The Biology of Pycnogonida

F. Arnaud and R. N. Bamber

Station Marine d’Endoume, F-13007 Marseille, France and Marine Biology

Unit, CEGB, Fuwley, Southumpton, Hunts SO4 ITW, U K

I. Introduction ., .. .. .. .. .. . . . . . . . . 2
11. Zoological Characteristics . . . . . . . . . . . . 3
A. Morphology .. . . . . . . . . . . . . 3
B. Anatomy .. .. .. .. . . . . . . .. 11
C. Classification .. . . . . . . . . . . . . . . . . 25
Ill. Physiology and Function . . . . . . . . . . . . . . . . 27
A. Salinity tolerance . . . . . . .. .. . . . . . . .. 21
B. Digestion , . .. .. .. .. .. . . . . . . .. 28
C. Respiration . . . . .. .. . . . . . . . . . . . . 29
D. Locomotion .. . . . . .. .. .. , _ ,. _. 30
E. Nerve function , . . . . . .. .. . . . . . . .. 32
F. Bioluminescence . . .. .. .. .. . . . . . . . . 33
IV. Life Cycle .. .. .. .. . . . . . . . . . . . . 33
A. Reproduction .. .. ‘. . . . . . . . . . . . . 33
B. Vitellogenesis ., .. .. . . . . . . . . 35
C . Spermiogenesis , . .. .. .. .. .. . . . . .. 35
D. Fertilization and egg-laying .. . . . . . . . . . . . . 36
E. Embryonic development . . .. . . . . .. . . . . . . 39
F. Postembryonic development .. .. .. . . . . . . .. 40
G . Breeding seasonality . . . . .. .. . . . . . . .. 43
v. Interrelationships with Other Organisms . . . . .. .. . . . . 44
A. Feeding .. . . . . . . . . . . . . .. . . . . 44
B. Pycnogonids as food . . . . . . . . . . . . . . .. 49
C. Commensalism and parasitism . . .. .. . . . . . . .. 49
D. Epibiosis on pycnogonids .. .. . . . . . . . . . . 53
E. Pycnogonid synecology . . . . .. .. .. .. . . . . 54
F. Pollution and pycnogonids .. .. . . . . . . . . .. 66
4 D V A N C t S I N MARINE BIOLOGY Cowrrghr 0 1987. by Academic Press Inc. (London) Lid.
VOLUME 74 ISBN 0-12-0261?4-3 All rights of reproducrron m any form reserved.

1
2 F. A R N A U D A N D R . N. BAMBER

VI. Zoogeography . . . . . . . . . . . . . . . . . . . . 61
A. Regional faunas . . . . . . . . . . . . . . . . . . 68
B. Deep-sea pycnogonids . . . . . . . . . . . . . . . . 12
C. Pycnogonids in plankton . . . . . . . . . . . . .. .. 15
VII. Palaeontology and Systematic Affinities . . . . . . . . . . . . 16
Acknowledgements .. . . . . . . . . . . . . . . . . 78
Appendix I .. .. .. . . . . . . . . . . . . . . 78
Appendix 2 .. .. . . . . .. .. ,. . . . . . . 85
References .. .. . . . . . . . . . . . . . . . . 86

I. Introduction
The Pycnogonida or “sea spiders” are exclusively marine invertebrates
numbering, to-date, about I000 species in 84 genera. In the past they were
referred to as the Podosomata or Pantopoda, a name persisting in some
European literature, and now surviving as the extant order of the Class (or
Subphylum) Pycnogonida. As they rarely occur in prolific density, are often
cryptic, and have little economic significance, they have long been regarded
as a “minor” group among the marine fauna, receiving little more than
superficial coverage in general zoology texts. Yet they are found from the
littoral fringe to the depths of the abyssal trenches, and from equatorial
waters and the tropics, through temperate seas, to both the Arctic and
Antarctic.
While the majority of species are epibenthic, a few are interstitial, some
are bathypelagic, and recently increasing numbers of commensal and para-
sitic species have been described, associated with coelenterate, poriferan,
molluscan and echinoderm hosts. Littoral pycnogonids tend to be small,
with a leg span of a few millimetres in some Callipallene and Rhynchothorax,
while deeper water and polar species tend towards gigantism, some Colos-
sendeis achieving a leg span of over 40 cm.
After the early monographs of, for example, Hoek (188 1a, the Challenger
expedition), Dohrn (1 88 I , Mediterranean species), Sars (1 891, North-
Eastern Atlantic) and Loman (1 908, the Siboga expedition), the class was
reviewed by Helfer and Schlottke (1 935), Fage (1 949) and King (1973), with
the comprehensive North-West Atlantic and North-West Pacific works of
Hedgpeth (1948, 1949) intervening. Almost all published work up to this
time concerned taxonomy and zoogeography, with regular descriptions of
new species or faunas; and though these themes remain preponderant in
recent pycnogonid literature, the development of marine biological and
oceanographic research since the 1960s has involved an increased interest in
pycnogonids, including their biology and ecology.
The first international symposium on pycnogonids was held under the
 THE BIOLOGY OF PYCNOGONIDA 3

auspices of The Linnean Society of London in October 1976, in honour of

Joel W. Hedgpeth and his major contribution to the study of the group over
some 40 years. The meeting was organized by our late friend and colleague
William G. Fry, and resulted in 238 pages of proceedings published in the
Society’s Zoological Journal (Vol. 63, 1978), which includes a comprehen-
sive pycnogonid bibliography of over 1100 references (Fry and Stock, 1978).
This review attempts to collate and summarize the current knowledge on
all known aspects of pycnogonid biology, drawing from both the latest
published and unpublished researches in this field, and is aimed at both
specialists and other marine biologists.

I I . Zoological Characteristics
A. Morphology

While pycnogonids (meaning “dense-knees”) have a consistent form of

typically four pairs of long multiarticulate legs held together by a compara-
tively small body (Fig. l), the genera represent a marked diversity on this

cephalon
\ ocdar

tarsus
FIG. 1. Diagrammatic representation of a pycnogonid, showing parts mentioned in the text
(after Child, 1979).
4 F. ARNAUD AND R. N. BAMBER

FIG. 2. Dorsal views of: A, Nymphon hampsoni; B, Pantopipetta auxiliata; C , Anoplodactylus

srellarus; D, Pycnogonum stearnsi; E, Achelia shepherdi. Scale line represents 1.0 mm for A,
0.6 mm for B, C and E and 2.0 mm for D.

basic plan (Fig. 2), ranging from compact forms such as Tanystylum and
Pycnogonum to the more elongate Nymphon and Colossendeis.
In the presumed primitive form (as shown by Nymphon), the body
comprises four somites or segments, each bearing a pair of walking legs; the
first of these, the cephalic somite or cephalon, bears the proboscis anteroven-
trally, the ocular tubercle holding the eyes dorsally, and three pairs of
appendages, the chelifores above the proboscis, the palps laterally, and the
ovigerous legs or ovigers ventrally. Palaeontologists consider this cephalon,
and including the first pair of walking legs, as a cephalosoma. Various
genera exhibit reductions in the cephalon appendages, to the point of
absence of ocular tubercle, chelifores, palps, or ovigers. Apart from a pair of
 THE BIOLOGY OF PYCNOGONIDA 5

dorsal

FIG. 3. Lateral views of: A, Colossendeis bicincta; B, Anoplodactylus stellatus; C, Pallenopsis

cidarihatus; D, Ascorhynchus prosurn (after Stock, 1978b, Nakamura and Child, 1983, and
Child, 1975). The scale line represents 12 mm for A, 0.6 mm for B and D and 2.0 mm for C .

walking legs, the second and third trunk somites bear nothing or are
ornamented with small to elaborate cuticular processes; the last trunk somite
also bears the abdomen, ending in the anal orifice.
Although pycnogonids are typically eight legged, nine polymerous species
from four families have been described to date, seven with five trunk somites
and 10 legs, distributed in either cold Antarctic or warm tropical waters, and
two species from the Antarctic with six trunk somites bearing 12 legs (Table
1). Most of these polymerous genera resemble known octopodous genera, as
suggested by their names (but not Pentacolossendeis (see Fry, 1978b)), and
would probably be synonymized without their extra trunk somites: they are
currently considered valid genera rather than aberrations.
The proboscis is a moveable organ involved in ingestion, bearing the
mouth at its tip, and shows considerable variation in shape and propor-
tionate length among the diverse pycnogonid families (Fig. 3; also 2B, D, E).
Fry and Hedgpeth (1969) discussed the difficulty in describing proboscides in
simple adjectives, and introduced a system of coordinates based on distal
 Table 1 GEOGRAPHICAL
DISTRIRUTION OF POLYMEROUS PYCNOGONIDS (A: ANTARCTIC;
T: TROPICAL),
AFTER A N D FRY,
HEDGPETH 1964

Family 10-legged species 12-legged species

Nymphonidae Penlanymphon antarcticum Hodgson, 1904 A Sexanymphon mirabilis Hedgpeth and Fry, 1964 A
Pentanymphon minutum Gordon, 1944 A
Colossendeidae Decolopoda australis Eights, 1835 A Dodecolopoda mawsoni Calman & Gordon, 1933 A
Drcolopoda antarctica Bouvier, 1905 = A
D. australis Eights
Ammotheidae Pentacolossendeis reticulata Hedgpeth, 1943 T
Pycnogonidae Pentapycnon charcoti Bouvier, 1910 A
Pentapycnon geayi Bouvier, 191 1 T
 , i A'

C,"'
I c.

I J

FIG. 4. The five main types of proboscis shape, A to D and J. The criteria involved are: the
presence o r absence, and position of one or two dilations; the relative diameters of the proboscis
at its insertion into the cephalic somite and at its distal end. X and Y indicate proximal and
distal diameters, Z indicates the midpoint of the longitudinal axis (after Fry and Hedgpeth,
1969). Using the additional code for proboscis curvature of 1 (straight), 2 (downcurved) and 3
(upcurved), a formula to describe proboscis morphology can be derived, as B " ' : 2 for
Colossendeis bicincta (Fig. 3A).
8 F. ARNAUD AND R. N. BAMBER

and proximal diameters, the presence and whereabouts of any dilations

along the proboscis, the type of curvature, etc. (Fig. 4). This system would
prove valuable if it were to come into common usage.
The proboscis has been shown to be capable of changing its volume under
the action of striated muscle in some genera (Austrodecus), but not in others
(Rhynchothorax) (Fry, 1965). Its mobility, predominantly in the vertical
plane, also varies between genera; perhaps the maximal mobility is found in
the genera Ascorhynchus and Hannonia, where the proboscis is connected by
an unsclerotized arthrodial membrane of soft chitin, and can be moved to lie
almost parallel to the trunk.
The proboscis is formed from three longitudinal elements (antimeres),
each ending distally in a chitinous lip; this gives an unusual triradial
symmetry to the proboscis. The chitinous lips may be hardened (Rhyncho-
thoru.Y, Parupalkne) or fringed with setae (Pseudopallene), and while usually
plain, the proboscides of some genera are ornamented with distal tubercles
(Anoploductylus stellatus, see Fig. 3), digitiform processes (Rhynchothorax
unicornis) or humps (Dromedopycnon acanthus); sexual dimorphism is
exhibited by Anopfoductylus digitatus, the four ventral processes on the
proboscis being developed only in the female.
The cephalon itself may be either compact (as in Tunystylum), or elongate
with an extended neck (Cullipallene), but this character can show marked
intraspecific variation (e.g. Bamber, 1982). As the other trunk somites, the
cephalon may bear dorsal ornamentation, such as tubercles (Fig. 3) or
anterior processes (“horns”).
The ocular tubercle, when present, is situated dorsally in the midline, and
typically bears four eyes, pigmented and of equal size. In some genera the
ocular tubercle may be situated at the posterior or anterior of the cephalon
(Fig. 2A, C), and may range from elaborate elongation (Figs. 2B, 3C) to a
low, rounded dome (e.g. Trygaeus communis, Colossendeis bicincta) or be
absent (e.g. Cilunculus alcicornis). The anterior eyes may be larger than the
posterior pair, while in many abyssal species the eyes are lacking (e.g.
Njmphon inerme, deep-sea Pallenopsis). A similar adaptation to darkness is
shown by the blind sand dwelling species of Rhynchothorax (the Californian
R. philopsummum, and the Mediterranean R. anophthalmus and R. alcicor-
nis).
The chelifores comprise a basal “stalk”, the scape, and a chela with one
moveable finger articulating on the “palm” of the fixed finger. These fingers
are primitively dentate, and are used for manipulation of food and, perhaps,
holding onto the substratum. They are present and functional in all larvae,
but again show degrees of reduction in adults of many genera. Ammotheids
show a range from non-functional chelae (all adults) with a two-segmented
scape (Ammothella) or a one-segmented scape (Ascorhynchus); all adults of
 THE BIOLOGY OF PYCNOGONIDA 9

FIG. 5. Nymphonella tupetis adult, dorsal, showing multisegmented palps and first walking
legs. Scale line = 2 mm.
-\

the Colossendeidae, Endeidae and Pycnogonidae show total loss of cheli-

fores.
The multi-segmented palps have sensory, feeding and cleaning functions.
They are absent in Endeids, Phoxichilidiids, members of the Pycnogonidae
and female Callipallenids; in male Callipallenids they are one-segmented in
Neopallene, two-segmented in Propallene and four-segmented in Oropallene.
Nymphon species have five segments in the palps, Ammothella and Colossen-
deis nine segments (Fig. 3A), and Ascorhynchus and Rhopalorhynchus 10; the
three species of the unusual genus Nymphonella have 1 1-segmented palps,
the distal two segments being further subdivided (Fig. 5). Austrodecus and
Rhynchothorax species possess acute spines at the tip of the palp which are
used to bore bryozoan zoaria during feeding.
The ovigers are used for cleaning, which may have been their primitive
function, and by the males to carry the eggs until hatching or longer (with
the possible exception of Colossendeis males, which have never been found
carrying eggs). Recently, Child (1979) has coined the term “strigilis” for the
four terminal oviger segments when in a characteristic configuration of a
sickle shape, the segments bearing denticulate spines and ending in a claw
(Fig. 6F, H). Pycnogonids have been observed in aquaria using the strigilis
to clean other limbs; presumably species whose ovigers are short, have few
segments or are devoid of spines do not use them for cleaning. They are borne
ventrally on the cephalon, normally between the insertion of the proboscis
10 F. A R N A U D A N D R . N. BAMBER

FIG. 6. Ovigerous legs of: A, Anoplodactylus stellatus (after Nakamura and Child, 1983); B,
Pjcnogonum stearnsi (after Fry, 1965); C, Nyrnphopsis acinacispinatus bathursti female and D,
male, enlargement of terminal segments (after Child, 1975); E, Pallenopsis cidaribatus male and
F, enlargement of terminal segments; G, Nyrnphon hampsoni male; and H, enlargement of
terminal segments (after Child, 1982~);J, Rhopalorhynchus claudus female (after Stock, 1975d).

and the first lateral processes; in species with an extended “neck” the ovigers
arise near its base, while in Ascorhynchus simile they are borne on lateral
extensions at the middle of the neck.
The presence or absence of ovigers and the number and configuration of
their segments are important diagnostic characters in pycnogonid taxonomy
(Fig. 6). The segment number ranges from 5-6 in Anoploductylus to a
maximum of 10 in many Ammotheids, Nymphonids and some Pycnogoni-
dae. Sexually dimorphic ovigers are common, including genera where the
male oviger is longer (but with the same number of segments), more robust
 THE BIOLOGY OF PYCNOGONIDA 11

FIG. 7. Scanning electron micrograph of the dorso-anterior view of Pseudopallene circularis

(National Museum of Wales Accession No. Z 1986.3.10), showing elaborate spination; A-
abdomen, C-hela, O-ocular tubercle; scale interval = 2 mm.

and more spinous (e.g. Tanystylum, Nymphon), and genera in which ovigers
are absent in the female (Endeis, Anoplodacrylus). Recently, three species of
Pycnogonum have been discovered in which the males are also lacking
ovigers: Stock (1 968) created the subgenus Nulloviger for P. anovigerum
Clark from New Zealand, to which must be added P. elephas from the South
Atlantic and P . africanum from the tropical Indian Ocean (Arnaud and
Child, in press). Males of these species carry the eggs in a cake-like mass on
the ventral surface of the body.
The trunk segments primitively articulate with each other, giving the
trunk flexibility; in some genera evidence of an articulation between the
cephalon and the first trunk somite is suggested by a feeble line (some
Pycnogonum and Austrodecus species) or fold (Parapallene nierstraszi) in the
cuticle. Many genera exhibit further fusion of some (e.g. Achelia and
Callipallene species) or all (e.g. Decolopoda, Tanystylum) of the trunk
somites, leading to increasing rigidity of the trunk. Laterally, each trunk
segment has a pair of lateral processes or crurigers to which the legs attach.
A variety of dorsal ornamentation is shown on the trunk somites and
particularly the lateral processes of some genera, ranging from simple spines
or tubercles (e.g. Fig. 2), to spires (Paranymphon), round massive projections
(Arnrnothea), columnar processes (Pycnogonum elephas), arborescent tu-
bercles (Pycnogonurn arbustum), or distal spurs (Cilunculus cactoides,Austro-
decus breviceps); the anterior and posterior surfaces of the lateral processes
may even bear spines (Cilunculus alcicornis, Elassorhis laterospina) or long
setae (Ascorhynchus simile) (e.g. Figs 2B, 3C and 7). The function of this
FIG. 8. Ambulatory legs of: A, Ascorhynchus breviscapus, female; and B, Rhopalorhynchus
cluudus (after Stock, 1968); C, Anoplodacfylus stellatus with enlargement of femoral cement
ducts (after Nakamura and Child, 1983); D, Nymphon hampsoni, with enlargement of claws,
and arrows indicating cement ducts (after Child, 1982~);E, Pycnogonum steurnsi (after Fry,
1965); F, Acheliu shepherdi (after Child, 1975).
 THE BIOLOGY OF PYCNOGONIDA 13

often elaborate ornamentation is not known; long setae may be an aid in

swimming.
The walking or ambulatory legs are of a consistent nine-segmented
pattern (Fig. 8), comprising a first coxa (articulating with the lateral
process), second and third coxae, femur, first and second tibiae, tarsus,
propodus and (“main-”) claw. As aids to grasping, particularly in species
found in algal or bryozoan-hydroid epifaunas, the propodus is often
endowed with ventral (“sole”) or proximal (“heel”) spines, or a mid- to
disto-ventral lamina (Fig. 8C, F); in these cases the propodus tends to be
arcuate and the main claw opposible. The main claw is commonly flanked by
two smaller auxiliary claws (Fig. 8D, F); these may be minute (some
Anoplodactylus species), single (the unique Elassorhis laterospina from the
Brazil slope with a single median auxiliary claw (Child, 1982c)), or may
replace the main claw (the curious Mediterranean Ammothella biunguiculata,
whose main claw is reduced to a mere bud). The legs may be short and stout
(e.g. all Pycnogonum species) or elongate (most Nymphon), naked or orna-
mented with tubercles, spines or long (swimming?) setae, as, for example,
advertised by the specific names of Pycnogonum tuberculatum, Hannonia
spinipes, Achelia echinata and Pallenopsis pilosa.
The (inevitable) exception to the consistent nine-segmented pattern is the
genus Nymphonella, all three species of which have the propodus and claw of
the first pair of walking legs modified by subdivisions into a multisegmented
“whip” similar to their palps (see Fig. 5).
The sexual pores generally open on the ventral surface of the second coxae
of all the legs in the female, and of the third and fourth legs of the male. The
female orifice is usually larger (to allow passage of the eggs), and mature
females usually show swollen femora wherein the eggs are stored prior to
mating. The male femora also contain specialized structures, e.g. the cement
glands. These are secretory glands which produce a cement used by the
males to maintain the eggs taken from the female in cohesive balls. The
cement glands, and in particular the pores on the surface of the femur
whence the cement is secreted, are variable in number and morphology, and
often taxonomically diagnostic.
In the large genus Anoplodactylus (ca. 110 species), the females are often
similar in closely related species, which are distinguished on male mor-
phology. Many male Anoplodactylus have long dorsal femoral spurs bearing
the cement gland pore at their tips, tubular in A . pulcher, chimney-shaped in
A . insignijormis. Twenty per cent of Anoplodactylus species have more than
one cement gland per femur (Nakamura and Child, 1983), while A . stellatus
from Sagami Bay, Japan, is unique in having three glands with unequal sized
pores, the most distal being the largest. The Japanese A . perforatus has
between 17 and 25 cribellate pores on each femur (Nakamura and Child,
1982), while A . multiclavus from the Virgin Islands has 3-5 clavate cups.
14 F. ARNAUD AND R. N. BAMBER

In t he genus Endeis the pores are numerous (up to 40), small, and
arranged in one or more rows on the femoral surface, while in Austrodecus
there is only one triangular cement tubercle. In the largest genus, Nymphon,
cement gland morphology is mostly unknown. N . tubiferum has a spectacu-
lar ventro-distal tube over half as long as the femur, and N . discorsicoxae
shows increasing numbers of glands from anterior to posterior legs (Child,
1982~).N . caementarum possesses not only six pores on the ventral surface
of each femur, but also three on the second coxae and seven on the first
tibiae (Stock, 1975d). The same author recorded tibia1 as well as femoral
cement gland pores in Ascorhynchus pararmatus and A . armatus.
The trunk terminates in the abdomen, which may be articulating, bent
ventrally or dorsally, truncate, tapering or clavate. The abdomen of Proto-
trygaeus ammothelloides is extreme in being nearly as long as the rest of the
trunk, while in Eurycyde raphiaster it is erect, taller than the ocular tubercle
and ends in six or seven long spines. Abdomens often bear spines or
tubercles continuing the theme of the dorsal body ornamentation (Fig. 7), or
may themselves contribute to the theme (e.g. Paranymphon spinosum, whose
abdomen and ocular tubercle mimic the distal spurs on the lateral pro-
cesses).

