection in an exposed position. Many insects use the camouflage effect of
swaying, with or without a gentle breeze. Among the amphipod crustaceans,
the Caprellidae live a similar kind of life among hydroids and show rough
similarity to pycnogonids in body shape, length of legs, clinging tarsal claws;
the frequent adherence of two posterior pairs of legs only at one moment
(Fig. 5 ) doubtless provides similar advantages. We may note the large claws of
the fossil Pulueoisopus. The pycnogonid resemblances to the Caprellidae
extend to the very reduced abdomen, inconspicuous head and small feeding
limbs.
ARACHNID AND PYCNOGONID LEGS
Pycnogonid leg joints are very revealing as to the probable ancestry of the
group. However, reference must first be made to leg joints in general. The
stepping movements of lizards, newts, polychaetes, crustaceans, onychophorans, myriapods, hexapods and Limulus all involve a promotor-remotor
swing of the leg-base on the body. In the above mentioned arthropods, where
jointed legs are present, this promotor-remotor movement takes place about a
ventral, oblique or vertical axis of swing (see Fig. 6a-c) and all lie in the transverse plane of the body. The usual coxa-body articulation of arthropods is
shown diagrammatically in Fig. 6d, where the concentric circles indicate the
cuticular overlap at the joint and the vertical line shows the axis of the
promotor-remotor movement at the joint. Drawings of the structure of typical
joints of various kinds are given in Manton (1958a, 1977). The nature of a
joint and how it works can be revealed by a variety of techniques designed to
Show:
(i) the positions and tightness of the articulations;
promotor
0
b
remotor
Od
a x l ~oi swing
Figure 6 . a-c. The axes of swing of coxae on the body, situated a, ventrally, as in many crustaceans, most diplopods, Collembola, etc; b, obliquely, as in Diplura, Onychophora, Symphyla,
etc.; c, laterally as in Chilopoda, Protura, etc.; the axis of the promotor-remotor swing in all is
in the transverse plane of the body; d, diagrammatic end-on view of the coxa-body joint, the
concentric circles represent the overlapping cuticle at the joint and the heavy vertical line shows
the axis of the promotor-remotor swing, as takes place in a-c.
10
S. M. MANTON
(ii) the site or sites of the greatest expansion of arthrodial membranes;
(iii) the flexures permitted at the joints when muscles are removed;
(iv) the natural restriction by the cuticle of movements to one plane or
otherwise ;
(v) the position of origin of the muscles. The greatest bulk is expected to
arise near the widest expanse of arthrodial membranes; shorter
muscles may arise from the podomere margins towards the articulations; muscles arising nearest to an articulation, if present, usually
provide stability to the joint rather than movement.
The disposition of muscles alone cannot provide us with sound understanding of locomotory mechanisms. The nature of articulations, including podomere and arthrodial membrane geometry, must be detailed exactly if such
mechanisms are to be described with any confidence. To do no more than
describe a joint as of a hinge or pivot type invites thorough misunderstanding
of the locomotory function of that joint.
Between two successive leg-podomeres, levatordepressor or flexor-extensor
movements take place as shown in Fig. 7d-e, but these simple movements
never constitute an entire stepping mechanism. Since arthropods hang down
from their legs (Fig. 40,the centre of gravity is kept low, a desirable feature in
animals whose weight is small compared with the forces exerted on them by
air and water currents. The legs must, therefore, operate largely at the sides
of the body, except in branchiopods and others with different priorities, and
not directly under the body, as in a dog.
In Lirnulus, and in myriapods and hexapods, the coxa provides the promotor-remotor swing at its proximal joint and levator-depressor movements
at its distal joint (Fig. 7f, h). The latter movement takes place about a horizontal axis set at right angles to that giving the promotor-remotor swing. The
more distal leg joints provide further levatordepressor and flexor-extensor
movements in the various animals.
I t came as a great surprise to find that the coxa-body joint in arachnids and
pycnogonids, alone among arthropods, does not provide a promotor-remotor
swing. The provisions for such a movement are various, or even absent, in the
several arachnid orders (Fig. 10 and below). Petrunkevitch, in his extensive
studies of palaeozoic arachnids, found great diversity in form of the coxae,
which he illustrated by 25 drawings (Petrunkevitch, 1949: figs 5-26). He
noted differences in coxal mobility, or the reverse, even within the same order
and contrasted this with other arthropods. His further comments are not
altogether justified by recent work, but his basic observations remain.