1. Morphological abnormalities

Abnormalities in pycnogonid morphology have been recorded affecting all

parts of the body, from the ocular tubercle and palps to the legs and
abdomen. They were first reviewed by Gordon (1932). Subsequently, Arita
(1936) illustrated a male Nymphonella tapetis with a supplementary leg on
the right side only; Hedgpeth (1947, pp 24 et seq.) summarized the most
conspicuous anomalies he had come across; Barnard (1954) recorded a male
Boehmia chelata with the ocular tubercle divided into two tubercles placed
transversely; Stock (1975d) reported a male Anoplodactylus portus from
Puerto Rico with a teratological right chela; recently a specimen of Achelia
echinata has been taken off Dorset, UK, with the second trunk somite
developed on the right side only, and hence only 7 walking legs (Fig. 9;
Bamber, unpublished data).

2. Size

The total body length of pycnogonids (as defined by Fry and Hedgpeth,
1969, i,e. from the dorsal anterior edge of the cephalon to the junction of the
last pair of lateral processes) ranges from less than 1 mm, with a leg span of
4 mm, for the very small species of Rhynchothorax, to over 10 cm body
length with a leg span of 25-3Qcm for the deepwater Colossendeis. The
 THE BIOLOGY OF PYCNOGONIDA 15

1 mrn

FIG. 9. Trunk and cephalon of male Achelia echinafa from Lyme Bay, Dorset, with abnormal
segmentation and thus only three legs on the left side.

maximum recorded leg span is 410 mm for a trunk length of 26 mm in a

specimen of C. meluncholicus from Grand Bahama, collected at a depth of
779m (Stock, 1975d), though Child (pers. comm.) mentions a C. colosseu
specimen at the Smithsonian Institute with a leg span of over 70 cm, body
length with proboscis less than 8 cm.
While most genera are consistent in size (the “large” Colossendeis and
Pallenopsis or “small” Austrodecus and Pantopipetta), others are variable,
for example the small Pycnogonum pusillum and P. plumipes of the Mediter-
ranean contrasting with the large Brazilian P. elephas. Similarly, families
show heterogeneity of size; for example in the Phoxichilidiidae most Anoplo-
ductylus speci&shave a leg span of a few millimetres compared to over 25 cm
for some Pullenopsis. Within species, females are commonly larger than
males.
Owing to the lack of information on the biology of, in particular, abyssal
species, it is difficult to determine comprehensively the factors influencing
size. Littoral species are almost invariably small, and clearly the larger long-
legged forms would be too fragile to withstand this high-energy environ-
ment; even the robustly-legged Pycnogonum littorale is significantly larger
offshore than littorally (Bamber, 1983a). Interstitial and commensal species
are also appropriately small. The very-large species are characteristic of deep
and polar waters, where there is a common theme amongst other animal
groups for low rates of metabolism and growth resulting in gigantism;
equally, a greater leg span may be advantageous to avoid sinking in fine
16 F. A R N A U D A N D R . N. BAMBER

abyssal mud bottoms, though a hindrance in shallow weed beds. Nonethe-

less, small forms also occur in deeper water, for example Cilunculus afcicor-
nis with a body length of 1.5 mm taken at over 1000 m depth (Bamber,
1983b).

3. Colour

Generally, pycnogonids are a translucent yellowish-brown to cream in

colour, or transparent; the sand dwelling Nymphonella and Ascorhynchus
species are whitish. However, many species do exhibit contrasting or bright
colouration. Some Antarctic Colossendeis are yellow, orange or red, and
Gordon (1932) reported C. glacialis was called the “harlequin” pycnogon by
its collectors in South Georgia. A form of the North-East Atlantic Nymphon
brevirostre with a red trunk colouration has been known since 1864 (the N .
rubrum of Hodge, 1865); N . maculatum from the Indian Ocean is “transpar-
ent or yellowish but bears numerous small black spots on the legs. The eyes
are brown-red’’ according to Stock (1964). The South Australian Pseudo-
pallene ambigua has a “straw-coloured” body with several dark carmine-red
stripes, for example on the coxae, femora and ocular tubercle (Stock, 1973);
regular chocolate brown banding on the body and legs is shown by
Ammoihea hilgendorfi (Ohshima, 1927a; Bamber, 1986). In many cases the
colour exhibited by pycnogonids is only the colour of their gut contents
showing through the hyaline cuticle. Thus, beautiful green or purple colours
are shown by Anoplodactylus virescens, and particularly Endeis species (E.
spinosa, E. viridis). The multicoloured Anoplodactylus evansi lives on a range
of pigmented hydroids, and Staples (1977) considers it “the most beautiful
representative of the South Australian pycnogonid fauna”; the sympatric
red Parapallene australiensis, however, exhibits a high degree of selectivity in
living only on the crimson alga Halopteris buski. Barnard (1954) reported
that Boehmia chelata, a South African endemic species, is darkly coloured
irrespective of the colour of alcyonarian on which it is found.

4. Morphological adaptations

Just as the colouration, or lack of it, in a pycnogonid contributes to its

crypsis and thus its adaptation to the environment, so the overall mor-
phology of the typical long-legged, multiarticulated form is admirably suited
to a life clambering amongst algae, hydroids, etc. Species living in more
specialized environments commonly show appropriate adaptations: thus
abyssal forms are normally blind; species living on tropical fringing or
barrier reefs, where wave action is very strong, show a condensed body form
with reduced spaces between lateral processes, short but robust legs, an
 THE BIOLOGY OF PYCNOGONIDA 17

arcuate propodus and heavy strong claws (e.g. Acheliana tropicalis, Anoplo-
dactylus arescus). The North-East Atlantic Pycnogonum littorale also fre-
quents exposed wave-washed shores, and lives almost ectoparasitically on
anemones rather than in an arborescent “clambering” environment; it too
shows an extremely robust morphology, with stout, short legs, no auxiliary
claws but strong main claws for grasping the anemone tissue firmly.
Perhaps the most pronounced specialization is shown by the psammophi-
lous species, the shallow water Nymphonella tapetis from Japanese and
Mediterranean waters, and Ascorhynchus arenicola and A . simile from the
Mediterranean infralittoral; they exhibit a combination of
lack of pigment (they are generally whitish)
reduction of ocular tubercle or blindness
dorso-ventral flattening of the body
elongate, well-separated lateral processes to increase the body surface
cylindrical leg segments
a soft, unornamented cuticle,
all characters representing adaptation to an infaunal mode of life.

B. Anatomy

While most of the internal anatomy of pycnogonids was studied a century

ago, certain aspects have been the subject of recent researches. The various
systems are reviewed only briefly here as a context for this recent work; more
detailed accounts and excellent figures may be found in Hoek (1881a, b),
Dohrn (1881) and Helfer and Schlottke (1935).
Pycnogonids possess neither a respiratory nor an excretory system. With
the very-large body surface area to volume ratio resultant from their peculiar
morphology, gaseous exchange is assumed to occur through the body
surface, while excretion and any osmoregulatory activity that exist may
occur at the body surface or in the gut.

1. Alimentary system

The alimentary canal in pycnogonids extends from the mouth at the tip of
the proboscis, into a foregut or oesophagus, thence through the cephalic and
trunk somites as a midgut, finally passing through the abdomen as the
hindgut and opening at the anal slit. However, owing to the restricted space
within the trunk, midgut caeca extend some way down the legs, often as far
as the tarsus, and even into the proboscis and chelifore bases in some species,
18 F. ARNAUD AND R. N. BAMBER

anus

FIG. 10. Nymphon australe, dorsal, showing gut and diverticula (after Richards and Fry, 1978).

for example some Endeis (the former only) and Nymphon australe (Richards
and Fry, 1978; see Fig. 10).
The proboscis has a triradial section, since it arises from the fusion of
three antimeres (one dorsal and two latero-ventral), and both the mouth and
oesophagus are consequently Y-shaped in cross-section (Fig. 11). The
foregut within the proboscis is lined with ectodermal cuticle continuous with
that of the outer surface of the proboscis, and, with the hindgut lining, is lost
on ecdysis. Towards the base of the proboscis the inner wall of the
oesophagus bears a sieve of long setae known as the “oyster basket”, whose
function appears to be the maceration of ingested food. The extrinsic and
intrinsic musculature of the proboscis and associated nervous system has
been comprehensively documented by Fry (1965) for two Antarctic species,
Austrodecus glaciale and Rhynchothorax australis, and the Californian Pyc-
nogonum stearnsi (Fig. 11).
The oesophagus continues into the cephalic somite, and opens through a
tripartite valve into the midgut at a point near the base of the ocular
tubercle; a similar tripartite valve exists at the junction of mid and hindgut.

2. Circulatory system

The relatively simple circulatory system is centred on the middorsal heart,

which extends in the trunk from the level of the first pair of legs back to the
base of the abdomen. A recent detailed study of the heart of Nymphon
macronyx and Boreonymphon abyssorum by Tjonneland et al. (1985), has
shown that the roof of the heart is formed by the inside of the body wall, and
the floor by cells of the horizontal septum attached to the gut. The heart is
assumed to be a phylogenetically reduced structure, functioning more as a
channel than a pump, and a significant contribution to pumping for
 THE BIOLOGY OF PYCNOGONIDA 19

A B

s
f

FIG. 11. Sections through the proboscis of Rhynchothorax australis: A, immediately after the
anterior surface; B, at the level of the main proboscis ganglia; and C , at the insertion of the
proboscis into the cephalon (after Fry, 1965). a-arthrodial membrane, c4 i r cu l ar muscle, f-
filter of setae, g-foregut, i-interradial muscle, I-lip tendon, m-main proboscis ganglion,
n-proboscis nerve, pproboscideal ganglionic commissure, r-radial muscle.

circulation may derive from gut peristalsis and leg movement. There are
paired lateral ostia opposite the second and third pairs of lateral processes,
and in some species a t least an unpaired posterior ostium.
A horizontal membraneous septum separates the entire body, including
appendages and proboscis, into two halves, the resulting dorsal sinus of
haemocoel having a smaller capacity than the ventral half. The circulation is
easily observed in transparent or translucent species. Blood generally flows
from the anterior of the heart into the proboscis, and outwards from the
trunk to the ends of the limbs in the ventral sinus, and returns along the
dorsal sinus; the septum has slits in the area of the lateral processes allowing
interconnection of the whole haemocoel. Pulses of blood flow, or “contrac-
tions”, have been counted at 120 to 180 per minute in Phoxichilidium
femoratum, while Endeis spinosa showed 172 systoles when in fresh condition
falling to 126136 one day later (Cole, 1910).
Blood corpuscles have been described for Anoplodactylus lentus by Daw-
son (1934), as variably-sized thin discs, irregularly oval or lenticular,
nucleate and very flexible; they varied from pink to purple and dark blue,
apparently in relation to the amount of pigment in the cells and its state of
oxidation or reduction. The pigment is neither haemoglobin nor haemeryth-
rin, and haemocyanin has only been found dissolved in the plasma. More
20 F. ARNAUD AND R. N . BAMBER

circurnoescphageal
corninissure
suboesophageal
stornodeal-

oviger nerve

FIG. 12. Nervous system: A, brain and anterior nerves of Nymphon, and distribution of trunk
ganglia of B, Nymphon pixellue; C , Dodecolopodu muwsoni; and D, Colossendeis australis.

recent studies by Redmond and Swanson (1968) on the Antarctic Ammothea

striuta have found small, elongate, granular blood cells, some 8 pm long by
6 pm wide, with an indistinct nucleus.

3 . Nervous system

The pycnogonid central nervous system is based on a ventral chain of

ganglia, with, in the cephalon, paired suboesophageal ganglia, circumoeso-
phageal commissures and supraoesophageal ganglia (Fig. 12); the paired
ganglia are fused to the point of a bilobed “mass”. From the cephalic
ganglia arise paired nerves for innervation of appendages (chelifores, palps)
where present, and the eyes and proboscis; the nerves in the latter, one along
each antimere, are interconnected by “ring nerves” giving a ladder-like
structure. The supraoesophageal ganglia comprise a brain, but comprising
only a protocerebrum and tritocerebrum, lacking a deutocerebrum. Of the
ventral ganglia, the first innervates the ovigers, and the following ganglia
each innervate one pair of legs; all ventral ganglia supply paired nerves to
the ventral body muscles, and the last supplies three paired nerves to the
abdomen.
The best known sense organs are the eyes: the majority of species have
four eyes borne on the ocular tubercle, though species living away from light
 THE BIOLOGY OF PYCNOGONIDA 21

show progressive reduction. A detailed analysis of the eye structure and light
responses in Nymphon gracile and Pycnogonum littorale is given by Jarvis
and King (1973, 1979). The simple eyes are composed of three layers. An
outer ectoderm layer producing the biconvex cuticular lens (shed during
ecdysis) is secreted by the underlying hypodermal cells; a middle layer of
columnar retinal elements (neurons) is bounded on the cuticular side by
translucent vitreous cells and on the inner side by similar but reflecting cells
forming the tapetum; the inner layer is of anucleate pigment cells, 3 4 cells
deep. The axon of each retinal neuron passes through the tapetum and
pigment layer independently, before they unite to form the ocellar nerve.
The eyes can detect light extending into blue and red wavelengths, but
presumably only detect intensity rather than forming images.
That the eyes are the only light-sensitive organs of the pycnogonid was
demonstrated by Cole (1901), who showed that Anoplodactylus lentus was
totally unresponsive to light variations after removal of its ocular tubercle.
Chemoreceptors certainly appear to exist on different parts of the body, as
Stock (1978a) demonstrated the ability of three species (Endeis spinosa,
Nymphon gracile and N . hrevirostre) to detect food-contaminated water.
While palps are likely sites for chemoreceptors in Nymphon species, Stock
found N . gracile still detected hydroids after ablation of chelifores, palps or
ovigers, and of course Endeis species do not possess these limbs. He
postulated the presence of chemoreceptors on innervated epidermal bristles,
sensory setae on the distal part of the proboscis, or perhaps on the walking
legs. Bifid hairs and hollow or cup-borne setae are common on pycnogonid
cuticles (Fig. 7), and are almost certainly sensory. Richter (1982) attributes a
chemosensory or thermosensory function to the “lateral sense organs” on
the ocular tubercle (“Sokolow’s organ”) of Anoplodactylus pygmaeus.

4. Reproductive system

Almost all pycnogonids are dioecious. The ovary is a paired, basically U-

shaped organ, lying in the trunk above the gut, and commonly extending
into the legs (Fig. 13). King and Jarvis (1970) have studied Nymphon gracile,
which shows vitellogenesis in the leg branches, and Pycnogonum littorale,
which shows an additional junction between the lateral branches of the
ovary (Jarvis and King, 1972). The ovary opens through a relatively large
genital pore, situated on the anteroventral part of each second coxa in most
pycnogonids, though in P. littorale the pores are on the posterodorsal face
and in Rhynchothorax on the ventral face of the 2nd coxae of the last pair of
legs only. The pore possesses a closing lid or operculum (Jarvis and King,
1972). Ova are usually stored in the dilated femurs of all legs prior to laying.
However, various species have been found in which the gravid females store
22 F. ARNAUD AND R. N. BAMBER

A n B

gonopore

FIG. 13. Female reproductive systems of: A, Nymphon gracile (after King and Jarvis, 1970);
and B, Pycnogonum littorale (after Jarvis and King, 1972).

the eggs in the greatly expanded second coxae, including Ascorhynchus

abyssi from the abyssal north Atlantic (Sars, 1891), A . ovicoxa from deep
waters off Florida (Stock, 1975d), the abyssal A . birsteini from off Peru
(Turpaeva, 1971c) and a new species of curious shallow-water tropical
Ammothella from South Madagascar (Arnaud, unpublished).
The testis is similarly a paired organ situated dorsally above the midgut,
with two lateral branches either uniting posteriorly (Nymphon, Colossendeis)
or fused along their length to form a sheet as in Pycnogonum tittorale (Fig.
14); branches extend down each leg as far as the male genital openings which
may be on the ventral face of second coxa on each leg (Colossendeis
colossea), of the last two pairs of legs (Nymphon robustum), or only the last
pair (some Pycnogonum and Rhynchothorax species). The male genital
opening is typically a small pore, often on a raised mound, but may be raised
on a ventral conical or tubular process (for example various Achelia and
Anoplodactylus species).
One true hermaphrodite species has been described, Ascorhynchus cor-
deroi, first taken from Brazil (Marcus, 1952), and subsequently from
Mauritius (Stock, 1965) and South-West Madagascar (Arnaud, unpub-
lished). Individuals had well developed ovaries overlying well-developed
testes, and were ovigerous. The occurrence of gynandromorphs has been
recorded recently in the genus Anoplodactylus. Child (1978) caught a large
 THE BIOLOGY OF PYCNOGONIDA 23

goncipo r e

FIG. 14. Male reproductive systems of: A, Nymphon gracile (after El-Hawawi and King, 1978);
and B, Pycnogonum liftorale (after El-Hawawi and King, 1978a).

collection of A . portus off the Pacific entrance of the Panama Canal, 12.5%
of which were gynandromorphs; while some specimens were fully bilateral
gynandromorphs with one half of the body of each sex, others were random
sexual mosaics, with mixed male and female characters variably present on
the body. Child and Nakamura (1982) found one gynandromorph in 600
specimens of the Japanese endemic A . gestiens; it had male ovigers, ripe
ovaries in all legs, eight genital pores and one reduced femoral cement gland
on the fourth left leg (Fig. 15). Karyotypic characteristics among pycno-
gonids remain poorly understood.

5. Integument

The pycnogonid integument consists of a chitinous layer over epithelium,

perforated by many pores; the epithelium may be pigmented (e.g. Parapal-
lene australiensis). Unlike that of Crustacea, the cuticle is never calcified.
Krishnan (1955) studied Propallene kempi and concluded that the cuticle is
hardened by disulphide linkages, as proposed for the arachnid Limulus.
Wyer (1972) found the cuticle would stain with Mallory’s triple stain only
after treatment with alkaline sodium sulphide, which breaks down sulphide
bonds.
24 F. ARNAUD AND R. N. BAMBER

A
ovary
\

\ ' ' ' ' midgut d'iverticulum

t e s t is

FIG. 15. Proximal leg segments of Anoploductylus gestiens: A, normal female; B, gynandro-
morph, with enlargement of cement gland; and C , normal male (after Child and Nakamura,
1982).

The surface pores lead from various cutaneous glands, some of which
appear to be mucus-secreting, others excretory. The cuticle also supports
various tubercles, spines and setae, some of which are undoubtedly sensory,
while others seem to serve only to accumulate silt and detritus. Paranymphon
spinosum commonly exhibits peculiar stellate structures on its lateral pro-
cesses, originally assumed to be epizooites; they are clearly integumental
structures, but their function is unknown. The cuticle is commonly exploited
as a substratum by sessile epizoans (see below), but these are lost at
moulting.
All pycnogonids have to moult their cuticle to grow. In Pycnogonum
fittorafe the cuticle splits such that each leg is shed separately, as a sleeve,
 THE BIOLOGY OF PYCNOGONIDA 25

and longitudinal lateral splits in the body cuticle allow it to be shed as a

dorsal and a ventral piece (Lotz and Buckmann, 1968). The dorsal piece
includes the eye coverings and the lining of the hindgut, while the ventral
piece includes the lining of the foregut, with the “oyster basket”. Palps and
ovigerous legs, where present, are shed as part of the ventral body piece. At
least Pycnogonum littoraze continues to moult after it has reached sexual
maturity (King, 1973).

C. Cluss$cation

Classification amongst the Pycnogonida has always been unstable, and the
subject of controversy. The fact that the group has been comparatively
understudied has led to the persistence of Victorian taxonomy, and the
promulgation of such bad habits as the classification of characteristics rather
than animals (qv Mayr, 1969). Stability was brought to pycnogonid taxo-
nomy by Hedgpeth (1947), using a system of common sense and traditional
morphological distinctions. His currently accepted classification (see also
Hedgpeth, 1982) is based on characters of easy distinction, such as presence
or absence of cephalic appendages or their number of segments, and more
recently features of the male cement gland and the presence or absence of a
strigilis on the oviger (Child, 1979).
As in any taxonomy, the higher categories are largely artificial groupings
of convenience. Hedgpeth advocated two orders within the class Pycno-
gonida, the Palaeopantopoda to cover all fossil pycnogonids, and the order
Pantopoda for living species. Within the latter were eight families, falling
into two groups (without implication of ordinal rank), the first three (below)
being those in which ovigers are absent in the females, whereas they are
present in both sexes in the other five (with Tanystylidae separated from the
Ammotheidae).
As Hedgpeth (1982) says
“There is no easily discernible evolutionary progression: attempts to construct
such family trees inevitably produce interlocking and anastomosingshrubbery
...
Higher taxonomic analysis by dichotomy based on presence or absence of
appendages leads to
“phylogenies which are almost automatically inverting and to overlapping sets
of genera . . .” (Fry, 1978b).
The Endeidae comprise a single genus, Endeis (20 species). Chelifores and
palps are absent, and the male oviger has seven segments.
The Pycnogonidae has the two genera Pycnogonum (47) and the polymer-
ous Pentapycnon (2). Chelifores and palps are again absent, and the legs are
characteristically short and heavy, without modified tarsi.
26 F. A R N A U D A N D R. N . BAMBER

The Phoxichilidiidae includes five genera, Phoxichilidium, Hodgsonia,

Phoxiphilyra and the very numerous Anoplodactylus (over 100 spp), and
recently Stock (1978~)has transferred Pallenopsis to this family from the
Callipallenidae. Palps are lacking, or rudimentary in Pallenopsis, but the
chelifores are present and chelate.
The Colossendeidae is dominated by the genus Colossendeis with at least
50 species, and also includes eight species of Rhopalorhynchus, two of Hedg-
pethia, and the polymerous genera Dodecolopoda and Decolopoda; the 10-
legged Pentacolossendeis has recently been transferred to the Ammotheidae
(Fry, 1978b). Long 10-segmented ovigers are present in both sexes, as are
long nine or 10-segmented palps; chelifores are only retained in the adult by
polymerous forms.
The Nymphonidae comprises nearly 200 Nymphon, six Heteronymphon,
three Boreonymphon, one Neonymphon, and the polymerous genera Penta-
nymphon (2) and Sexanymphon (1, see Fig. 22). Two-segmented chelifores
and five-segmented palps are present, and 10-segmented ovigers are present
in both sexes.
The Callipallenidae includes 20 genera (Callipallene, Pseudopallene, Oro-
pallene, etc.) in a rather heterogeneous collection of over 100 species; palps
are reduced or absent, and the chelae usually short and heavy.
The Ammotheidae is larger again (36 genera and perhaps 200 species),
and certainly polyphyletic. Ovigers are nine or 10-segmented, in both sexes,
palps present, and chelifores two segmented, though in many genera the
chelae are reduced to knobs.
This convenient structure of families is frequently changing. Many
workers have separated the Tanystylidae (including Tanystylum and Austro-
decus) from the Ammotheidae, and subsequently the Austrodecidae (Austro-
decus) from the former, to be joined by the genus Pantopipetta. The status of
the Family Rhynchothoracidae for the single genus Rhynchothorax is receiv-
ing increasing support. There are in addition certain genera whose affinities
are doubtful, e.g. Queubus, Hannonia.
Fry (1978b) subjected some 45 morphological characters for each genus
(though only 37 available for every genus) to multivariate statistical analysis,
and produced a new taxonomy based on five orders and 30 families. Some
conclusions, such as the positioning of Boreonymphon amongst the Colos-
sendeids and Phoxichilidium amongst the Ammotheids are at least surpris-
ing, and will require corroborative evidence or, in Fry’s own words, exacting
and minute study, before becoming universally accepted. Nonetheless, his
thesis that the extant pycnogonids are too diverse a group to be placed in a
single order is indisputable. At the opposite extreme, many species are badly
in need of clarification, and for example, the vast genus Nymphon requires a
monumental effort to resolve its undoubted species synonymies. Too many
 THE BIOLOGY OF PYCNOGONIDA 27

species are distinguished on the characters of one or a few individuals

(admittedly sometimes all that is available) in a class which is known to
exhibit intraspecific morphological variation (e.g. Bamber, 1982). Pro-
cedures of multivariate statistics are again only recently being applied at
specific and generic levels (e.g. Bamber, 1982, 1985a), but do offer less
subjective or opinionated conclusions on distinction or synonymy.
Munilla and de Haro (1981) have approached the problem using electro-
phoretic techniques for nine Mediterranean species from the Catalan coast.
They concluded that the Nymphonidae, with a low number of protein
fractions, were the most primitive family of those they studied (not including
the Colossendeidae), while the Pycnogonidae and Callipallenidae were the
most highly evolved. King et al. (1986) also used electrophoretic techniques
for species discrimination in the genus Endeis.
A synthesis of the current classification of families and genera is given as
Appendix 2.

111. Physiology and Function

Pycnogonids occur over a wide bathymetric range from the tide-line to

abyssal trenches. Consequently, their tolerance of environmental character-
istics is variable, the littoral forms being adapted to variations of tempera-
ture, salinity and possibly desiccation, while abyssal species are subjected to
high hydrostatic pressure and low (polar) or high (hydrothermal vents) but
stable temperatures. In the former case light may be a significant environ-
mental stimulus, while it is perpetually absent in the latter. Such varied
ecological conditions may be expected to influence greatly physiological
processes.
Despite their appropriateness as laboratory animals, being small, often
transparent and slow moving, pycnogonids have not been the subject of
much study regarding ultrastructure and physiology. It has taken the recent
attempts to elucidate arthropod phylogeny to stimulate such studies as that
of the fine muscle structure by Totland and Kryvi (1986). However, in many
areas, as in pycnogonid cytology, too little knowledge is yet available.

A. Salinity Tolerance

That pycnogonids are not exclusively marine was shown by Wolff (1976),
who studied estuarine pycnogonids in the Netherlands. He observed that
Nymphon rubrum ( = brevirostre) tolerated salinities of 11-12%0, and could
28 F. ARNAUD AND R. N. BAMBER

penetrate estuaries some way inland; most other species tolerated down to
15%0(Achelia echinata, Callipallene brevirostris, Pycnogonum littorale), or
required higher salinities than this (Anoplodactylus petiolatus, A . pygmaeus,
Phoxichilidium femoratum), the latter group of species occurring no further
upstream than the mouths of the Rhine, Meuse and Scheldt.
The salinity tolerances of ~ y ~ ~ gracife
h o n and Achefia echinata were
tested in the laboratory by El-Hawawi and King (1978b) over a range from
34%0to distilled water and at different temperatures. Both species were more
tolerant of low or varying salinity at lower temperatures, and adults were
more tolerant than larvae both at high temperatures and in varying salinity.
N . gracile, which occurs higher on the shore in warm summer months, was
more tolerant than A . echinata.

B. Digestion

Digestive processes in pycnogonids have been little studied. The status quo
suggested phagocytic uptake within the gut (Schlottke, 1933). Recently,
Richards and Fry (1978) investigated food uptake and digestion, particu-
larly in two Antarctic species, Nymphon uustrale and N . orcadense, and
concluded that phagocytosis was not the process involved, despite numerous
attempts to induce it; rather their numerous histological and vital dye
methods suggested a sequence of micropinocytosis, followed by fusion of
primary lysosomes with pinocytotic vesicles, digestion of the contents of the
secondary lysosomes so formed, the formation of residual bodies (enigmo-
somes) and autophagic vacuoles, and possible migration and release of
residual bodies into the gut lumen. The midgut cells were found secreting
various enzymes, such as proteases (a trypsin-like enzyme in N . orcadense),
carbohydrases (amylase, DNAase and RNAase substrate film tests gave
unclear results, leading to negative results after incubation for two weeks at
0 "C), and nucleases. Acid-phosphatase activity found in the foregut was
interpreted as associated with the ingested prey. Alkaline-phosphatase was
also detected, but with results too variable for confirmation.
These authors also reported (ibid) on the long resistance to starvation
exhibited by the Arctic Nymphon hirtipes and the Antarctic N . australe and
N . orcadense, which survived apparently undamaged for up to 18 months
without food. Their guts took two months to actually empty. Subsequent
compensatory nutritional possibilities include reduced metabolic rate, tissue
resorption, cuticular uptake, or filter feeding, all promising areas for future
investigation.
 THE BIOLOGY OF PYCNOGONIDA 29

C. Respiration

Historical difficulties in obtaining pycnogonid specimens of large enough

size and in large enough numbers have precluded studies on respiration until
recently. Douglas et al. (1969) collected seven species of large pycnogonid by
scuba-diving or shallow trawling in the Antarctic, and measured oxygen
consumption at temperatures from 0-1.2 "Cin the laboratory (natural water
temperatures being - 1.9-0 'C): consumption ranged from 0.004-0.014 ml
O,/g/h (Table 2), some three times lower than values observed in Arctic
isopods (Scholander et ul., 1953).
TABLE2. OXYGENCONSUMPTION OF SOME ANTARCTIC PYCNOGONIDSOBSERVED AT
PALMER IN JANUARY-FEBRUARY
STATION 1969 (AFTER DOUGLAS
et al., 1969)
0, con-
sump-
Surface Net tion
area Volume Weight (ml/
Species Sex (cm')* (ml) (g) g/h)
Ammothea carolinensis Leach F. 53.2 3.9 2.9 0.011
Ammothea carolinensis Leach M. 55.6 4.2 4.0 0.012
Ammothea carolinensis Leach M. 52.8 2.3 3.7 0.014
Pallenopsis cf. patagonica (Hoek) F. 56.3 3.4 2.2 0.013
Pallenopsis cf. patagonica (Hoek) M. 29.8 1.5 1.4 0.007
Colossendeis australis Hodgson F. 136.2 17.0 11.0 0.006
Colossendeis australis Hodgson M. 114.3 12.1 7.3 0.009
Colossendeis megalonyx Hoek M. 35.3 1.8 0.8 0.014
Colossendeis robusta Hoek M. 42.2 2.6 1.9 0.014
Colossendeis scotti Calman F. 95.0 10.1 9.4 0.010
Colossendeis scotti Calman F. 124.9 14.7 5.9 0.009
Colossendeis scotti Calman M. 82.0 7.4 7.2 0.008
Decolopoda australis Eights F. 84.0 6.8 4.9 0.004
Decolopoda australis Eights M. 53.0 3.7 3.0 0.011

*Calculated by W. E. Stout.

Blood samples (about 0.5 ml for a large Ammothea striuta) were analysed
after centrifugation for metallic and chloride content, and were found to
show rather high concentrations of potassium and magnesium, suggestive of
ionic regulation (Redmond and Swanson, 1968). However, since sampling is
impossible without puncturing the gut, some contamination by gut fluids is
possible; the authors suggest that, if such contamination is the case, then the
gut epithelium may be an important site for ionic regulation. They further
discovered large quantities of (unidentified) proteins in the blood, but no
evidence of a respiratory pigment.
30 F. ARNAUD AND R. N. BAMBER

3.
TABLE OXYGEN CONSUMPTION OF TWO NORTHEUROPEAN SHALLOW-WATER PYCNO-
GONIDS AT A TEMPERATURE OF 10 “C (AFTER DRESCO-DEROUET,
1978, MODIFIED).*

0, consumption
Species Weight (mg) (mligih)
Nymphon gracile 6.88 0.097
10.34 0.070
10.92 0.106
15.50 0.062
17.93 0.065
23.55 0.054
Endeis spinosa 7.60 0.101
11.20 0.100
11.31 0.102
11.85 0.064
13.20 0.073
16.40 0.055
*Mean values upon 3 measures of experiments.

More recently, Dresco-Derouet (1978) studied the respiratory metabolism

of two coastal European species, Nymphon gracile and Endeis spinosa. The
results (Table 3) are an order of magnitude greater than those in Table 2,
and are equivalent to some of the highest respiratory intensities recorded for
littoral or sublittoral crustaceans. The oxygen consumption was increased
for pycnogonids in a group (i.e. greater than the sum of their isolated
consumptions), and increased up to five times in specimens during copula-
tion.

D. Locomotion

In recent decades the study of the functional morphology of locomotory

mechanisms amongst arthropods has been actively studied by various
authors. Manton (1978) has collated her studies, and highlighted the double
ability of pycnogonids, viz walking and swimming, two mechanisms which
can require conflicting organization of the body. All locomotory function
depends on the muscle formation in relation to the articulation of the rigid
exoskeleton, enabled by unthickened cuticle (arthrodial membrane) at the
numerous joints. Manton (ibid), referring to the unique coxa-body joint of
pycnogonids, providing levator-depressor movements, said that “walking is
not the primary concern of these animals”; these joint movements produce
an easy raising and lowering of the whole body on fixed tarsi, as used during
feeding or swimming.
 THE BIOLOGY OF PYCNOGONIDA 31

1. Walking

Walking in pycnogonids is famously slow. Schram and Hedgpeth (1978)

analysed cine-film of walking in several Antarctic species, including poly-
merous forms. They distinguished two “morphogroups”, the first of short-
legged crawling species such as Pentapycnon charcoti, the second of long-
legged walking species (Colossendeis australis, C. angusta, Pallenopsis pata-
gonica, etc.) in which the legs suspend the body some distance from the
substrate. They describe in detail the musculature and joint movements of
the legs, observing no difference with polymerous species other than appar-
ently improved coordination. While the body-first coxa joint shows very
reduced mobility, the coxa l k o x a 2 joint possesses very large flexor-
extensor muscles, and is the only promotion-remotion joint in the leg.
Amplification of small joint movements is enabled by the long leg segments.
Extension of joints lacking extensor (tibia 2-tarsus) or any (tarsus-propodus)
muscles is yet to be accounted for, but may rely on hydrostatic pressure. The
overall morphology allows the pycnogonid to move forward, backward or
sideways without reorientating the trunk.

2 . Swimming

Active swimming has been reported in the long-legged genera Anoplodacty-

lus, Callipallene and Nymphon (see also below under “tropism”). Grassle et
al. (1975) directly observed the swimming of the large benthic Colossendeis
colossea during a dive of the research submersible “Alvin” at 1900 m depth
on the North American continental slope, and described it as follows:
“The swimming movements were like the opening and closing of an umbrella.
On the ‘closing phase’, the limbs were brought together and the animal was
propelled upward into the water; on the ‘opening phase’, the limbs were
extended away from the body and thus slowed the sinking rate. Through such
alternate activities of rising and sinking, the pycnogonid moved along the
bottom.”
Many Colossendeis and other species have been observed folding their legs
dorsally into a “basket” posture (Schram and Hedgpeth, 1978) reducing
body surface resistance and allowing rapid sinking to the bottom. Staples
(1977) illustrated this characteristic posture in Stylopallene longicauda from
Australia.
Morgan (1977, 1978) studied swimming in the small benthic North
Atlantic species Nymphon gracile; this behaviour was coordinated with ebb
tide currents to allow an offshore migration. The legs beat in a metachronal
rhythm starting at the posterior pair. Oxygen consumption during minimal
activity before swimming was just over 100 p10, per gram of wet weight per
32 F. ARNAUD A N D R. N . BAMBER

hour, rising to approach 300 as activity increased; transformation of

biochemical to mechanical energy in the muscle was estimated at 25%
efficiency. N . gracile could swim for some 52 h before depleting its fuel
reserves, though each bout of swimming lasted from less than 30min to
about 6 h, synchronizing with the tide.
While only the longer-legged genera would seem capable of active swim-
ming, the only specializations of leg morphology are possibly the long setae
on the legs of some Pallenopsis (as also on the trunk of Ascorhynchus simile).

3. Tropism

Both positive and negative phototropism has been recognized in pycnogo-

nids. Cole (1901) observed positive phototropism in swimming Anoplodacty-
lus lentus, Callipallene brevirostris and Endeis spinosa in response to “light of
moderate intensity (diffuse daylight)”. Fage (1932) reported numerous
catches in plankton samples of the benthic Nymphon gracile and (occasion-
ally) C. brevirostris off South-Western France at night using a light, and
Ohshima (1 933a) obtained Propallene longiceps,C. amaxana and a juvenile
Anoplodactylus off Japan “at night using an acetylene light”. Le Calvez
(1 950) similarly caught the curious sand-dwelling Nymphonella tapetis at
night with a light off the French Mediterranean coast, including males,
females and juveniles. In New Zealand, Clark and Carpenter (1977)
observed four pycnogonids “swimming vigorously into the light from the
direction of open water, maintaining this activity and remaining near the
water’s surface for over an hour”. They were identified as Ammothea
magniceps on capture, the first record of such behaviour for this true benthic
species, and the first record of such sustained directional swimming.
Negative phototropism was first reported for Pycnogonum littorale by
Prell (1910). More recently it has been reported for the littoral Mediterra-
nean species Rhynchothorax anophthalmus, twice recorded from shaded
habitats off Marseille, R. alcicornis, from coralligeneous algae in the same
area, and R. alcicornis, from 6-8cm deep amongst roots of the marine
phanerogam Posidonia oceanica (Arnaud, unpublished data).

E. Nerve Function

In their comparative studies of neural conduction velocity in Antarctic

organisms, MacDonald and Ensor (1975) included the pycnogonid Colos-
sendeis robusta along with the isopod Glyptonotus antarcticus and various
fish. At ambient temperatures ( - 1.9 “C) the two arthropods had the lowest
velocities: the slowest fibres in the leg of C. robusta had a velocity of 0.03 mi
s, close to the velocity of a coelenterate nerve net, and which compares with
120m/s in mammalian fibres. At higher temperatures (up to 28 “ C ) the
 THE BIOLOGY OF PYCNOGONIDA 33

nerves contracted and became stiff, probably owing to denaturation of their

collagen. This slow neural conduction velocity may help explain the ubiqui-
tous sluggishness of pycnogonids.
While a neurosecretory function has been suggested for certain large nerve
cells in Phoxichilidium femoratum and Endeis spinosa, and the cerebral
“Sokolow’s organ” found in some pycnogonids (Hanstrom, 1965), the
endocrine system, if present, is as yet unknown. Behrens and Buckmann
(1983) have isolated two ecdysteroids in Pycnogonum littorale, one 20-
hydroxyecdysone, the other unknown, though similar to ecdysone.

F. Bioluminescence

Herring (1 983) studied the spectral characteristics of luminous marine

organisms in the laboratory; he found that the legs of Colossendeis ?gigantea
(? = C. proboscidea) had an emission maximum of 485nm with a half
bandwidth of 84 nm at 18-25 “C, corresponding to a blue-green light, “to
which the visual pigments of most marine animals are most sensitive”. Since
the experiment involved pretreatment with hydrogen peroxide, and thus was
not strictly in vivo the results must be treated with caution. Earlier, Calman
(1923) claimed that C. colossea showed phosphorescence, and this phenom-
enon is also reported for Nymphon gracile by Jarvis and Isaac (in King,
1973).

IV. Life Cycle

A. Reproduction

Studies on the reproductive processes in pycnogonids were begun last

century by Hoek (1881a), Dohrn (1881) and Morgan (1891); more recent
advances over the past 15 years have been possible with the advent of
modern cytological and electron microscopic techniques.
All pycnogonid families are known to produce eggs which hatch into
protonymphon larvae with the notable exception of the Colossendeidae.
Despite the large number of species described in the genus Colossendeis, and
their frequency of capture, nothing is known about reproduction in this
family; no males have been found carrying eggs or larvae, and some
alternative life history strategy, possibly direct development or internal
brooding, is suspected. Similarly, Nakamura and Child (1983) commented
on the fact that, while great numbers of Ascorhynchus utinomii were collected
over a six-year period in Nabeta Bay, Japan, no larvae or juveniles were
found; they suggest a possible commensal or parasitic relationship with a
larger sessile invertebrate.
34 F. A R N A U D A N D R. N. BAMBER

mitochondrion

nucleus w i t h single
adielectronic inclusion

-
_I
W
I-
>
W
ooplasm with densely
packed free ribosomes
LT
a

active golgi complex

/
micropinocyt osis

ribosomes a t t a c h e d t o
endoplasmic r e t i c u l u m

flocculent m a t e r i a l
in r o u g h e.r.

&protein c a r b o h yolk
y d r a tpel u s

3
1 1 -nucleus

FIG. 16. Cellular processes during egg development in Nymphon gracile (after Jarvis and King,
1978).

The pycnogonid species which have been studied in detail are, for
practical expediency, those which have occurred in considerable numbers in
the areas concerned, viz Pycnogonurn littorale, Nymphon gracile, N . hrevi-
rostre and N . leptocheles from North European coasts, PropaIlene kempi from
India and P . longiceps from Japan.
 THE BIOLOGY OF PYCNOGONIDA 35

B. Vitellogenesis

Vitellogenesis in pycnogonids has been studied using histochemical and

electron microscopic techniques by Jarvis and King (1978). A previtello-
genesis takes place in the ovaries in the trunk, producing oocytes with a large
nucleus, Fatty yolk appears in the oocytes as lipid and phospholipid
droplets, produced intra-oocytically; these break down as the yolk rationa-
lizes to B typical platelet. This synthesis of yolk within the oocyte, associated
with annulate lamellae of the endoplasmic reticulum (Fig. 16), with only a
limited amount of pinocytosis later in development, is considered a primitive
type of vitellogenesis, closely resembling that of annelids and the horseshoe
crab, Limulus polyphemus. The time to egg production is much longer than
processes involving yolk contribution from outside the oocyte, as for
example in insects.
Vitellogenesis in Nymphon gracile occurs in the coxal and femoral diverti-
cula of the ovaries, exclusively in the diverticula in Endeis spinosa, but
throughout the ovary in Pycnogonum littorale. Achelia echinata females in
South Wales were found to produce ova for 4-5 months after the first
appearance of previtellogenic oocytes.