Figure 7. Diagrams illustrating different types of leg-jointing and resultant movements. a-c. Promotor-remotor swing of diplopod coxae on the sternite; a, showing the coxa cut short; c, a
longitudinal view showing promotor-remotor swing which automatically gives a rocking movement, shown also in b. d, e. Pivot and hinge joints respectively. Arrowed lines indicate the
principal muscles and movements. f. Transverse section of the trunk, hatched, of Limulus and
appended leg 5 ; arthrodial membrane shown in black; heavy line indicates axis of promotorremotor swing of coxa on the body; large black spots indicate the positions of articulations.
g. The adductor-abductor movement of the coxa on the body used in chewing. h. Diagrammatic
end-on views of the joints of the leg shown in f. The concentric rings indicate the overlapping
cuticle at the joints shown above, the heavy lines show the axes of movement, and the spots
mark the main articulations. i, j. Stepping movements of left leg IV of a scorpion in lateral
and dorsal views respectively. The flexed and extended positions are drawn superimposed.
There is no promotor-remotor swing and the positions of the rocking joints are marked. From
Manton (1973a). For further description see text.
PYCNOGONID FORM, FUNCTION AND EVOLUTION
Counter rock
Figure 7
11
S. M. MANTON
12
SCORPION
SPIDER
GALE 2DtS
SCUTIGERA
top gear
Figure 8 . To show the fields of movement of the legs of various arthropods. The heavy vertical
lines show the progressive positions of the limb-tips relative to the limb-base during the propulsive backstroke and the thin lines show the positions of the legs at the beginning and end of the
backstroke. In every example the fields of movement are fanned out; in Scutigera the legs are
long and many and the fields overlap considerably and this overlap is less when legs are fewer.
After Manton (1952).
PYCNOGONID FORM, FUNCTION AND EVOLUTION
13
The fields of movement of a leg (Fig. 8 ) about its base on the body may
spread equally in front of and behind this base, or, where legs are few, the
fanning out of the bases may be very marked, as also in some pycnogonids
(Fig. 4b). This results, during the propulsive backstroke, in anterior legs
moving from an outstretched to a flexed position, while the posterior legs are
flexed at the beginning of the backstroke and outstretched in a posterior
direction at the end of this movement.
The terms used so far to describe movements at joints have the precise
meanings indicated. There is another movement, which takes place about the
longitudinal axis of the leg, and which I have called “rocking”. This also has a
precise meaning; the rock takes place alternately in opposite directions. It
may be a small movement and serves different purposes in the terrestrial
arthropods which use it. No rocking has been seen in an aquatic arthropod.
Rocking occurs in centipedes, pauropods and symphylans by similar
mechanisms. It takes place also in proturans and diplurans, but by different
means. In myriapods and in proturans the rocking occurs about a ventral close
union of the coxa and sternite, so that the dorsal surface of the leg is displaced
forwards on the remotor backstroke and backwards on the forward stroke
(Fig. 9). In diplurans the rocking is intrinsic, within the leg itself, but has the
same effect as in the above uniramians. In the Lepismatidae and Pterygota
little or no rocking takes place. The jumping leg movements of the Machilidae
probably require no rocking. The rocking movement in the above arthropods
assists leg extension during the backstroke at joints lacking extensor muscles.
That there can be no particular difficulty in the animals making their own
extensor muscles is shown by the presence of antagonistic pairs of muscles at
all or most joints along the legs of Pterygota and Malacostraca. The absence of
distal extensor muscles may have the function of lightening the distal part of
the leg, as in a horse, and so facilitating speed (for further details see Manton,
1965,1966,1972,1973a).