C. Spermiogenesis

Van Deurs (1974) described in detail the sperm cells of Nymphon leptocheles
and N . brevirostre, finding them a primitive type: “the motile sperm consists
of a somewhat elongated head, a kind of midpiece and a long tail; an
acrosome is absent.” The sperm of N . gracile (Fig. 17) consists of a head,
about 13 pm long and without an acrosome, a middle-piece of about 2.5 pm,
containing the posterior of the nucleus, the mitochondria and a centriole
forming the basal body of the flagellum, and a tail, a free flagellum some
27 pm long with an 18 + 0 axoneme pattern (El Hawawi and King, 1978a). In
N . leptocheles the tail is 30 pm long with a 12 + O axoneme pattern, and in N .
brevirostre a 9 + 0 pattern (Van Deurs, 1973).
The spermatozoa of Pycnogonum littorale are somewhat aberrant, being
nonflagellated and unmotile, clavate and some 160pm in length, with a
simple axoneme. The sperm consists of only a small vesiculated nucleus,
highly modified mitochondria (perhaps with reduced metabolic activity),
and a complex system of microtubules. The process of spermiogenesis in this
species results in a considerable reduction in nuclear volume, but with no
chromatin condensation, while there is an increase in the number and
complexity of microtubules present (King and El Hawawi, 1978). The
function of the microtubule system is unknown, but it may assist the entry of
36 F. ARNAUD AND R. N. BAMBER

FIG. 17. Mature sperm of Nymphon gracile, showing cross sections along its length (after El-
Hawawi and King, 1978a).

the sperm into the egg. Since the eggs of this species are released in a single
large mass, into the centre of which the sperms are released, they have little
need for motility or energy; since activity of the mitochondria is reduced, the
microtubule system may supply this small energy requirement, and ATP-ase
activity has been associated with microtubules in other animals.

D. Fertilization and Egg Laying

The mating behaviour of Propallene longiceps has been studied in detail in

the laboratory by Nakamura and Sekiguchi (1980). They distinguished five
steps from copulation, or pairing, to egg transfer:
1. the male holds the female, stimulating oviposition
 THE BIOLOGY OF PYCNOGONIDA 37

mature eggs

I
/I

3
gono po r e

FIG. 18. Process of release of one of two mature eggs in the femur of PropaIlene longiceps (after
Nakamura and Sekiguchi, 1980).

2. mature eggs are released from the ovary in the femur of the female, and
forced towards the genital pore
3. the female holds the eggs with her ovigerous legs
4. the eggs are transferred from the female to the male
5. the male forms the eggs into a bracelet-like eggs mass around each
ovigerous leg, where they are carried until hatching.
Mating may take from a few minutes in Anoplodactylus lentus (Cole, 1901)
to a few hours in Nymphon gracile and P. longiceps, and up to five weeks in
Pjmogonum littorale (Jarvis and King, 1972). During pairing, the relative
positions of the partners are different in these last two species. In P . liftorale,
the female of which lacks ovigers, King and El Hawawi (1978) report that
the male climbs on the female's back, then crawls over her head to lie
beneath her, such that they cling together with their genital apertures
touching; as the egg mass is extruded by the female, it is collected by the
ovigers of the male, and the whole spawning of the female is carried in a
large ball beneath the male. In PropaIlene Iongiceps, the male attaches to the
dorsal side of the female, facing the same direction, and holds her at the base
of her chelifores with his chelae; the four distal segments of the male's
ovigers normally grasp the female's second walking legs. The male flexes his
38 F. ARNAUD A N D R. N. BAMBER

ovigers while the female folds her walking legs. The male, lying on his back,
holds the female to his ventral surface for an hour or more.
The female P. longiceps usually has two mature eggs in the femoral ovary
diverticulum; during mating they are released singly from the ovary, distort-
ing in the restricted space around the ovary (Fig. 18). The eggs move inwards
through the 3rd coxa to the genital pore on the 2nd coxa, through which
they pass. This migration of the first egg takes some 10-25 min from release
to laying, the second egg following 3-5 min later. The female collects the laid
egg with her ovigers, and the male bends his fourth legs to bring the genital
pore on the 2nd coxa to a position close to the egg, maintaining this position
for 5-10 min while actively moving his ovigers. Since eggs removed from the
female at this stage develop normally, fertilization has occurred.
In the fourth phase the male releases his hold on the female by his chelae,
the eggs are transferred to the ovigers of the male by movements of the
female's distal oviger segments, and the couple separates.
The male femoral cement glands secrete mucus with which he covers the
eggs, forming a bracelet-like structure around his oviger, each of the
normally eight eggs attached singly to the bracelet by a thread; the mucus
hardens after 24h. One male may bear 4-6 bracelets on each leg, the
maximum observed being 1 1. Experiments involving marking some females
showed that each bracelet contains eggs from a single female, but a male
may carry bracelets from several females, the most recent being' collected
proximally on the ovigers. Observations of the state of maturity of embryos
in the up to eight egg balls held on the ovigers of male ArnmothelZa longipes
(Bamber, unpublished data) also showed that development was uniform in a
single ball, but different balls showed different ages of embryo, inferring
their collection from different females.
The detailed account of mating of Propallene longiceps from Nakamura
and Sekiguchi (1980) is of the most complete observations, but in many
respects may be peculiar to this species, since parts of the process observed in
other species differ in relative position of partners, duration of copulation,
number of eggs laid, configuration of egg balls, etc.
For example, in Endeis spinosa all the eggs in the femur mature at the
same time, rather than just two (Sanchez, 1959). The eggs are collected in
bracelets in Propallene species, in spherical balls around the oviger in
Nymphon, Phoxichilidium and Achelia species (and most other genera), in a
single cake-like mass in Pycnogonum (even in the absence of male ovigers) or
in a long ribbon in Nymphonella tapetis. The diameter of the eggs ranges
from 21-36pm in Anoplodactylus antillianus, to 70pm in N . tapetis, to
120 pm in Pycnogonum littorale, 300 pm in Propallene longiceps and 400-
500pm in P. kempi.
 THE BIOLOGY OF PYCNOGONIDA 39

E. Embryonic Development

The details of pycnogonid embryology were first discussed by Morgan

(1 89 1) for Tunystylum orhiculure and Phoxichilidiurn mu.uillure ( = P. femoru-
tum). The processes of blastulation and gastrulation follow a typical arthro-
pod pattern, depending on the amount of yolk in the egg; the different
strategies in pycnogonids were described by Helfer and Schlottke (1935) and
reviewed by King (1973).

FIG. 19. Blastulation and gastrulation in Pycnogonum littorale (after Helfer and Schlottke,
1935). m-mesoderm rudiment; e+ndoderm rudiment.

Pycnogonids with small eggs containing a moderate amount of yolk (e.g.

Pycnogonum, Fig. 19) undergo regular cleavage to produce equal-sized
blastomeres. One of these cells moves into the blastocoel to become the
endoderm rudiment; adjacent cells also migrate inwards and around the
endoderm to form the mesoderm. The blastopore so formed by this
gastrulation lies on the dorsal side of the embryo; when it closes, the central
endoderm tissue breaks down to form a syncytium. Pycnogonids with large
yolky eggs (e.g. Nymphon) undergo unequal segmentation during cleavage,
leading t o gastrulation by epiboly. The ectoderm develops as a dome of
40 F. A R N A U D A N D R. N. BAMBER

micromeres which grows over the macromeres; macromere cells immediately

beneath the dome become isolated to form the mesoderm rudiment, the
remainder forming the endoderm, again fusing to produce a syncytium rich
in yolk.
After gastrulation, stomodeum formation is early; midgut forms as a
thick-walled sac within the endodermal syncytium, which then connects to
the ectodermal stomodeum. Mesodermal cells predominantly go to make
muscle in the appendages, scattered residual cells eventually giving rise to
the lateral heart walls, blood cells and, later, the reproductive system; the
formation and development (or regression) of a coelom in pycnogonids is
not known. Ectodermal cells give rise also to the nervous system, initially as
five ganglionic swellings: the first develops dorsally into the protocerebrum,
the second relates to the chelifores, normally moving to fuse with the first;
the remainder stay ventral, corresponding to pairs of appendages, the last
dividing to supply the adult limb pairs as they develop.
Eventually, as the embryo differentiates, three pairs of larval appendages
are formed, with spination, and a proboscis develops around the stomo-
deum; the embryo has become a protonymphon larva.

F. Post-embryonic Development

The eggs of almost all pycnogonids hatch to produce a protonymphon larva.

These larvae (Fig. 20) typically have three pairs of appendages, a pair of
chelifores (whether present in adults or not) and two pairs of ambulatory
appendages (or larval legs), together with an anterior proboscis bearing the
mouth. The appendages have characteristic spines associated with them,
often surprisingly elongate (e.g. Phoxichilidium femoratum), which are prob-
ably actively used to retain the larvae in a cohesive ball on the adult. There is
also a cement gland in the chelifore which can secrete an elongate filament,
which may either assist in attachment to the adult or to a host species for
parasitism, or may be an aid in passive distribution analogous to the byssal
drifting of lamellibranch postveligers. The larval legs d o not develop into
adult limbs, but the latter appear as trunk somites are added sequentially to
the posterior of the larva at each successive moult, each pair of legs taking
two moults to achieve full segmentation in Nymphon brevirostre (Bamber,
unpublished data).
Detailed postembryonic development has been most completely studied in
Propallene longiceps by Nakamura (1981) during laboratory rearing. He
distinguished nine moults from hatching to adult. The first moult occurs at
the same time as hatching, the first instar larva splitting “at the base of the
chelifores in a transverse direction.” The second instar larva (Fig. 21A)
 THE BIOLOGY OF PYCNOGONIDA 41

FIG. 20. Protonymphon larvae of A, Nymphon leptocheles; B, Paranymphon spinosum; C,

Ammothelia iongipes; D, Pycnogonum iittorale; and E, Phoxichilidium femoratum. All scale lines
are 50 pm.

shows differentiated chelifores and proboscis anteriorly, and primordial

ambulatory legs; the second moult, 3 H 8 h after hatching, gives rise to the
3rd instar larva, and during this stage the ocular tubercle and larval
ambulatory limbs develop over 5-6 d (Fig. 21 B,C). The third moult gives rise
to the free-swimming 4th larva, measuring 0.5 mm in body length and with a
pair of chelifores, two pairs of ambulatory legs, and a complete digestive
tract with diverticulae in all appendages. This larva leaves the male 3 G
60min after the 3rd moult, and swims using the two pairs of ambulatory
legs; it initially shows positive phototaxis, swimming towards the surface,
but after 2-3 h shows a negative phototaxis. At this stage the larvae could be
fed on live Artemiu, of which they would suck the body fluids.
After 10-12 d, the fourth moult produces the 5th instar larva, of 0.6 mm
length with three pairs of legs, and initial gonad development. The fifth
42 F. ARNAUD AND R. N. BAMBER

s t ornodeurn

A B C

FIG. 2 I . Larval development of Propallene longiceps: A, 2nd instar; B, 3rd instar; C, late 3rd
instar. ventral above, lateral below (after Nakamura, 1981).

moult after a further 10-13 days results in the 6th instar larva, 1.0 mm long
with four pairs of legs, and now able to swallow Artemiu larvae whole. The
7th instar appears after a further 10-13 days, at 1.4mm length with fully
segmented ovigers and legs. This stage lasts from weeks to months, and
many 7th instar larvae died. The 8th instar larvae were 1.7 mm long, and
females had oogonia in the leg diverticulae of the ovary. The 8th moult
produces the 9th instar, or subadult, at 1.9 mm length, males showing
primordial palps. After another 1-2 months, the 2.2mm adult form is
acquired with the ninth moult, the animals showing full sexual differen-
tiation.
This free-living larval development appears to be uncommon for most
pycnogonids, whose larvae are presumed to pass through a parasitic stage on
an invertebrate host. These larvae generally reach the stage of development
equivalent to the 3rd instar described above on the male ovigers, but
progress little further: Pycnogonum littorale larvae have been kept alive but
unchanging at this stage for 11 months in the absence of the male (Bamber,
unpublished data). At the other extreme, the larvae of the Arctic-sub-Arctic
Boreonymphon abyssorum remain on the male to a late stage of development,
and are still associated as juveniles a quarter the body length of the adult
but without ovigers (e.g. Bamber, 1983b), perhaps equivalent to the 6th
instar stage described above. Hedgpeth (1963) notes the same prolonged
larval association in other Arctic nymphonids, Nymphon hirtipes, N . sluiteri
 THE BIOLOGY OF PYCNOGONIDA 43

and N . rohustum, in the case of the last-named the young being carried until
well over a third the size of the adult.
Hodge (186 1) described the development of the larvae of Phoxichilidium
femoratum as a parasite on Coryne, where they developed in “cysts” until
equivalent to the fifth instar stage described above (three pairs of legs).
Dogie1 (191 1) recorded Pycnogonum littorale ‘‘larvae’’ as ectoparasites on
the polyps of Clava multicornis and Anoplodactylus petiolatus larvae in
polyps of Campanularia petiolatus “where they are parasitic for 8-10 days”.
Okuda (1940) has figured seven stages in the development of Achelia
alaskensis living parasitic under the manubrium of the anthomedusa Polyor-
chis karafutoensis, but he did not succeed in finding older stages. Fry and
Hedgpeth (1969) suggested that the protonymphon stages of most if not all
species of Achelia are passed in the tissues of the organisms on which the free
juveniles and adults feed.
Jarvis and King (1972) report the possibility of nine moults in the male
and 10 or 11 in the female of Pycnogonum tittorale. Behrens (1984) reared
the larvae in the laboratory as ectoparasites on Clava multicornis. They took
an average of 83 days (at 15OC) to progress from protonymphon larva
through five moults to the “juvenile stage”, having lost the larval appen-
dages at the fifth moult, but with only three pairs of walking legs; the fourth
pair is added at the next moult.
The abundance of yolk in the larvae of the common Indian littoral species
Propallene kempi led Gnanamuthu (1950) to suggest the possibility of direct
development without a parasitic stage (as P. longiceps).
Bourdillon (1952) described the parasitization of the hydroid Coryne
muscoides by larvae of Anoplodactylus virescens. He described three sites of
parasitism, within polyps, within polyp buds, or within the hydrocaulus
(“lateral kystes”), and postulated ingestion of the protonymphon larvae by
the active polyps, whence the larvae may settle and develop anywhere within
the hydroid. Hydroid cell material was found within the pycnogonids’ guts
at this stage. The larvae moult to a free living form at the six-legged stage,
whence they commence to feed on the Coryne polyps.

G. Breeding Seasonality

Probably owing to their infrequent occurrence as dense, accessible popu-

lations, there have been very few field studies of pycnogonid life cycles based
on regular, frequent sampling. Notable exceptions are the recent studies of
Munilla (1980a,b; 1982) on littoral species off Spain. Otherwise, information
exists as sporadic records scattered through the literature, or accumulated
seasonal observations.
44 F. ARNAUD AND R. N. BAMBER

Munilla (1980b) found Achelia echinata males to be carrying eggs (oviger-

ous) from August until May, with three peaks of abundance of ovigerous
males in that period associated with the production of mature eggs in the
females. Oogenesis was estimated at two months, as was the duration from
larva to fully-legged juvenile. In the same area, Ammothella longipes was
breeding throughout the year, though again with peaks in intensity regulated
by egg production in the female; oogenesis was again estimated at two
months, and juvenile life lasted three months (Munilla, 1980a). Male
Tanystylum orbiculare were ovigerous from February to November, with a
peak density in May and June (Munilla, 1982a).
Nakamura and Child (1983) found that in the Japanese Anoplodactylus
perforatus, egg-carrying (ovigerous) males were present from May to
October, inferring a single breeding season associated with warm summer
water temperatures. Male Propallene longiceps and Ascorhynchus ramipes are
ovigerous all year, with suggestions of two peaks of breeding, and a 150-d
life cycle in the former; A . utinomii appears to have a breeding season of
late summer to autumn (Nakamura and Sekiguchi, 1983).
Accumulated data for the southern North Sea (Bamber, 1983a) show that
ovigerous males of sublittoral Nymphon species and Phoxichilidiumfemora-
tum were recorded over the winter months, from November to April, while
littoral species (Ammothella longipes and Pycnogonum littorale) were oviger-
ous for most of the year including summer months. Similar data for the
north-west Mediterranean (Arnaud, unpublished) show a tendency for all
species to reproduce in the autumn and early winter, ovigerous males
occurring mainly between September and February (e.g. November and
December for Anoplodactylus angulatus, Ammothella uniunguiculata, Asco-
rhynchus castelli and Nymphonella tapetis), with some earlier (Trygaeus
communis, June to December) and later species (Anoplodactylus petiolatus,
December to April). Postlarvae were recorded from June to December for
Ammothella biunguiculata, March to April for T. communis, and April to
August for A . uniunguiculata.

V. Interrelationships w i t h Other Organisms

A. Feeding

Pycnogonids are generally carnivorous grazers: they puncture the cell or

body wall of their prey and suck out the contents through their proboscis.
Smaller prey items may be ingested whole. The food tissue is macerated by
the setal “oyster basket” in the base of the proboscis.
Being sluggish invertebrates, they feed on sessile or slow moving prey
 THE BIOLOGY OF PYCNOGONIDA 45

species. Many have commonly been found to feed on sponges, cnidarians or

bryozoans, but other prey species recorded are lamellibranchs, gastropods,
echinoderms, and polychaetes, as well as some algae; some species also feed
on organic detritus or carrion. Ryland (1976) stated that “of marine
arthropods, pycnogonids are the greatest consumers of bryozoans”; in
South Wales, Anoplodactyluspygmaeus and A . angulatus have been found on
Bowerbankia and Achelia echinata on Bugula.
Wyer (1972) found Achelia echinata preying directly on both the hydroid
Dynamena pumila and the bryozoan Flustra foliacea. Its feeding on the latter
bryozoan has been described by Wyer and King (1973): the pycnogonid uses
the sensory bristles on the tips of its palps to locate the distal angles of a
zooid, then lowering the cephalon, inserts its proboscis at an angle of 60”
through the orifice of the zooid; the pycnogonid then moves forwards, the
proboscis becoming vertical to the zooid and rupturing its frontal mem-
brane. The A . echinata feeds for about ten minutes, its proboscis plunged
into the zooid.
The commonly littoral Pycnogonum littorale has long been known to feed
on actinians. Gruet (1972) reported on this species living in Sabellaria
alveolata reefs on the French Atlantic coast, feeding on Sagartia elegans
(commonly 3 4 specimens on one anemone) and once on Cereus peduncula-
tus. Wyer and King (1974) listed the various actinians on which P. littorale
has been recorded feeding (Actinia equina, Urticina felina, Anemonia sulcata
and Calliactis parasitica), and described how this species grips with its stout,
single claws, and uses its robust legs to exert pressure while inserting the
chitinized proboscis lips into the host tissues for suction. Bamber (1985b)
describes how, in the laboratory, P . littorale also fed on Actinia and Urticina,
but showed greatest preference for C. parasitica and Adamsia carciniopados,
to the point of consuming the entire anemone! This preference is curious in
that in the field these species are inaccessible to the slow pycnogonid, when
being carried on the shells of pagurids. Staples (1977) also cited actinians as
the exclusive prey of the south Australian P. aurilineatum, particularly
Corynactis australis and Actinia tenebrosa.
Rhynchothorax species are suspected of preferentially feeding on bryo-
zoans, always occurring on substrata rich in these sessile invertebrates
(Arnaud, unpublished observations); Clark (1976) came to the same conclu-
sion when examining the functional morphology of the tube-shaped probos-
cides and perforating palp bristles in both this genus and Austrodecus.
Achelia echinata is also found in tufts of the bryozoan Bugula turbinata,
but here it feeds on the organic detritus accumulated in the older parts of the
colony (Ryland, 1976). Wyer and King (1974) described five cases of
detritivory by Nymphon gracile after 21 d starvation: they were observed
cleaning their legs and trunk with their ovigers, whence the accumulated
46 F. A R N A U D A N D R. N. BAMBER

detritus was passed to the chelifores and then to the mouth. Stout and
Shabica (1970) noted that the Antarctic Colossendeis robusta, Decolopoda
and Pallenopsis “were observed to feed in the soft sediments”, either on the
sediment itself or epilithic diatoms. In the same area Shabica (1971) reported
C. robusta and C. megalonyx megalonyx preying directly on the slow moving
Antarctic limpet Patinigera polaris (Nacella concinna). Achelia cheluta also
feeds on molluscs (Benson and Chivers, 1960), destroying ctenidial, gonadal
and mantle tissue of the Californian Mytilus californianus.
While some species have a broad diet, others can be very selective:
Phoxichilidium femoratum was found by Loman (1907) to prefer Tubularia
as food, and even preferred the gonophores to the body of the polyps. In the
laboratory, Stock (1 978a) tested pycnogonids for preference between water
flowing over combinations of presence or absence of potential prey. He
found that Nymphon brevirostre, N . gracile and Endeis spinosa not only
showed a preference for prey-associated water, but also distinguished
between coelenterate species. Fry (1965) tested Antarctic pycnogonids with a
choice of 16 potential prey items presented simultaneously in a circular dish.
A clear preference was shown for major prey items, which were those to
which the feeding morphology of the pycnogonids (Austrodecus glaciale and
Rhynchothorax australis) was preadapted.
Lotz (1968) experimented on four species (Achelia echinata, Nymphon
brevirostre, Callipallene brevirostris and Anoplodactylus petiolatus), trying to
make them accept nonhydroid food. The first three species could not be kept
alive without hydroid food, and died within a maximum of 88d. A .
petiolatus, however, survived for more than nine months, feeding on small
pieces of Mytilus edufis mantle; it was also observed to catch small mobile
polychaetes and swallow them whole, and even catch small copepods,
seizing them with the terminal claws of the first or second walking legs:
indeed, given a choice, it preferred copepods to Mytilus flesh. These results
accord with the frequent finding of A . petiolatus in sublittoral benthic mud
communities,
Necrophagy has been found in pycnogonids by using carrion-baited traps
in the Antarctic (Arnaud, 1972), where, along with other necrophagous
invertebrates, five pycnogonid species were caught a t Adelie Land and four
at King George Island, representing three families (Table 4); necrophagy is
considered an adaptive strategy among marine invertebrates in the cold
Antarctic environment (Arnaud, 1977).
It is likely that several pycnogonids may also feed on mucus produced at
the surface of sponges, corals, gorgonarians, anthozoans, and certain mol-
luscs and ophiurans. On Aldabra Atoll, Sloan (1979) studied the association
between Anoplodactylus ophiurophilus and three species of tropical ophiurans;
 THE BIOLOGY OF PYCNOGONIDA 47

he found that, of 571 pycnogonids collected from Ophiocoma doderleini,

only four were on the aboral surface, similarly only two of 33 on the aboral
surface of 0. pica, and none on the aboral surface of 0. erinaceus. Since
these three ophiurans feed by mucus entrapment of particles between the
arm spines, the concentration of pycnogonids on the oral surface, near the
mouth, suggests attraction to the mucus rather than a casual association for
locomotion or protection. Perhaps the proteinaceous mucus produced by
Nucella concinna (vide Hargens and Shabica, 1973) accounts for its pred-
ation by the two Colossendeis species mentioned above.

TABLE4. ANTARCTICNECROPHAGOUS PYCNOGONIDS (AFTER ARNAUD,1972 AND

ORIGINAL DATA)

Adelie Land South Shetland Is.

Species (depth in m) (depth in m)

Nymphon australe 24-45

Pentanymphon antarcticum 320 60
Ammothea carolinensis 60
A . clausi 60
A . glacialis 320
Colossendeis m. megalonyx 35
C. robusta 85
C. scotti 90

More recent work has revealed that pycnogonids may also be algivorous.
Wyer and King (1974) observed that the British littoral Ammothella longipes
ate small shoots of the red alga Gigartina stellata. Bamber and Davis (1982)
studying the feeding of Achelia echinata in Southampton Water, UK, found
this species surprisingly eating Grifithsiajlosculosa and Enteromorpha: using
14C-labelled weeds, the pycnogonid was found to take up activity in
proportion to the concentration of I4C in the weed. The experimental design
and analyses precluded seawater, bacteria, epiphytes or any passive uptake
as the source of 14C in the A . echinuta. As a suitable food source, an alga
must have a relatively thin cell wall, and A . echinata was never found eating
thick-walled Fucus or Laminaria.
Pycnogonid feeding was aptly summarized by the anonymous writer
(1980) who said;
“apparently, the preferred foods of pycnogonids are largely those organisms
not eaten in any quantities by commercially exploited demersal fishes. Pycno-
gonids seem to form part of a slow energy ‘shunt’, returning the energy of
organic detritus only slowly to the fishes’ food webs by their own death and
decomposition or via invertebrate predators”.
 TABLE
5. PYCNOGONIDS
IN DIET OF OTHER ANIMALS (FROM THE LITERATURE AND ORIGINAL DATA)

Shrimp Dic~hcdopupa"dulus
honnieri Pullenopsis jut tingle
P. scoaariu
North Atlantic
North Atlantic
400
400
1 Arnaud, 1972
Lit hodid Lithode.s murruvi Pycnogonum platy lophum Crozet Is (South 165-180 Arnaud and Do-Chi. 1977
Indian Ocean)
FISHES
Nototheniu coriiceps negleciu Penianymphon antarcticum Adelie Land and Plamer 10 Arnaud, 1972
& Achelia sp. Archipelago (Antarctica)
Chai1inu.s himuculutus Anoplodactylus pectinus Tulear reefs (SW Madagascar) 4 Arnaud, 1973
Ammothella indica Tulear reefs 4 Amaud, 1973
Hulichoeres hivittuius Cullipallene brevirostrum Puerto Rico 3 Stock, 1975d
Cheiloductylus mucropterus Nymphon rnuorianu New Zealand 146165 Godfriaux, 1974
Coryphuenoides zuniophorus Colossendeis sp. (juv) North Atlantic
Nuezumiu ueyuulis Anoplodactylus typhlops North Atlantic1 120-900
Chrysohlephus puniceus Pycnogonum forie off Natal coast
Rhopalorhynchus gracillimurn (Southern East
Nymphon setimanus Africa)
Trivnutomus hunsoni Nymphon sp. (broken) Palmer Archipelago
Trrmutomus scoiti Nymphon sp. (juv) Palmer Archipelago
unidentified species Pentapycnon charcoii Ross Sea (Antarctica) 534-549 Fry and Hedgpeth, 1969
 THE BIOLOGY OF PYCNOGONIDA 49

B. Pycnogonids as Food

There are very few published records of pycnogonids as food for other
marine invertebrates or vertebrates. As animals with a heavily chitinized
exoskeleton and little in the way of muscle content in the trunk and legs,
rarely occurring in great numbers, they probably do not offer an attractive
source of food.
Table 5 lists the pycnogonid species identified from fragments in the guts
of sub-Antarctic king crabs and north Atlantic shrimps, together with
various records from the stomachs of commercial and non-commercial fish.
From these few records, it appears that pycnogonids are ingested more
incidentally than actively, and they do not constitute an appreciable part of
any predator’s diet.

C . Commensalism and Parasitism

There are a number of pycnogonid-host relationships recorded in the

literature (Table 6). Those of pycnogonids living as ectosymbionts are
considered here under commensalism, whilst those damaging their hosts as
ecto or endoparasites are discussed under parasitism. In the latter category
should also be included the parasitic associations of many protonymphon
larvae (Section IV above), which behaviour is probably the norm in
pycnogonids. There are in addition certain borderline cases, such as Pycno-
gonum littorale which in its feeding strategy described above is an effective
ectoparasite on Actinia and Urticina (indeed, young P. littorale have been
taken inside the Actinia enteron in Northumberland, where they are virtual
endoparasites), though moving from one prey host to another without
normally killing them.

1. Commensalism

Pycnogonids living on the surface of sponges may benefit from the supply of
oxygenated water and food in the currents induced by the sponge’s feeding
activity. However, as in the case of the eight pycnogonid species listed below
on a glass sponge from the Crozet Islands, the sponge may offer the only
suitable hard substratum on a soft bottom, and the association be thus
coincidental.
Pycnogonids are found as ectosymbionts on echinoderms other than
holothurians, living free among the pedicellaria and tube-feet without being
evicted, in an apparent “cleaning symbiosis”, the pycnogonids cleaning the
oral surface of the asteroid or ophiuroid during feeding in return for shelter.
 6. RELATIONSHIPS
TABLE BETWEEN PYCNOGONIDS AND THEIR HOSTS

Depth
Host Species Locality (m) Reference Relationship
~CYOCORALS
~~

Alc 1(mum pu' rfic um Tunysrylum an I homasi i Akkeshi Bay ? Utinomi, 1954 Ectocom?
(as Anthomuctus sp )
Chri cogorgiu pupillow .?Asrorhynchus spec. B 4" 43'22"s- 730 Stock. 1953 Endopar
118" 53' 18"E
Boehmia iheluiu S . coast of 0-70 Barnard, 1954 Ectocom
South Africa
HYDROMEDUSAE
Po1yorchi.s kurufuroensis Achelie alu.skensis Akkeshi Bay '1
Okuda, 1940 Ectopar
POLY CH AETES
Audouiniu au.srruli,s YHunnoniu s p Langebaan Lagoon shallow Stock, 1959 Ectopar
N W Capetown, S. A water
MOLLUSCS
Scuphandcr punc,/o.srriuius Ascorhynchus endoparusiricus Azores Is 159CL1655 Arnaud, 1978 Endopar
Terhys liymrinu Njwphon purasiiicum Naples, Italy ? Merton, 1906 Ectopar
Arminiu vuriolosu Ammorheu sp.H6jo, Japan ? Ohshima, 1933b Ectopar
Aplysiu hcwJdic!i Ascorhynchus sp. A Timer I . littoral Stock, 1953 Ectopar
Myii1u.s culifbrniunus Arheliu cheluru California shallow Benson and Chivers, Endopar
water 1960
Rutlitupes philippinurutn Nynphonellu iupetis Fukuoka, Japan shallow Ohshimd. 1927b Endopar
Prororhucu jc4)ensi.s water
Theoru luru Nymphonella tapeii.r Tomioka B., Japan 5-10 Kikuchi, 1976 Endopar
Hiutellu oricwiulis Nymphonella rapetis Fukoshima, Japan 2 4 Ogawa and Matsuzaki, Endopar
1985
Tellinu pernu A.scorhynchus sp. I Tulear reefs 6 Amaud, unpublished Endopar
Madagascar
Tdlitiu sp. juvenile Ascorhynchus sp. 2 Tulear reefs infralittoral Arnaud, unpublished Endopar
ECHINODERMS
Echinoids
Strongylricc,ntrorus sp. Pycnosomiu s trongylocentroti W. Sakhalin I 75 Losina-Losinsky, 1933 Ectocom
Euciduris trihu1oide.s
Holothurians
1
Anoploduciylus insign formis
Ascorhynchus custellioides
CuraCao
Curacao
1
1
Stock, 1975d
Stock, 1975d
Ectocom
Ectocom

Siichopus ,juponicu.s Ammothella hiunguiculuiu Kii, Japan shallow Ohshima, 1927a Ectopar
water
Holothuriu luhricu moehii Ammotheu hilgendorfi Kii shallow Ohshima, 1927a Ectopar
water
Ophiuroids

I
Ophiocomu doderleini, eulittoral Sloan, 1979; Ectocom
Anoploductylus ophiurophilus Aldabra Atoll
0. picu and 0. rrinuceus lagoon Stock, 1979
Asteroids
Culliusier corynrtes Pycnosomiu usierophilu Philippine Is. 379407 Stock, 1981a Ectocom
Acunihuster p1unc.i Pycnogonum pusillum Dahlak Archipel. 1 Stock, 1964 Accidental
Crinoids
Unidentified species
("black crinoid") 1
Rhopalorhynchus gracillimum
Anoploductylus pulcher
Kolumadulu
(Maldive Islands)
Carpenter, 1908 Ectocom
Ectocom
52 F. A R N A U D A N D R. N. BAMBER

Thus 26 adults, juveniles and larvae of Pycnosomia asterophila were taken

from the oral surface of Calliaster corynetes in the Philippines (Stock,
1981a). Sloan (1979) observed the common habit of the tenacious pycno-
gonid Anoplodactylus ophiurophilus to grasp tube-feet of its ophiuroid host in
its chelae, suggesting their potential as “podia1 feeders”. Losina-Losinsky
(1933) found 19 Pycnosomia strongylocentroti firmly fixed by their chelae
among the spines of a Strongylocentrotus species from the Tatar Strait.

2. Parasitism

Pycnogonids causing damage to their hosts are considered parasites. The

typical ectoparasitic association is shown by Nymphon parasiticum, origi-
nally described by Merton (1906) as living on the Mediterranean planktonic
nudibranch Tethys leporina, its proboscis inserted into the nudibranch’s
tissues sucking its body fluids. The many larval pycnogonids reported from
North Atlantic medusae by Lebour (1916) may also be regarded as ectopara-
sites, being preferentially fixed in the manubrium or at the junction of the
manubrium and the stomach. It is easy to postulate larvae parasitic on
benthic hydroids moving into the gonothecae and attaching to medusae
before their release. More recently, Child and Harbison (1986) have
recorded the association of adult and juvenile Pallenopsis scoparia with the
mesopelagic scyphomedusa Periphylla periphylla, and this may be the
unidentified pycnogonid found on the same host by Mauchline (1984).
Hedgpeth (1962) also suggests such an association for Pallenopsis calcanea.
The numerous specimens of Ammothea hilgendor3 recorded by Ohshima
(1927a) attached to the soft-bodied holothurian Holothuria lubrica moehii in
Japan may also be an example of ectoparasitism, though this species is
commonly recorded as free-living elsewhere.
Endoparasitism by pycnogonids is only known to occur in association
with molluscs. The first case was cited by Ohshima (1927b) of infestation of
the Japanese bivalve Tapes (Ruditapes) philippinarum by the curious
ammotheid Njwzphonella tapetis (see Fig. 5). Of 144 bivalves examined in
April 1926, 51 were parasitized by a total of 99 N . tapetis, while in August of
the same year only six Tapes among 80 were infected with a total of eight
parasites. Adults have been found subsequently “free in the sand”
(Ohshima, 1933b). Other host bivalves were Protothaca jedoensis, and since
then Kikuchi (1976) rediscovered the parasite in Theora lata; most recently,
Ogawa and Matsuzaki (1985) found this pycnogonid parasitic in Hiatella
orientalis, though they could find no adults.
Benson and Chivers (1960) found both young and adult Achelia chelata in
Mytilus californianus, from 1-21 per bivalve, and damaging them to the
point of atrophy.
 THE BIOLOGY OF PYCNOGONIDA 53

Unfortunately some parasites are only known as juveniles, and are thus
impossible to describe as species (these may indeed be described as free-living
adults). There are two recent unpublished records of endoparasites in
transparent juvenile shells of Tellina perna collected off Madagascar from
littoral reef sands. The first parasite is a whitish Ascorhynchus, very similar
to Stock’s ( 1 953) “species A” which he described as ectoparasitic on the gills
of Aplysia benedicti on the shore of Timor Island. The new specimen has a
dorsal length of 1.8 1 mm, with a typical proboscis 1.03 mm long; palps and
4th legs are fully developed and minute oocytes are visible in the 4th femurs.
The second parasite is also an Ascorhynchus, 0.93mm in length with a
0.62 mm proboscis, found holding firmly onto the gills of the bivalve above
the foot.
The first record of infestation of a shelled gastropod was of the blind
Ascorhynchus endoparasiticus found in the pallial cavity of Scaphander
punctostriatus, a deep-sea opisthobranch from the Azores (Arnaud, 1978);
the distal leg segments of the pycnogonid protruded through the orifice of
the mantle cavity. Three of six Scaphander collected in November 1971 were
parasitized, by one or two A . endoparasiticus; the largest of these, which
occupied all the 12 mm long pallial cavity posterior to the opisthobranch’s
kidney, was a mature female with open genital pores and many small oocytes
in the femora. Endoparasitism of the adult female poses some questions over
the mating behaviour of this species.
It can be seen from the above and Table VI that the large majority of
commensals and parasites are of the family Ammotheidae.

D. Epibiosis on Pycnogonids

The hard cuticle of slow-moving pycnogonids offers a ready substratum for

colonization by sessile organisms between moults; encrusting epibionts have
been recorded from all parts of the body, including the cephalon, ocular
tubercle, proboscis, trunk and legs. Such epibiosis occurs despite the clean-
ing function of the ovigerous legs, though these would probably be unable to
remove encrusting bryozoans. King (1 973) reported that Nymphon gracile
males become heavily encrusted during the time they are carrying eggs or
larvae on the ovigers, at which time they are unable to preen or moult. The
development of epibionts at other times, and particularly on colossendeids
which are apparently never ovigerous, gives some indication of the infre-
quency of moulting in adult pycnogonids.
Epizooites are relatively common on Antarctic species (Arnaud, 1972),
and include sponges, hydroids, bryozoans, brachiopods, foraminifera, ser-
pulids and cirripedes: the frequent occurrence of the latter on large Colossen-
54 F. ARNAUD AND R. N. BAMBER

deu species was also reported by Newman and Ross (1971) who found
Lithoscalpellum discoveryi a common epizoite in the Ross Sea and around
South Georgia Island. Elsewhere, Bamber (1983b) records hydroid epi-
zoites on Colossmdcis urcuuta and Paranymphon spinosum and foramini-
ferans o n Nymphon stroemi, all from deep waters around the British Isles.
In shallower temperate waters hydroids, protozoans, ectoprocts, bryo-
zoans, . algal sporelings and postveliger bivalves have all been recorded
attached to pycnogonids. Pipe (1982) studied the epizoites on Phoxichilidium
femoratum from the North Sea. He collected five out of six individuals with
epizoites, identified as filamentous bacteria (?Leucothrix), peritrich ciliates
and suctorians, and the hydroid Opercularella lacerata. Attachment sites
were typically on the dorsal surfaces of the proximal leg segments and the
lateral processes; chelifores, distal legs segments and the ventral surface in
general were extremely lightly fouled, and the ovigers, proboscis and central
regions of both surfaces of the trunk were virtually clean. In all cases fouling
cover was 1% or less.
Hedgpeth (1964) reported on an unidentified Antarctic prosobranch
mollusc which had laid rows of eggs on the longer leg segments (femur and
tibia 1) of two specimens and the ventral surface of a third specimen of
Colossendeis megalonyx megalonyx, trawled between 220 and 270 m near the
South Shetland Islands.
Vagile (freely motile) invertebrates have also been recorded as pycnogonid
epifauna. Halacarid mites and free-living nematodes, while not infrequent,
are probably simply treating the pycnogonid as part of the surrounding
substratum. Arnaud (1972) described a more positive association between
Pentanymphon antarcticum and the small munnid isopod Coulmania frigida:
eight of 105 pycnogonids collected in Adelie Land bore a total of 10 of these
isopods, one having 3 clinging to its legs.
There have been few reported cases of epibionts on tropical or subtropical
pycnogonids, suggesting a greater frequency of moulting in warmer waters.

E. Pycnogonid Synecology

For many years pycnogonids were neglected in ecological studies, owing to

their rarity in samples, their supposed minor ecological significance, and
difficulties in non-specialist identification. But as more appropriate and
efficient sampling strategies and equipment have developed, together with
more systematic analysis and careful sorting of samples, pycnogonids have
become better studied in communities, and many new species in genera of
small pycnogonids have been revealed (e.g. Austrodecus, Pantopipetta,
Rhynchothorax). As a result, many recent ecological reports and regional
 THE BIOLOGY OF PYCNOGONIDA 55

monographs include pycnogonids, which appear as a small, but not negli-

gible, fraction of the benthic community.
Even so, quantitative estimates of pycnogonid density are very infrequent.
Of the psammophilous species, Ascorhynchus simile has been recorded at
0.12 individuals/dm3 off Marseille at about 6 m depth, Hannonia sp. at 0.21/
dm3 off northwest Madagascar and Anoplodactylus arescus at 0.66/dm3 at
Mayotte Island (Comoro Islands, Indian Ocean) and 12 individuals/dm3 on
the Tulear Reef Barrier, SW Madagascar, both at 6 m depth (Arnaud,
unpublished data). For epibenthic species, Grassle et al. (1975) observed the
abyssal Colossendeis colossea at up t o 0.87/ha on the North American
continental slope; Nymphon hirtipes at more than 40/m2 are reported at
200 m depth in Anonymous (1980); Schmidt and Buckman (1971) recorded
71 individuals/m2 of Pycnogonum littorale in the shallow German Baltic
mussel zone. At Marion Island in the southern Indian Ocean, Tanystylum
cavidorsum was present at a maximum density of 14/m2 (mean 5/m2),
representing a biomass of 10mg/m2 (dry weight) and an energy value of
0.2 kJ/m2 (Blankley and Grindley, 1985). From cruises in the Bay of Biscay,
Sibuet and Segonzac (1985) were able to relate density of total pycnogonids
with depth: the maximum density was 8.4/ha at 1950 m, falling to 4.6/ha at
2120m, 1.6/ha at 3350m, 0.3/ha at 4200m and O.l/ha at 4750m.