In the arachnids there are many ways of achieving rocking and the movement usually serves quite different purposes from those of the uniramians. As
an example, stepping by leg IV of the scorpion is shown in Fig. 7i and j. Rocking at the coxa-trochanter joint and counter rocking at the tarsus 1-tarsus 2
joint turns the knee close over the dorsal surface during the forward stroke, at
the same time swinging the tarsus far forwards and so providing a maximum
stride. During the propulsive backstroke the rocking turns the leg the other
way, as it extends; compensation occurs at the tarsus 1-tarsus 2 joint, so that
the claws remain squarely on the ground during the propulsive backstroke.
Flexor-extensor movements alone at the joints would result in unsuitable
upward projection of the knee for a burrowing animal, the stride would be
short and the speed consequently slower. There are as many as four rocking
joints in spiders; and the rocking joints in the various arachnid orders are
differently situated and differently contrived and serve various purposes.
Figure 10 shows diagrammatic end on views of leg joints in several arachnid
orders, the circles indicating the overlapping margins of successive podomeres.
The heavy straight lines indicate the axes of swing at the joints, and the curved
double-arrowed lines show the position of rocking movements (for details see
Manton, 1973a). The pycnogonids lack rocking joints of all kinds. Rocking
joints cannot be a fundamental attribute of either certain uniramians or of
1
L
Joiiadnr exo>na
SrIlVHd
PXO3 JO .?UlHS
PYCNOGONID FORM, FUNCTION AND EVOLUTION
15
particular arachnid orders because of the variety in construction and position
of such joints and in the services rendered. The absence of such joints is presumably a primitive feature.
The pycnogonids have more in common with arachnids in their leg jointing
than with any other arthropodan taxon. Arachnids and pycnogonids both lack
the promotor-remotor swing at the coxa-body joint, such as occurs in other
arthropods. Among living recorded arachnids the spiders alone have a little
coxal movement. In other arachnids the coxa is fixed on the body and does
not move (Fig. 10). Members of some, but not all, arachnid orders contrive a
secondary promotor-remotor swing, but this occurs at a variety of fairly
proximal joints (see vertical lines on Fig. 10 marking the axes of swing). The
scorpions show an unique condition lacking any joint providing a promotorremotor swing and these animals depend upon rocking and simple flexorextensor movements (see Fig. 7i, j).
The coxa-body joint in pycnogonids is unique in providing levatordepressor movements which give easy raising and lowering of the body on
fixed tarsi, useful in feeding, swimming (Fig. 11) and in camouflage swaying.
The singular nature of this joint emphasizes the habits suggested here as being
of prime importance in directing the evolution of the group. The more distal
joints are shown in Fig. lla-c. The fanning out of the legs of pycnogonids
(Fig. 4b) facilitates both swimming and swaying, but also ensures easy shifting
of the body forward, backwards, sideways, up and down during feeding, while
the tarsi remain fixed.
The lateral protuberances of the body which carry the coxae (Figs l a and
4b) are needed for housing the extrinsic coxal muscles, which can thereby
pull largely in line with the coxal cuticle and not at an acute angle from it, as
would occur if no protuberances were present. Other arthropods have most
elegant devices for keeping muscles and their tonofibrils in line with one
another, e.g. the arcuate sclerite muscles at the spider’s femur-patella joint, the
cuticular infolding carrying the muscles which return the collembolan springing organ to its resting position, and the remotor muscles of the copepod
swimming feet, which arise from flexible cuticle near the coxa (Manton,
1958b, 1972, 1973a and Perryman in Manton, 1977). Pycnogonids share with
the arachnids a versatility in joint construction not found in other arthropods.
Since no aquatic arthropods of any taxon have been found to possess a
rocking joint, it is probable that the rocking appertains to faster terrestrial
locomotion than takes place in normal stepping in the water. The absence of
Figure 9. Diagrams to illustrate leg action including rocking in centipedes. a. Lateral view of
some segments of Lithobius. Stiff sclerites are mottled, flexible cuticle is white. Heavy black
shows sclerotized ribs of cuticle. The legs are cut off near the base. The coxa is expanded dorsoventrally, and it is united closely at one point with the sternite, labelled on segment 12.Leg 10
is in the promotor position, leg 11 in the remotor position, and leg 12 shows the levated position. The coxa is drawn similarly on all segments; three coxal muscles are shown passing
obliquely upwards. Contraction of the right and left hand muscles from each coxa will rock
the dorsal part of the coxa forwards and contraction of the middle muscle will rock it backwards. b. Diagram of a left leg-base of the centipede Cormocephalus with the leg cut off at the
trochanter. The range of the rocking movement is shown by the two heavy lines directed
obliquely upwards and the axis of swing of the levator-depressor movement at the coxatrochanter joint is also shown. T t e coxa-trochanter joint has a heavy hinge-like anterior
articulation while the posterior articulation at this pivot joint is almost absent. From Manton
(1965).