1 . Marine vegetal communities

Most vegetal community studies relate to temperate areas, particularly the

Mediterranean over the past 20 years (Table 7): superficial photophilic algal
communities have been investigated on the Spanish coast by Haro (1965,
1966) and Munilla (1981, 1982b), in Sicily by Krapp (1973a), the North
Adriatic by Krapp-Schickel and Krapp (1 975) and the Mediterranean coast
of Turkey (Izmir Bay) by Arnaud (1976), as well as much previously
unpublished data.
Table 7 summarizes the species associated with different algal biotopes.
The comparative richness of Halopteris scoparia (Stypocaulon scopariuin),
with 14 pycnogonid species in the Marseille area, is evident. The Cystoseira
species are similarly rich in French waters, despite two being from sheltered
waters (C. crinita and C. fifimbriata) and the third ( C . stricta) from exposed
coasts in moderately polluted waters. Padina pavonica lives in high sedimen-
tation conditions and offers little shelter owing to its umbrella shape: it
supports five species in both the Marseille area and Izmir Bay, but with only
two in common.
Coralline algae also support a diverse pycnogonid fauna, with eight
species occurring in Corallina mediterraenea, three species common to the
eastern and western Mediterranean; nine species are associated with the
 7.
TABLE PYCNOCONIDS ASSOCIATED WITH MEDITERRANEAN
SHALLOW WATER ALGAL BIOTOPES

Stypocaulon
scoparium =
Hulopteris Cystoseira Cystoseiru Cyst oseira Padina Corallinu Jania
scopariu crinitu j i m br ia t a stricta pa vonica mediterranea rubens
_ _ ~ ____ ~ _ _ _
Arnmotkc~llulongipes HMO A0 0 0 A0 0
A . hiunguiculuiu 0
A . uniunguiculata HMO A0 KO A0 0
Achelia echinuta HMKO A0
A . lringi MO 0 0
A . simp1e.u M K
A . wlg(iris HM
A s c o r h y n h s custelli H
Tcinjs tylum con ir o.c tre 0 A0 KO 0 0 A0
T . orhicularp HO 0 0 0 A 0
Trygrreus communis 0 0 0 0
Anoploriucty1u.v angulutus MO 0 0 0 0 0
A . perio1utu.v 0 A
A . pygmueus 0 A0 KO 0 A A 0
A . viwsc~rns 0 A 0 0 A A0
Endeis spinosa H 0
Pynogonum pusillurn 0 0
Cullipullene hrevirostris H
C. emuciata KO KO KO 0 0 0
C. phuntomci K A

( N B A = Arnaud, 1976; H = Haro 1965, 1966; K = Krapp, 1973a and Krapp-Schickel and Krdpp, 1975; M = Munilla 1981, 1982b; 0 = Arnaud, original
data based on material collected by G. Desrosiers, D. Dumay and M. Menioui in Marseille area at depths between 1 and 1.50m).
 THE BIOLOGY OF PYCNOGONIDA 57

coralline Jania rubens which lives epiphytically on other coralline algae. On

the Northumberland coast of the North Sea, Bamber (1983a) records seven
species from Corallina ofJicinalis, again all small or shorter legged forms
(ammotheids, callipallenids, phoxichilidiids), and this alga is commonly the
most favoured by pycnogonids in British Waters (e.g. Bamber and Hender-
son, 1983). The soft filamentous red alga GrlfJithsiaJEosculosain Southamp-
ton Water, UK, supported Achelia echinata, Anoplodactylus pygmaeus,
Endeis spinosa and (rarely) Ammothea hilgendorfi (Bamber and Davis, 1982;
Bamber, 1986).
The abundance of pycnogonids in these superficial biotopes shows a
similar pattern to their diversity; for example, from equivalent samples in the
Marseille area, there were 242 individual pycnogonids in Stypocaulon
scoparium, 127 in Cystoseira crinita, 36 in C. jimbriata and only seven in
Padina pavonica (Menioui, 1983). Nonetheless, in the richest areas pycno-
gonids only comprise about 5% of the total fauna (Menioui, loc. cit.).
The morphology of these algae is clearly important in determining their
ability to shelter pycnogonids: finely branched algae, with a complexity of
crevices to entrap detritus, a high surface area for epiphytic colonization (a
potential food resource), or mucus production or thin cell walls to offer
feeding opportunities, support more diverse and dense pycnogonid faunas
(e.g. Cystaseira spp.) than less elaborate species such as Padina which offer
poor shelter.
Another algal biotope investigated by Hong (1980) in the Marseille area
between 10 and 30m depth is the “coralligene” formation of encrusting
calcareous algae such as Pseudolithophyllum cabiochae, Neogoniolithon
mamillosum and Mesophyllum lichenoides. Their settlement leads to a cre-
viced, cryptic micro-environment colonized by small skiaphilous (shade-
loving) species of sponges, crustose bryozoans and brachiopods; pycnogo-
nids represent only some 1-2% of this community. Over five sites in the Fos-
sur-Mer region, showing different degrees of pollution, Achelia echinata, A.
vulgaris and Callipullene spectrum were ubiquitous, Rhynchothorax mediter-
raneus and Pycnogonum plumipes were limited to cleaner waters, and
Tanystylum conirostre, Achelia langi and A . longipes appeared at the most
polluted site.
The Mediterranean seagrass Posidonia oceanica has large flat blades
which are not favourable to colonization by pycnogonids: only Endeis
spinosa, Tanystylum conirostre, Nymphon gracile and Callipallene brevirostris
occurred on these leaves in the Marseille area, compared with 16 species
amongst the rhizome mat, rich in trapped particles and detritus (Table 8),
though some of these species (Anoplodactylus petiolatus, Rhynchothorax
alcicornis) were only associated with the dead rhizome mat of polluted beds.
Haro (1967) found eight species of pycnogonids and Munilla (1 98 1) nine
species in the Posidonia beds of the Catalan coast.
 TABLE
8. PYCNOGONIDS
FROM SEAGRASS
BEDS IN TROPICAL REGIONS

Scagrass Species Locality Depth (m) References

~~ ~ ~ ~~ ~~ ~ ~. ~~ ~~~ ~- ~~ ~

Tlialassiu testudinum (or Eurjcyde raphiaster Galeta I. (Panama Caribbean) intertidal Child, 1979
“turtle grass”) Ascorhynchus latipes Galeta I. intertidal Child, 1979
Achelia suwayai Galeta I. intertidal Child, 1979
Ammothella pucifica Kunduchi (Tanzania) 1 Stock, 197%
Thdmsia sp. Euryryde raphiaster Bonaire I. (West Indies) 0.104.50 Stock, 1975d
Achelia sactwyai Bonaire I. 1 Stock, 1975d
Ammothella exornuta Curapo 0.5-1 Stock, 1979b
A . mareusi CuraCao 0.25-1 Stock, 1979b
Nymphon,floridanurn Puerto Rico I . 1 Stock, 1975d
N . aemulurn Antigua I. 0.50 Stock, 1975d
Callipullene hrevirostvis Bonaire 1. C u r a p o , Florida - Stock, 1975d, 1979b
Pigrogromitus timsanus Panama Canal Zone 0.360.60 Child, 1979
Anoploductylus hutangensis Antigua I., Florida; 0.50-1 Stock, 1975d;
Belize reef 1 Child, 1982a
A . allotrius Panama Canal Zone 0.360.60 Child, 1979
A . monotveniu Aruba 0- 1 Stock, 1979b
A . p w tinus Florida, Antigua - Stock, 1975d
A . portus Curacao 0.25-1 Stock, 1979b
Endeis ,fluccida Florida 0- 1 Stock, 1975d
E. spinosa Belize reef 1 .so Child, 1982a
Laurenciu papillosa Eurycyde raphiaster
(red alga) Achelia sawuyai
A scorhy n ch us la t ipes
Ammothella marcusi
A . rugulosa
A . spinfera
Njmphopsis duodorsopinosu
Pigrogrornitus fimsanus Galeta Island intertidal Child, 1979
Anoploductylus evelinae (Panama Caribbean)
 A . .jonesi
A . hatangensis
A . monotremu
A . multiclavus
Rhynchothorux urchitrctus
Aimthophora ( 2 specks) Eurycydc. ruphiaster
Achelia sauuyai
Ascorhynchus Iutipes
'4mniot h d a murcusi
A . rugulosu
A . spinifi.ru intertidal Child, 1979
Anoplodactylus hatungensis
A . rnonotremu
A . multicluvus
A . allotrius
Cullipallene emaciuta

Hulophilu dc1cipicx.c. Rhopulorhynchus lomuni Tulkar (S. Madagascar) 4-5 Arnaud

Hulophilu sp. Nymphon cf. .fixxi Aqaba (Red Sea) 15 Arnaud
Anoploductylus cribellatus Aqaba 1.30 Arnaud
Sj'r ingotlium isoet i/hlium Ammo thdlu indica Tulear intertidal Arnaud
Syingodium sp Propnllene urdua Kunduchi (Tanzania) 0.7-1 Stock, 1975c
C'yniorloceri .rcrrulutu Propullme cf. kernpi TulCar intcrtidal Arnaud
60 F. ARNAUD A N D R. N. BAMBER

In tropical regions, seagrasses are more diverse, and their beds also
support pycnogonid communities (Table 8). Thalassia beds in the Caribbean
support 16 species, Laurencia papillosa beds 14 species, including seven in
common with Thalassia. The seagrass beds of Halophila spp., Syringodium
spp. and Cymodocea serrulata from the Indian Ocean have been little
studied, and only six associated pycnogonid species are recorded.
The tropical floating alga Sargassum acts as a benthic substratum with
regard to its pycnogonid community. 11 species have been recorded on
.Sargassum from the tropical Atlantic and Caribbean (Table 9), all character-
istic bottom-living species of the tropical Atlantic.
Finally, recent studies have identified 16 species of pycnogonid (Table 10)
which live amongst the roots of the Caribbean mangroves Rhizophora
mangle or Avicennia sp. As in all these vegetal communities, there is a
dominance of Anoplodactylus and ammotheid species. No data are yet
available for mangroves from Africa, Asia or Australia.
In polar waters, the invertebrate fauna associated with the large Antarctic
and sub-Antarctic Phaeophyceae has been investigated by Arnaud (1 974).
At the Kerguelen Islands, the upper infralittoral Durvillaea antarctica has
very long, smooth fronds, and grows in exposed conditions; the hard,
massive roots offer little shelter, and the only pycnogonid found on this alga
was Tanystylum oedinotum. At the Crozet Islands a cluster of D. antarctica
roots stranded on the beach contained two Pycnogonum platylophum and
three Tanystylum cavidorsum. Fragments of these large algae are probably
significant in the dispersal of marine invertebrates by the west wind drift.
The giant kelp Macrocystis pyrifera accumulates detritus in its more
hospitable holdfast, and Nymphon brevicaudatum and Tanystylum styligerum
were commonly found in the holdfasts at the Kerguelen Islands, as well as
Austrodecus breviceps on the blades of the kelp.
Finally, the large thalli of Himantothallus grandifolius lie on the sea bed,
with the holdfast attached to a stone, trapping sedimentary material. Nine
pycnogonid species were found among these holdfasts on the coast of Adelie
Land, viz. Nymphon adareanum, N . australe, Heteronymphon exiguum,
Austropatlene tcherniae, Pallenopsis vanhoeffeni, Anoplodactylus australis,
Endeis australis, Achelia communis and Austrodecus fagei.

2. Sessile invertebrate communities

It is often difficult to distinguish between pycnogonids in communities

associated with specific sessile invertebrates, and species which are utilizing
that invertebrate as a food resource. For example, the dozen pycnogonids
recorded from the “corals” Porites, Pocillopora and Acropora (Stock, 1975d,
1979, 1982; Child, 1979) are probably attracted to feed, or present by
 TABLE
9. PYCNOGONlDA FROM FLOATING SUI"ga.Y.YUm(DEPTH < TO 2 M )

Species Locality References

~ - ~~

Puerto Rico
Puerto Rico
Puerto Rico
Puerto Rico Stock, 1975d
Puerto Rico
Puerto Rico
Puerto Rico
C u r a p o ; Guadeloupe, Bermuda Stock, 1954; Bourdillon, 1955
Antigua, Florida, Puerto Rico Stock, 1975d
Puerto Rico Stock, 1975d
Atlantic Ocean (39'N-41 'W and Stock, 1954
44ON-31"W).
 TABLE10. PYCNOGONIDS
FROM MANGROVE ROOTS OF THE CARIBBEAN
REGION

Rhizophora Avicennia Species Locality References

+ Achelia sawayai Bonaire, Puerto Rico, Florida,
Bahia de Ascension (Mexico Stock, I97Sd, 1979b;
Caribb.),
Belize recf Child, 1979, 1982a
+ + Ammothella appendiculata Bonaire, Florida, Curaqao, Stock, 1975d, 1979b;
Belize reef Child, 1982a
+ + Ammothella exornata St Martin I., Bonaire; Belize reef Stock, 197Sd, 1979b; Child, 1982a
+ Ammothella marcusi Belize reef Child, 1982a
t Tanystylum tuhirostre Belize reef Child, 1982a
+ Tanystylum conirostre Bonaire Stock, 1979b
+ t Tanystylum geminum St Martin I., Bonaire Stock, 1975d, 1979b
+ Hidgpethius tridentatus Belize reef Child, 1982a
+ + Callipallenr hrevirostris Bonaire, Florida Stock, 197SQ 3979b
+ Pigrogromitus timsanus Florida; Belize reef Stock, 1975d; Child, 1982a
+ Anoplodactylus hatangensis Belize reef Child, 1982a
t Anoplodactylus evrlinur Belize reef Child, 1982a
? ? Anoplodwtylus insignifiirmis Curacao Stock, 1975d
+ Anoploductylus prctinus Curaqao; Belize reef Stock, 1979b; Child, 1982a
+ Anoplodactylus portus Curacao; Belize reef Stock, 1975d, 1979b; Child, 1982a
+ Anoplodactylus stri Belize reef Child, 1982a
 THE BIOLOGY OF PYCNOGONIDA 63

accident. Frith (1976) found Nymphon gracile, Achelia echinata and Pycno-
gonuni littorale on the sponges Halichondria panicea and Hymeniacidon
perleve at Portsmouth, UK, but in low numbers, and these three are
common littoral pycnogonids in this area.
Child (1 979) found seven species associated with intertidal Zoatzthus
sociatus in Panama, and Barnard (1954) found Boehmia chelata common on
branching alcyonarians (of many species) in South Africa, as well as among
hydroids and polyzoa in the littoral zone.
The large hexactinellid sponges of the sub-Antarctic Indian Ocean offer a
hard substratum on otherwise muddy bottoms. Along with many other
invertebrates, 12 species of pycnogonid have been found on the external
surface of these “glass sponges” (Arnaud, unpublished); one sponge speci-
men from 150 m depth bore 19 pycnogonids of eight species, including three
Tanystylunz species (one new to science), Endeis viridis, Pycnogonum plat)’-
lophunz, Austrodecus, Achelia and a Njimphon. None of the 12 species found
was sponge specific.
Nonetheless, the pycnogonid species associated with sessile invertebrate
epifaunal communities, whether for feeding or for appropriate hosts for
their protonymphon larvae, differ from those dominant in vegetal communi-
ties. While the latter are mainly small or shorter-legged species, particularly
ammotheids and Anoplodactylus species, hydroid and arborescent bryozoan
communities support many of the more graceful, longer-legged species,
particularly nymphonids. In a sublittoral epifaunal community off North-
umberland, UK, Bamber (1983a) recorded Nymphon brevirostre, N . hirtum,
N . grossipes and Pseudopallene circularis, the last three not being recorded
from other habitats in the area.

3. Pycnogonids in soft sediments

The majority of pycnogonids are associated with hard substrata since it is

these that support the algae or sessile invertebrates on which most species
feed or shelter. A few species are regularly, or obligately, associated with soft
sediments.
The Mediterranean fine sands off Marseille are the preferred habitat for
three pycnogonid species. Ascorhynchus arenicola is found in shallower
sands from 3.5 m-1 1 m depth, being replaced by A . simile which occurs from
5 m-90 m. Nymphonella tapetis, originally described from Japan, lives as a
bivalve parasite in its larval stage, but adults are free-living in sand, where
Picard (1965) regarded it as highly characteristic of this substratum off
Marseille; several potential bivalve hosts live in this substratum. The
specimens attracted to light by Le Calvez (1950; see above) were also over
littoral sandy bottoms, and the nine specimens of Nymphonella lecalvezi
64 F. A R N A U D A N D R. N. BAMBER

(? N. tapetis) were also taken from fine sands (Guille and Soyer, 1967). The
South African Nymphonella lambertensis is also psammophilous (Stock,
19.59); in subsequent samples from the same locality it was found intersti-
tially from the surface of the sand to 30cm below the surface (Arnaud,
unpublished).
Another species living in sand is the aptly named Rhynchothorax philo-
psammum, a minute interstitial species from California. The circumtropical
Anoplodactylus arescus is associated with unstable sands, often in large
numbers in the infralittoral (Arnaud, 1973), where it may feed on interstitial
hydroids. A. cribelfatus lives in these same sand habitats, but in far lower
numbers. ,
Muddy bottoms are commonly frequented by Anoplodactylus petiolatus; it
was remarkably abundant on sediments up to 22% silt in the Bay of Biscay
(Arnaud, 1974a), and was frequently taken in offshore muddy sediments of
up to 50% silt off Northumberland (Bamber, 1983a). In occidental Mediter-
ranean deeper waters Paranymphon spinosum and Anoplodactylus massilien-
sis are typical of the muddy shelf sea bed (Arnaud, unpublished). Abyssal
species are most commonly associated with fine muds, including many
Ascorhynchus, most Paflenopsis and Colossendeis species, and the deepest
recorded pycnogonids, Nyrnphon longitarse caecum and N . tripectinatum
from the Japanese Trench.

4. Pycnogonids in fouling communities

Pycnogonids are common members of the vagile fauna which settles rapidly
on developed fouling communities of sessile bryozoans and hydroids.
Experiments using fouling panels immersed for several months in shallow
waters off Civitavecchia, Italy (Chimenz et al., 1979), and for up to four
years in deeper waters off Nice, France (Arnaud, unpublished) recorded 15
and 10 species respectively (Table 1 I), 7 common to the two sites, including
Anoplodactylus pygmaeus and Endeis spinosa. These two species rapidly
colonized hydroid fouling in a sheltered cupro-nickel pump-intake screen at
1 m depth in Southampton Water, UK, producing breeding populations
within nine months (Bamber and Turnpenny, 1986), and E. spinosa is the
most common settling pycnogonid in open water above 750-850m in the
Mediterranean.
Child (1979) collected pycnogonids from fouling panels on both sides of
the Panama Canal (Table 12); in comparing these data with Table 11, it can
be seen that the genera Ammothella and Anoplodactylus are best represented
in both, and Ammothella appendiculata and Anoplodactylus portus are
common to fouling communities from the temperate Mediterranean and
tropical regions. A . portus has also been reported in large numbers from a
TABLE
11. PYCNOGONIDS IN FOULING FROM THE MEDITERRANEAN SEA (AFTER CHIMENZ
et al., 1979 AND ARNAUD, ORIGINAL DATA)

Species Civitavecchia (0-8 m) Nice (47-537 m)

Ammothella appendiculata 14 1
A . longipes 3 1
A . uniunguiculata 3 0
Achelia echinata 47 460
A . langi 3 0
A . vulgaris 0 327
Tanystylum conirostre 2 0
T . orbiculare 43 0
Ascorhynchus castelli 2 2
Trygaeus communis 2 0
Anoplodactylus angulatus 2 0
A . petiolatus 2 4
A . portuJ 109 0
A . pygmaeus 15 77
Endeis charybdaea 0 22
E. spinosa 3 380
Callipallene brevirostris 11 0
Pycnogonum plumipes 0 1

12 COMPARISON
TABLE BETWEEN PYCNOGONIDFAUNA FROM FOULING ON BOTH SIDES OF
THE PANAMACANALZONE(TABULATED AFTER CHILD,1979)
Species P

Ammothella appendiculata*
A . exornata
A . rugulosa'
A . spinijera
Ascorhynchus castellioides'
A . latipes
Eurycyde raphiaster
Tanj,stylum gem inum
T. isthmiacum isthmiacum +
Aclielia sawayai* +
Callipallene emaciata* +
C. solicitatus
Anoplodactylus batangensis' +
A . evelinae
A . insigniformis' +
A . erectus
A . reimerae
Nymphon jlor idan um +
(C = species on settling plexiglass plates, 5 x 15cm, left at 8-10m below the reeftop for
approximately 2 months on Galeta I., Caribbean Coast; P = species settled on similar plates
during the same experiment time but placed at 8 m deep, with a tidal range of 6 m , on Isla
Taboguilla, Pacific entrance of Panama Canal.) (The species marked with a * were already
reported from fouling communities by Stock, 1975d from Middle America.)
66 F. ARNALJD AND R. N. BAMBER

fouling community in Curacao Island (Stock, 1975d) and from central Italy
(Arnaud, unpublished data), both in power plant systems. Staples (1982)
found Anoploductylus tuhiferus, Endeis straughani, Parapallene australiensis
and Pigrogromitus timsanus in the cooling water system of Gladstone Power
Station, Australia.
Other tropical and subtropical records include five species from the Gulf
of Aqaba (Stock, 1970), again including Ammothella and Anoplodactjllus;
Stock (1975d) also found in the Caribbean area many of the species listed by
Child (as indicated in Table 12) together with an additional five species;
Capriles (1970) recorded Pallenoides ? spinulosa from Sargassum fouling of a
boathouse in Puerto Rico, and Child et al. (1982b) found Ammothella
stauromata, Anoploductylus glandulifer, A . marshal1r.nsi.v and Endah nodosa
in intertidal fouling in the Marshall Islands.
Records from ship fouling are less frequent, but Stock (1959) collected
Ammothella indica from ships’ hulls in Durban Bay, South Africa, and
Bamber (1979) collected Endeis picta (? E . straughani) from a dense Balanus
tintinnabulum fouling community on a ship from Ghana. Both Krapp and
Sconfietti (1983) and Bamber (1986) suspect that the introduction of the
previously Pacific Ammothea hilgendorfi to the Lagoon of Venice (on fouling
panels) and Southampton Water respectively is a result of their transport in
fouling on ships’ hulls.

F. Pollution and Pycnogonids

Of the many recent studies on marine pollution, few have provided much
information on the influence of various pollutants on pycnogonids.
Studies over the last I5 years on the sea areas near Marseille affected by a
variety of industrial pollution have provided some information. Shallow
areas (0-5m deep) affected by domestic waste from the town supported a
good population of Ammothella appendiculatu, other species being rare
(Achelia echinata, A . langi, A n o p l o d a c t j k pygmaeus and Nymphon gracile).
In the outer gulf, shallow sandy or muddy bottoms enriched with organic
pollution supported Tanystjlum conirostre, T. orbiculare and Anoplodactylus
petiolatus, while at greater depths (80-95 m) Paranymphon spinosum was the
only species tolerant of organic pollution.
The regression of the seagrass Posidonia oceanica beds on the Mediterra-
nean coasts is a result of the effects of turbidity from organic detritus. In
highly turbid areas the plant develops a covering of sessile filter-feeding
animals, which in turn provide a food source for pycnogonids. Comparisons
of the pycnogonid faunas between areas of high, moderate and no pollution
(Table 13) show a similar diversity throughout, though some change in the
 THE BIOLOGY OF PYCNOGONIDA 67

TABLE 13 EFFECTS OF POLLUTION ON PYCNOGONIDS FROM THF MARINk PHANEROGAM

P O ~ O O M(xeutnLu
M D ~ L I L( REH I Z O M ~ S )I N THE MARSFILLE ARLA, BETWEEN 1 1 AND 33 M
DLEP ( A R ~ A U O UR, I G I ~ A LDATA)

Unpolluted Moderately Highly

Species collected in area polluted area polluted area
living rhizomes (Port-Cros I.) (Marseille gulf) (gulf of Fos/
Mer)
.-

+
~~ ~~ ~ ~

Anitnotliella hiuriguiculatu
A . longipes +
A . iinitrnguiciilato +
Ascortijwhus custelfi +
Trj'gueiis cotnrnunis +
A clirliu ecliinuta + + +
A . wlguris + + +
A tio~plorliic.tj~ltis ungulu tus +
A . petiolirtus + +
A. pj.gt~irrcu.s + +
Ciilliptr llr n e brc. viros t r is +
Cullipiillenc~pliuntonia + +
Pjuiogotium nodulosum + +
RIiyncliotliora.y ulcicornis +
Tunjwjhini conirostre +
En iteis .spinosu +
species. Anoplodactylus species are again shown to be tolerant of pollution,
while Achelia echinatu, with its diverse feeding behaviour seems euryokous.
While only Anoplodactylus virescens was found near the cooling water
effluent of the power plant at Fos-sur-Mer (Arnaud, unpublished data),
pycnogonids are common members of cooling water system fouling com-
munities (see above); A . pygmaeus and Achelia echinuta were common on the
red alga Grifithsiaflosculosa around the power station discharge at Fawley,
Southampton Water, and any normally littoral species from temperate zones
will have evolved to greater extremes of temperature than that of a cooling
water effluent.
Generally, pycnogonids seem tolerant of the direct effects of pollution, but
are either reduced or favoured by the effects of that pollution on their food
resources.

VI. Zoogeography
The available information on pycnogonid distribution is biased by the
greater intensity of collection and study in some areas, particularly near
marine laboratories. Thus the Western Mediterranean fauna is better known
68 F. A R N A U D A N D R. N. BAMBER

than that of the Eastern Mediterranean, and the North Atlantic better than
the South Atlantic. A recent study of the South African east shelf and slope
(Arnaud and Child, 1987) has revealed 13 new species in 39 collected,
bringing the Southern African list to one hundred, while virtually all new
collections from deep-sea sampling produce new species or new geographic
records. Information is particularly lacking for areas such as the South
American Pacific, the Argentine and Brazilian basins, parts of Australasia
and the numerous Pacific islands.
It does seem to be the case that increasing knowledge indicates greater
distribution of species and less endemism, a trend which will increase as
many of the international synonymies are realized and corrected by more
careful taxonomy and availability of material.
Classical theories on zoogeography are well documented (e.g. Hedgpeth,
1957), and are not repeated here. Pycnogonids are no different from other
groups in their accordance with accepted biogeographic zones. Generally,
pycnogonids have limited abilities for migration. However, large Colossen-
dris species may be able to walk a significant distance on the sea bed.
Bathypelagic species have better potential for large scale movement by water
currents, the only efforts needed on their part being to stay in the water
column. There is again potential for species whose larval or older stages are
parasitic on medusae, and may thus be afforded transport in the plankton,
while species common in fouling communities may be transported down
current by floating weed or wood, or over substantial distances on the hulls
of ships. Some deep-water species, an under-recorded group, show remark-
able world-wide distributions, including Colossendeis angusta, commonly
recorded from the Pacific, Indian and Atlantic Ocean basins (Hedgpeth,
1948), and Pallenopsis mollissirnu and P . tydrmani, known from off Ireland
and Japan (Bamber, 1985a; Child, 1982~).

A. Regional Faunas

The well worked faunas of the North Atlantic, North Pacific and Arctic have
been comprehensively discussed by Hedgpeth (1948, 1949, 1963) and King
(1973). Arctic and sub-Arctic-boreal faunas are dominated by the Nympho-
nidae. These faunas can be divided into a circumpolar boreal-Arctic group, a
high-Arctic deep water group, and the independent Pacific boreal and
Atlantic boreal faunas which are assumed to have evolved separately
(Hedgpeth, 1963). The two deep basins on either side of the Lomonosov
Ridge are still unknown, and should provide interesting contributions to the
faunal groupings of this region when sampling is feasible. The Sea of
 THE BIOLOGY OF PYCNOGONIDA 69

Okhotsk has a high proportion of endemic species, and its fauna has
presumably developed independently. No pycnogonids are known to show a
classic Lusitanian distribution.
The shallow-water species of the Mediterranean basin are becoming well-
known. The dominant genera are Anoplodactylus (at least six indigenous
species), Ammothella and Rhynchothorax each with five species, and Asco-
rhynchus with four species. True deep-water forms are very scarce, since the
Mediterranean is a recent sea, recolonized from the Atlantic through
shallower water. Paranymphon spinosum is the deepest resident species,
occurring at over 1000 m. This species also occurs on both sides of the North
Atlantic, together with the northwestern shallow-water species, particularly
Achelia, Anoplodactylus and Tanystylum species. Pycnogonum littorale has
not yet colonized Mediterranean waters, whereas P. nodulosum is the only
Mediterranean species in common with the South African fauna. Three of
the Rhynchothorax species ( R . mediterraneus, R. monnioti and R. anophthal-
mus) are common to the Mediterranean and the Azores (Arnaud, 1974b). In
common with other animal groups, the pycnogonid fauna now includes
lessepsian migrants, to date Anoplodactytus digitatus, A . portus and Pigro-
gromitus timsanus. Ammothea hilgendoyfi, a widely distributed inhabitant of
the north temperate and tropical Pacific Ocean, has appeared in the Adriatic
by presumed migration on ships’ hulls (Krapp and Sconfietti, 1983).
The Antarctic pycnogonid fauna (over 100 species, Fry, 1964) is richer
than the Arctic (some 40 species, Hedgpeth, 1963), and includes the majority
of the World’s polymerous species (there being none in the Arctic, Table 1).
Colossendeis and nymphonid species are common, some species occurring in
considerable numbers: Calman (1 9 15) reported 240 Nymphon australe in a
sample of 600 pycnogonids off McMurdo Sound, while of 1800 specimens
examined by Gordon (1932), two-thirds were of the genus Nymphon;
Arnaud (1972) found 61% nymphonids (43% Nymphon australe) in 850
specimens from Adelie Land. The diversity of the Antarctic fauna is
demonstrated by Fry and Hedgpeth (1969). Of the polymerous species, the
10-legged ones are not uncommon in numbers of species (seven) or speci-
mens; however, the two 12-legged species are very rare. Sexanymphon
mirahilis (Fig. 22) is known only from the eight type specimens, while
Dodecolopoda munsoni is known from four individual records, one male
from MacRobertson Land (1931), another from the Ross Sea (1959), a
female from the South Orkney Islands (1965) and most recently an adult
male in Prydz Bay, off MacRobertson Land, in 525m in January 1985
(Arnaud, unpublished data). The large size of the latter species (leg lengths
200-240 mm) makes it impossible to miss in a sample, and thus its rarity to
date is the more remarkable.
70 F. ARNAUD AND R. N. BAMBER

FIG. 22. Dorsal view of Sexanymphon mirahilis, holotype (from Hedgpeth and Fry, 1964).

The Antarctic and Arctic faunas have no species in common; the former
shows a greater biogeographic originality than the latter with its strong
boreal affinities, presumably because of their different geological ages.
The sub-Antarctic pycnogonid fauna shows origins in the Antarctic
fauna, with the same genera, but isolation has led to some differentiation at
the species level. For example, at Kerguelen Island, 49" S: the Antarctic
NJwiphon australe is replaced by N . brevicaudatum and N . gracilipes, Endeis
uu.stra1i.s by E. 1,iridi.s.and the numerous Aclwliu species by several Tanj>-
. s r ~ . l u n i ;but the Kerguelen shelf is colonized by the Antarctic colossendeids.
including Decoloporlu ait.sfralis and Pycnogonum gaini. The Crozet and
Marion (Prince Edward Islands, 46" S) show a similar fauna with sub-
Antarctic endeids, nymphonids and Tanysrylum species, and Antarctic shelf
Colossrndris rnegu/onj~s(Arnaud, unpublished data). The isolated islands
remain under t h e influence of the Antarctic shelf. probably by migrations
 THE BIOLOGY OF PYCNOGONIDA 71

along the oceanic ridges (such as the Kerguelen-Gaussberg Ridge); the

Quaternary glaciations will also have been important in determining zoogeo-
graphic isolation, and current proximity to the continent is significant in
developing a separate fauna. Thus the more southerly (54”) and glaciated
Bouvet Island (Atlantic Ocean) fauna includes the large ammotheids
Anu??othea carolinensis and A . allopodes, Njwiphon australe. two Pallenopsis
and Endei,r australis. all characteristic of the Antarctic fauna. Fry and
Hedgpeth (1969) discuss the division of these faunas into the Antarctic and
south temperate morphogroups.
The South African fauna from initial work by Barnard (1954) is becoming
increasingly studied (Stock, 1959, 1963, 1981b; Arnaud and Child, 1987),
with a species total approaching 100. The dominant genus is Nymphon (21
species), followed by Pycnogonum, Pallenopsis and Parapallene (nine, seven
and six species respectively). The callipallenids and ammotheids show
marked diversity at both generic and specific level, and there are several
representatives of the pycnogonid fauna endemic to this area, including the
genera Queubus (Q. ,jamesanus) and Boehmia (B. chelata, B. Iongirostris and
B. ruberosa). At the species level other endemics are Pycnogonurn forte,
Ammothella setacea and Parapallene algoae. Their endemism may be ephem-
eral, as three other “classic” South African endemics have recently been
found to be more widespread: Discoarachne (Tanystylum) brevipes has been
recorded from Amsterdam and Saint Paul Islands in the southern Indian
Ocean (Arnaud, 1974b), and in drifting weed between South Africa and St.
Helena (Arnaud et al., 1976); of the once endemic genus Hannonia, H . typica
has now been found on the Somalia coast (Stock, 1982), and the other
species H . spinipes from the Ivory Coast and Madagascar, where a new
species of the genus has been found (Arnaud, unpublished).
The local hydrography is responsible for biogeographic boundaries within
the South African fauna. The cold Benguela Current from the south is
responsible for the northward extension of colder-water species on the West
coast, while warmer water is brought south by the Agulhas Current to the
East coast, with a cool inshore counter current flowing towards Natal. The
pycnogonid fauna of the shelf and slope can thus be divided into an Atlantic
component (cold temperate), an endemic component (South coast warm
temperate) and an Indo-Pacific component (the subtropical East coast
species). The fourth component is the abyssal species, mostly blind, belong-
ing to the genera Njwphon, Pantopipetta and Colossendeis.
The Australian pycnogonids have been well documented by Clark (1963,
1970) and Child (1 975), but much of the large coastline is yet to be studied;
Child anticipated a doubling of species number from the small littoral
pycnogonids. There are currently 72 species, dominated by callipallenids and
ammotheids, and eight species of Njwzplian. There are stronger affinities with
72 F. ARNAUD AND R. N. BAMBER

the East Indies fauna than the warm-water Indian Ocean (Child, 1975), but
real associations can only be determined after the South Asiatic coasts and
Northern Territory Australian coasts have been adequately studied. The
New Zealand fauna, with about 90 species according to Clark (1983), shows
few relationships with the south Australian, but rather an independence. It
too awaits better study.
The Japanese fauna can be divided, North to South, into Arctic, temper-
ate and tropical regions, with a deep-sea group (see Hedgpeth, 1949;
Utinomi, 1962, 1971; Nakamura and Child, 1983). Of the over 100 described
species, 44 are ammotheids, 12 are callipallenids, 17 are nymphonids and 19
phoxichilidiids. Krapp (1973b) discusses an early Tethys connection
involved in the relationship between Japanese and Mediterranean pycno-
gonids, with common species in Ammothella biunguiculata, Nymphonella
tapetis and Callipallene phantoma, as well as the generally widespread
Aclielia ecliinuta and Parunymphon spinosum.*

B. Deep-sea Pycnogonids
Definitions of “deep-sea” are arbitrary divisions of a continuum. True
‘abyssal’ forms are taken to be those occurring below 2000m depth; in
pycnogonid faunas there is a transitional zone from bathyal (over 250 m) to
abyssal, between 2000 and 2500 m. Hadal or “ultra-abyssal’’ species are
those below 6000m depth. Fage (1956) reported 54 species which he
considered abyssal; modifying his list (some species did not reach 2000 m,
others were unnamed), and including more recent data (Turpaeva 1971a,b,c;
Stock 1978b,c, 1981b; Child 1982c) produces a list of 96 world abyssal
species (Table 14).
The major oceans have experienced different degrees of study for these
deep faunas; some analysis of the best studied, the Atlantic, is possible,
though even here each new survey confirms how understudied deep waters
are. The 125 species known to live deeper than 250m, comprise a bathyal
group of 51 species, an abyssal group of 25 species, a bathyal-abyssal group
of nine species, a shelf-bathyal group of 33 species and a shelf-abyssal group
of seven species. Some of the species in the latter two groups extend to the
littoral zone. The only family not represented in this list is the Endeidae,
though the Pycnogonidae only has representatives in the shelf-bathyal and
shelf-abyssal groups; there is thus no taxonomic pre-adaptation to deep-
water life in pycnogonids.
The Atlantic is separated longitudinally by the Mid-Atlantic Ridge, on
either side of which is a north to south progression of basins more or less
*See Stock. J . H. (1986) Bu//e/in of Murine Science 38, 399441 for a recent review of the
Caribbean pycnogonids.
 THE BIOLOGY OF PYCNOGONlDA

14.
TABLE PYCNOGONIDS FROM BELOW 2000 M DtPTH, OR FROM SHALLOW TO ABYSSAL
DEPTHS (*DATA FROM F A G E , 1956, INCLUDED)

Species Depth (m)

Ammotheidae
Ammothella tubicen 1980-1 995
* Ascorh.ynchus abyssi 14154392
* A . agassizi 1007-2877
* A . armatus 1429-2515
A . athernum 2862
A. birsteini 6040
A . bucerus 5035-5210
A. cuculum 993-39 10
* A . glaber 1520-2516
A . inflatum 2745-6070
A. losinalosinskii 3145-3250
A . mariae 3145-3250
A. ovicoxa 403-2095
A . turritus 19004400
Cilunculus acanthus 2440-2700
C. tubicinis 2800
Megarhethus brevicheliferus 45&2500
Sericosura mitrata 219-2117
* Paranymphon spinosum 1262300

Phoxichilidiidae
* Anoplodactylus neglectus (= A . typhlops) 587-3620
* Pallenopsis californica 1820-2362
P. comosa 3200
P. guineensis 1949-1986
* P. longirostris 145-3065
P. longiseta 3050
* P. mollissima 924-3500
P. oscitans 197G-3550
* P. pilosa 160-3567
* P. profunda 2906
P. tritonis 4 1&288 5
P. tydemani caraibica 897-3 356

Austrodecidae
Pantopipefta angusra 4560
* P. australis 2450
P. brevicauda (= P. longituberculata*) 587-6 I 50
P. capensis 2745-2900
P. lata 355&3675
* P. weberi 100-3700
Callipallenidae
* Callipallene acus 915-3800
 TABLE
14. (cont.)

Species Depth (m)

__
C. rnargarita 454-2200
Mirnipallene atlantis 1000-2200
Neopallene uaorensis 1200-2 100

Pycnogonidae
Pjicn ogon urn gain i 70-2495

Colossendeidae
* Colossendeis angusta 157-5200
c. UrcLtatu 1350hl060
* C. articuluta ( = Hedgpethia articulatu) 1944-3610
* C. bicincta 1920-3050
* C. brevipes 4846
* C . bruurii 4390
* c. clalnta 9942715
* C. colossea 157-5200
* C. cucurhita 1350W400
C. yruci1i.s 2930
* C. hoeki 3112
* C. ,jciponicu 7034390
c. kptwhynchus 3615
* C. niacerrima 5084411
* C. megalonyr rnegalonys 7-5000
C. ni. orcadensr 3 98 7 4 0 0 5
c. ni. scoreshii 143-5221
* C. media 4032
C. niinor 1035-3200
* C. niinufn 1200-3430
C. robustu 0.3-3610
c. oculifera 2145-2900
* C . fenera 1600-3035
* C . subminuta 2150

Nymphonidae
* Boreonjxiphon robustun? 28-2278
I f r teronjrnpli on abyssale 3570
H . bioculniuni 2975-3940
H . poiisitor 2022-2800
H . profundurn 4985-6800
* N J w p h o n conipactuwi 2013-3248
* N . dissiniilis 1924
* .v, ,frn1orale 4050-6650
* .&I. galatlieae 5340-5890
* N. grucilipes 10-3055
.V. iicitlalr 443 5-5 780
* N . illli,lalurm 25 16-2928
 THE BIOLOGY OF PYCNOGONIDA 75

TABLE
14. (cOl71.)

Species Depth (m)

-. ~ ~ ~~ ~ ~ . ..

N . liotnpsoni 1000-2200
* N . inernze 36104585
N . kurilokumchaticutn 2770-2820
N . laterospinum 18944632
* N . longicollum 39484600
* N . longicosa 3 18-2570
N . australe cuecuni 7370
* N . noctum 2871
* N . procerum 2450-6090
* N. p r ~ f u i i ~ u n ~ 323 1
N , sanders i 38 1 5 4 4 35
N . spic,atum 3815
N . ienellutn 398-2452
* N . tenuimanum 3398
N . tripectinatum 7370
N . Iidvisense 4500-5040
Sexan~niphonniiruhilis 2760-2820

isolated from one another by various Rises (the Azores Rise, the Cape Rise,
etc.). Data from the separate deep Atlantic basins suggest a certain
endemism, but this is most likely an artifact of the unequal sampling and
knowledge of some of them (for example, the Brazil Basin has only revealed
six species to date). Colossendeis colossea is common to the Argentine, Cape
and West European Basins, the latter two also having C. macerrima,
Pantopipetta brevicauda (P. longituberculata), Anoplodactylus typhlops and
Nymphon laterospinum; the North American and West European Basins
only have N . laterospinum and Paranymphon spinosum in common.
Known hadal species are few, including Pantopipetta longituberculata,
Ascorhynchus birsteini, and Nymphon procerum which is known from the
North and South Atlantic and Pacific Oceans. Turpaeva (1971a,b,c) found
nine species in the Kurile-Kamchatka Trench, 13 in the Japanese Trench,
including four Ascorhynchus and the deepest recorded pycnogonids, Nym-
phon longitarse caecum and N. tripectinatum at 7370 m; Ascorhynchus bir-
steini has been caught in the Peru Trench (6040 m).

C . Pjwogoniu's in Plankton
While records exist of pycnogonids taken in plankton samples (Anoplodacty-
US petiolatus, Endeis spinosa, E. mollis), it is unlikely that these are other
than accidental catches. Species such as A . petiolatus which have been
recorded in association with medusae, may well become detached from such
76 F. ARNAUD AND R. N. BAMBER

hosts during sampling. Twenty-two specimens of Propallene kempi were

reported from six Madras plankton samples by Gnanamuthu (1950), but
when placed in an aquarium “they were not planktonic in the true sense of
the term”. Stock (1 975a,c) described P. urduu in considerable numbers in
nocturnal plankton in Tanzania over Syringodium grass at 0.7 m depth. The
records of deeper water Pallenopsis species in midwater samples (Hedgpeth,
1962; Mauchline, 1984) are considered to represent bathypelagic behaviour,
and again these species are associated with medusan hosts. If their swimming
is merely a process to maintain themselves in the water current rather than
achieve independent directional locomotion, they may be strictly interpreted
as planktonic. However, such an interpretation is stretching the category of
“temporary” plankton to the limit of “ephemeral” plankton.