3
S. M. MANTON
16
1
MEROSTOMATA
ARACHNIOA
Rock
@
c, I t
Counter- rock
Counter-rock
Counter- rock
Figure 10. Diagrammatic end-on views of the joints of the legs of living Chelicerata, anterior
end to the left. The double circles represent the cuticular overlap of the two successive podomeres at a joint. The large black spots represent cuticular articulations, the heavy lines show the
axes of movement at the joints and the curved, double-arrowed lines indicate rocking at a joint.
The fixed coxa in the arachnids and the great variety in the movements taking place at more
distal joints in the arachnids stand in marked contrast to the movements at leg joints in the
myriapods and hexapods where considerable uniformity exists (cf. Manron, 1973a: Fig. 15).
After Manton (1973a).
Figure 11. Pycnogonid leg jointing and movements. a. Diagram of the leg of Decolopoda
anrarcrica, in anterior view, appended from the lateral protuberance of the body. Pivot joints,
with horizontal axes of swing, are marked by black spots, an end-on view of such a joint being
shown in c. A pivot joint with a vertical axis of swing lies at the coxa-trochanter 1 joint, as
shown in b. The axis of che levator-depressor movement at the base of the cox8 is just dorsal to
the equatorial level, as shown, so facilitating the depressor movement, the power stroke, in
swimming. b. Diagram of the coxa-trochanter 1 joint with vertical axis of swing. c. Diagram of
the other leg joints with a horizontal axis of swing giving levatordepressor movements caused
by antagonistic muscles. Conventions on a and b as for Fig. 10. d. Nymphon gracile in anterior
view. On the right four positions of the downward stroke of the leg in swimming are marked
1-4. On the left four positions 5-8 show the recovery upward leg movement offering less resistance to the water. From Morgan (1971).
PYCNOGONID FORM, FUNCTION AND EVOLUTION
17
3
Figure 1 1
18
S. M. M A N T O N
a rocking joint indicates, therefore, that pycnogonids have never been terrestrial a t any stage. The secondarily modified arachnid joints declare themselves as such by their morphology.
In pycnogonids there are no pressure isolating mechanisms at the joints or at
the bases of the legs. Without isolating mechanisms (so far found only in Onychophora), a general increase in hydrostatic pressure generated by trunk
muscles could favour leg extension momentarily, but would hinder
simultaneous flexure of other legs such as occurs in normal walking or
swimming.
The swimming of pycnogonids depends on the levatordepressor movements
at the leg-base, facilitated by the nature of the coxa-body joint, described
above (Fig. l l ) , and a locomotory rhythm in which legs of a pair move in
unison and the alternate legs along the body perform the propulsive downstroke (adductor movement) while each adjacent leg pair performs the recovery
upward (abductor) swing (see Morgan, 1971). This locomotory rhythm leads to
continuous swimming, unlike that of a medusa or a lobster. The efficiency of
pycnogonid swimming is enhanced by slight promotor-remotor movements
being superimposed on the main adductor-abductor movements. The successive
legs of arachnids in walking use this same phase difference of about 0.5 of a
pace, or cycle of leg movements, although here legs of a pair step in opposite
phase to one another (Manton, 1973a: figs 16 and 17). Uniramian leg movements are rarely like this (summarized in Manton, 1973a: figs 7-9). It is noteworthy that the chewing movements of the prosomal gnathobases of Limulus
take place in the transverse plane of the body and every other leg pair is in the
adductor (biting) phase, while alternate leg pairs are in the recovery (abductor)
phase. In walking, the legs of Limulus use an entirely different sequence
dependent upon a promotor-remotor movement of the coxa-body junction. I t
is usually a slow “pattern” of gait with relative durations of forward and
backward strokes of about 2:8 and a small phase difference between successive
legs of about 0.1-0.2 of a cycle of leg movements, and not 0.5 as in a swimming
pycnogonid. In walking, the pycnogonids display the same predominance of a
phase difference between successive legs of 0.5, a long time interval k (see
Manton 1973a, 1977), and the irregularity in stepping so characteristic of
arachnids and different from hexapods. Such rhythms have not been recorded
from crustaceans.