VII. Palaeontology and Systematic Affinities

Recognized fossil pycnogonids are extremely rare, though with such a group
of animals probably largely unknown to many palaeontologists, it is
tempting to assume many unrecognized or mis-identified specimens in fossil
collections. The first to be assigned to the pycnogonids was Palaeoisopus
problematicus of Broili (1 928). Its confused history, as suggested by its name,
is discussed by Hedgpeth (l978), who proceeded to review the status of fossil

FIG. 23. Fossil pycnogonids: A, Palaeoisopus problematicus; B, partial reconstruction of

Palaeopanropus maucheri (cephalon unknown); and C , Palaeothea devonica (after Bergstrom, ei
a/., 1980). Scale line represents 60 mm for A, 20 mm for B and 2 mm for C.
 THE BIOLOGY OF PYCNOGONIDA 77

-0
Tertiary
-100
Mesozoic
- 200 Pycn o g onid a
Permian I
-loo
Carboniferous
Oevonlan
Silurian I
i
,
I
?
.I .2 1 3

Ordovician ' I
I
'.
\
- 5 0 0 ___
\

\ .'
'
-
\ a
Cambrian
\ / _- -
- 570 - I

FIG. 24. Schematic evolutionary relationship between chelicerates and pycnogonids, drawn to
a logarithmic scale (after Bergstrom et al., 1980). I-Palaeoisopus, 2-Palaeopantopus, 3-
Palaeothea.

pycnogonids and described a new species from the Jurassic, Pentapalaeo-

p j m o n inconspicua. Most recently, Bergstrom et ul. (1980) have comprehen-
sively reexamined the pycnogonid fossils, including a remarkable series of X-
radiographs, during which they discovered another new species; however,
their studies concluded that Hedgpeth's Pentapalaeopycnon inconspicua is in
fact a Phyllosoma larva.
The three known fossil species (Fig. 23) therefore are all Devonian.
Palaeoisopus problematicus, known from over 50 specimens, is a large
animal, reaching at least 125 mm in body length; its flattened, setose limbs
clearly suggest a swimming pycnogonid, and it may have preyed on
crinoids; there are no gut diverticulae in the limbs. Palaeopantopus maucheri
is known from three specimens, though these show differences which may
represent more than one species. It is smaller than Palaeoisopus (body length
15 mm), and has a walking rather than swimming morphology. Both of
these species have a segmented abdomen (the former with a telson), and they
are regarded as primitive pycnogonids belonging to extinct (separate) orders.
The third species, Palaeothea devonica is known only from the type speci-
men, but is clearly a modern pycnogonid of the extant order Pantopoda. The
specimen is only some 5 mm in length and unfortunately not preparable, but
from X-radiographs shows (coincidental) similarities to Pigrogromitus.
78 F. ARNAUD AND R. N. BAMBER

The systematic position of the pycnogonids within the Arthropoda has

long been a matter of debate. They have been most closely associated with
the Chelicerata, and the phylogenetic relations of this group have been
extensively discussed by Hammen (1 977), Grasshoff (1978), Manton (1 978),
Schram and Hedgpeth (1978) and Bergstrom et al. (1980), but with conflict-
ing conclusions. Bergstrom et al. (1980) discuss the demerits of Manton’s
(1978) use of coordination in locomotion as a systematic character linking
the pycnogonids to the arachnids. Nonetheless, current theories, particu-
larly relating to possible synapomorphies in body segmentation, the absence
of a deuterocerebrum, the tail “spine” of Pa/aeoisopus, and other morpho-
logical and embryological features, favour placing the Pycnogonida within
the Chelicerata, in association with the Xiphosuran-Scorpionid groups, but
deriving from primitive merostomes (Fig. 24). The best available alternative
remains the consideration of the Pycnogonida as a unique and distinct
subphylum.

Acknowledgements

Thanks are due to many colleagues from the Centre d’Oceanologie de Marseille
(Station Marine d’Endoume) who kindly supplied the material on which are based
much of the original data in the Tables (especially Drs G. Desrosiers, J. S. Hong, D.
Leung Tack, M. Menioui, J. Picard, B. A. Thomassin, A. Willsie and H. Zibrowius)
and to the foreign researchers who kindly loaned Nymphonella material (Drs K .
Nakamura and S. Kikuchi); also to D r P. G. Oliver of the Department of Zoology,
National Museum of Wales, for SEM facilities and D r A. W. H. Turnpenny for
word-processing facilities.

Appendix 1
Alpliaheticnl list of species mentioned in the text, with ctuihorities.

Ac-lielia ulaskensis (Cole, 1904)

A . chelata (Hilton, 1939)
A . coinmuizis (Bouvier, 1906)
A . echinata Hodge, 1864
A . grucilis Verrill, 1900
A . lungi Dohrn. 1881
‘4.sawuyui Marcus, 1940
A . shephercti Stock, 1973
A . siniples Giltay, 1934
A . vuIgmis (Costa. 1861)
Aclirliunu tropicalis Arnaud, 1971
Amniothea allopodes Fry and Hedgpeth, 1969
A . carolinensis Leach, I8 14
A . cluusi Pfeffer, 1889
 THE BIOLOGY OF PYCNOGONIDA 79

A . glacialis (Hodgson, 1907)

A . hilgendorfi (Bohm, 1879)
A . magniceps Thomson, 1884
A . srriata (Mobius. 1902)
Ammothella uppendiculatu ( Dohrnl 1881)
A . hiunguicularu (Dohrn, 1881)
A . exornuta Stock, 1975
A . indicu Stock, 1954
A . longipes (Hodge, 1864)
A . marcusi Hedgpeth, 1948
A . pucifica Hilton, 1942
A . rugulosa (Verrill, 1900)
A . setacea (Helfer, 1938)
A . spinifera Cole, 1904
A . stauroniutu Child, 1982
A . tubicen Stock, 1978
A . uniunguiculuta (Dohrn, 1881)
Anoplodactjlus allotrius Child, 1979
A . ungulutus (Dohrn, 1881)
A . antillianus Stock, 1975
A . urescus Du Bois Reymond Marcus, 1959
A . uustralis (Hodgson, 1914)
A . batangemis (Helfer, 1938)
A. rrihellatus Calman, 1923
A . digitatus (Bohm, 1879)
A . erectus Cole, 1904
A . evansi Clark, 1963
A . evelinae Marcus, 1940
A . gesfiens (Ortmann, 1890)
A . glandulifer Stock, 1954
A . insignzformis Stock, 1975
A . jonesi Child, 1974
A . lentus Wilson, 1878
A . marshallensis Child, 1982
A . mussilienszs Bouvier, 19I6
A . monotrema Stock, 1979
A . multiclavus Child, 1977
A . ophiurophilus Stock, 1979
A . parvus Giltay, 1934
A . pectinus Hedgpeth, 1948
A . perforatus Nakamura and Child, 1982
A . petiolatus (Kroyer, 1844)
A . portus Calman, 1927
A . pulcher Carpenter, 1907 ?A. tubiferus
A . pygmaeus (Hodge, 1864)
A . reimerae Child, 1979
A . suxatilis (Calman, 1923) A . digitatus
A . stellatus Nakamura and Child, 1983
A . stri Child, 1979
A . tubiferus (Haswell, 1885)
80 F. ARNAUD AND R. N. BAMBER

A . typhlops Sars, 1888

A . virescens (Hodge, 1864)
Ascorhynchus abyssi Sars, 1877
A . agassizi Schimkewitsch, 1893
A . arenicola (Dohm, 1881)
A . armatus (Wilson, 1881)
A. athernum Child, 1982
A . birsteini Turpaeva, 1971
A . breviscapus Stock, 1968
A . bucerus Turpaeva, 1971
A . castelli (Dohrn, 1881)
A . castellioides Stock, 1957
A . corderoi Du Bois Reymond Marcus, 1952
A . cuculum Fry and Hedgpeth, 1969
A. endoparasiticus Arnaud, 1978
A . glaber Hoek, 1881
A . i$atum Stock, 1963
A . latipes Cole, 1906
A . losinalosinskii Turpaeva, 1971
A . mariae Turpaeva, 1971
A . ovicoxa Stock, 1975
A . pararmatus Stock, 1975
A . prosum Child, 1983
A . ramipes (Bohm, 1879)
A . simile Fage, 1942
A . turritus Stock, 1978
A . utinomii Nakamura and Child, 1982
Austrodecus breviceps Gordon, 1938
A . fagei Stock, 1957
A . glaciale Hodgson, 1907
Austropallene tcherniae Fage, 1952
Boehmia chelata (Bohm, 1879)
B. longirostris Stock, 1957
B. tuberosa Mobius, 1902
Boreonymphon abyssorurn (Norman, 1873)
Callipallene acus (Meinert, 1898)
C. arnaxana Ohshima, 1933
C. brevirostris (Johnston, 1837)
C. emaciata (Dohrn, 1881)
C. margarita (Gordon, 1932)
C. phantoma (Dohrn, 188 1)
C. soliciiatus Child, 1979
C. spectrum (Dohm, 1881)
Cilunculus acanthus Fry and Hedgpeth, 1969
C. alcicornis Stock, 1978
C. cactoides Fry and Hedgpeth, 1969
C. tubicinis Child, 1982
Colossendeis angusta Sars, 1877
C. arcuata A. Milne-Edwards in Filhol, 1885
C. australis Hodgson, 1907
 THE BIOLOGY OF PYCNOGONIDA 81

C. bicincta Schimkewitsch, 1893

C. brevipes Hoek, 1881
C. bruuni Fage, 1956
C. clavata Meinert, 1898
C. colossea Wilson, 1881
C. cucurbita Cole, 1909
C. gigantea Stuxberg, 1887 = C. proboscidea
C. glacialis Hodgson, 1907
C. gracilis Hoek, 1881
C. hoeki Gordon, 1944
C. japonica Hoek, 1898
C. leptorhynchus Hoek, 1881
C. macerrima Wilson, 1881
C. media Hoek, 1881
C. megalonyx Hoek, 1881
C. m. megalonyx Fry and Hedgpeth, 1969
C. m. orcudense Hodgson, 1908
C. m. scoresbii Gordon, 1932
C. melancholicus Stock, 1975
C. minor Schimkewitsch, 1893
C. mirzuta Hoek, 1881
C. oculfera Stock, 1963
C. proboscidea (Sabine, 1824)
C. robusta Hoek, 1881
C. scotti Calman, 1915
C. subminuta Schimkewitsch, 1893
C. tenera Hilton, 1943
Decolopodu untarctica Bouvier, 1905
D. australis Eights, 1834
Dodecolopoda mait9soni Calman and Gordon, 1933
Dromedopycnon acanthus Child, 1982
Elassorhis laterospina Child, 1982
Endeis australis (Hodgson, 1907)
E. charybdaea (Dohrn, 1881)
E. Jaccida Calman, 1923
E. moNis (Carpenter, 1904)
E. nodosa Hilton, 1942
E. picta Bamber, 1979 ?E. straughani
E. spinosa (Montagu, 1808)
E. straughani Clark, 1970
E. viridis Pushkin, 1976
Eurycyde raphiaster Loman, 1912
Hannonia spinipes Stock, 1956
H . typica Hoek, 1881
Hedgpethia articulata Turpaeva, 1973
Hedgpethius tridentatus Child. 1974
ffeteron~mphonabyssale (Stock, 1968)
H . bioculatum Turpaeva, 1956
H . e.uiguum (Hodgson, 1927)
H . ponsitor Child, 1982
82 F. ARNAUD AND R . N. BAMBER

H . profundurn Turpaeva, 1956

Megarhethis brevichel~/erus(Hedgpeth, 1948)
.Mimipcillene atlantis Child, 1982
Neopallent, a-orensis Arnaud, 1974
Nymphon adareanurn Hodgson, 1907
N . uemulurn Stock, 1975
N. austrule Hodgson, 1902
N . a. caecum Gordon, 1944
N. hrevicautiurum Miers, 1875
N. hrevirostre Hodge, 1863
N. caementarum Stock, 1975
N . conipuctum Hoek, 1881
N. cii.c.corsico.rae Child, 1982
N . tlissimilis Hedgpeth, 1949
N . ,femorale Fage, 1956
N. jioridunum Hedgpeth, 1948
N . foxi Calman, 1927
N . galatheue Fage, 1956
N . gracile Leach, 1814
N . gracilipes Miers, 1875
N . grossipes (Kroyer, 1844) (?O. Fabricius)
N . hodale Child, 1982
N.hamutum Hoek, 1881
N.hampsoni Child, 1982
N . hirtipes Bell, 1853
N . hirtum (Fabricius, 1780)
N . inerme Fage, 1956
N. kurilokamchuticum Turpaeva, 1971
N. laterospinum Stock, 1963
N . leptocheles Sars, I888
N. longicollum Hoek, 1881
N . longico.vu Hoek, 1881
N. longitarse Kroyer, 1844
N . mucronj3.r (Sars, 1877)
N . niaculatum Carpenter, 1910
N. muoriana Clark, 1958
N . noetuin Hilton, 1942
N. orcadense (Hodgson, 1908)
N . ptrrarificum Merton, 1906
N . pi.rellae Scott, 1912
N. procerum Hoek. 1881
N.profundun? Hilton, 1942
N . rohusrum Bell. 1855
N.santlersi Child, 1982
N . seriniunus Barnard, 1946
A’. sluireri Hoek. I88 1
N. spicurimi Child, 1982
N . stroemi Kroyer, I844
N . tenellum (Sars, 1888)
N. renuimanum Hodgson, 19 14
 THE BIOLOGY OF PYCNOGONIDA 83

N . tripectinatum Turpaeva, 1971

N . tubiferum Stock, 1978
N . walvisense Stock, 1981
Nymphonella lamhertensis Stock, 1959
N . leculvezi Guille and Soyer, 1967
N . tapetis Ohshima, 1927
Nymphopsis acinacispinatus bathursti Williams, 1940
N . duodorsospinosa Hilton, 1942
Palaeoisopus problematicus Broili, 1928
Palaeopantopus muucheri Broili, 1929
Palaeothea deuonica Bergstrom, Sturmer and Winter, 1980
Pallenoides spinulosa Stock, 1955
Pallenopsis calcanea Stephensen, 1933
P. californicu Schimkewitsch, 1893
P. cidaribatus Child, 1975
P. comosa Stock, 1975
P. guineensis Stock, 1975
P. juttingae Stock, 1964
P. longirostris Wilson, 1881
P. longiseta Turpaeva, 1957
P. mollissima (Hoek, 1881)
P. oscitans (Hoek, 1881)
P. patagonica (Hoek, 1881)
P. pilosa (Hoek, 1881)
P. prqfunda Hilton, 1942
P. scoparia Fage, 1956
P. tritonis Hoek, 1883
P. tydemani Loman, 1908
P. vanhoefleni Hodgson, 1914
Pantopipetta angusta Stock, 1981
P . australis (Hodgson. 1914)
P. auxiliata Stock, 1968
P. breuicauda Stock, 1963 (?P.longituberculata)
P. capensis (Barnard, 1946)
P. latu Stock, 1981
P. longituberculata (Turpaeva, 1955)
P. weberi (Loman, 1904)
Paranymphon spinosunz Caullery, 1896
ParapaIlene algoae Barnard, 1946
P. australiensis (Hoek, 1881)
P. nierstraszi Loman, 1908
Pentacolossendeis reticulata Hedgpeth, 1943
Pen tunymphon antarcticum Hodgson, 1904
p . minuturn Gordon, 1944
Pentapalueopycnon inconspicun Hedgpeth, 1978
Pentapyenon charcoti Bouvier, 1910
P . grayi Bouvier, 191 I
Phoxichilidium firnoraturn (Rathke, 1799)
p . masillare Stimpson, 1853 ( P . femorutunz)
Pigrogromitus titnsunus Calman, 1927
84 F. ARNAUD AND R. N. BAMBER

Propallene arduu Stock, 1975

P. kernpi (Calman, 1923)
P. longiceps (Bohm, 1879)
Protrygaeus ammothelloides Stock, 1975
Pseudopallene ambigua Stock, I956
P. circularis (Goodsir, 1842)
Pycnogonum arbustum Stock, 1966
P. aurilineatum Flynn, 1919
P. forte Barnard, 1954
P. guini Bouvier, 1910
P. littorule (Strom, 1762)
P. nodulosum Dohrn, 1881
P. platvlophum Loman, 1923
P. plumipes Stock, 1960
P. pusillum Dohrn, 1881
P. stearnsi Ives, 1892
P. tuberculatum Clark, 1963
Pycnogonum Nulloviger anovigerum Clark, 1956
P. ( N ) africanum Calman, 1938
P. ( N ) elephas Stock, 1966
Pycnosomia asrerophila Stock, 1981
P. strongylocentroti (Losina-Losinsky, 1933)
Queubus jamesanus Barnard, 1946
Rhopalorhynchus claudus Stock, 1975
R. gracillimum Carpenter, 1907
R. lomani Stock, 1958
Rhynchothorax alcicornis Krapp, 1973
R. anophthalmus Arnaud, 1972
R. architectus Child, 1979
R. australis Hodgson, 1907
R. mediterraneus Costa, 1861
R. monnioti Arnaud, 1974
R. philopsummum Hedgpeth, 1951
R. unicornis Fage and Stock, 1966
Sericosura mitrata (Gordon, 1944)
Sr.runytnphon miruhilis Hedgpeth and Fry, 1964
Sfjfopullene longicuuda Stock, 1973
Tanystylurn anthomasti Hedgpeth, 1949
T. brevipes (Hoek, 1881)
T . cavidorsum Stock, 1957
T. conirosrre (Dohrn, 1881)
T. getninum Stock, 1954
T. istl7miocum Stock. 1955
T. oeclinotum Loman, 1923
T. orhiculare Wilson, 1878
T. stvligerum (Miers, 1875)
T. tirhirostre Stock, 1954
Trj,grrrus communis Dohrn, 1881
 THE BIOLOGY OF PYCNOGONIDA 85

Appendix 2
Families and genera of Pycnogonida. This classijication is a necessary compromise
intended to represent the greatest areas of agreement in current thinking, based on
traditional morphological taxonomy but utilizing the ideas of Fry (1978) to resolve
certain controversies. Attempts at higher levels of classification are currently so
conjectural as to be pointless at present.

Fossil Genera
Palaeoisopodidac Hedgpeth. 1978 Palaeopantopodidae Hedgpeth, 1955
Pulaeoisopus Broili, 1928 Pulaeopantopus Broili, 1929
Incertae sedis
Palueothea Bergstrom et a/.. 1980
Living Genera
Nymphonidae Wilson, 1878 Mugnummothcm Fry and Hedgpcth,
Boreonymphon Sars, 1888 1969
Heteronyniphon Gordon, 1932 Megarhethus Child, 1982
Ntmymphon Stock, 1955 Njwphopsis Haswell, 1884
Nymphon Fabricius, I794 Ourhynchus Hoek, 1881
Njwphonella Ohshima, 1927 Purunj.nzphon Caullery. 1896
Pentan.vmphon Hodgson, I904 Pentacolos.c.cndeis Hedgpeth, 1943
Se.uunj'mphon Hedgpeth and Fry, Pigrogrornitus Calman, 1927
1964 Prototrygueus Stock, 1974
Pj'cnofiagilia Hcdgpeth, 1948
Ammotheidae Dohrn, 1881 Pycnosoniia Losina-Losinsky, 1935
Achclirr Hodge, 1864 Scipiolus Loman, 1908
Acheliunu Arnaud, 1971 Sericosurci Fry and Hedgpeth, 1969
Au'uncorostris Fry and Hedgpcth, T u n j , s t j h n Miers, 1879
1969 T/iuvmustupycnon Fry and Hedgpeth,
Ammotheu Leach. 1814 1969
Amniothella Verrill, 1900 Trj~gaeusDohrn, 1881
Ananimothea Fry and Hedgpeth, 1969
Ascorhjnchus Sars, 1877 Endeidae Norman, 1908
Athernopjvwn Fry and Hedgpeth, Eiideis Philippi, 1843
1969
Austroraptus Hodgson, 1907
Boehniia Hoek, 1881 Callipallenidae Hilton, 1942
Culj,psopynon Hedgpeth, 1948 Anoropallene Stock, 1956
Chonorhw Nakamura and Child, 1983 AustropallenP Hodgson, 1915
Cihiriculus Loman, 1908 Callipallene Flynn, 1929
Decache/a Hilton, 1939 Cheilopallene Stock, 1955
Droniedopjwioi? Child, 1982 Clavigeropallene Pushkin, 1974
Elassorhis Child. 1982 Hannonia Hoek, 1881
E p l i ~ ~ r o g ~ ~ nHedgpeth,
ziza 1943 Metupcrllene Schimkewitsch 1929
Gir!~cj~dc~ Schiodte, 1857 Mimipallene Child. 1982
Hcj&pethiu.r Child. 1974 Neopallene Dohrn, 1881
H m i c h e / u Stock. I954 Oropulleiw Schimkewitsch, 1929
Ht>teroficigiIiaHedgpeth, 1943 Pallenella Schimkewitsch. 1909
86 F. ARNAUD AND R. N. BAMBER

Austrodecidae Stock, 1954

Pallenoides Stock, 1950 Austrodecus Hodgson, 1907
Parupallene Carpenter, 1892 Puntopipetin Stock, 1963
Propallene Schimkewitsch, 1909
PseudopaIlene Wilson, 1878 Colossendeidae Hoek, 1881
fycnotheu Loman, 1920 Colossendei~Jarzynsky, 1870
Seguapallene Pushkin, 1975 Decolopoda Eights, 1835
Siphopallene Clark, 1963 Dodecolopoda Calman and Gordon, 1933
Spasmopalhe Stock, 1968 Hedgpethiu Turpaeva, 1973
St.dopallene Clark, 1963 Rhopulor1z)~nchusWood Mason, 1873

Phoxichilidiidae Sass, 1891 Rhynchothoracidae Fry, 1978

Anoplodactylus Wilson, I878 Costa, 1861
Rh~~tzclzotlroru.~
Hodgsoniu Schimkewitsch, 1929
Pallenopsis Wilson, 1881 Pycnogonidae Wilson, 1878
fhoxichilidiun~Milne-Edwards, 1840 Pentapyenon Bouvier, 1910
Pho.~iplzilyraStock, 1974 Pycnogonum Brunnich, I764

Tncertae sedis
Nunonymphon McCloskey, 1967
Queubus Barnard, 1946
Synonymies accepted herein in addition to those listed by Fry (1978):
Discoarachne Hoek, 1881 = Tanysrylum Miers, 1879
Ecleipsothremma Fry and Hedgpeth, 1969 = Ammothea Leach, 1814
Kyphomia Helfer, 1938 = Ammothella Verrill, 1900

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