CONCLUSIONS
The general body form of pycnogonids can be regarded as modified arachnid
morphology associated primarily with feeding on large prey which does not
walk away and with camouflage effects. The peculiarities of pycnogonid structure fit in well with such a supposition. In size the proboscis may be large, as in
Figs l b and 4a, or small, while food-polyp size is various. The pycnogonid
ovigers, situated between the palps and first walking legs, have long been
considered to be a reason for rejecting a supposed pycnogonid-arachnid
affinity. But some pycnogonids have increased their walking leg pairs to five
or even six, showing that the group has the capacity for increasing leg numbers.
PYCNOGONID FORM, FUNCTION A N D EVOLUTION
19
The presence of ovigers anteriorly seems to be another such manifestation and
does not appear to be a valid reason for rejecting the possibility of pycnogonidarachnid affinity. Sometimes, as in Fig. l a , there is anterior elongation of the
body. The reduction of the abdomen of the fossil Pulueoisopzis (Lehmann,
1959) has not gone so far as in modern pycnogonids and Caprellidae.
A remarkable pycnogonid feature is the absence of respiratory and excretory
systems. But with such a large surfaceholume ratio and slow movements this
may be understandable. With a reduction in size of the trunk, it is not surprising to find the viscera invading the legs, just as happens sometimes to the
crustacean carapace.
A supposed relationship between pycnogonids and arachnids is much
strengthened by Stdrmer’s (1970) description of the earliest known terrestrial
arachnid Alkeniu, of quite advanced type, living in the Lower Devonian at the
same time as gilled scorpions existed in the water. This must mean that the
ancestors of Alkeniu left the water millions of years before the scorpions
became terrestrial. Indeed, not until the Carboniferous do scorpions with
spiracles appear among the known fossils. There must, therefore, have been
more than one line of aquatic arachnids, and more than one transition to the
land. The suggestion that pycnogonids have descended from a line of aquatic
arachnids which never became terrestrial seems reasonable.
The habits with which the evolution of a taxon of arthropods is associated
may be easy to recognize, as in the case of the various orders of centipedes,
pauropods, symphylans and iuliform millipedes, but the habit of prime significance, among many accomplishments performed by a taxon, may not be at all
obvious. For example, in Polyxenus (Diplopoda, Pselaphognatha) the habit of
over-riding survival significance appears to be that of clinging and living on
glass-smooth ceilings of rock crevices; such habits are not exercised all the time,
but they appear to have led to the evolution of the curious external and
internal morphology and the peculiar gaits of Polyxenus, so very different from
that of other diplopods (Manton, 1956).
The presence of the unique coxa-body joint of pycnogonids, which provide
levator-depressor movements, indicates that walking is not the primary concern
of these animals. On the contrary, the ability to move the body up and down
and in any direction without altering the tarsal holds, appears to be the
capacity with which the leg-base, feeding behaviour and evolution of the
general morphology of the Pycnogonida is concerned. Walking and swimming
are also performed and the details of leg-jointing suit these movements also.
However, the habit of major evolutionary significance rests with camouflage
and the feeding technique.
Thus, pycnogonid morphology appears to have evolved in the sea from an
unknown early arachnid group which never left the sea and whose progress
towards survival was associated with feeding habits which are unique among
arthropods.
It is a pleasure to find new evidence supporting the tentative views of
Calman & Gordon (1933) and the equally cautious classification of Hedgpeth
(1955) when he placed the Pantopoda and Palaeopantopoda as two orders
within the Pycnogonida. Of Taxonomy, Hedgpeth wrote (1962): “Just what
good is this sort of thing?”. I leave him to pronounce on the present
contribution.
20
S. M. MANTON
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